Indexed in MEDLINE, PubMed, and PubMed Central PRSRT STD US POSTAGE National Library of Medicine PAID 500 NE Multnomah St, Suite 100 PORTLAND OR PERMIT NO 1452 Portland, Oregon 97232 Volume 18 No. 4 — Fall 2014

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A peer-reviewed journal of medical science, social science in medicine, and medical humanities

Original Research & Contributions 4 Mindfulness-Based Stress Reduction in an Integrated Care Delivery System: One-Year Impacts on Patient-Centered Outcomes and Health Care Utilization 10 Improving Appropriate Use of Pulmonary Computed Tomography Angiography by Increasing the Serum D-Dimer Threshold

and Assessing Clinical Probability 16 Testing for Meningitis in Children with THE PERMANENTE JOURNAL Bronchiolitis 21 Impact of Implementing Glycated Hemoglobin Testing for Identification of Dysglycemia in Youth 29 Most Common Dermatologic Topics Published in Five High-Impact General Medical Journals, 1970-2012: Melanoma, Psoriasis, Herpes Simplex, Herpes Zoster, and Acne 32 Prevalence of Hypovitaminosis D and Its Association with Comorbidities of Childhood Obesity 40 A Pilot Study Comparing Anatomic Failure after Sacrocolpopexy with Absorbable or Permanent Sutures for Vaginal Mesh Attachment 45 Differences in Perceived Difficulty in Print and Online Patient Education Materials Special Reports 52 Behavior Medicine Specialist 58 Mindful Mood Balance: A Case Report of Web-Based Treatment of Residual Depressive Symptoms 64 Thinking about Thinking and Emotion: The Metacognitive Approach to the Medical Humanities that Integrates the Humanities with the Basic and Clinical Sciences Editorial

89 Healthy Behavior Change in Practical Settings Follow @PermanenteJ Printed on acid free paper.

The Permanente Journal Fall 2014 Volume 18 No. 4 See inside for additional content ISSN 1552-5767 as well as articles found only online www.thepermanentejournal.org

Fall 2014/ Volume 18 No. 4 The ORIGINAL RESEARCH 21 Impact of Implementing Glycated Books published by & CONTRIBUTIONS Hemoglobin Testing for Identification PermanenteJournal Permanente authors: 4 Mindfulness-Based Stress Reduction of Dysglycemia in Youth. in an Integrated Care Delivery Vinutha Vijayadeva, PhD; Gregory A Mission: The Permanente Journal advances System: One-Year Impacts on Patient- Nichols, PhD knowledge in scientific research, clinical Centered Outcomes and Health Care At both, Kaiser Permanente Hawaii and medicine, and innovative health care delivery. Utilization. Tracy McCubbin, MD; Kaiser Permanente Northwest, fasting Sona Dimidjian, PhD; Karin Kempe, plasma glucose testing was significantly Is This Normal? MD, MPH; Melissa S Glassey; Colleen more common in 2009 and HbA1C testing The Essential Guide to Circulation: 25,000 print readers per Ross, MS; Arne Beck, PhD was more common in 2012, but the Middle Age and Beyond quarter, 6900 eTOC readers, and in Mindfulness-based stress reduction (MBSR) characteristics of the overall population John Whyte, MD, MPH did not change. At both sites, the 2013, TPJ content had 1 million page programs have demonstrated clinical ef- ISBN-10: 160961450X fectiveness for both mental and physical characteristics of youth at risk of diabetes views—660,000 of those on TPJ articles changed substantially with a much greater ISBN-13: 978-1609614508 on PubMed. Viewers visited from health conditions. Less research exists on health services utilization, self-efficacy, or proportion being female and children Emmaus, PA: Rodale Press; 2012 187 countries/territories. work productivity outcomes. A prospective younger than age 10 years. The size Paperback: 272 pages single cohort design evaluated an 8-week and composition of the population $15.99 MBSR program for 38 Kaiser Permanente of youth identified with diabetes was Colorado members with chronic pain, not affected. chronic illness, or stress-related problems. 29 Most Common Dermatologic Topics Repeated measures analyzed at 8 weeks Published in Five High-Impact and 1 year showed significant improve- General Medical Journals, 1970-2012: ments in self-reported mental and physical Melanoma, Psoriasis, Herpes Simplex, function, pain, psychological symptoms, Herpes Zoster, and Acne. and self-efficacy, but not in work produc- Handbook of Anesthesia, Backlit Aspens Young M Choi; Aram A Namavar, MS; 5th edition tivity. There were also significant decreases Jashin J Wu, MD Near Monitor Pass, at 1 year for visits to: primary care, spe- John J Nagelhout, Karen L Plaus California 2012 Internists frequently diagnose herpes cialty care, and the Emergency Depart- ISBN-10: 145571125X by Stuart Hahn, MD simplex, herpes zoster, and acne, which ment, and for hospital admissions. ISBN-13: 978-1455711253 This photograph of a are also common dermatologic topics beautifully lit aspen 10 Improving Appropriate Use of published. The authors conducted an Philadelphia, PA: Saunders; 2013 grove in autumn was Pulmonary Computed Tomography independent search of the Thomson Paperback: 864 pages taken in the Sierra Angiography by Increasing the Serum Reuters’ Science Citation Index for $70.95 Nevada Mountains near D-Dimer Threshold and Assessing common dermatologic topics, limited to the border of California Clinical Probability. Sydney Char; the period 1970 to 2012. The five most and Nevada. Hyo-Chun Yoon, MD, PhD common dermatologic topics published in five high-impact general medical journals Dr Hahn retired from The Permanente A retrospective review was conducted of all patients undergoing pulmonary com- were melanoma, psoriasis, herpes simplex, Medical Group in 2010. He has been seri- herpes zoster, and acne. ously exploring photography since 2000 puted tomography angiogram during 2 and has an interest in both wildlife and separate 12-month intervals: 1 before the 32 Prevalence of Hypovitaminosis D and landscape photography. For further infor- implementation of an increased D-dimer Its Association with Comorbidities of mation about his artwork, Dr Hahn can threshold and recommendation for formal Childhood Obesity. Ronald Williams, Luck Just Happens clinical probability assessment, and the be contacted at: [email protected]. MD, FAAP, FACP; Marsha Novick, MD; Paul Crane ANNOUNCEMENT: other after regional implementation. The Erik Lehman, MS prevalence of pulmonary embolism de- ISBN-10: 1479798290 ISBN-13: 978-1479798292 tected by computed tomography angiog- We conducted a retrospective chart CME Credits Now Available for Reviewers raphy increased from 4.7% to 11.7%, but review from 155 obese children aged Bloomington, IN: XLibris; 2013 only 4% of patients had a formal clinical 5 to 19 years who attended the Penn Paperback; 182 pages probability assessment recorded in their State Children’s Hospital Pediatric $19.99 electronic medical record. Multidisciplinary Weight Loss Program from November 2009 through November The Permanente Journal is happy to announce 16 Testing for Meningitis in Children with 2010. Under the latest Institute the availability of Continuing Medical Education Bronchiolitis. Michael Stefanski, MD, of Medicine definitions, vitamin D credits for completing manuscript reviews for 93 LETTERS TO THE EDITOR MPH; Ronald Williams, MD, FAAP, deficiency (< 20 ng/mL) and insufficiency FACP; George McSherry, MD; Joseph (20-29 ng/mL) was present in 40% The Permanente Journal. Physicians are now eligible 95 BOOK REVIEWS Geskey, DO, MBA and 38% of children, respectively. African-American race, winter/spring to receive up to 15 AMA PRA Category 1 Credits 96 CME EVALUATION FORM The authors present a retrospective, case-control study of hospitalized infants season, hyperinsulinemia, elevated Crush Step 1: The Ultimate per year (3 AMA PRA Category 1 Credits per systolic blood pressure, urban location, USMLE Step 1 Review younger than age one year diagnosed manuscript). With this change, we have launched with viral bronchiolitis who underwent and total numbers of comorbidities were significantly associated with Theodore X O’Connell, lumbar puncture as part of an evaluation Ryan A Pedigo, Thomas E Blair our new For Reviewers home page on our Web site: for meningitis. The presence of apnea, hypovitaminosis D (< 30 ng/mL). Obese ISBN-10: 1455756210 cyanosis, meningeal signs, positive urine children should be considered for routine www.thepermanentejournal.org/reviewers.html. ISBN-13: 978-1455756216 culture results, and young age were fac- vitamin D screening. tors found to be preliminarily associated Philadelphia, PA: Saunders; 2013 Paperback: 680 pages The Permanente Journal with the performance of a lumbar punc- ture in the setting of bronchiolitis. Young $37.75 500 NE Multnomah St, Suite 100 age was the only significant clinical factor The Portland, Oregon 97232 found after multivariable regression; no www.thepermanentejournal.org other demographic, clinical, laboratory, PermanenteJournal or radiologic variables were found to be ISSN 1552-5767 significant.

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40 A Pilot Study Comparing Anatomic edge and experience used to treat mental system was associated with cost savings, Failure after Sacrocolpopexy with illness into the medical home to help the shorter lengths of stay, and decreased mor- Absorbable or Permanent Sutures for primary care physician improve the care tality. However, two studies suggested in- Vaginal Mesh Attachment. of all patients in the medical home. creased hospital cost after implementation. Jasmine Tan-Kim, MD, MAS; Shawn A Intensivists working these systems are able Special Report Menefee, MD; Quinn Lippmann, MD, to more effectively treat ICU patients, pro- 58 Mindful Mood Balance: A Case Report MPH; Emily S Lukacz, MD, MAS; Karl M viding better clinical outcomes for patients of Web-Based Treatment of Residual Luber, MD; Charles W Nager, MD at lower costs compared with hospitals Depressive Symptoms. without a tele-ICU. The authors reviewed the medical records Jennifer Felder, MA; Sona Dimidjian, of 193 women who underwent sacrocol- PhD; Arne Beck, PhD; Jennifer M Boggs, popexy with 2 different types of sutures MSW; Zindel Segal, PhD CASE STUDIES attaching polypropylene mesh to the Residual depressive symptoms are associ- vagina: delayed absorbable sutures (me- 85 Vasal Injury During Inguinal ated with increased risk for relapse and dian follow-up, 43 weeks) and permanent Herniorrhaphy: A Case Report and Review impaired functioning. Although there sutures (median follow-up, 106 weeks). of the Literature. Lawrence Flechner, is no definitive treatment, Mindfulness- Failure rates for the 45 subjects in the MD, PhD; James Smith, MD, MS; Patrick Based Cognitive Therapy (MBCT) has delayed absorbable group and 148 sub- Treseler, MD, PhD; John Maa, MD been shown to be effective, but access is jects in the permanent suture group were An injury to the vas deferens during limited. Mindful Mood Balance (MMB), similar and not statistically different in any inguinal herniorrhaphy from a Web-based adaptation of MBCT, was compartment: apical, anterior, or posterior. possible tethering of the vas has designed to address this care gap. The Delayed absorbable monofilament suture not, to our knowledge, previously authors describe a composite case that is appears to be a reasonable alternative to been described in the surgical representative of the course of interven- permanent suture for mesh attachment to literature. We report a case of tion with MMB and its implementation in the vagina during sacrocolpopexy. iatrogenic injury of the vas deferens a large integrated delivery system. MMB that occurred during elective hernia may be a cost-effective and scalable op- 45 Differences in Perceived Difficulty in repair in a 28-year-old man who tion in primary care for increasing access Print and Online Patient Education had previously sustained blunt to treatments for patients with residual Materials. Michael Farnsworth, MA trauma to the abdomen and pelvis. depressive symptoms. Patients are often intimidated by the task of reading patient education materials, Special Report perceiving the materials’ difficulty levels 64 Thinking about Thinking and Emotion: EDITORIAL Book Review as prohibitive, even when they do not The Metacognitive Approach to the 89 Healthy Behavior Change page 95 exceed the patients’ reading abilities. Medical Humanities that Integrates the in Practical Settings. Some first-year college students per- Humanities with the Basic and Clinical Scott Young, MD ceived online patient education materials Sciences. Quentin G Eichbaum, MD, The core principle of implementing to be more difficult to read than print- PhD, MPH, MFA, MMHC, FCAP healthy behavior change is making the based ones—even when the reading The explosion in medical knowledge has healthy choice the easy choice. Putting level of the patient education materials exceeded the capacity of the individual this motto into practice requires removal was similar. Patients’ perceptions of the human brain to absorb the entirety of this of barriers to live a healthy lifestyle. It is difficulty of patient education materials knowledge. This suggests we can no lon- important to look at the bigger picture influenced their ability to effectively learn ger expect medical students to continue when helping patients reach optimal from those materials. simply memorizing facts. Instead, we health, looking closely at exercise levels Special Report must develop in students a competency and home life. Environmental factors 52 Behavior Medicine Specialist. as flexible thinkers and agile learners so cause strain and present challenges also. Phillip Tuso, MD, FACP, FASN they can adeptly deal with new knowl- The Care Management Institute and edge, complexity, and uncertainty in a Kaiser Permanente are changing default A behavioral medicine specialist is a rapidly changing world. Such a compe- behaviors so optimal lifestyles become the psychologist who works in the medical tency would entail not only cognitive norm, rather than the exception. home with the primary care physician. but also emotional skills essential for the The key to achieving Total Health will be to holistic development of their professional transform the current health care system identity. This article will argue that meta- LETTERS TO THE EDITOR from a focus on treating disease to a focus cognition—“thinking about thinking (and 93 Narratives In Medical Education: on preventing disease. This transforma- emotion)”—offers the most viable path The Next Steps. tion will require complex behavior change toward developing this competency. interventions and services not usually pro- 94 Plant-Based Diets in Crohn’s Disease. vided in the medical home. The behavioral medicine specialist will bring the knowl- REVIEW ARTICLES 76 A Business Case for Tele-Intensive Care Units. Alberto Coustasse, DrPh, MD, MBA, MPH; Stacie Deslich, MA, MS; Deanna Bailey, MS; Alesia Hairston, MS; David Paul, DDS, PhD ONLINE SOUL OF THE HEALER A tele-intensive care unit (tele-ICU) uses 20 Okavango Evening telemedicine, in an intensive care unit ONLY David Clarke, MD (ICU) setting, to care for critically ill pa- See page 2 for additional content 28 The Snorer tients by off-site clinical resources. This lit- David A Dumbrell erature review examined a large number from The Permanente Journal of studies of implementation in hospitals. available online only. 51 Morning Mist The evidence supporting cost savings Brad Christian McDowell, MD was mixed. Implementation of a tele-ICU 63 Moose Antlers of Eielson Sally J Cullen, MD, MS

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EDITOR-IN-CHIEF: Tom Janisse, MD, MBA EDITORIAL BOARD ASSOCIATE EDITOR-IN-CHIEF: Lee Jacobs, MD Maher A Abbas, MD, FACS, FASCRS Ellen Cosgrove, MD Tieraona Low Dog, MD Digestive Disease Institute, Cleveland Vice Dean, Academic Affairs, Director of Education, Program in SENIOR EDITORS Clinic, Abu Dhabi, UAE; Associate University of Washington School of Integrative Medicine, University of Professor of Surgery, Cleveland Medicine, Seattle, Washington Arizona; Clinical Assistant Professor, Vincent Felitti, MD Preventive Medicine, Book Reviews Clinic Lerner College of Medicine Quentin Eichbaum, MD, PhD, MPH, Department of Medicine, Clinical Gus M Garmel, MD, FACEP, FAAEM Clinical Medicine of Case Western Reserve University, MFA, MMCH, FCAP Lecturer, University of Arizona Arthur Klatsky, MD Original Articles Cleveland, Ohio Assistant Dean for Program Develop- College of Pharmacy, Tucson Scott Rasgon, MD Corridor Consult Richard Abrohams, MD ment; Associate Director of Transfu- Lewis Mehl-Madrona, MD, PhD, MPhil Internal Medicine and Geriatrics, sion Medicine; Associate Professor Director of Geriatric Education, Maine The Southeast Permanente Medical of Pathology; Associate Professor of Dartmouth Family Medicine Residency; ASSOCIATE EDITORS Group, Atlanta, Georgia Medical Education and Administra- Director of Education and Training, Mikel Aickin, PhD Fábio Ferreira Amorim, MD, PhD tion; Director, Fellowship Program Coyote Institute, Augusta, Maine Biostatistics Professor of Medicine, Escola in Transfusion Medicine; Member, Michel M Murr, MD, FACS James J Annesi, PhD, FAAHB, FTOS, FAPA Superior de Ciências da Saúde in Vanderbilt Institute for Global Professor of Surgery, Director of Health Behavior Research the Department of Research and Health; Vanderbilt University School Bariatric Surgery, University of South Marthie Baker, MS, MA, RN Scientific Communication, Brasilia, of Medicine, Nashville, Tennessee Florida Health Science Center, Nursing Research Brazil Linda Fahey, RN, NP, MSN Tampa, Florida Ricky Chen, MD Stanley W Ashley, MD Regional Manager, Quality and Sylvestre Quevedo, MD Medicine in Society Chief Medical Officer, Brigham and Patient Safety, Patient Care Services, Department of Medicine and Global Kaiser Permanente, Southern Gary W Chien, MD Women’s Hospital; 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The Permanente Journal/ Fall 2014/ Volume 18 No. 4 3 credits available for this article — see page 96.

ORIGINAL RESEARCH & CONTRIBUTIONS Mindfulness-Based Stress Reduction in an Integrated Care Delivery System: One-Year Impacts on Patient-Centered Outcomes and Health Care Utilization

Tracy McCubbin, MD; Sona Dimidjian, PhD; Karin Kempe, MD, MPH; Melissa S Glassey; Colleen Ross, MS; Arne Beck, PhD Perm J 2014 Fall;18(4):4-9 http://dx.doi.org/10.7812/TPP/14-014 Editor’s note: Please see related article on page 58. individuals report chronic pain2; nearly half of them experience Abstract poor control over their symptoms, highlighting the limitations Background: Mindfulness-based stress reduction (MBSR) pro- of drug therapy as well as the complexity of the psychosocial grams have demonstrated clinical effectiveness for both mental and physical aspects of chronic pain. and physical health conditions. Less research exists on health Mindfulness-based therapies, which include mindfulness- services utilization, self-efficacy, or work productivity outcomes. based cognitive therapy and mindfulness-based stress reduction Objective: To assess one-year outcomes of MBSR in patients (MBSR), have emerged as effective treatments for a variety of with chronic pain, chronic illness, or stress-related problems, conditions, including chronic pain, anxiety, depression, and measuring functional status, pain, self-efficacy, depression, psychological distress.3-8 Such treatments aim to help patients anxiety, somatization, psychological distress, work productivity, develop an understanding of their vulnerabilities to illness and and changes in health services utilization. to build resilience through shifting cognitive, affective, and be- Methods: A prospective single cohort design evaluated an havioral responses to both internal distress and external stressors. eight-week MBSR program for Kaiser Permanente Colorado Through the practice of mindfulness, which has been described members. Patient-reported measures were collected at baseline, as paying attention, on purpose and without judgment in the eight weeks, and one year following MBSR. Differences in health present moment,3 patients are taught to increase awareness and services utilization were compared from six months before MBSR acceptance and to develop more skillful ways of responding to to six months following the one-year anniversary of MBSR. mental and physical experiences. Results: Most of the 38 participants were white (28; 74%), MBSR is typically delivered as a group intervention in eight female (30; 79%), employed part-time (35; 92%), and average class sessions with a separate six-hour retreat. In addition, one age 52.6 years, with multiple comorbidities (averaging 16.4 recent study has looked at the feasibility of an online mindfulness unique diagnoses), the most common being joint or back pain program for stress management.8 Patients who benefit from this (28; 74%) and psychological disorder (20; 53%). Repeated mea- type of therapy include those experiencing stress-related illness sures analyses at 8 weeks (n = 26) and at 1 year (n = 24) showed such as irritable bowel syndrome, muscle tension, fibromyalgia, significant improvements in self-reported mental and physical and chronic migraine,9-12 as well as patients who have chronic function, pain, psychological symptoms, and self-efficacy, but diseases or chronic pain and are not coping well because of not work productivity. Significant decreases at 1 year were ob- anxiety, depression, stress, or lack of family support.13 served for visits in primary care (-50%, p < 0.0001), specialty Since the publication of Kabat-Zinn’s original study on care (-38%, p = 0.0004), and the Emergency Department (-50%, mindfulness training in the medical setting,14 a burgeoning p = 0.04), and for hospital admissions (-80%, p = 0.02). literature has described the effectiveness of MBSR and similar Conclusion: The MBSR program was associated with im- mindfulness-based therapies on a variety of outcomes, including provements in several patient-centered outcomes over 1 year pain, function, quality of life, and psychological symptoms.4-8,15 and reductions in health services utilization up to 18 months. However, few have examined the effect of MBSR on health care utilization—a question of interest to health care systems that Introduction might support an MBSR program if it demonstrated reductions Chronic diseases are the leading causes of death and dis- in the unnecessary use of health care services.16,17 In addition, ability in the US. It is estimated that one of two adults in the US patient-centered outcomes such as self-efficacy and work pro- experiences at least one chronic illness and seven of ten deaths ductivity have not been studied extensively. If MBSR improves are attributable to chronic disease.1 As many as one in three function, pain, and psychological symptoms, then it might also

Tracy McCubbin, MD, is the Medical Director for the Centers for Complementary Medicine at Kaiser Permanente in Denver, CO. E-mail: [email protected]. Sona Dimidjian, PhD, is an Associate Professor in Psychology and Neuroscience at the University of Colorado Boulder. E-mail: [email protected]. Karin Kempe, MD, MPH, is the Medical Director of Clinical Prevention Services for Kaiser Permanente in Denver, CO. E-mail: [email protected]. Melissa S Glassey is the Business Services Manager for the Centers for Complementary Medicine for Kaiser Permanente Colorado in Aurora. E-mail: [email protected]. Colleen Ross, MS, is a Research Analyst at the Kaiser Permanente Institute for Health Research in Denver, CO. E-mail: [email protected]. Arne Beck, PhD, is the Director for Quality Improvement and Strategic Research at the Kaiser Permanente Institute for Health Research in Denver, CO. E-mail: [email protected].

4 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Mindfulness-Based Stress Reduction in an Integrated Care Delivery System: One-Year Impacts on Patient-Centered Outcomes and Health Care Utilization

be expected to increase participants’ self-efficacy—that is, their a chronic illness, or a stress-related problem. Individuals were confidence in being able to manage their chronic pain and/ excluded from participation if they had a poorly controlled or illness.18-20 Similarly, improvements in general function and psychiatric illness, severe antisocial behavior, or dementia; symptoms might also lead to improvements in work function, lacked English language skills; or were participating in a concur- including less absence from work and increased productivity rent study. Additional inclusion criteria were applied during a while at work. Such findings would be of considerable interest to 30-minute intake interview in which a clinical psychologist, who employers when evaluating the benefit of MBSR for their work- served as one of the MBSR instructors, took a brief medical and force members. Moreover, most outcomes of MBSR are measured psychiatric history, determined final eligibility for participation, immediately following the eight-week class and at six months, and obtained informed consent from participants. The additional though some studies have examined longer-term outcomes inclusion criteria assessed at the intake interview were the fol- for selected patient populations.21,22 Additional research on the lowing: has appropriate goals and expectations for the MBSR persistence of the aforementioned outcomes would be of value. class, including understanding the difference between attempts We report here the results of an MBSR program provided to alleviate pain and attempts to alleviate suffering; agrees to through group classes in a large integrated care delivery system, participate fully in the program and make a commitment to beginning in 2005. The aims of this study were to assess the the home practice of meditation and movement/exercise; un- impact of MBSR on a broad range of patient-centered outcomes, derstands his or her diagnosis and believes s/he has received including health and functional status, pain, work productivity appropriate medical evaluation and treatment and/or mental impairment, self-efficacy, symptoms of depression, anxiety, health services for medical conditions or psychiatric diagnoses; somatization, and overall psychological distress, and to assess and understands MBSR as a complement to medical care. changes in health care utilization. After the intake interview, participants completed baseline We hypothesized that MBSR would questionnaires on health and functional status, psychological 1. increase participants’ mental and physical functional status, symptoms, self-efficacy, and work productivity. work productivity, and self-efficacy 2. reduce symptoms of depression, anxiety, somatization, and Intervention psychological distress The eight-week MBSR program was offered through KPCO’s 3. decrease primary care, specialty care, mental health, Emer- Center for Complementary Medicine, which provided comple- gency Department visits, and hospital admissions. mentary medicine services at three outpatient clinics in the Denver and Boulder metropolitan areas. Classes were led by one Methods of two instructors (a clinical psychologist and a family physician) Design and Procedures trained to provide the Kabat-Zinn program of MBSR.23 This study was a prospective, single cohort design with Mindfulness-based stress reduction is an 8-week group patient-centered outcomes assessed at the beginning and end of intervention combining meditation techniques with psycho- the eight-week MBSR program and at one year after the baseline education to improve an individual’s capacity to manage stress, assessment. Changes in health care utilization were compared for reduce the impact of physical and psychological symptoms, and the six-month period before the first MBSR class and the six-month maximize the ability to thrive through all of life’s circumstances. period after the one-year anniversary of completion of the last The intervention consisted of eight 2- to 2.5-hour classes con- class. The study protocol was approved by the Kaiser Permanente ducted once a week and a 6-hour guided retreat held before Colorado (KPCO) institutional review board on August 25, 2005. the last class. Participants were also asked to complete 30 to 45 minutes of home practice and awareness exercises each Study Participants day. Core practices include a guided body scan, mindfulness Participants were all members of KPCO, a large, not-for-profit, movement (yoga), and sitting and walking meditation. The integrated health care system that provides comprehensive, pre- core skills taught included: paid medical coverage to over 600,000 members in Colorado’s • understanding of attitudes, perceptions, and unskillful thought Denver, Boulder, and Colorado Springs metropolitan areas. Data patterns for the present study were obtained from 38 participants for • understanding and modulating one’s reaction to stressors whom 18 months of health services data were available. These • recognizing pleasant and unpleasant emotions, thoughts, and participants were enrolled in 7 separate MBSR class cycles con- sensations ducted from September 2005 through June 2009. • using mindfulness in daily activities including interpersonal Study participants initially were referred by primary care communication physicians from two of KPCO’s outpatient clinics following an • focusing attention on internal states and sensations (such as informational meeting to describe the program and distribute awareness of the breath) and maintaining an open, nonjudg- program flyers. Flyers for patients describing the study were also mental, self-monitoring attitude. posted in outpatient clinics where KPCO offered other comple- mentary and alternative medicine services (eg, massage therapy, Outcome Measures acupuncture, chiropractic therapy) to encourage self-referral. Participants completed questionnaires on health and func- Participation in the MBSR program was open to Health Plan tional status, psychological symptoms, self-efficacy, and work members who were aged 18 years or older, with chronic pain, productivity at baseline before the MBSR class, at the final session

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 5 ORIGINAL RESEARCH & CONTRIBUTIONS Mindfulness-Based Stress Reduction in an Integrated Care Delivery System: One-Year Impacts on Patient-Centered Outcomes and Health Care Utilization

of the MBSR class, and one year after the last MBSR session, when Table 1. Baseline characteristics of 38 mindfulness-based stress they were contacted by phone to complete the questionnaires. reduction class participants Data on visits to primary care, specialty care (eg, orthopedics, Demographic characteristic n (%) neurology, cardiology), the Emergency Department, and hospital Women 30 (79) admissions were collected from KPCO’s electronic administrative Men 8 (21) and claims data for the period of six months before the class White racea 28 (74) (baseline) and six months following the one-year anniversary of the last MBSR class (follow-up). Hispanic 26 (68) Patient self-report measures included the following: Age, mean (SD), years 52.6 (10.2) • Medical Outcomes Study Short-Form 36 Health Survey.24,25 Employed part-time 35 (92) Developed by Ware and colleagues,26 the Medical Outcomes Prevalent symptoms/diagnoses Study Short-Form 36 Health Survey is a validated self-report Joint and/or back pain 28 (74) instrument that measures overall health (“How would you rate Psychological disorders 20 (53) your health?” with responses on a Likert-type scale ranging Chronic upper respiratory disorders 15 (39) from “poor” to “excellent”) and 8 specific domains of func- Female genitourinary symptoms 11/30 (37) tion. The 8 scales can be combined into 2 summary scales,27 Number of unique diagnoses, mean (SD) 16.4 (10.2) which measure physical function (physical component sum- a Race and ethnicity data were obtained from health care visit data rather than self- mary [PCS]) and mental function (mental component summary report. Smaller denominators for these are the result of missing data. [MCS]). We report here on results for the rating of overall SD = standard deviation. health, PCS, MCS, and the pain subscale. A higher score on all of these measures indicates better health and function. analyses using SAS Proc Mixed, allowing for differing numbers • Health and Work Performance Questionnaire. The Health and of measurements and times of measurements, were employed Work Performance Questionnaire, validated by Kessler and to examine change over time in self-reported patient outcomes colleagues,28 provides a global assessment of work absence from baseline through eight weeks and one year following the and productivity impairment caused by health conditions. It is MBSR program. used to calculate, over the previous 2 weeks, the percentage of hours worked (number of hours one actually worked divided Results by the number of hours one was expected to work), as well Initially, 45 participants were eligible for and attended the first as a rating of one’s usual job performance on a 10-point scale, MBSR class. However, 7 individuals ended their KPCO Health with higher values representing higher levels of productivity. Plan membership before the 1-year follow-up period and thus • Brief symptom inventory (BSI-18). The BSI-18 assesses self- were ineligible for study participation. Results are reported for reported symptoms of depression, anxiety, and somatization the remaining 38 participants for whom 1-year health services and provides a global severity index of overall psychological utilization and self-report data were available. Table 1 provides distress.29 Lower scores on the BSI-18 indicate lower symptoms. descriptive statistics of these study participants. • Self-efficacy. Self-efficacy questions have been developed Follow-up questionnaire data were obtained from 26 (68%) and widely used by Lorig and Holman30 and others for as- participants at 8 weeks and 24 (63%) at 1 year. To determine sessing patients’ confidence in managing a variety of health whether participants who did not complete follow-up question- conditions, including arthritis and other chronic diseases.31 naires differed from those who did complete them, we analyzed Self-efficacy questions were used to assess MBSR participants’ differences between these 2 groups in demographic characteris- ratings of their confidence (0 = “not at all confident,” 10 = tics, baseline questionnaire scores, and health services utilization. “extremely confident”) in undertaking several activities: No significant differences for any of these variables were found. - “Do all the things necessary to manage conditions on a Repeated measures analyses of scores from the Medical regular basis” Outcomes Study Short-Form 36 Health Survey, BSI-18, and Self- - “Do things other than just take medication to reduce how Efficacy measures (Table 2) showed significant changes from much your illness affects your everyday life” baseline to 8 weeks and 1 year. Improvements in mean MCS - “Control any other symptoms or health problems you have and bodily pain scores were seen at 8 weeks, averaging 7.5 so that they don’t interfere with the things you want to do.” (p < 0.01) and 4.5 (p < 0.05), respectively; and the magnitude of improvement was greater at 1 year, averaging 11.8 and 5.7, Data Analyses respectively (p < 0.01 for both scores). The PCS and general All analyses were conducted using SAS, version 9.1.3 (SAS health scores also increased at 8 weeks by an average of 3.1 and Institute, Cary, NC). Analyses comparing one-year question- 4.4, respectively (p < 0.05 for both), but remained unchanged naire completers with noncompleters were performed using from 8 weeks to 1 year. Wilcoxon and χ2 tests for continuous and categorical variables, The BSI-18 scores for anxiety, depression, and somatization and respectively. The signed-rank test was used to assess change the global severity index all declined significantly from baseline to in utilization of health care services (ambulatory, primary, and 8 weeks, with reductions ranging from 42% to 54% (p < 0.01 for all specialty care visits, Emergency Department visits, and hospital scores). These scores continued to decline at 1 year, with reduc- admissions) from baseline to follow-up. Repeated measures tions from baseline ranging from 54% to 65% ,with the exception

6 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Mindfulness-Based Stress Reduction in an Integrated Care Delivery System: One-Year Impacts on Patient-Centered Outcomes and Health Care Utilization

of somatization, which remained unchanged from 8 weeks to 1 studies reporting improvements in both psychological and physi- year (p < 0.01 for all scores at 1 year compared with baseline). cal outcomes following MBSR.3-7 The 3 self-efficacy items showed increases in average scores Moreover, at the one-year follow-up, ratings for MCS and from baseline to 8 weeks ranging from 0.5 to 1.4. Two of the symptoms of anxiety and depression continued to improve, 3 increases were significant: “confidence in managing conditions” whereas the eight-week reductions in ratings for PCS, general (p < 0.05) and in “controlling symptoms so they don’t interfere health, pain, and somatization were sustained, suggesting with activities” (p < 0.01). However, all 3 self-efficacy scores that the magnitude of longer-term benefits of MBSR are … the magnitude decreased between 0.4 and 1.8 points from baseline to 1 year, greater for mental symptoms compared with physical and these decreases were significant for 2 items: “confidence symptoms and function. Other research on longer-term of longer-term in managing conditions” and in “doing things other than taking outcomes of MBSR also has shown positive results.32 benefits of MBSR medication to reduce effects of illness in everyday life” (p < 0.05 Our findings regarding self-efficacy were more equivo- are greater for both items). cal. Although significant increases were seen at eight for mental Although the Health and Work Performance Questionnaire weeks for two of the three items (“confidence in man- symptoms variables of percentage of expected hours worked and produc- aging conditions” and in “controlling symptoms so they compared tivity ratings increased from the baseline to 8 weeks by 9% and don’t interfere with activities”), there also were decreases with physical 6%, respectively, these increases were not significant. At 1 year, in all three items at one year compared with baseline, two symptoms and the percentage of expected hours worked decreased slightly but of which were significant (“confidence in managing con- function. remained above baseline by 4%, whereas productivity ratings ditions” and in “doing things other than taking medication decreased by 6% from baseline. Neither result was significant. to reduce effects of illness in everyday life”). Although Health services utilization (Table 3) decreased significantly these findings suggest that increases in self-efficacy resulting from from baseline to follow-up in visits to primary care (p < 0.0001), MBSR may be more short-lived than other outcomes, this result specialty care (p = 0.0004), and the Emergency Department may also reflect the small sample size. Still, they suggest that (p = 0.04), and in hospital admissions (p = 0.02). MBSR participants could benefit from additional interventions after eight weeks that support their ongoing confidence in their Discussion ability to manage their conditions more effectively. Completion of the MBSR program at KPCO was associated The percentage of expected work hours completed and with statistically significant and clinically meaningful improve- self-ratings of usual job performance showed small, nonsig- ments at eight weeks in health and functional status, pain, nificant increases following the MBSR classes, although these symptoms of depression, anxiety, somatization, and overall measures decreased at one year. Neither of the changes at one psychological distress. These results are consistent with other year was significant.

Table 2. Descriptive statistics and univariate tests of patient questionnaire scores at baseline, eight weeks, and one year Baseline, mean 8 weeks, mean 1 year, mean Outcome measured (SD) (n = 38) (SD) (n = 26) p value (SD) (n = 24) p value SF-36 Health Survey Mental composite score 41.9 (12.7) 49.4 (9.0) 0.0003 53.7 (5.0) < 0.0001 Physical composite score 46.9 (9.8) 50.0 (7.5) 0.0503 49.4 (8.6) 0.1461 Bodily pain 45 (10.3) 49.5 (9.2) 0.0363 50.7 (8.3) 0.0036 General health 46.9 (10.2) 51.3 (6.1) 0.0170 51.3 (8.1) 0.0289 Brief symptom inventory Anxiety 4.8 (4.1) 2.8 (2.4) 0.0009 1.7 (1.9) < 0.0001 Depression 4.3 (4.7) 2.2 (2.8) 0.0049 1.6 (2.0) 0.0013 Somatization 2.8 (2.7) 1.3 (1.5) 0.0151 1.3 (2.5) < 0.0001 Global severity index 11.9 (9.4) 6.3 (5.8) 0.0005 4.6 (4.8) < 0.0001 Self-efficacy On a scale of 1 to 10, how confident are you that you can: Do all the things necessary to manage conditions on a 7.4 (2.3) 8.6 (1.9) 0.0411 5.8 (3.6) 0.0222 regular basis? Do things other than just take medication to reduce how 7.8 (2.4) 8.3 (2.4) 0.3248 6.0 (3.7) 0.0878 much your illness affects your everyday life? Control any other symptoms or health problems you have 7.1 (2.0) 8.5 (1.2) 0.0001 6.7 (2.8) 0.8549 so that they don’t interfere with the things you want to do? Work Productivity Performance Percentage of expected work hours completed 84.5 (26.8) 92.3 (15.5) 0.1067 88.0 (12.3) 0.8486 Self-rating of usual job performance, 0-10 7.2 (2.6) 7.6 (2.9) 0.5923 7.1 (3.3) 0.9295 SD = standard deviation.

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ascertain longer trajectories of improvement or relapse beyond Table 3. Comparison of health services utilization before and after mindfulness-based stress reduction (MBSR) those most often measured at eight weeks following completion programa of the MBSR class. Finally, we believe that having electronic medical data on clinic visits, hospitalizations, and diagnosis Mean (SD) codes available for analysis is a significant strength, facilitated b Ambulatory visits Baseline Follow-up p value by the KPCO model of care. Primary care 1.8 (1.5) 0.9 (1.1) < 0.0001 This study had several limitations. Our sample size for analysis Specialty care 7.8 (12.1) 4.8 (6.1) 0.0004 was small in comparison with other published studies, limiting Emergency Department 0.2 (0.6) 0.1 (0.4) 0.04 statistical power and possibly generalizability. Despite the small Hospital admissions 0.1 (0.4) 0.02 (0.2) 0.02 number of participants, our analyses yielded interesting and a Comparison of use of services for 38 participants with at least 18 months of encouraging results across a broad set of patient-centered mea- continuous Health Plan membership. Baseline measurements encompass the sures, as well as objective measures of health services utilization. 6 months before the first MBSR class and the 1-year statistics represent the 6 months after 1 year of follow-up. However, our results may not be generalizable to other health b p values using signed-rank tests. care settings. Finally, this was a single cohort study with no com- SD = standard deviation. parison group. Study participants were already engaged in care by virtue of the enrollment strategy and could have experienced Health services utilization decreases from baseline to follow- decreases in their physical and mental distress and improvements up were substantial across outpatient primary and specialty care in their symptoms independent of the mindfulness practices, visits, Emergency Department visits, and hospital admissions. perhaps related to psychosocial support from the group or their These findings also point to potential reductions in costs asso- usual care. However, given that these individuals were referred ciated with MBSR through reductions in health care utilization, or self-referred to the program because of their chronic pain, even in a cohort where the mean age was older than age 50 chronic illness, or long-term stress-related disorders, and that years. We postulate that because patients are more confident in they each had an average of more than 16 unique diagnoses, it is managing their conditions, they are less likely to visit their physi- unlikely that their symptoms spontaneously improved. Moreover, cian. Anxiety and somatization symptoms drive people to seek a recent meta-analysis of the most rigorously designed, random- care, and by decreasing this aspect of an illness, utilization is also ized controlled trials of MBSR demonstrated positive effects on decreased. Although a formal cost analysis of the MBSR program depression, anxiety, and psychological distress in people with linked to reductions in health care costs and improvements in chronic disease, albeit smaller in magnitude than those reported patient-centered outcomes is beyond the scope of this paper, in this study.4 these results should be of interest to health care administrators considering a health plan benefit for MBSR. Conclusion Unlike Rosenzweig et al,4 we did not investigate differential Our results support the provision of MBSR as a standard effects of MBSR on the basis of specific pain conditions owing intervention for patients with chronic pain, chronic illness, and to limited sample sizes for specific diagnostic categories and, stress-related disorders in clinical settings such as KPCO and sug- equally important, because the high prevalence of medical and gest that participation in the MBSR program is associated with psychiatric comorbidities limited our ability to differentiate the substantial clinical benefit for such patients, as well as significant participants into unique diagnostic categories. Likewise, we did reductions in health services utilization. Over time, the program not control for age. at KPCO has grown in enrollment and popularity and is a valued This study contributes in several ways to the literature on the resource for patients and health care professionals. v effectiveness of MBSR. First, we assessed the impact of MBSR on health services utilization, showing large and sustained decreases Disclosure Statement in this outcome over one year. Second, we studied MBSR in a The author(s) have no conflicts of interest to disclose. multimorbid, heterogeneous patient population as seen in a community care delivery setting such as KPCO, increasing the Acknowledgments generalizability of our results to real-world health care systems. Funding was obtained through the Kaiser Permanente Colorado Innovations Grant program. Third, a broad set of patient-centered measures was used, includ- Mary Corrado, ELS, provided editorial assistance. ing self-efficacy and work productivity in addition to the more typically evaluated outcomes of health and functional status and References psychiatric symptoms. The finding of attenuations in participants’ 1. Chronic disease prevention and health promotion [Internet]. Atlanta, GA: self-efficacy for managing their conditions provides useful infor- Centers for Disease Control and Prevention; 2014 May 21 [cited 2013 Dec mation about the possible need for additional self-management 19]. Available from: www.cdc.gov/chronicdisease/index.htm. 2. Health, United States, 2006 with chartbook on trends in the health of support after completion of the class. In addition, we suggest Americans. Hyattsville, MD: US Department of Health and Human Services, that assessment of work productivity as a domain of function National Centers for Disease Control and Prevention; National Center for is important to both MBSR participants and employers, despite Health Statistics; 2006 Nov. 3. Kabat-Zinn J. An outpatient program in behavioral medicine for chronic our nonsignificant results pertaining to this outcome. Changes pain patients based on the practice of mindfulness meditation: theoretical in health care utilization and patient-centered outcomes were considerations and preliminary results. Gen Hosp Psychiatry 1982 Apr;4(1):33- obtained during a one-year follow-up period, allowing us to 47. DOI: http://dx.doi.org/10.1016/0163-8343(82)90026-3.

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4. Rosenzweig S, Greeson JM, Reibel DK, Green JS, Jasser SA, Beasley D. 18. Jerant A, Moore M, Lorig K, Franks P. Perceived control moderated the Mindfulness-based stress reduction for chronic pain conditions: self-efficacy-enhancing effects of a chronic illness self-management variation in treatment outcomes and role of home meditation practice. intervention. Chronic Illn 2008 Sep;4(3):173-82. DOI: http://dx.doi. J Psychosom Res 2010 Jan;68(1):29-36. DOI: http://dx.doi.org/10.1016/j. org/10.1177/1742395308089057. jpsychores.2009.03.010. 19. Marks R, Allegrante JP, Lorig K. A review and synthesis of research evidence 5. Bohlmeijer E, Prenger R, Taal E, Cuijpers P. The effects of mindfulness-based for self-efficacy-enhancing interventions for reducing chronic disability: stress reduction therapy on mental health of adults with a chronic medical implications for health education practice (part II). Health Promot Pract 2005 disease: a meta-analysis. J Psychosom Res 2010 Jun;68(6):539-44. DOI: http:// Apr;6(2):148-56. DOI: http://dx.doi.org/10.1177/1524839904266792. dx.doi.org/10.1016/j.jpsychores.2009.10.005. 20. Marks R, Allegrante JP, Lorig K. A review and synthesis of research evidence 6. Hofmann SG, Sawyer AT, Witt AA, Oh D. The effect of mindfulness-based for self-efficacy-enhancing interventions for reducing chronic disability: therapy on anxiety and depression: a meta-analytic review. J Consult Clin implications for health education practice (part I). Health Promot Pract 2005 Psychol 2010 Apr;78(2):169-83. DOI: http://dx.doi.org/10.1037/a0018555. Jan;6(1):37-43. DOI: http://dx.doi.org/10.1177/1524839904266790. 7. Grossman P, Niemann L, Schmidt S, Walach H. Mindfulness-based stress 21. Kabat-Zinn J, Lipworth L, Burney R, Sellers W. Four-year follow-up of a reduction and health benefits. A meta-analysis. J Psychosom Res 2004 meditation-based program for the self-regulation of chronic pain: treatment Jul;57(1):35-43. 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Andersen SR, Würtzen H, Steding-Jessen M, et al. Effect of mindfulness- 28. Kessler RC, Barber C, Beck A, et al. The World Health Organization based stress reduction on sleep quality: results of a randomized trial among Health and Work Performance Questionnaire (HPQ). J Occup Environ Danish breast cancer patients. Acta Oncol 2013 Feb;52(2):336-44. DOI: Med 2003 Feb;45(2):156-74. DOI: http://dx.doi.org/10.1097/01. http://dx.doi.org/10.3109/0284186X.2012.745948. jom.0000052967.43131.51. 14. Kabat-Zinn J, Lipworth L, Burney R. The clinical use of mindfulness meditation 29. Zabora J, BrintzenhofeSzoc K, Jacobsen P, et al. A new psychosocial screening for the self-regulation of chronic pain. J Behav Med 1985 Jun;8(2):163-90. instrument for use with cancer patients. Psychosomatics 2001 May- DOI: http://dx.doi.org/10.1007/BF00845519. Jun;42(3):241-6. DOI: http://dx.doi.org/10.1176/appi.psy.42.3.241. 15. Baer RA. Mindfulness training as a clinical intervention: a conceptual and 30. 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Contentment

For some patients, though conscious that their condition is perilous, recover their health simply through their contentment with the goodness of the physician.

­— Precepts, Hippocrates, c460 – c370BC, ancient Greek physician

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ORIGINAL RESEARCH & CONTRIBUTIONS Improving Appropriate Use of Pulmonary Computed Tomography Angiography by Increasing the Serum D-Dimer Threshold and Assessing Clinical Probability

Sydney Char; Hyo-Chun Yoon, MD, PhD Perm J 2014 Fall;18(4):10-15 http://dx.doi.org/10.7812/TPP/14-007

measure patient serum D-dimers. The Abstract manufacturer’s threshold for a positive Objective: To determine whether the implementation of an increased D-dimer thresh- serum D-dimer value is 0.4 µg/mL. In old value and clinical probability assessment increases the prevalence of pulmonary August 2012, our health maintenance embolism (PE) in patients undergoing pulmonary computed tomography angiography organization’s (HMO) Medical Group (PCTA) in an Emergency Department setting. attempted to decrease use of PCTA by Methods: A retrospective review of all patients undergoing PCTA during 2 separate engaging with the ED to increase the D- 12-month intervals, 1 before the implementation of an increased D-dimer threshold dimer threshold value for a positive result and recommendation for formal clinical probability assessment and the other after within our institution from 0.4 µg/mL to regional implementation. The primary outcome measure was the prevalence of acute 1.0 µg/mL. The increase in the D-dimer PE in each of the samples. threshold value was designed to increase Results: After the implementation of the increased D-dimer threshold and recom- specificity without reducing sensitivity mendation for formal clinical probability assessment, the prevalence of PE detected to detect PE by PCTA on the basis of by PCTA increased from 4.7% to 11.7% (p < 0.001). Among all PCTAs performed results from both a review of patients after the new guidelines were promulgated, 8.6% were still performed on patients in our own electronic medical record who had serum D-dimer values lower than the threshold of 1.0 µg/mL. Despite the (EMR)10,11 and from the published litera- recommendation for formal clinical probability assessment before ordering a PCTA, ture.12,13 ED physicians were requested only 4% of patients had a formal clinical probability assessment recorded in their to use a clinical algorithm (preferably, electronic medical record. but not limited to, the Wells criteria) Conclusion: The implementation of an increased D-dimer threshold value increased the to determine pretest probability for PE. prevalence of PE in patients undergoing PCTA in an Emergency Department setting, but The Wells criteria includes 7 symptoms more consistent application of clinical probability assessment remains an elusive target. or characteristics of medical history and physical examination. A patient receives Introduction intermediate or high clinical risk of PE a score depending on which criteria they Three multicenter Prospective Investi- and an increased serum D-dimer could possess, as determined by Wells et al.7 gations of Pulmonary Embolism Detection reduce the use of PCTA without signifi- The score indicates the likeliness of a (PIOPED) studies have evaluated radio- cantly increasing the risk of missed PE.7-9 PE diagnosis. Using the Wells criteria or nuclide ventilation perfusion, computed other validated clinical algorithms was a tomography, and magnetic resonance im- Objective recommendation rather than a require- aging to detect pulmonary embolism (PE; In this study, we sought to determine ment for ordering a PCTA. PIOPED I, II, and III, respectively).1-3 The whether the implementation of an in- We obtained institutional review overall prevalence of PE exceeded 20% creased D-dimer threshold value and board approval with a waiver of consent for each study: 33% for PIOPED I, 23% for formal clinical probability assessment to retrospectively review a common PIOPED II, and 28% for PIOPED III. Yet increases the prevalence of PE in pa- EMR to determine the age, sex, D-dimer in several single-center studies evaluat- tients undergoing PCTA in an Emergency result, if any, and PCTA result of all pa- ing the efficacy of pulmonary computed Department (ED) setting. tients seen in the ED of the HMO with tomography angiography (PCTA), the a possible diagnosis of acute PE who prevalence is less than 10%, suggesting Materials and Methods underwent PCTA. that PCTA is overutilized.4-6 Our institutional laboratory uses One of the authors reviewed and as- Recent studies have suggested that the STA D-DI latex agglutination assay signed Wells scores for the patients on the limiting use of PCTA to patients with an (Diagnostica Stago, Parsippany, NY) to basis of the EMR information associated

Sydney Char was a Summer Research Assistant in Diagnostic Imaging. She is studying Biomedical Engineering at Tufts University in Medford, MA. E-mail: [email protected]. Hyo-Chun Yoon, MD, PhD, is Assistant Chief of Diagnostic Imaging at the Moanalua Medical Center in Honolulu, HI. E-mail: [email protected].

10 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Improving Appropriate Use of Pulmonary Computed Tomography Angiography by Increasing the Serum D-Dimer Threshold and Assessing Clinical Probability

with the ED encounter leading to the PCTA, likely diagnosis. For a chief complaint (standard deviation [SD]) age among all unless the ED physician had already as- of unilateral leg pain or swelling, PE patients was 59.2 (18.0) years (range, signed a Wells score or used another clini- was assumed the most likely diagnosis 16-96 years). For men, the average cal assessment algorithm for the patient. unless there was a specific finding in (SD) age was 59.2 (17.4) years (range, The reviewer was masked to the D-dimer the reported history to suggest a more 19-90 years). For women, the average value as well as the PCTA result for ev- likely alternative diagnosis. (SD) age was 59.2 (18.0) years (range, ery patient. However, because the EMR The Wells criteria scores segregated 16-96 years). including the ED physician note was patients into 3 clinical risk strata for PE: The overall prevalence of PE as reviewed to determine each patient’s low (score < 2); intermediate (score 2-6); determined by PCTA in the 2008-2009 clinical probability, the emergency phy- and high (score > 6).7 The subjects were cohort was 4.7% (24/510). Three hun- sician’s clinical probability assessment also segregated on the basis of their dred forty-seven patients (68.0%) had a was known if it was recorded in the serum D-dimer levels into those with D-dimer drawn at the time of their PCTA. physician’s note. The Wells criteria have negative (<1.0 μg/mL) or positive (>1.0 Of these, 18 proved to have PE by PCTA been validated as a method to stratify μg/mL) serum D-dimer using the latex (5.2%). Of the 161 patients who had a a patient’s clinical probability of PE.7 agglutination technique. serum D-dimer level of at least 1.0 µg/ Points were assigned for each of the Two data sets each covering 12 mL, there were 15 cases of PE demon- following clinical signs or symptoms: months were collected, 1 before and strated by PCTA, a prevalence of 9.3%. PE as likely or more likely than any 1 after implementation of the higher Conversely, there were 186 subjects who alternative diagnosis, 3.0 points; signs D-dimer threshold and recommenda- had a D-dimer level less than 1.0 µg/mL, or symptoms of deep venous thrombo- tion of using a clinical decision rule. but only 1 (0.5%) proved to have PE. sis (leg swelling or painful palpation in The former spanned from June 1, 2008 Among these 186 subjects, there were the region of a deep vein), 3.0 points; through May 31, 2009, and the latter from 160 who had a D-dimer level of at least heart rate higher than 100 beats/min, 1.5 September 1, 2012 through August 31, 0.4 µg/mL, which included the patient points; immobilization (bed rest for 3 2013. The 2 data sets were compared who had a PE documented by PCTA. consecutive days) or surgery within past to see whether there was a significant This 58-year-old man had a D-dimer 4 weeks, 1.5 points; previous diagnosis change in the prevalence of PE and level of 0.95 µg/mL. Of 163 patients of PE or deep venous thrombosis, 1.5 patient characteristics. without a D-dimer level drawn at the points; hemoptysis, 1.0 points; active All statistical analysis was performed time of PCTA, there were 6 (3.7%) who malignancy (within past 6 months), 1.0 using STATA, version 7.0 (Stata, College proved to have PE. Excluding 3 patients points. Most of these clinical signs and Station, TX). in this group with known PE undergo- symptoms could be determined unam- ing follow-up PCTA for persistent or biguously from the EMR. Results progressive symptoms, only 3 (1.9%) of We used the following algorithm to The ED of this HMO, with about 160 proved to have PE by PCTA. determine whether PE was as likely or 227,000 members, sees approximately The clinical probability of PE was more likely than any alternative diag- 36,000 patients annually. The number estimated for each of the patients in nosis: If the patient’s chief complaint of members within this HMO has not the 2008-2009 cohort using the Wells on record was shortness of breath or appreciably changed from 2008 to 2013. criteria.7 Among 36 patients with high dyspnea, then we assumed PE was the From June 1, 2008, through May 31, clinical probability for PE, there were 5 most likely diagnosis unless 1) the pa- 2009, before implementation of the (13.9%) who had PE diagnosed by PCTA. tient had a history of congestive heart higher D-dimer threshold, the ED saw Only 18 (5.5%) of the 328 moderate-risk failure and chest x-ray was suggestive 510 consecutive patients who under- patients had PE by PCTA. Finally, there of edema, 2) the patient had signs and went PCTA for possible PE. This will was only 1 (0.7%) among 146 patients symptoms of a respiratory infection be referred to as the 2008-2009 cohort with low risk who had PE by PCTA. and an abnormal chest x-ray, or 3) the in the rest of this article. There were Table 1 shows the prevalence of patient had a history of asthma/chronic 198 men and 312 women. The average positive PE by PCTA segregated by serum obstructive pulmonary disease and clinical symptoms of an asthma/chronic obstructive pulmonary disease exacer- Table 1. Prevalence of positive pulmonary computed tomography angiography bation. If the patient’s chief complaint segregated by Wells criteria score for clinical probability of pulmonary embolism was chest pain, then we assumed PE and serum D-dimer level for patients in the 2008-2009 cohort was the most likely diagnosis unless the a patient had a history of coronary artery Wells/D-dimer < 1 (%) > 1 (%) ND (%) Total (%) disease, prior myocardial infarction, or < 2 (low) 0/52 (0) 1/41 (2.4) 0/53 (0) 1/146 (0.7) cardiomyopathy. However, if the chest 2-6 (intermediate) 0/130 (0) 12/108 (11.1) 6/90 (6.7) 18/328 (5.5) pain was further described as substernal, > 6 (high) 1/4 (25.0) 4/12 (33.3) 0/20 (0) 5/36 (13.9) crushing, or radiating to the back or left Total 1/186 (0.5) 17/161 (10.6) 6/163 (3.7) 24/510 (4.7) arm, PE was not assumed to be the most a ND = serum D-dimer not drawn.

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 11 ORIGINAL RESEARCH & CONTRIBUTIONS Improving Appropriate Use of Pulmonary Computed Tomography Angiography by Increasing the Serum D-Dimer Threshold and Assessing Clinical Probability

probability assessment for the 2012-2013 Table 2. Prevalence of positive pulmonary computed tomography angiography segregated by Wells criteria score for clinical probability of pulmonary embolism cohort. Again, the prevalence of PE de- and serum D-dimer levels for patients in the 2012-2013 cohort tected by PCTA is very low in all patients with a serum D-dimer level less than 1.0 Wells/D-dimer < 1 (%) > 1 (%) ND (%)a Total (%) µg/mL, irrespective of the patients’ clini- < 2 (Low) 0/25 (0) 5/108 (4.6) 1/ 75 (1.3) 6/208 (2.9) cal probability assessment. All patients 2-6 (Intermediate) 0/22 (0) 21/151 (13.9) 17/113 (15.0) 38/286 (13.3) in the second cohort with intermediate > 6 (High) 0/0 (0) 12/28 (42.9) 8/25 (32.0) 20/53 (37.7) or high clinical probability of PE had a Total 0/47 (0) 38/287 (13.2) 26/213 (12.2) 64/547 (11.7) prevalence of PE exceeding 10% of their a ND = serum D-dimer not drawn. PCTA studies, irrespective of whether they had a serum D-dimer of at least 1.0 µg/mL or did not have one drawn. D-dimer and retrospective clinical prob- was 11.7% (64/547). There were 334 pa- There was a statistically significant ability using the Wells criteria for the tients (61.1%) who had a D-dimer drawn difference between cohorts in their age 2008-2009 cohort. As expected, the prev- at the time of their PCTA. Of these, 38 and sex distributions. The 2012-2013 alence of PE detected by PCTA is very (11.4%) proved to have PE by PCTA. Of cohort was older than the 2008-2009 low in all patients with a serum D-dimer the 287 patients with a serum D-dimer cohort (2012-2013 age: 63.4 [18.0]; 95% level less than 1.0 µg/mL, irrespective level of at least 1.0 µg/mL, there were CI, 61.8-64.9 years; vs 2008-2009 age: of the patients’ clinical probability as- 38 cases (13.2%) of PE demonstrated 59.2 [18.0]; 95% CI, 57.6-60.7 years; sessment. In the 2008-2009 cohort, only by PCTA. There were 47 patients who t = -3.776, p < 0.001). Also, men con- when patients had a serum D-dimer of had a D-dimer level less than 1.0 µg/ stituted only 38.8% of the 510 patients at least 1.0 µg/mL and an intermediate mL. None of these patients proved to in the 2008-2009 cohort, but they repre- or high clinical probability of PE did the have PE. Among these 47 patients, 28 sented 45.7% of the 547 patients in the prevalence of PE exceed 10% in PCTA had a D-dimer greater than 0.4 µg/mL. 2012-2013 cohort (χ² = 5.116, p = 0.024). studies. Interestingly, none of the 20 pa- Of 213 patients without a D-dimer level There was a significantly higher preva- tients with a high clinical probability of drawn at the time of PCTA, 26 (12.2%) lence of PE detected by PCTA in the PE determined retrospectively from their proved to have PE. Excluding 3 patients 2012-2013 cohort (11.7%) than for the EMR but who did not have a D-dimer in this group with known PE undergoing 2008-2009 cohort (4.7%) (χ² = 16.917, level recorded at the time of the PCTA follow-up PCTA for persistent or progres- p < 0.001). had detectable PE. sive symptoms, 23 (11.0%) of 210 proved Despite the recommendation that From September 1, 2012, through to have PE by PCTA. all patients undergoing PCTA have a August 31, 2013, the ED saw 547 con- The clinical probability of PE was es- D-dimer drawn without compromising secutive patients who underwent PCTA timated for each of these patients in the patient care, there was a significantly for suspected PE. This will be referred 2012-2013 cohort using the Wells criteria. higher proportion of patients who un- to as the 2012-2013 cohort in the rest of Among 53 patients with high clinical derwent PCTA without having a D-dimer this article. There were 250 men and 297 probability for PE, 20 (37.7%) had PE level drawn in the 2012-2013 cohort women. The average (SD) age among diagnosed by PCTA. Only 38 (13.3%) of (38.9%) than in the 2008-2009 cohort all patients was 63.3 (18.0) years (range, the 286 moderate-risk patients had PE (32.0%) (χ² = 5.609, p = 0.018). 3-97 years). For men, the average (SD) by PCTA. Finally, among 208 patients Among patients who did have a se- age was 63.5 (17.7) years (range, 16-96 with low risk, there were 6 (2.9%) who rum D-dimer drawn before PCTA, there years). For women, the average (SD) age had PE by PCTA. was a much higher proportion of pa- was 63.3 (18.0) years (range, 3-97 years). Table 2 shows the prevalence of tients who had a serum D-dimer level less The overall prevalence of PE as deter- positive PE by PCTA segregated by se- than 1.0 µg/mL in the 2008-2009 cohort mined by PCTA in the 2012-2013 cohort rum D-dimer and retrospective clinical (53.6%) than in the 2012-2013 cohort

Table 3. The number of individuals for whom each of the Wells criteria were present for each cohort 2008-2009 cohort, 2012-2013 cohort, Wells criteria n = 510 (%) n = 547 (%) χ² p value Pulmonary embolism considered the most likely diagnosis 335 (65.7) 234 (42.8) 55.726 <0.001 Signs or symptoms of deep venous thrombosis 64 (12.5) 103 (18.8) 7.752 0.005 Tachycardia (heart rate > 100) 153 (30.0) 196 (35.8) 4.056 0.044 Recent prolonged immobility or major surgery 65 (12.7) 92 (16.8) 3.510 0.061 Prior history of pulmonary embolism or deep venous thrombosis 37 (7.3) 59 (10.8) 3.986 0.046 Hemoptysis 11 (2.2) 20 (3.7) 2.084 0.149 Active or recent cancer 92 (18.0) 128 (23.4) 4.603 0.032

12 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Improving Appropriate Use of Pulmonary Computed Tomography Angiography by Increasing the Serum D-Dimer Threshold and Assessing Clinical Probability

(14.1%) ( ² = 118.155, p < 0.001). In Criteria were mentioned. This is despite χ Table 4. Number of pulmonary addition, among patients with a D-dimer computed tomography angiographies the Medical Group’s recommendations level less than 1.0 µg/mL, there was a performed per 1000 Emergency that some type of pretest clinical prob- much higher proportion of patients who Department visits within each study ability assessment of PE be performed in had a serum D-dimer level between 0.4 period addition to ordering the serum D-dimer and 1.0 µg/mL in the 2008-2009 cohort before ordering a PCTA. Month 2008-2009 2012-2013 (86%) than in the 2012-2013 cohort When we compared the ED physi- September 11.74 13.28 (60%) (χ² = 16.840, p < 0.001). cians’ clinical probability of PE against Though there was no significant October 15.67 7.36 our study’s retrospectively determined difference between the 2 cohorts for November 13.94 10.08 clinical probability, there was concor- prevalence of PE detected by PCTA December 13.43 13.08 dance in the assessed level of risk for among patients with a D-dimer value January 18.49 10.41 20 of 22 patients. However, a 40-year- less than 1.0 µg/mL (2008-2009: 0.5% February 16.22 14.25 old woman with tachycardia and active vs 2012-2013: 0%, Fisher exact = March 16.92 11.86 cancer was noted as “low risk” for PE 1.000, p = 0.80) and at least 1.0 µg/mL April 21.62 13.97 whereas we recorded moderate risk (2008-2009: 10.6% vs 2012-2013: 13.2%, May 18.70 11.72 (Wells score, 2.5), and a 59-year-old χ² = 0.689, p = 0.407), there was a sig- June 14.71 13.65 woman presenting with syncope and a nificant difference among patients who July 15.18 17.45 remote history of PE was noted as “high did not have a D-dimer value drawn August 11.06 13.33 risk,” however we recorded moderate (2008-2009: 3.7% vs 2012-2013: 12.2%, Average 15.64 12.54 risk (Wells score, 4.5). χ² = 8.620, p = 0.003). Table 3 lists the presence of the Discussion individual Wells criteria in each of the For patients with either intermedi- In August 2012, the serum D-dimer patient cohorts on the basis of their ate or high clinical risk, there was a threshold level for positive possible review of the EMR. We recorded a 23% significant difference in the prevalence acute PE was increased in our institution higher prevalence of the first criterion of PE between cohorts (intermediate: from at least 0.4 µg/mL to at least 1.0 (PE as the most likely diagnosis) for 2008-2009: 5.5% vs 2012-2013: 13.3%, µg/mL, on the basis of both a literature patients in the 2008-2009 cohorts than χ² = 11.211, p = 0.001; high: 2008-2009: review and our own experience, which in the 2012-2013 cohorts. Since this 13.9% vs 2012-2013: 37.7%, χ² = 6.035, suggested that an increased threshold criterion is worth 3 points in the Wells p = 0.014). This difference may be ex- would increase specificity without re- algorithm and its presence gives the plained by the much higher proportion ducing sensitivity.9-13 patient at least an intermediate clinical of patients with intermediate clinical We demonstrated a significant decrease risk, the fact that 101 more patients in risk in the 2012-2013 cohort who had a in the number of PCTAs performed per the earlier cohort met this criterion likely serum D-dimer greater than 1.0 µg/mL 1000 ED visits as well as a significant explains the smaller proportion of low- than in the 2008-2009 cohort (52.8% vs increase in the prevalence of positive risk patients in the 2008-2009 cohort 32.9%, χ² = 24.734, p = 0.001). However, studies after the implementation of the (28.6%) compared with the 2012-2013 there is no statistically significant differ- recommendations (from 4.7% to 11.7%). cohort (38.0%) (χ² = 10.465, p = 0.001). ence in the proportion of patients with We suggest that this increase in prevalence When we compared the 2 cohorts serum D-dimer of at least 1.0 µg/mL in the of positive PCTA studies represents more for the prevalence of PE detected by patients at high clinical risk (χ² = 3.293, appropriate patient selection for PCTA PCTA among patients with low clinical p = 0.07). because the prevalence of PE has in- risk as retrospectively assessed using Table 4 lists the number of PCTAs creased in those patients who had a serum the Wells criteria, there was no sig- performed per 1000 ED visits by month D-dimer drawn as well as those who did nificant difference (2008-2009: 0.7% vs during each study period. There was a not. The same selection process results 2012-2013: 2.9%, Fisher exact = 0.247, statistically significant decrease in the in an overall decrease in the number of p = 0.14). However, the one patient monthly PCTAs performed per 1000 PCTAs ordered per 1000 ED visits. with acute PE in the 2008-2009 cohort ED visits during the later 2012-2013 On the basis of the results, patients and 5 of the 6 patients with acute PE in study period (rank sum test, Z = -2.483, with high clinical risk as assessed using the 2012-2013 cohort all had a serum p = 0.01). a clinical algorithm such as the Wells D-dimer level less than or equal to 1.0 Although many of the ED physicians criteria may not require a serum D-dimer µg/mL. One patient with acute PE had a mentioned the possibility of PE within a before proceeding to PCTA. Conversely, low clinical probability of PE as assessed list of other differential diagnoses, only patients with low clinical risk may not retrospectively and did not have a serum 22 (4.0%) of 547 physician notes spe- require a serum D-dimer to be drawn D-dimer. No patients with low clinical cifically mentioned a clinical probability to avoid a PCTA. This emphasizes the probability and serum D-dimer less than of PE. In only 4 of the 22 notes was a importance of documenting a high or low 1.0 µg/mL had acute PE detected by specific Wells score given. In one other clinical probability in the medical record PCTA in either cohort. note, the Pulmonary Embolism Rule-out using some type of decision rule. Patients

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 13 ORIGINAL RESEARCH & CONTRIBUTIONS Improving Appropriate Use of Pulmonary Computed Tomography Angiography by Increasing the Serum D-Dimer Threshold and Assessing Clinical Probability

with intermediate clinical risk benefit most Study Limitations Disclosure Statement from a serum D-dimer evaluation because A primary limitation of this study The author(s) have no conflicts of interest only those patients with an elevated was the necessity to assign Wells scores to disclose. D-dimer need to proceed with PCTA. retrospectively through EMR review. There are still a number of EMR review provides less information in Acknowledgment Mary Corrado, ELS, provided editorial patients in the 2012-2013 co- comparison with direct patient examina- Only 4% of assistance. horts with low serum D-dimer tion because not every finding may be the notes levels who underwent PCTA. documented electronically. In our ED, … mention References The reason for this is unclear physicians may mentally estimate their 1. PIOPED Investigators. Value of the ventilation/ a clinical because the retrospective as- patient’s pretest probability of PE us- perfusion scan in acute pulmonary embolism. probability Results of the prospective investigation of sessment of the clinical risk for ing a standard algorithm such as the pulmonary embolism diagnosis (PIOPED). of PE. … only PE was either low or moderate Wells criteria, but they rarely record JAMA 1990 May 23-30;263(20):2753- 5 of these … for all 47 of these patients. It that clinical probability in their written 9. DOI: http://dx.doi.org/10.1001/ jama.1990.03440200057023. mention [use] is also unclear how older age notes. To increase the documentation 2. Stein PD, Fowler SE, Goodman LR, et al; of a clinical and male sex in the 2012-2013 of clinical probability, it may be neces- PIOPED II Investigators. Multidetector cohort compared with the sary to include a step in the computed computed tomography for acute pulmonary decision embolism. N Engl J Med 2006 Jun rule … 2008-2009 cohort influenced tomography ordering process where the 1;354(22):2317-27. DOI: http://dx.doi. the higher prevalence of PEs. physician is required to input a clinical org/10.1056/NEJMoa052367. The implementation of the probability assessment. A pop-up screen 3. Stein PD1, Chenevert TL, Fowler SE, et al; PIOPED III (Prospective Investigation of higher D-dimer threshold set to at least could be included within the ordering Pulmonary Embolism Diagnosis III) Investigators. 1.0 µg/mL did not reduce the sensitiv- process that requires the physician to Gadolinium-enhanced magnetic resonance ity of PCTA for the detection of acute angiography for pulmonary embolism: a input specific findings that could then multicenter prospective study (PIOPED III). PE. Only 1 among all 233 patients in generate a clinical probability assessment Ann Intern Med 2010 Apr 6;152(7):434-43, both cohorts with a D-dimer value less using a standard algorithm such as the W142-3. DOI: http://dx.doi.org/10.7326/0003- than 1.0 µg/mL was noted to have PE 4819-152-7-201004060-00008. Wells criteria. 4. Prologo JD, Gilkeson RC, Diaz M, Asaad J. detected by PCTA. Given the published A population analysis based on an CT pulmonary angiography: a comparative coincidental PE rate of approximately HMO population may not be repre- analysis of the utilization patterns in emergency department and hospitalized 2% among all patients undergoing chest sentative of other clinical settings. Our patients between 1998 and 2003. AJR Am computed tomography for reasons other study results, although indicative of a J Roentgenol 2004 Oct;183(4):1093-6. DOI: than PE, this higher D-dimer threshold is general community hospital, may not be http://dx.doi.org/10.2214/ajr.183.4.1831093. 14-16 5. Abcarian PW, Sweet JD, Watabe JT, Yoo acceptable. applicable for other institutions, such as HC. Role of a quantitative D-dimer assay in We did not achieve a reasonable tertiary institutions or academic institu- determining the need for CT angiography level of compliance among ED physi- tions where more selective populations of acute pulmonary embolism. AJR Am J Roentgenol 2004 Jun;182(6):1377-81. DOI: cians with respect to documenting their may be encountered. http://dx.doi.org/10.2214/ajr.182.6.1821377. pretest clinical probability assessment Finally, this HMO uses only one 6. Donohoo JH, Mayo-Smith WW, Pezzullo within the medical record. Only 4% method of serum D-dimer measurement JA, Egglin TK. Utilization patterns and diagnostic yield of 3421 consecutive of the notes on the 547 patients in the (STA D-DI). It is unclear whether the use multidetector row computed tomography 2012-2013 cohort made mention of a of the 1.0 µg/mL threshold value could pulmonary angiograms in a busy emergency clinical probability of PE. In only 5 department. J Comput Assist Tomogr 2008 be applied to other methods of D-dimer May-Jun;32(3):421-5. DOI: http://dx.doi. of these 22 notes was there a specific measurement, although other authors org/10.1097/RCT.0b013e31812e6af3. mention of a clinical decision rule such have suggested different threshold 7. Wells PS, Anderson DR, Rodger M, et al. as the Wells criteria or the Pulmonary Excluding pulmonary embolism at the bedside values with other methods of serum D- without diagnostic imaging: management of Embolism Rule-out Criteria. Although dimer measurement.12,13 We recommend patients with suspected pulmonary embolism there is controversy as to the most ap- that those institutions that use a differ- presenting to the emergency departmet by using a simple clinical model and d-dimer. propriate decision rule to be used for ent D-dimer assay, review their own Ann Intern Med 2001 Jul 17;135(2):98-107. patients being evaluated for PE, there is PCTA results to ensure that the higher DOI: http://dx.doi.org/10.7326/0003-4819- no controversy as to recording the clini- threshold does not significantly reduce 135-2-200107170-00010. 17 8. van Belle A, Büller HR, Huisman MV, et al; cal likelihood assessment. Because this their sensitivity for the detection of PE. Christopher Study Investigators. Effectiveness HMO has a fully integrated EMR for all of managing suspected pulmonary embolism emergency, ambulatory, and hospital- Conclusion using an algorithm combining clinical probability, D-dimer testing, and computed based services including radiology The implementation of an increased tomography. JAMA 2006 Jan 11;295(2): ordering, a higher rate of compliance D-dimer threshold value increased the 172-9. DOI: http://dx.doi.org/10.1001/ will likely entail the use of some type prevalence of PE in patients undergoing jama.295.2.172. 9. Gimber LH, Leong J, Todoki L, Yoon HC. of electronic decision support tool em- PCTA in an ED setting, but more con- Avoiding unnecessary pulmonary CT bedded within the radiology ordering sistent application of clinical probability angiography by using a combination of mechanism that requires the input of a v clinical criteria and D-dimer thresholds. Open assessment remains an elusive target. Journal of Radiology 2013;3:78-84. DOI: clinical pretest probability. http://dx.doi.org/10.4236/ojrad.2013.32012.

14 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Improving Appropriate Use of Pulmonary Computed Tomography Angiography by Increasing the Serum D-Dimer Threshold and Assessing Clinical Probability

10. Hirai LK, Takahashi JM, Yoon HC. A 2012 Apr;10(4):572-81. DOI: http://dx.doi. outpatients. Clin Radiol 2010 Jan;65(1):1-5. prospective evaluation of a quantitative org/10.1111/j.1538-7836.2012.04647.x. DOI: http://dx.doi.org/10.1016/j.crad. D-dimer assay in the evaluation of acute 13. Kabrhel C, Courtney D, Camargo CA Jr, et al. 2009.09.003. pulmonary embolism. J Vasc Interv Radiol Potential impact of adjusting the threshold 16. Dentali F, Ageno W, Becattini C, et al. 2007 Aug;18(8):970-4. DOI: http://dx.doi. of the quantitative D-dimer based on pretest Prevalence and clinical history of incidental, org/10.1016/j.jvir.2007.04.020. probability of acute pulmonary embolism. asymptomatic pulmonary embolism: a meta- 11. Gimber LH, Travis RI, Takahashi JM, Goodman Acad Emerg Med 2009 Apr;16(4):325-32. analysis. Thromb Res 2010 Jun;125(6):518-22. TL, Yoon HC. Computed tomography DOI: http://dx.doi.org/10.1111/j.1553- DOI: http://dx.doi.org/10.1016/j.thromres. angiography in patients evaluated for acute 2712.2009.00368.x. 2010.03.016. pulmonary embolism with low serum D-dimer 14. Hui GC, Legasto A, Wittram C. The 17. Lucassen W, Geersing GJ, Erkens PM, et al. levels: a prospective study. Perm J 2009 prevalence of symptomatic and coincidental Clinical decision rules for excluding pulmonary Fall;13(4):4-10. DOI: http://dx.doi.org/10.7812/ pulmonary embolism on computed embolism: a meta-analysis. Ann Intern Med TPP/09-060. tomography. J Comput Assist Tomogr 2008 2011 Oct 4;155(7):448-60. DOI: http://dx. 12. Kline JA, Hogg MM, Courtney DM, Miller Sep-Oct;32(5):783-7. DOI: http://dx.doi. doi.org/10.7326/0003-4819-155-7- CD, Jones AE, Smithline HA. D-dimer org/10.1097/RCT.0b013e31815a7aea. 201110040-00007. threshold increase with pretest probability 15. Farrell C, Jones M, Girvin F, Ritchie G, unlikely for pulmonary embolism to decrease Murchison JT. Unsuspected pulmonary unnecessary computerized tomographic embolism identified using multidetector pulmonary angiography. J Thromb Haemost computed tomography in hospital

Excessive Bed Rest

I had known that excessive bed rest gave rise to thromboembolic complications. … The death rate from thromboembolism was always much less at the County Hospital … When [the County Hospital patients] got up to go to the bathroom, [they] dislodged only tiny clots from their veins and these did not harm them when they got to the lungs and were dissolved, while the wealthier patients … [at a private hospital] who remained in bed and formed large clots in their legs and pelvises suffered the major consequences of large pulmonary emboli.

— William Dock, MD, 1898-1990, cardiologist, known for coining “Sutton’s Law”

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 15 ORIGINAL RESEARCH & CONTRIBUTIONS Testing for Meningitis in Children with Bronchiolitis

Michael Stefanski, MD, MPH; Ronald Williams, MD, FAAP, FACP; George McSherry, MD; Joseph Geskey, DO, MBA Perm J 2014 Fall;18(4):16-19 http://dx.doi.org/10.7812/TPP/14-015

carry substantial morbidity and mortality rates, the incidence of Abstract concurrent meningitis in infants and children with clinical viral Viral bronchiolitis accounts for almost 20% of all-cause bronchiolitis has been reported to be less than 1% to 2%.5-13 hospitalizations of infants (ie, children younger than age 1 In the appropriate clinical setting, performance of a lumbar year). The annual incidence of fever in viral bronchiolitis has puncture (LP) is necessary to make the diagnosis of meningitis been documented at 23% to 31%. However the incidence of and to ensure appropriate treatment, but this must be weighed concurrent serious bacterial infections is low (1%-7%), with against the adverse effects and potential yield of the study. The meningitis occurring in less than 1% to 2% of cases, but lumbar performance of an LP is anxiety provoking to parents14 and has puncture is performed in up to 9% of viral bronchiolitis cases. been reported to contribute to parental dissatisfaction with the

To our knowledge, no study has examined clinical factors that care their infant receives.15 Moreover, physicians must balance influence a physician’s decision to perform a lumbar puncture the very small chance of meningitis occurring in viral bronchi- in the setting of viral bronchiolitis. olitis against the possible iatrogenic complications, including We present a retrospective, case-control study of hospitalized morbidity of LP, intravenous line placement, and unnecessary infants younger than one year diagnosed with viral bronchiolitis use of broad-spectrum antibiotics. We examined clinical factors who underwent lumbar puncture as part of an evaluation for that may influence a physician’s decision to perform an LP in meningitis. The objective of the study was to determine clinical the setting of viral bronchiolitis. factors that influence a physician’s decision to perform a lumbar puncture in the setting of viral bronchiolitis. Although the pres- Methods ence of apnea, cyanosis, meningeal signs, positive urine culture Study Design and Setting results, and young age were factors found to be preliminarily A retrospective, case-control study of 42 hospitalized infants associated with the performance of a lumbar puncture in the younger than age 1 year who had International Classification of setting of bronchiolitis, young age was the only significant Diseases, Ninth Revision (ICD-9) codes of bronchiolitis (ICD-9: clinical factor found after multivariable regression; no other 466.11 or 466.19) and underwent LP were matched 1:4 with demographic, clinical, laboratory, or radiologic variables were children who had ICD-9 codes of bronchiolitis without LP (168 found to be significant. controls) from January 1, 2001, through December 31, 2011 (Figure 1). The study was conducted at Penn State Children’s Introduction Hospital, an academic tertiary care children’s hospital located in Viral bronchiolitis is the most common cause of lower re- Hershey, PA. The Penn State Milton S Hershey Medical Center’s spiratory tract infection in children younger than age 1 year, institutional review board approved this study with waiver of accounting for almost 20% of all-cause infant hospitalizations.1,2 informed consent. The burden of disease is most prevalent in the fall and winter months, with peak incidence occurring in children between Data and Study Definitions ages 2 to 6 months.3,4 The clinical course of viral bronchiolitis is A standardized abstraction form was used to collect the fol- characterized by an upper respiratory prodrome and subsequent lowing data from both cohorts of hospitalized patients: age; sex; lower respiratory tract symptoms and signs, including cough, prematurity; chronic lung disease; insurance type; admitting wheeze, increased respiratory rate (RR), and increased effort. service (critical care vs general pediatrics); presence or absence The incidence of fever in the setting of bronchiolitis has been of apnea, cyanosis, tachypnea, fever, and meningeal signs; results documented at 23% to 31%.5 of urine culture, blood culture, chest radiographs, respiratory When fever develops, so too does the dilemma of determin- syncytial virus (RSV) testing, cerebrospinal fluid culture, and ing whether the fever is a consequence of the viral infection or white blood cell count if obtained; and hospital length of stay. a superimposed serious bacterial infection (SBI). In bronchiol- The presence of prematurity and chronic lung disease were itis patients, the incidence of concurrent SBI is low (1%-7%), noted from the medical history. Insurance type was classified with most being urinary tract infections (1%-5.5%).5-9 Although as commercial or governmental. Patients who were admitted to the sequelae of bacterial meningitis are well documented and either the neonatal intensive care unit or the pediatric intensive

Michael Stefanski, MD, MPH, is an Internist and Pediatrician at Penn State University Hershey Medical Center in PA. E-mail: [email protected]. Ronald Williams, MD, FAAP, FACP, is a Professor of Pediatrics and Internal Medicine at Penn State Hershey Children’s Hospital in PA. E-mail: [email protected]. George McSherry, MD, is a Pediatrician in the Division of Infectious Diseases at Penn State Hershey Children’s Hospital in PA. E-mail: [email protected]. Joseph Geskey, DO, MBA, is Vice President of Medical Affairs at Doctors Hospital in Columbus, OH. E-mail: [email protected].

16 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Testing for Meningitis in Children with Bronchiolitis

care unit were classified as critical care; otherwise, patients 1884 patients discharged with ICD-9 for acute bronchiolitis were classified as general pediatrics. The presence of apnea (Ages 0-98 years) and cyanosis were noted as present if these terms were noted in the medical record. The definition of tachypnea was based on age-defined RR of the World Health Organization guidelines: 939 excluded for age > 1 year (< 2 months, RR > 60/min; 2-12 months, RR > 50; 1-5 years, ° RR > 40). Fever was defined as a temperature of 38.0 C or 945 with age < 1 year greater. Meningeal signs were considered present if there was a notation of neck stiffness, bulging fontanel, inconsolable ir- ritability/crying, Kernig sign, or Brudzinski sign. 42 had lumbar puncture performed 903 cid not have documented A urinary tract infection was defined by the presence of (identified by ICD-9 procedure code) lumbar puncture more than 50,000 colony-forming units of a single pathogenic organism from a urine culture obtained by transurethral cath- eterization or more than 1000 colony-forming units obtained by Control patients randomized suprapubic aspiration. A bloodstream infection was defined as 42 cases of lumbar puncture performed a known bacterial pathogen from the blood whereas bacterial 168 control patients selected meningitis was defined as the isolation of a bacterial patho- in the setting of bronchiolitis gen from the cerebrospinal fluid. Chest radiographs that were interpreted as having an alveolar infiltrate, air bronchogram, Case-controls matched or consolidation were classified as having pneumonia (World ratio 1:4 Health Organization criteria).16 Bronchiolitis was classified as RSV if a positive result was obtained from either antigen testing Figure 1. Selection of case-control participants. A total of 42 patients were or culture from nasal secretions. selected as cases on the basis of International Classification of Diseases, Ninth Revision (ICD-9) procedure code of lumbar puncture. Each case was matched Statistical Analyses with 4 control patients who were selected at random from the remainder of the cohort meeting inclusion criteria of an ICD-9 discharge diagnosis of acute Descriptive statistics were prepared for all variables includ- bronchiolitis without documentation of a lumbar puncture being performed ing frequencies and percentages for categorical variables (eg, during the hospitalization. The total number of patients studied was 210. sex, apnea) and means, standard deviations, and quartiles for quantitative variables (eg, white blood cell count, length of stay). Age was considered as both a quantitative (age in days) Table 1. Bivariate analysis of factors associated with lumbar puncture and categorical (< 30, 30-59, 60-179, and > 180 days) variable. in acute bronchiolitis Bivariate analyses were conducted to assess the relationship Controls, Cases, a between each variable and LP using χ2 or Fisher exact tests Variable n = 168 (%) n = 42 (%) p value for categorical variables and logistic regression for quantita- Clinical features tive variables. All variables showing a marginal (p < 0.10) or Apnea 18 (10.7) 14 (33.3) 0.0003 significant (p < 0.05) relationship with LP were included in Cyanosis 22 (13.1) 14 (33.3) 0.0019 a multivariable regression model, and backward elimination Tachypnea 99 (59.3) 23 (54.8) 0.5953 was used to arrive at a final model, keeping all significant Fever 78 (46.4) 21 (50.0) 0.6783 variables. To further examine the effect of age on the findings, Meningeal signs 2 (1.2) 5 (11.9) 0.004 cases were matched on age category to controls in a 1:1 ratio Diagnostic studies using a greedy algorithm. Generalized estimating equations, Positive urine culture 2/41b (3.9) 6/32b (18.8) 0.0501 an extension of logistic regression that takes into account the Positive blood culture 5/69b (7.2) 1/37b (2.7) 0.6625 matching, were used to examine the relationship of LP to the Positive chest radiograph 14/148b (9.5) 4/40b (10.0) > 0.99 17,18 remaining variables. All analyses were conducted using SAS, Positive RSV 74/143b (51.7) 25/42b (59.5) 0.3744 version 9.2 (SAS Institute Inc, Cary, NC). WBC count 12.6 (0.50-49.00c) 11.2 (4.00-28.40) 0.1915 Demographic characteristics Results Age in days 141 (1-336 d) 44 (7-210 d) < 0.0001 None of the patients with acute bronchiolitis had docu- Male sex 102 (60.7) 25 (59.5) 0.8878 mented meningitis. However, the presence of apnea, cyanosis, Prematurity 44 (26.2) 14 (33.3) 0.3544 meningeal signs, positive urine culture results, and young age were factors associated with the performance of an LP in Chronic lung disease 18 (10.7) 3 (7.1) 0.4902 e bronchiolitis (Table 1). The presence of a fever and tachypnea Commerical insurance 86 (51.2) 24/41 (58.5) 0.699 were not associated with testing for meningitis. RSV status Admit service critical care 16 (9.5) 8 (19.0) 0.1026 also did not influence the decision to perform an LP, nor did a p value ≥ 0.10 included in multivariable regression model. b Positive results out of number tested. admission to a critical care service. There was a significant c Range of WBC counts in the tested population. difference in the mean age (44 days) of the LP cohort compared d Age range in days. with the mean age of the control group (141 days [p < 0.001]). e 24 cases of 41 total cases with documented insurance had commercial insurance. RSV = respiratory syncytial virus; WBC = white blood cell count.

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 17 ORIGINAL RESEARCH & CONTRIBUTIONS Testing for Meningitis in Children with Bronchiolitis

exclude a serious infection. To our knowledge, no previous Table 2. Adjusted multivariable regression model for performance of lumbar puncture in acute bronchiolitis studies have examined why hospitalized young infants with bronchiolitis undergo LP to exclude meningitis. A recent study Variable 95% CI p value reported that children with influenza were more likely to un- Apnea 0.232-4.303 0.3883 dergo LP testing than children with other respiratory illnesses, Cyanosis 0.421-8.344 0.999 but the percentage of children with RSV was not reported.19 Meningeal signs 0.277-79.57 0.2838 The only other significant predictor of an LP in this study was Positive urine culture result 0.558-17.776 0.1940 age 3 months or younger; there were no cases of meningitis. Age in days 0.964-0.994 0.0058 Despite its low yield, a common reason for screening for CI = confidence interval. SBI in infants is the presence of fever. A systematic review of 11 studies reporting rates of SBIs in infants younger than Table 3. Multivariable analysis with backward elimination 90 days reported a weighted rate of urinary tract infection of based on age categories for performance of lumbar 3.3%, with no cases of reported bacteremia in 8 of 11 studies puncture in children with acute bronchiolitis and no reported cases of meningitis at all.9 As a result, these Variable 95% CI p value authors and others have suggested a more selective approach to screening for SBI in young infants with bronchiolitis,20,21 Apnea 0.179-4.085 0.8455 particularly if they are RSV-positive.7,8 However, there have Cyanosis 0.526-12.126 0.2470 been at least 2 case reports of infants with RSV bronchiolitis Meningeal signs 0.238-72.473 0.3287 and meningitis.11,22 To understand the reasons that physicians Positive urine culture result 0.475-15.711 0.2603 elect to perform a procedure for a condition with such an Age 30-59 days vs < 30 days 0.169-2.062 0.4092 infrequent occurrence, we sought to ascertain whether there Age 60-179 days vs < 30 days 0.026-0.452 0.0023 were any demographic, clinical, laboratory, or radiologic Age ≥ 180 days vs < 30 days 0.011-1.032 0.0533 variables that would be associated with the clinical decision CI = confidence interval. to perform an LP. Our results suggest the most significant factor associated In addition to the significant quantitative difference in age with performing an LP is young age. The presence of fever in between the 2 groups, there was a significant difference in the young infants and a positive RSV test result did not influence categorical age variable. The number (and percentage) of the 42 the decision to perform an LP. Although the study was not infants who underwent lumbar testing at less than age 30 days, designed to determine whether a clinician should perform 30-59 days, 60-179 days, and 180 days or older were 18 (42.8%), an LP in hospitalized children with bronchiolitis, it is reas- 13 (31.0%), 10 (23.8%), and 1 (2.4%), respectively (p < 0.001). suring that despite a high rate of urinary tract infection and However, the presence of fever combined with age as either bacteremia no child had documented meningitis. a quantitative variable (age in days) or a categorical value However, there are several limitations to our study. Even (< 30 days, 30-59 days, 60-179 days, and > 180 days) was not though we used clinical variables that might influence a clini- associated with performance of an LP (data not shown). cian to perform an LP, the most accurate diagnostic combina- After the multivariable regression model and back- tion is unclear, particularly in this young age group.23 We also ward elimination were performed, the only variable did not assess whether these specific demographic, clinical, … the most that remained significant was age (Table 2). Similarly, and laboratory variables would lead physicians to perform accurate when categorical values of age were used, younger more or fewer LP procedures compared with other screening diagnostic infants were more likely to undergo performance of tools that physicians in academic centers use in the evalu- combination an LP than were older infants (Table 3). ation of young febrile infants, such as the Rochester, NY;24 is unclear, When cases were matched on age category to con- Philadelphia, PA;25,26 Boston, MA;27 or Pittsburgh, PA28 criteria. particularly trols and general estimating equations were used to These screening tools use the presence of fever to determine in this examine the relationship of LP to the remaining vari- further evaluation, but there have been reports of infants with young age ables, there were no significant results. meningitis who either do not have a fever or do not appear 20 group. Case controls were well matched regarding age as sick. Another limitation of our study is that we retrospec- there was no significant difference in the age of the tively analyzed administrative data so we cannot exclude 168 controls versus the remaining 777 infants who the possibility that cases of bronchiolitis, meningitis, and LP met control criteria but were not selected for the study. The were missed owing to inappropriate coding or incomplete median length of stay for patients who underwent an LP documentation by the physician. These limitations portend was 5 days versus 4 days for those who did not undergo further investigation, particularly expanding the case-control the procedure, though this difference was not found to be study to a multicenter evaluation with other children’s hos- statistically significant. pitals. Given that an infant’s initial evaluation often occurs in the Emergency Department, cross-referencing inpatient data Discussion with emergency room data can further highlight the clinical Although the likelihood of having meningitis in acute factors that determine the performance of an LP in the setting bronchiolitis is negligible, infants still undergo LP testing to of viral bronchiolitis.

18 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Testing for Meningitis in Children with Bronchiolitis

Conclusion 12. Kuppermann N, Bank DE, Walton EA, Senac MO Jr, McCaslin I. Risks for bacteremia and urinary tract infections in young febrile children with Despite these limitations we can conclude that LPs are still bronchiolitis. Arch Pediatr Adolesc Med 1997 Dec;151(12):1207-14. DOI: performed in hospitalized children with acute bronchiolitis, http://dx.doi.org/10.1001/archpedi.1997.02170490033006. particularly in young infants, despite an extremely low likeli- 13. Bilavsky E, Shouval DS, Yarden-Bilavsky H, Fisch N, Ashkenazi S, Amir J. A prospective study of the risk for serious bacterial infections in hospitalized hood of having a positive result, which may lead to a longer febrile infants with or without bronchiolitis. Pediatr Infect Dis J 2008 hospital length of stay, increased parental anxiety, and unneces- Mar;27(3):269-70. DOI: http://dx.doi.org/10.1097/INF.0b013e31815e85b1. sary exposure to broad-spectrum antibiotics. v 14. Haimi-Cohen Y, Amir J, Harel L, Straussberg R, Varsano Y. Parental presence during lumbar puncture: anxiety and attitude toward the procedure. Clin Pediatr (Phila) 1996 Jan;35(1):2-4. DOI: http://dx.doi. Disclosure Statement org/10.1177/000992289603500101. The author(s) have no conflicts of interest to disclose. 15. Kramer MS, Etezadi-Amoli J, Ciampi A, et al. Parents’ versus physicians’ values for clinical outcomes in young febrile children. Pediatrics 1994 May;93(5):697-702. Acknowledgment 16. World Health Association Pneumonia Vaccine Trial Investigators’ Group. Mary Corrado, ELS, provided editorial assistance. Standardization of interpretation of chest radiographs for the diagnosis of pneumonia in children. Geneva, Switzerland: Department of Vaccines and Biologicals, World Health Organization; 2001. References 17. Liang KY, Zeger SL. Longitudinal data analysis using generalized linear 1. Hall CB, Weinberg GA, Iwane MK, et al. The burden of respiratory syncytial models. Biometrika 1986;73(1):13-22. DOI: http://dx.doi.org/ virus infection in young children. N Engl J Med 2009 Feb 5;360(6):588-98. 10.2307/2336267. DOI: http://dx.doi.org/10.1056/NEJMoa0804877. 18. Zeger SL, Liang KY. Longitudinal data analysis for discrete and continuous 2. Yorita KL, Holman RC, Sejvar JJ, Steiner CA, Schonberger LB. Infectious outcomes. Biometrics 1986 Mar;42(1):121-30. DOI: http://dx.doi. disease hospitalizations among infants in the United States. Pediatrics 2008 org/10.2307/2531248. Feb;121(2):244-52. DOI: http://dx.doi.org/10.1542/peds.2007-1392. 19. Khandaker G, Heron L, Rashid H, et al. Comparing the use of, and 3. Mansbach JM, Pelletier AJ, Camargo CA Jr. US outpatient office visits for considering the need for, lumbar puncture in children with influenza or bronchiolitis, 1993-2004. Ambul Pediatr 2007 Jul-Aug;7(4):304-7. DOI: other respiratory virus infections. Influenza Other Respir Viruses 2013 http://dx.doi.org/10.1016/j.ambp.2007.03.006. Nov;7(6):932-7. DOI: http://dx.doi.org/10.1111/irv.12039. 4. Shay DK, Holman RC, Newman RD, Liu LL, Stout JW, Anderson LJ. 20. Antonow JA, Hansen K, McKinstry CA, Byington CL. Sepsis evaluations in Bronchiolitis-associated hospitalizations among US children, 1980-1996. hospitalized infants with bronchiolitis. Pediatr Infect Dis J 1998 Mar;17(3): JAMA 1999 Oct 20;282(15):1440-6. DOI: http://dx.doi.org/10.1001/ 231-6. DOI: http://dx.doi.org/10.1097/00006454-199803000-00011. jama.282.15.1440. 21. Liebelt EL, Qi K, Harvey K. Diagnostic testing for serious bacterial infections 5. Melendez E, Harper MB. Utility of sepsis evaluation in infants 90 days in infants aged 90 days or younger with bronchiolitis. Arch Pediatr of age or younger with fever and clinical bronchiolitis. Pediatr Infect Adolesc Med 1999 May;153(5):525-30. DOI: http://dx.doi.org/10.1001/ Dis J 2003 Dec;22(12):1053-6. DOI: http://dx.doi.org/10.1097/01. archpedi.153.5.525. inf.0000101296.68993.4d. 22. St Jacques DM, Barton LL, Rhee KH. Risk of serious bacterial infections in 6. Levine DA, Platt SL, Dayan PS, et al; Multicenter RSV-SBI Study Group of infants with bronchiolitis. Arch Pediatr Adolesc Med 1998 Aug;152(8):819-20. the Pediatric Emergency Medicine Collaborative Research Committee of the American Academy of Pediatrics. Risk of serious bacterial infection in young 23. Curtis S, Stobart K, Vandermeer B, Simel DL, Klassen T. Clinical features febrile infants with respiratory syncytial virus infections. Pediatrics 2004 suggestive of meningitis in children: a systematic review of prospective Jun;113(6):1728-34. DOI: http://dx.doi.org/10.1542/peds.113.6.1728. data. Pediatrics 2010 Nov;126(5):952-60. DOI: http://dx.doi.org/10.1542/ peds.2010-0277. 7. Purcell K, Fergie J. Concurrent serious bacterial infections in 2396 infants and children hospitalized with respiratory syncytial virus lower respiratory tract 24. Dagan R, Powell KR, Hall CB, Menegus MA. Identification of infants unlikely infections. Arch Pediatr Adolesc Med 2002 Apr;156(4):322-4. DOI: http:// to have serious bacterial infection although hospitalized for suspected sepsis. dx.doi.org/10.1001/archpedi.156.4.322. J Pediatr 1985 Dec;107(6):855-60. DOI: http://dx.doi.org/10.1016/S0022- 3476(85)80175-X. 8. Titus MO, Wright SW. Prevalence of serious bacterial infections in febrile infants with respiratory syncytial virus infection. Pediatrics 2003 25. Baker MD, Bell LM, Avner JR. Outpatient management without antibiotics of Aug;112(2):282-4. DOI: http://dx.doi.org/10.1542/peds.112.2.282. fever in selected infants. N Engl J Med 1993 Nov 11;329(20):1437-41. DOI: http://dx.doi.org/10.1056/NEJM199311113292001. 9. Ralston S, Hill V, Waters A. Occult serious bacterial infection in infants younger than 60 to 90 days with bronchiolitis: a systematic review. 26. Baker MD, Bell LM, Avner JR. The efficacy of routine outpatient Arch Pediatr Adolesc Med 2011 Oct;165(10):951-6. DOI: http://dx.doi. management without antibiotics of fever in selected infants. Pediatrics org/10.1001/archpediatrics.2011.155. 1999 Mar;103(3):627-31. DOI: http://dx.doi.org/10.1542/peds.103.3.627. 10. Geskey JM, Beck MJ, Brummel GL. Neonatal fever in the term infant: 27. Baskin MN, O’Rourke EJ, Fleisher GR. Outpatient treatment of febrile infants evaluation and management strategies. Curr Pediatr Rev 2008;4(2):84-95. 28 to 89 days of age with intramuscular administration of ceftriaxone. DOI: http://dx.doi.org/10.2174/157339608784462052. J Pediatr 1992 Jan;120(1):22-7. DOI: http://dx.doi.org/10.1016/S0022- 3476(05)80591-8. 11. McGregor RS, Tung J. Concurrent meningitis/serious bacterial infection in an infant hospitalized with respiratory syncytial virus. Arch Pediatr 28. Herr SM, Wald ER, Pitetti RD, Choi SS. Enhanced urinalysis improves Adolesc Med 2002 Oct;156(10):1055. DOI: http://dx.doi.org/10.1001/ identification of febrile infants ages 60 days and younger at low risk for archpedi.156.10.1055. serious bacterial illness. Pediatrics 2001 Oct;108(4):866-71. DOI: http://dx.doi. org/10.1542/peds.108.4.866.

Entitled

After nine months of pregnancy, a mother is entitled to have her baby get safe care. To expose her newborn to infection is criminal.

— Béla Schick, 1877-1967, Hungarian-born American pediatrician, founder of the Schick test

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 19 SOUL OF THE HEALER

Okavango Evening photograph

David Clarke, MD

The Okavango River system begins in Angola in southwest Africa. It flows almost 1000 miles to terminate in Botswana in the Okavango Delta. The delta, an enormous oasis in a very arid climate, supports a wide variety of vegetation and wildlife.

Dr Clarke is President of the Psychophysiologic Disorders Association and an Assistant Director at the Oregon Health & Science University Center for Ethics.

20 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 credits available for this article — see page 96.

ORIGINAL RESEARCH & CONTRIBUTIONS Impact of Implementing Glycated Hemoglobin Testing for Identification of Dysglycemia in Youth

Vinutha Vijayadeva, PhD; Gregory A Nichols, PhD Perm J 2014 Fall;18(4):21-27 http://dx.doi.org/10.7812/TPP/14-029

years.8 The ADA9 currently recommends Abstract that children with a body mass index Objectives: To determine the impact of the introduction of the glycated hemoglobin (BMI; calculated as weight in kilograms (HbA ) assay for diabetes mellitus diagnosis among children and adolescents aged 1C divided by height in meters squared) 6-17 years and to describe the composition of the population of patients with, and at equal to or greater than the 85th per- risk for, diabetes using fasting plasma glucose test and HbA1C assay. centile for age and sex and with any 2 Research Design and Methods: The Kaiser Permanente Hawaii (KPHI) and Kaiser of these risk factors: family history of Permanente Northwest (KPNW) sites identified a 2009 and a 2012 cohort of youth type 2 diabetes in first- or second-degree who were aged 6-17 years and continuously enrolled in their cohort year and for 1 relative, race/ethnicity (Native American, year prior. We excluded youth with a type 1 or type 2 diabetes diagnosis before their African American, Latino, Asian Ameri- cohort year. can, Pacific Islander), signs of insulin re- Results: In both sites, fasting plasma glucose testing was significantly more common sistance, and maternal history of diabetes in 2009 and HbA1C testing was more common in 2012. The proportion with either or gestational diabetes mellitus during test increased from 2.56% to 4.02% in KPNW and from 3.18% to 10.48% in KPHI, the child’s gestation should be screened but the characteristics of the population did not change between 2009 and 2012. In for diabetes starting at age 10 years or both sites, the characteristics of youth at risk of diabetes changed substantially with at the onset of puberty. Given the rise in a much greater proportion being female (KPNW: 39% vs 55%; KPHI: 35% vs 46%; p type 2 diabetes among youth, however, < 0.001 for both) and children younger than 10 (KPNW: 7% vs 32%; KPHI: 11% vs earlier screening may be appropriate, 39%; p < 0.001 for both) between 2009 and 2012. The size and composition of the but data on prevalence of diabetes and population of youth identified with diabetes was not affected. at-risk children in their first decade of Conclusions: Adoption of the HbA1C assay for diabetes diagnosis has increased life is scant. glycemia testing among youth aged 6-17 years and has altered the composition of the Our primary objective was to deter- population identified as at risk for diabetes. These findings have important ramifica- mine the impact of the introduction of tions for targeted screening and diabetes prevention efforts. the HbA1C assay for diabetes diagnosis among children and adolescents aged 6 Introduction not perfectly overlap, so the substitu- to 17 years. Secondarily, we describe the

Before 2010, the American Diabetes tion of HbA1C assay for diagnosis would composition of the population of patients Association (ADA) recommended the use likely change the composition of the with, and at risk for, diabetes resulting of fasting plasma glucose (FPG) test, ca- diabetes and at-risk population, which from the differential use of FPG test and

sual plasma glucose tests if symptoms of in turn would alter the epidemiology HbA1C assay. hyperglycemia were present, or 75 g oral of hyperglycemia.4,5 To our knowledge, glucose tolerance tests to diagnose diabe- the population effects of implementing Methods 1 tes. Following a consensus report from HbA1C assay for diagnosis of diabetes The study sites were Kaiser Perma- the International Expert Committee,2 and for identification of individuals at nente (KP) Hawaii (KPHI) and Kaiser the ADA recommended the inclusion of risk for diabetes has not been reported Permanente Northwest (KPNW), 2 group-

the glycated hemoglobin (HbA1C) assay in an outpatient population. model health maintenance organizations as a diagnostic tool in its 2010 Clinical Preventing type 2 diabetes onset in that provide integrated health care to ap- Practice Recommendation.3 Among the children is becoming increasingly im- proximately 220,000 members in Hawaii and 475,000 members in the Portland, advantages of the HbA1C assay is that portant because of the dramatic rise in it does not require the patient to fast, the prevalence of at-risk children and OR, area. Both KPHI and KPNW main- thereby potentially providing increased adolescents6 and the subsequent risk tain similar electronic medical record screening opportunities. However, it of developing diabetes in adulthood.7 databases that contain information on

is widely recognized that HbA1C assay, Furthermore, type 2 diabetes is a grow- all inpatient admissions, pharmacy dis- FPG, and oral glucose tolerance tests do ing problem among youth aged 10 to 19 penses, outpatient visits, and laboratory

Vinutha Vijayadeva, PhD, is a Research Associate at the Center for Health Research in Honolulu, HI. E-mail: [email protected]. Gregory A Nichols, PhD, is a Senior Investigator at the Center for Health Research in Portland, OR. E-mail: [email protected].

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 21 ORIGINAL RESEARCH & CONTRIBUTIONS Impact of Implementing Glycated Hemoglobin Testing for Identification of Dysglycemia in Youth

tests. In each site, we identified 2 cohorts: analyze meaningfully, and because they We used the mean of all values when the first cohort included individuals have similar risk factors for developing multiple BMI percentile measures in a identified from January 1, 2009, through diabetes, we combined them as “minority year were available. December 31, 2009, and the second from race/ethnicity.” This study was reviewed Clinicians at both KP Regions have January 1, 2012, through December 31, and approved by the KPHI and KPNW access to the national guidelines, which 2012. The cohorts consisted of youth institutional review boards. track very closely to ADA recommenda- who were aged 6-17 years in their cohort tions. The ADA9 currently recommends year and were continuously enrolled in Glucose Testing and Body that children with a BMI equal to or their cohort year and for 1 year prior. We Mass Index Percentile greater than the 85th percentile for age excluded members with an International Laboratories at KPHI and KPNW use and sex and with any 2 of these risk Classification of Diseases, Ninth Revision College of American Pathologists profi- factors: family history of type 2 diabetes diagnosis of type 1 or type 2 diabetes ciency testing as recommended by the in first- or second-degree relative, race/ before their cohort year. We specifi- ADA, and both sites are certified by the ethnicity (Native American, African cally selected 2009 because it was the National Glycohemoglobin Standardiza- American, Latino, Asian American, Pacific

year before HbA1C assay was endorsed tion Program. In Hawaii, the HbA1C as- Islander), signs of insulin resistance, by the ADA for use as a diagnostic test say is run on two instruments: Bio-Rad and maternal history of diabetes or for diabetes, and 2012 because it was Variant II and Bio-Rad Variant II Turbo gestational diabetes mellitus during the the most recent full year available after (Bio-Rad Laboratories, Hercules, CA); child’s gestation should be screened for

HbA1C assay was endorsed. The use of KPNW uses Cobas Integra 800 (Roche diabetes starting at age 10 years or at the 2012 allowed sufficient time to have Diagnostics, USA). onset of puberty. However, there is no

elapsed for full effect of the use of HbA1C We assessed the proportion of each mandated policy and KP clinicians are assay to be observed. Age, sex, height, cohort that received an FPG test or free to practice medicine in the way they

weight, race/ethnicity, FPG, and HbA1C HbA1C test in their cohort year. At-risk believe best suits their patients, but they were obtained from the electronic medi- for diabetes and diabetes was diagnosed are encouraged to consult and follow cal record. Self-reported race/ethnicity with a single diagnostic laboratory value. national guidelines. is routinely collected upon Health Plan We then determined the proportion enrollment, and patients can report up that met diagnostic criteria for being at Statistical Analysis to 5 races and 5 ethnic groups. For the risk for diabetes (FPG 100-125 mg/dL All analyses were conducted with

analysis, we have grouped race/ethnicity or HbA1C 5.7%-6.4% [39-46 mmol/mol]) SAS software, version 9.3 (SAS Institute, into 2 categories. Patients are grouped as or for having diabetes (FPG > 126 mg/ Cary, NC). Within each study site, we

non-Hispanic whites if they indicate such dL or HbA1C > 6.5% [>48 mmol/mol]). compared mean values using Fisher with no other race/ethnicity indicated. If multiple values of a given test were exact tests and proportions or categories Patients who indicate a single nonwhite available, we considered any elevated using χ2 tests. We present the results race, Hispanic ethnicity, or multiple value above the appropriate diagnostic separately for KPHI and KPNW to ex- races are considered as minority, which level as indicative of that form of hyper- amine the consistency of the findings includes Asian, Hawaiian Pacific Islander, glycemia. BMI percentile was estimated across two different geographic loca- and other mix. Individual minority race/ from the charts provided by the Centers tions with a decidedly different mix of ethnicity categories were too small to for Disease Control and Prevention.10 race/ethnicity.

Table 1. Population characteristics in two sites Cohort KPNW KPHI characteristics 2009, n = 58,442 2012, n = 58,353 p value 2009, n = 26,255 2012, n = 26,199 p value Mean age, years 11.8 11.8 0.978 11.7 11.7 0.921 Age 6-9 years 17,299 (29.6%) 17,272 (29.6%) 0.977 8273 (31.5%) 8265 (31.5%) 0.9277 Age 10-17 years 41,143 (70.4%) 41,081 (70.4%) 17,982 (68.5%) 17,934 (68.5%) Female 29,864 (51.1%) 29,818 (51.1%) 0.960 12,829 (48.9%) 12,796 (48.9%) 0.961 BMI percentiles, n 39,966 29,969 14,919 12,348 < 5th 639 (1.6%) 90 (0.3%) <0.001 393 (2.60%) 365 (3.00%) 0.1424 5th-84th 21,981 (55.0%) 11,508 (38.4%) 8773 (58.8%) 7324 (59.3%) 85th-94th 7993 (20.0%) 7672 (25.6%) 2504 (16.8%) 2082 (16.9%) ≥ 95th 9352 (23.4%) 10,699 (35.7%) 3249 (21.8%) 2577 (20.9%) Race/ethnicity, n 40,546 39,966 21,810 21,758 Minority race/ethnicitya 6812 (16.8%) 6714 (16.8%) 0.998 18,611 (85.3%) 18,566 (85.3%) 0.993 a Minority race/ethnicity: includes Asian, Hawaiian Pacific Islander, and other mix. BMI = body mass index; KPHI = Kaiser Permanente Hawaii; KPNW = Kaiser Permanente Northwest.

22 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Impact of Implementing Glycated Hemoglobin Testing for Identification of Dysglycemia in Youth

Results betes by cohort year and study site. Discussion

The 2009 and 2012 cohorts were In both KPNW and KPHI, mean age Following the addition of the HbA1C of nearly identical size in both KPNW for youth at risk for diabetes declined assay for diagnosing diabetes, our (~58,000) and KPHI (~26,000) (Table 1), significantly between 2009 and 2012, comparison of 2009 and 2012 cohorts and the demographic composition of the owing to a much larger proportion from KPHI and KPNW found that the cohorts in both sites was similar in each aged 6 to 9 years in 2012 (KPNW: 7% proportion of youth aged 6-17 that are year. Mean age was 11.8 years in both vs 32%; KPHI: 11% vs 39%; p < 0.001 tested and subsequently identified as at KPNW cohorts, and 11.7 years in both for both sites). In addition, a sig- risk for diabetes has risen dramatically.

KPHI cohorts. In both sites, the percent- nificantly larger proportion of females Despite differential uptake of HbA1C test- age of female participants was identical were identified in 2012 in both sites ing and the substantially different racial between cohort years (KPNW 51.1%; (KPNW: 39% vs 55%; KPHI: 35% vs composition of the two sites, we found KPHI 48.9%). In KPNW, the number with 46%; p < 0.001 for both sites). Follow- similar patterns of testing. Moreover, a BMI measurement was substantially ing the pattern of the total cohorts, the we observed important differences in lower in 2012, but the distribution of BMI distribution of BMI percentile shifted the size and composition of the result- percentile was significantly different with significantly at KPNW but not at KPHI ing populations identified as at risk for a greater proportion in the upper per- among at-risk youth. The proportion developing diabetes. centiles. The BMI percentile distribution at risk for diabetes that was of minor- In KPHI, a best practice alert was put was not significantly different between ity race/ethnicity was not significantly in place in 2010, which probably in- cohorts in KPHI. About 17% of each different between cohorts at either creased screening, and KPNW changed KPNW cohort and 85% of each KPHI site. At KPHI, mean age among those their established best practice alert from

cohort were of minority race/ethnicity. identified with diabetes was higher FPG test to HbA1C assay after departmen- In both settings, FPG testing was in 2009 compared with 2012 (13.8 vs tal grand rounds and lectures. At both significantly more common in 2009 com- 11.5, p = 0.044), but there were no sites the best practice alert triggers for

pared with 2012, but HbA1C testing was other differences between cohorts in all 6- to 18-year-olds with BMI equal to more common in 2012 (Table 2). The the characteristics of youth identified or greater than the 85th percentile. So proportion with either test increased with diabetes at either site (Table 4). the results at least partially reflect the from 2.56% to 4.02% in KPNW and from Table 5 displays the percentage test- power of the electronic medical record

3.18% to 10.48% in KPHI (p < 0.001 for ed with either FPG test or HbA1C assay, to enhance clinical care. both sites). The proportion identified the percentage at risk for diabetes, and Current ADA guidelines recommend as at-risk for diabetes by either test in- the percentage with diabetes for key screening for diabetes among youth creased significantly in both sites from age, sex, BMI, and racial/ethnic strata. beginning at age 10 years when other 2009 to 2012 (KPNW: 0.19% vs 1.34%; Testing was more common at KPHI, risk factors such as overweight/obesity KPHI: 0.56% vs 1.77%, p < 0.001 for both but overall the results were consistent are present.9 The increased use of the

sites), but the proportion identified with across all strata; similar percentages HbA1C assay resulted in 32% to 39% of diabetes was not significantly different were found in each cohort year, and youth at risk for diabetes being younger in either site. similar changes were observed from than age 10 years in 2012, compared Table 3 displays the characteristics 2009 to 2012 regardless of the age, sex, with 7% to 11% in 2009. A recent study of youth identified as at-risk for dia- BMI, or race/ethnicity strata. of primarily Hispanic obese adolescents

Table 2. Laboratory testing for diabetes and at risk for diabetes in 2009 and 2012 KPNW KPHI Cohort 2009, 2012, 2009, 2012, characteristics n = 58,442 n = 58,353 p value n = 26,255 n = 26,199 p value Fasting plasma glucose (FPG) test done 1455 (2.49%) 432 (0.74%) <0.001 775 (2.95%) 276 (1.05%) <0.001

Glycated hemoglobin (HbA1C) test done 82 (0.14%) 2066 (3.54%) <0.001 154 (0.59%) 2671 (10.20%) <0.001

Any FPG or HbA1C test done 1496 (2.56%) 2346 (4.02%) <0.001 835 (3.18%) 2745 (10.48%) <0.001 Impaired fasting glucose (FPG 100-125 mg/dL) 94 (0.16%) 18 (0.03%) <0.001 92 (0.35%) 42 (0.16%) <0.001 Diabetes using FPG (≥ 126 mg/dL) 12 (0.02%) 6 (0.01%) 0.158 6 (0.02%) 2 (0.01%) 0.289

Impaired HbA1C (5.7% - 6.4% [39-46 mmol/mol]) 18 (0.03%) 764 (1.31%) <0.001 67 (0.26%) 434 (1.66%) <0.001

Diabetes using HbA1C (≥6.5% [≥48 mmol/mol]) 18 (0.03%) 18 (0.03%) 0.861 8 (0.03%) 23 (0.09%) 0.007

At-risk for diabetes (FPG 100-125 mg/dL or HbA1C 111 (0.19%) 782 (1.34%) <0.001 146 (0.56%) 463 (1.77%) <0.001 5.7%-6.4% [38-46 mmol/mol])

Diabetes (FPG ≥126 mg/dL or HbA1C ≥ 6.5% 23 (0.04%) 18 (0.03%) 0.761 12 (0.05%) 23 (0.09%) 0.062 [≥ 48 mmol/mol]) KPHI = Kaiser Permanente Hawaii; KPNW = Kaiser Permanente Northwest.

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 23 ORIGINAL RESEARCH & CONTRIBUTIONS Impact of Implementing Glycated Hemoglobin Testing for Identification of Dysglycemia in Youth

Table 3. Characteristics of youth at risk for diabetes in 2009 and 2012 Cohort KPNW KPHI characteristics 2009, n = 111 2012, n = 782 p value 2009, n = 146 2012, n = 463 p value Mean age, years 13.3 11.5 <0.001 13.04 10.5 <0.001 Age 6-9 years 8 (7.2%) 246 (31.5%) <0.001 16 (11.0%) 182 (39.3%) <0.001 Age 10-17 years 103 (92.8%) 536 (68.5%) 130 (89.0%) 281 (60.7%) Female 43 (38.7%) 426 (54.5%) 0.002 51 (34.9%) 211 (45.6%) 0.0236 BMI percentiles, n 111 759 133 399 < 5th 0 (0.0%) 0 (0.0%) 0.001 1 (0.80%) 2 (0.50%) 0.368 5th-84th 16 (14.4%) 48 (6.3%) 12 (9.0%) 41 (10.3%) 85th-94th 13 (11.7%) 52 (6.9%) 18 (13.5%) 79 (19.8%) ≥ 95th 82 (73.9%) 659 (86.8%) 102 (76.7%) 277 (69.4%) Race/ethnicity, n 65 564 128 434 Minority 15 (23.1%) 174 (30.9%) 0.196 118 (92.2%) 414 (95.4%) 0.156 BMI = body mass index; KPHI = Kaiser Permanente Hawaii; KPNW = Kaiser Permanente Northwest.

Table 4. Characteristics of patients with diabetes in 2009 and 2012 Cohort KPNW KPHI characteristics 2009, n = 22 2012, n = 20 p value 2009, n = 12 2012, n = 23 p value Mean age, years 12.5 12.7 0.855 13.8 11.5 0.044 Age 6-9 years 5 (22.7%) 4 (20.0%) 0.830 1 (8.3%) 7 (30.4%) 0.216 Age 10-17 years 17 (77.3%) 16 (80.0%) 11 (91.7%) 16 (69.6%) Female 14 (63.6%) 10 (50.0%) 0.373 6 (50.0%) 10 (43.0%) 0.713 BMI percentiles, n 22 20 10 18 < 5th 0 1 (5.0%) 0.297 0 0 0.712 5th-84th 9 (40.9%) 7 (35.0%) 2 (20.0%) 2 (11.1%) 85th-94th 6 (27.3%) 2 (10.0%) 1 (10.0%) 1 (5.6%) ≥ 95th 7 (31.8%) 10 (50.0%) 7 (70.0%) 15 (83.3%) Race/ethnicity, n 18 18 11 21 Minority 2 (11.1%) 4 (22.2%) 0.371 11 (100%) 21 (100%) N/A BMI = body mass index; KPHI = Kaiser Permanente Hawaii; KPNW = Kaiser Permanente Northwest.

concluded that the use of HbA1C assay to HbA1C assay in youth if a universal changes or medication can reduce or was associated with increased diabetes recommendation were made. delay diabetes onset in adults,12-15 but

screening in primary care. The percent- It appears that the ease of using HbA1C evidence of whether such preventive age of obese teens (> 95th percentile) assay increased the number of youth success applies to youth is scant. One screened for diabetes increased from being tested. Despite the increase, how- recent study in adolescents (aged 10 40% in period 1 (April 19, 2008, to ever, we did not observe a change in the to 17 years) at high risk of developing October 19, 2009) to 47% in period 2 number of cases identified with diabe- type 2 diabetes showed that a 6-month (May 3, 2010, to November 3, 2011).11 tes, but we did see a substantial increase lifestyle intervention combined with Our study was not limited to obese in those identified as at risk for diabetes. metformin showed a modest weight 16 youth and included a wider age range, Whether this means that HbA1C assay loss and increased insulin sensitivity, thus providing a more comprehensive inappropriately identifies individuals but it was not of sufficient duration to analysis of the adoption and effective- or that FPG testing misses patients who assess risk of diabetes onset. Research

ness of the HbA1C assay in overweight should be identified as at risk cannot be is needed to determine effective risk and normal weight youth. determined from these data. In any case, reduction strategies for youth. There are no specific recommenda- it appears that targeted screening has As type 2 diabetes becomes increas-

tions for the use of HbA1C assay in the increased as a result of the use of HbA1C ingly common among younger indi- pediatric population, and we hope this assay, allowing for greater opportunity viduals, the lifetime risk of developing article highlights the need for them. The to intervene. This is important because complications will likely rise. However, increase in use we observed is probably targeted intervention is essential for the there is evidence that effective glycemic based on recommendations for adults. If efficient use of diabetes prevention re- control early in the course of both type so, our study shows the effect of moving sources. There is no doubt that lifestyle 1 and type 2 diabetes can reduce the

24 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Impact of Implementing Glycated Hemoglobin Testing for Identification of Dysglycemia in Youth

risk of microvascular and macrovascular identifies more men than women with these observational data. However, our 17,18 28 disease. HbA1C assay is clearly an hyperglycemia, although whether this objective was not to estimate prevalence effective method for identifying future metabolic difference between sexes ap- but to assess the impact of introducing 19,20 diabetes risk, and being at risk for plies to youth is unclear. In any case, our the HbA1C assay as a diagnostic tool. diabetes is associated with increased results suggest that the risk of diabetes The finding that glucose testing rates are prevalence of retinopathy and nephrop- among young females, the likelihood increasing should result in a more repre- athy,21 chronic kidney disease,22 and of future gestational diabetes, and the sentative analysis sample in the future. cardiovascular disease.23,24 Furthermore, number of pregnancies complicated by We did not differentiate between type these complications are all associated existing diabetes may be considerably 1 and type 2 diabetes, a very difficult with duration of diabetes.25-27 Therefore, greater than previously believed. task when limited to observational data. in terms of prevention of type 2 diabetes Our study has several limitations. It is This might have resulted in dispropor- and its complications, early recognition likely that those receiving glucose tests tionately identifying children with type with targeted screening is essential. are ordered for youth believed to be 1 diabetes. Nonetheless, increased use

We also observed a shift in the sex more at risk for diabetes, so our results of HbA1C assay did not affect diabetes distribution of those identified as at risk should not be viewed as an outcome of identification but had a marked effect for diabetes following implementation general screening efforts. Whether the on the size and composition of the at-

of HbA1C assay, with substantially more proportions we identified as at risk for risk population. Therefore, the inability females recognized in 2012 than in 2009. diabetes or with diabetes represent true to distinguish between type 1 and type This is not surprising given that FPG prevalence cannot be determined from 2 diabetes is probably negligible. We

Table 5. Percentage tested, percentage at risk for diabetes, and percentage with diabetes for key age, sex, body mass index, and racial/ethnic strata KPNW KPHI Cohort 2009 2012 2009 2012 characteristics n % (n) n % (n) p value n % (n) n % (n) p value Testeda Age 6-9 17,299 1.1 (190) 17,272 3.2 (553) <0.001 8273 0.8 (136) 8265 6.3 (1033) <0.001 Age 10-17 41,143 3.2 (1317) 41,081 4.4 (1808) <0.001 17,982 1.2 (699) 17,934 4.8 (1712) <0.001 Boys 28,578 2.5 (714) 28,535 3.4 (970) <0.001 13,426 1.6 (439) 13,403 5.2 (1,387) <0.001 Girls 29,864 2.6 (776) 29,818 4.6 (1372) <0.001 12,829 1.2 (396) 12,796 5.3 (1,358) <0.001 BMI < 85th 22,621 1.3 (294) 11,598 3.0 (348) <0.001 9166 0.7 (122) 7689 2.2 (367) <0.001 BMI ≥ 85th 17,345 2.4 (416) 18,371 3.0 (551) 0.027 5753 6.0 (625) 4659 19.2 (1995) <0.001 Non-Hispanic white 33,734 2.6 (877) 33,252 4.4 (1463) <0.001 3199 1.2 (79) 3192 4.3 (274) <0.001 Minority race/ethnicity 6812 3.0 (204) 6714 5.2 (349) <0.001 18,611 1.8 (660) 18,566 6.1 (2257) <0.001 At risk for diabetes Age 6-9 17,299 0.1 (17) 17,272 1.4 (242) <0.001 8273 0.1 (16) 8265 1.1 (182) <0.001 Age 10-17 41,143 0.3 (123) 41,081 1.3 (534) <0.001 17,982 0.4 (130) 17,934 0.8 (281) <0.001 Boys 28,578 0.2 (57) 28,535 1.2 (342) <0.001 13,426 0.4 (95) 13,403 0.9 (252) <0.001 Girls 29,864 0.2 (60) 29,818 1.5 (447) <0.001 12,829 0.2 (51) 12,796 0.8 (211) <0.001 BMI < 85th 22,621 0.1 (23) 11,598 0.4 (46) <0.001 9166 0.1 (13) 7689 0.3 (43) <0.001 BMI ≥ 85th 17,345 0.2 (35) 18,371 0.7 (129) <0.001 5753 1.2 (12) 4659 3.4 (356) <0.001 Non-Hispanic white 33,734 0.2 (67) 33,252 1.2 (399) <0.001 3199 0.2 (10) 3192 0.31 (20) 0.066 Minority race/ethnicity 6812 0.2 (14) 6714 2.6 (175) <0.001 18,611 0.3 (118) 18,566 1.1 (414) <0.001 With diabetes Age 6-9 17,299 0.03 (5) 17,272 0.02 (3) 0.74 8273 0.01 (1) 8265 0.04 (7) 0.034 Age 10-17 41,143 0.04 (16) 41,081 0.04 (16) 0.866 17,982 0.03 (11) 17,934 0.04 (16) 0.332 Boys 28,578 0.03 (9) 28,535 0.03 (9) 0.635 13,426 0.02 (6) 13,403 0.05 (13) 0.107 Girls 29,864 0.05 (15) 29,818 0.04 (12) 0.417 12,829 0.02 (6) 12,796 0.04 (10) 0.315 BMI < 85th 22,621 0.04 (9) 11,598 0.07 (8) 0.253 9166 0.01 (2) 7689 0.01 (2) 0.86 BMI ≥ 85th 17,345 0.08 (14) 18,371 0.03 (6) 0.175 5753 0.1 (8) 4659 0.2 (16) 0.031 Non-Hispanic white 33,734 0.05 (17) 33,252 0.04 (13) 0.719 3199 0 3192 0 Minority race/ethnicity 6812 0.03 (2) 6714 0.06 (4) 0.413 18,611 0.03 (11) 18,566 1 (22) 0.055 a Using either fasting plasma glucose or glycated hemoglobin assay. BMI = body mass index; KPHI = Kaiser Permanente Hawaii; KPNW = Kaiser Permanente Northwest.

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 25 ORIGINAL RESEARCH & CONTRIBUTIONS Impact of Implementing Glycated Hemoglobin Testing for Identification of Dysglycemia in Youth

determined those at risk and those with In conclusion, the 2010 introduction The many faces of diabetes in American youth: type 1 and type 2 diabetes in five race and diabetes with a single diagnostic labora- of the HbA1C assay to diagnose diabetes ethnic populations: the SEARCH for Diabetes in tory value. A one-year period may be appears to have increased the propor- Youth Study. Diabetes Care 2009 Mar;32 Suppl too short to capture those with confirma- tion of youth receiving glycemia tests. 2:S99-101. DOI: http://dx.doi.org/10.2337/ dc09-S201. tory tests or to determine whether the As a result, many more youth are now 9. American Diabetes Association. Standards test we did capture was itself confirma- being recognized as at risk for develop- of medical care in diabetes—2013. Diabetes tory. In any case, we acknowledge that ing diabetes, and a greater proportion Care 2013 Jan;36 Suppl 1:S11-66. DOI: http:// dx.doi.org/10.2337/dc13-S011. our results may overstate the number of them are younger (< age 10 years) 10. Growth charts [Internet]. Atlanta, GA: Centers with diabetes. Large proportions of our and female. This change in the number for Disease Control and Prevention; 2010 Sep samples did not have race/ethnicity and composition of at-risk youth has 9 [cited 2014 Jun 16]. Available from: www. cdc.gov/growthcharts/. recorded, but racial differences among important implications for the delivery 11. Love-Osborne KA, Sheeder J, Svircev A, Chan those with available data did not affect of diabetes prevention efforts. v C, Zeitler P, Nadeau KJ. Use of glycosylated the results. Furthermore, findings were hemoglobin increases diabetes screening for at-risk adolescents in primary care settings. remarkably similar between the two Disclosure Statement Pediatr Diabetes 2013 Nov;14(7):512-8. DOI: sites, suggesting that our results are Gregory A Nichols, PhD, receives fund- http://dx.doi.org/10.1111/pedi.12037. robust and unaffected by race/ethnicity. ing for unrelated research support from 12. Tuomilehto J, Lindström J, Eriksson JG, et al; Finnish Diabetes Prevention Study Group. FPG may be skewed because we were GlaxoSmithKline, AstraZeneca, Bristol-Myers Squibb, Novartis, and Merck. The author(s) Prevention of type 2 diabetes mellitus by unable to reliably differentiate between have no other conflicts of interest to disclose. changes in lifestyle among subjects with routine values captured during “well impaired glucose tolerance. N Engl J Med 2001 May 3;344(18):1343-50. DOI: http://dx.doi. child” visits and those captured during Acknowledgment org/10.1056/NEJM200105033441801. acute events that could affect the values. We would like to thank Valentyna 13. Knowler WC, Barrett-Connor E, Fowler Approximately half of the enrolled chil- Pishchalenko (Kaiser Permanente Hawaii) SE, et al; Diabetes Prevention Program Research Group. Reduction in the incidence dren did not have BMI data available. for her support with data acquisition. of type 2 diabetes with lifestyle intervention It is possible that results for those with Mary Corrado, ELS, provided editorial or metformin. N Engl J Med 2002 Feb assistance. 7;346(6):393-403. DOI: http://dx.doi. and without BMI data were different. org/10.1056/NEJMoa012512. However, the testing data, which is 14. Buchanan TA, Xiang AH, Peters RK, et al. the main emphasis of this article, are References Preservation of pancreatic beta-cell function 1. American Diabetes Association. Diagnosis and and prevention of type 2 diabetes by based on whole samples regardless of classification of diabetes mellitus. Diabetes pharmacological treatment of insulin resistance availability of BMI. Although use of the Care 2009 Jan;32 Suppl 1:S62-7. DOI: http:// in high-risk Hispanic women. Diabetes 2002 HbA assay to diagnose diabetes ap- dx.doi.org/10.2337/dc09-S062. Sep;51(9):2796-803. DOI: http://dx.doi. 1C 2. International Expert Committee. International org/10.2337/diabetes.51.9.2796. pears to have increased the proportion Expert Committee report on the role of 15. Ramachandran A, Snehalatha C, Mary of youth receiving glycemia tests, other the A1C assay in the diagnosis of diabetes. S, Mukesh B, Bhaskar AD, Vijay V; Indian unmeasured factors such as education Diabetes Care 2009 Jul;32(7):1327-34. DOI: Diabetes Prevention Programme (IDPP). The http://dx.doi.org/10.2337/dc09-9033. Indian Diabetes Prevention Programme shows (of both provider and parent) cannot be 3. American Diabetes Association. Diagnosis and that lifestyle modification and metformin ruled out. Last, our data came from two classification of diabetes mellitus. Diabetes prevent type 2 diabetes in Asian Indian Regions of a comprehensive integrated Care 2010 Jan;33 Suppl 1:S62-9. DOI: http:// subjects with impaired glucose tolerance (IDPP- dx.doi.org/10.2337/dc10-S062. Erratum in: 1). Diabetologia 2006 Feb;49(2):289-97. DOI: health system that has excellent informa- Diabetes Care 2010 Apr;33(4):e57. DOI: http:// http://dx.doi.org/10.1007/s00125-005-0097-z. tion technology support. Whether the dx.doi.org/10.2337/dc09-2368. 16. Garnett SP, Gow M, Ho M, et al. Optimal 4. Sacks DB. A1C versus glucose testing: testing rates and the resulting propor- macronutrient content of the diet for a comparison. Diabetes Care 2011 adolescents with prediabetes; RESIST a tions we report could be generalized to Feb;34(2):518-23. DOI: http://dx.doi. randomised control trial. J Clin Endocrinol other settings is unknown. org/10.2337/dc10-1546. Metab 2013 May;98(5):2116-25. DOI: http:// The purpose of this research was 5. Bonora E, Tuomilehto J. The pros and cons of dx.doi.org/10.1210/jc.2012-4251. diagnosing diabetes with A1C. Diabetes Care 17. Nathan DM, Cleary PA, Backlund JY, et al; to address whether the endorsement 2011 May;34 Suppl 2:S184-90. DOI: http:// Diabetes Control and Complications Trial/ dx.doi.org/10.2337/dc11-s216. Epidemiology of Diabetes Interventions and of HbA1C assay for diagnosing diabetes 6. Li C, Ford ES, Zhao G, Mokdad AH. Prevalence Complications (DCCT/EDIC) Study Research affected the screening, detection, and of pre-diabetes and its association with Group. Intensive diabetes treatment and composition of populations of youth clustering of cardiometabolic risk factors and cardiovascular disease in patients with with dysglycemia. Although our data hyperinsulinemia among US adolescents: type 1 diabetes. N Engl J Med 2005 Dec National Health and Nutrition Examination 22;353(25):2643-53. DOI: http://dx.doi. answered that question, whether screen- Survey 2005-2006. Diabetes Care 2009 org/10.1056/NEJMoa052187. ing is adequate or not is unknown. Feb;32(2):342-7. DOI: http://dx.doi. 18. Holman RR, Paul SK, Bethel MA, Matthews DR, Unfortunately, because this was an ob- org/10.2337/dc08-1128. Neil HA. 10-year follow-up of intensive glucose 7. Nguyen QM, Srinivasan SR, Xu JH, Chen control in type 2 diabetes. N Engl J Med 2008 servational study we cannot determine W, Berenson GS. Fasting plasma glucose Oct 9;359(15):1577-89. DOI: http://dx.doi. clinician rationale for testing in either levels within the normoglycemic range in org/10.1056/NEJMoa0806470. cohort year, nor can we assess whether childhood as a predictor of prediabetes and 19. Zhang X, Gregg EW, Williamson DF, et al. A1C type 2 diabetes in adulthood: the Bogalusa level and future risk of diabetes: a systematic all who should be screened are being Heart Study. Arch Pediatr Adolesc Med review. Diabetes Care 2010 Jul;33(7):1665-73. screened. This is a vitally important 2010 Feb;164(2):124-8. DOI: http://dx.doi. DOI: http://dx.doi.org/10.2337/dc09-1939. question that we hope to answer with org/10.1001/archpediatrics.2009.268. 20. Gregg EW, Geiss L, Zhang P, Zhuo X, 8. Mayer-Davis EJ, Bell RA, Dabelea D, et al; Williamson DF, Albright AL. Implications of future research. SEARCH for Diabetes in Youth Study Group. risk stratification for diabetes prevention: the

26 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Impact of Implementing Glycated Hemoglobin Testing for Identification of Dysglycemia in Youth

case of hemoglobin A1c. Am J Prev Med 2013 individuals followed for 12.4 years. Diabetes DOI: http://dx.doi.org/10.1016/j. Apr;44(4 Suppl 4):S375-80. DOI: http://dx.doi. Care 1999 Feb;22(2):233-40. DOI: http://dx.doi. jdiacomp.2006.04.001. org/10.1016/j.amepre.2012.12.012. org/10.2337/diacare.22.2.233. 27. Fox CS, Sullivan L, D’Agostino RB Sr, Wilson 21. Gabir MM, Hanson RL, Dabelea D, et al. 24. Levitan EB, Song Y, Ford ES, Liu S. Is nondiabetic PW; Framingham Heart Study. The significant Plasma glucose and prediction of microvascular hyperglycemia a risk factor for cardiovascular effect of diabetes duration on coronary heart disease and mortality: evaluation of 1997 disease? A meta-analysis of prospective studies. disease mortality: the Framingham Heart Study. American Diabetes Association and 1999 Arch Intern Med 2004 Oct 25;164(19):2147-55. Diabetes Care 2004 Mar;27(3):704-8. DOI: World Health Organization criteria for DOI: http://dx.doi.org/10.1001/archinte. http://dx.doi.org/10.2337/diacare.27.3.704. diagnosis of diabetes. Diabetes Care 2000 164.19.2147. 28. Unwin N, Shaw J, Zimmet P, Alberti KG. Aug;23(8):1113-8. DOI: http://dx.doi. 25. Kundu D, Roy A, Mandal T, Bandyopadhyay U, Impaired glucose tolerance and impaired fasting org/10.2337/diacare.23.8.1113. Ghosh E, Ray D. Relation of microalbuminuria glycaemia: the current status on definition and 22. Fox CS, Larson MG, Leip EP, Meigs JB, Wilson to glycosylated hemoglobin and duration intervention. Diabet Med 2002 Sep;19(9):708- PW, Levy D. Glycemic status and development of type 2 diabetes. Niger J Clin Pract 2013 23. DOI: http://dx.doi.org/10.1046/j.1464- of kidney disease: the Framingham Heart Study. Apr-Jun;16(2):216-20. DOI: http://dx.doi. 5491.2002.00835.x. Diabetes Care 2005 Oct;28(10):2436-40. DOI: org/10.4103/1119-3077.110159. http://dx.doi.org/10.2337/diacare.28.10.2436. 26. Romero P, Salvat M, Fernández J, Baget M, 23. Coutinho M, Gerstein HC, Wang Y, Yusuf S. Martinez I. Renal and retinal microangiopathy The relationship between glucose and incident after 15 years of follow-up study in a sample cardiovascular events. A metaregression analysis of Type 1 diabetes mellitus patients. J Diabetes of published data from 20 studies of 95,783 Complications 2007 Mar-Apr;21(2):93-100.

Chief Weapon of Offence

In the fight which we have to wage incessantly against ignorance and quackery among the masses and follies of all sorts among the classes, diagnosis, not drugging, is our chief weapon of offence. Lack of systematic personal training in the methods of the recognition of disease leads to the misapplication of remedies, to long courses of treatment when treatment is useless, and so directly to that lack of confidence in our methods which is apt to place us in the eyes of the public on a level with empirics and quacks.

— William Osler, MD, 1849-1919, Canadian physician and one of the four founding professors of Johns Hopkins Hospital

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 27 SOUL OF THE HEALER

The Snorer Handcrafted figures and mechanisms aluminum, brass, wood, fabric

David A Dumbrell

�The internal mechanisms and figures of this clockspring-powered automaton are entirely handcrafted. (See it in action at: www.davestudiorama.com/the-snorer.html.) When wound up, the clockspring mounted into the side of this piece drives five cams, each of which manipulates the hand-painted figures much like strings on a marionette. One cam mechanism opens and closes the figures’ eyes, another turns the heads or makes an arm swing, and yet another causes the wife to sit up. The result is the following scene: husband because of wife’s snoring, pushes her, and goes back to sleep, and then she wakes up shocked before going back to sleep as well.

Mr Dumbrell is retired and lives in Vancouver, British Columbia, Canada. More of his work can be seen at: www.davestudiorama.com.

28 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Most Common Dermatologic Topics Published in Five High-Impact General Medical Journals, 1970-2012: Melanoma, Psoriasis, Herpes Simplex, Herpes Zoster, and Acne

Young M Choi; Aram A Namavar, MS; Jashin J Wu, MD Perm J 2014 Fall;18(4):29-31 http://dx.doi.org/10.7812/TPP/14-056

matologic diagnoses made by internists during this period were Abstract dermatitis, bacterial skin infections, tinea, acne vulgaris, and herpes Context: General practitioners frequently encounter skin zoster. By highlighting these common diagnoses, it was antici- diseases and are accustomed to diagnosing the most common pated that skin disease educational programs for internists would dermatologic conditions. be tailored to these diseases. Moreover, this study demonstrated Objective: We sought to determine the most common der- that diagnoses such as psoriasis, actinic keratosis, seborrheic matologic topics published in five high-impact general medical keratosis, skin cancer, and benign tumors were commonly made journals (New England Journal of Medicine, The Lancet, the by dermatologists but not by internists. These findings elucidated Journal of the American Medical Association, British Medical the overlapping yet differing role of the dermatologist and the Journal (now The BMJ), and Annals of Internal Medicine). internist, espousing the need for further communication and alli- Design: We conducted an independent search of the Thomson ance in diagnosing a wide range of skin diseases. Reuters’ Science Citation Index for common dermatologic topics, The purpose of our study was to determine the most com- limited to the period 1970 to 2012. mon dermatologic topics published from 1970 to 2012 in five Main Outcome Measure: Total number of publications deal- high-impact general medical journals. We sought to analyze ing with each dermatologic topic considered. whether these journals, having the largest readership in medi- Results: The five most common dermatologic topics published cine, targeted the common dermatologic diagnoses made by were melanoma, psoriasis, herpes simplex, herpes zoster, and internists or focused on skin diseases more commonly diagnosed acne. Melanoma and psoriasis were the top two dermatologic by dermatologists. topics published in each journal except for Annals of Internal Medicine. Methods Conclusions: Internists frequently diagnose herpes simplex, We analyzed data from the Thomson Reuters Science Cita- herpes zoster, and acne, which are also common dermatologic tion Index. The five high-impact general medical journals we topics published. Although internists infrequently diagnose considered, based on the highest impact factors, were the New melanoma and psoriasis, they are major topics for general England Journal of Medicine (NEJM), The Lancet, the Journal medical journals because of their increased community aware- of the American Medical Association (JAMA), British Medical ness, major advancements in therapeutic research, and their Journal (now The BMJ), and Annals of Internal Medicine. For nondermatologic manifestations. each of these journals, we conducted an independent search for each of the dermatologic topics included in the study, limited Introduction to the years 1970 to 2012. The topics chosen were a modified Skin diseases are commonly encountered by general prac- list from the top dermatologic diagnoses made by internists and titioners, and in today’s health care system, most patients are 2 dermatologists (Table 1). evaluated first by their primary care physician before seeing a Two independent reviewers analyzed search results to de- dermatologist. It is estimated that 6% of primary care outpatient termine whether an article met the dermatologic topic under visits are skin-related, and 60% of cutaneous diagnoses are made consideration. A consensus was achieved for all articles included. by nondermatologists.1 As the role of the general practitioner All types of publications (original research, case reports, review continues to grow, it remains imperative that these physicians articles, meta-analyses, editorials, etc) were eligible for the study. are equipped to manage general dermatologic conditions. If an article dealt with more than one possible topic, the topic To determine which skin diseases internists most commonly that best fit the primary objective of the article was chosen. Top- encounter, Feldman et al2 analyzed the National Ambulatory ics without 20 or more papers in any of the 5 general medical Medical Care Survey data from 1990 to 1994. The top five der- journals were not mentioned.

Young M Choi is a Clinical Research Fellow in Dermatology at the Los Angeles Medical Center in CA and a Fourth-Year Medical Student at the David Geffen School of Medicine at the University of California, Los Angeles. E-mail: [email protected]. Aram A Namavar, MS, is a Student of Global Medicine at the Keck School of Medicine in Los Angeles, CA. E-mail: [email protected]. Jashin J Wu, MD, is the Director of Dermatology Research at the Los Angeles Medical Center in CA. E-mail: [email protected].

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 29 ORIGINAL RESEARCH & CONTRIBUTIONS Most Common Dermatologic Topics Published in Five High-ImpactMost Common General Dermatologic Medical Journals, Topics 1970-2012:Published in Melanoma, Five High-Impact Psoriasis, General Herpes Simplex, Medical Herpes Journals, Zoster, 1970-2012: and Acne Melanoma, Psoriasis, Herpes Simplex, Herpes Zoster, and Acne

Results herpes simplex (56) made up the next highest proportion of A total of 2627 articles dealing with at least 1 of the 24 der- topics, followed by abscess (35), urticaria (27), atopic dermatitis/ matologic topics mentioned in Table 1 were included in the eczema (26), and squamous cell carcinoma (22). study. From our combined data, the top 5 dermatologic topics Annals of Internal Medicine was the only journal wherein published in the 5 high-impact general medical journals were melanoma (22) was not the most common dermatologic topic. melanoma (708 articles), psoriasis (455), herpes simplex (366), In fact, melanoma was the fourth most prevalent. Preceding herpes zoster (253), and acne (165), as shown in Table 1. The melanoma in prevalent articles was herpes simplex (43), herpes Lancet had the highest total number of dermatologic publications zoster (33), and psoriasis (29); see Figure 1. (744), followed by British Medical Journal (661), NEJM (630), JAMA (419), and Annals of Internal Medicine (173). Discussion Melanoma was overwhelmingly the most common dermato- It has become customary for general practitioners to diagnose … certain logic topic in each of the journals except for Annals of Internal common skin conditions. For these physicians, primary sources dermatologic Medicine (Figure 1). In NEJM, the second most common topic for up-to-date information are general medical journals, namely topics with was psoriasis (100 articles), followed by herpes simplex (97) the five high-impact journals (NEJM, The Lancet, JAMA, British increased and herpes zoster (71). The other dermatologic topics were Medical Journal, and Annals of Internal Medicine). By study- relevance relatively uncommon in that journal. In The Lancet, the second ing the prevalence of common dermatologic topics published to internal most common topic was also psoriasis (144), followed by herpes in these journals, we attempted to provide insight into their medicine simplex (102) and acne (49). There were also notable contribu- emphasis on certain skin conditions. have greater tions to the dermatologic literature about herpes zoster (40), Of the five high-impact general medical journals, we found that The Lancet and British Medical Journal, which have their numbers of atopic dermatitis/eczema (40), urticaria (32), and abscess (28). In JAMA, herpes simplex (with 68 articles) was the second foundation in the United Kingdom, published more articles on publications. most common dermatologic topic, followed by psoriasis (48) common dermatologic topics. In the United Kingdom, physicians and herpes zoster (46). Acne (36), urticaria (30), and squamous must complete two years of foundation training and two years of cell carcinoma (22) followed in number of contributions. Mela- core medical training before entering dermatology as a specialty.3 noma (158) and psoriasis (134) were 2 greatly favored topics in This is in contrast to the US, where medical school graduates are the British Medical Journal. Herpes zoster (63), acne (60), and required to complete only one year of internal medicine, general surgery, or pediatrics internship before entering dermatology residency. Perhaps in the United Kingdom, dermatology is inte- grated more with internal medicine, leading to a greater number Table 1. Total umber of articles for each dermatologic topic of dermatologic publications in their general medical journals. Dermatologic topic Number In our analysis, we found that herpes simplex, herpes zoster, Abscess 95 and acne were three of the top five dermatologic topics published. Acne 165 This coincides with the fact that these topics were also among the Actinic keratosis 15 top ten dermatologic diagnoses made by internists.2 Melanoma Atopic dermatitis/eczema 88 and psoriasis, on the other hand, were the top two dermatologic Basal cell carcinoma 55 topics published but are diagnoses rarely made by internists.2 Carbuncle 0 As mentioned by Feldman et al,2 melanoma, despite being Cellulitis 62 rarely diagnosed by internists, is important to internal medicine Contact dermatitis 37 because of its serious nature. Some consider the early detection Epidermoid cyst 0 of melanoma, which has a 5-year survival rate of 98% if detected Furuncle 6 early and 15% with distant metastasis,4 to be the responsibility of 5 Herpes Simplex 366 primary care physicians. Furthermore, a “new era” of targeted Herpes Zoster 253 and immune-based therapies for melanoma has been ushered in 6 Impetigo 18 by recent advancements in melanoma research. Many of these Melanoma 708 findings have gained publication in prestigious general medical 7-9 Psoriasis 455 journals. It is not surprising, therefore, that melanoma was the most common dermatologic topic published in 4 of the 5 high- Pyoderma gangrenosum 29 impact general medical journals we studied. Rosacea 16 Psoriasis, like melanoma, is another diagnosis infrequently Seborrheic dermatitis 8 made by internists but was found in our study to be the second Seborrheic keratosis 6 most common dermatologic topic published. With a prevalence Squamous cell carcinoma 92 of 1% to 3%, psoriasis is likely to be encountered by general Stasis dermatitis 0 practitioners.10 Moreover, as a systemic inflammatory disease, Tinea 31 psoriasis is compounded by psoriatic arthritis in 10% to 30% of Urticaria 120 cases.10 Psoriasis has also been associated with a significantly Viral exanthem 3 increased risk of myocardial infarction, stroke, and peripheral Total 2627 vascular disease, possibly because of accelerated atherosclerosis

30 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS MostMost Common Dermatologic Dermatologic Topics Topics Published Published in Five in High-Impact Five High-Impact General General Medical Medical Journals, 1970-2012:Journals, 1970-2012: Melanoma, Psoriasis, Herpes Simplex, Herpes Zoster, and Acne Melanoma, Psoriasis, Herpes Simplex, Herpes Zoster, and Acne

Figure 1. Frequency of common dermatologic topics mentioned in five high-impact general medical journals. JAMA = Journal of the American Medical Association; NEJM = New England Journal of Medicine.

in the setting of an inflammatory state.11 These systemic manifes- Acknowledgment tations, as well as the increasing prevalence of this dermatologic Kathleen Louden, ELS, of Louden Health Communications provided condition, make psoriasis a very relevant disease to internal editorial assistance. medicine and the general medical journals. We acknowledge limitations in our study. Access to journal articles may have been References 1. Federman DG, Concato J, Kirsner RS. Comparison of dermatologic diagnoses limited by our university’s subscriptions, but all resources avail- by primary care practitioners and dermatologists. A review of the literature. able were used to obtain articles. Certain articles that addressed Arch Fam Med 1999 Mar-Apr;8(2):170-2. DOI: http://dx.doi.org/10.1001/ multiple topics were categorized under one topic, considered archfami.8.2.170. 2. Feldman SR, Fleischer AB Jr, McConnell RC. Most common dermatologic the best fit by the reviewer. We referenced a study by Feldman problems identified by internists, 1990-1994. Arch Intern Med 1998 Apr et al,2 who analyzed the National Ambulatory Medical Care 13;158(7):726-30. DOI: http://dx.doi.org/10.1001/archinte.158.7.726. Survey data from 1990 to 1994. Likely, diagnosing patterns of 3. Krishna SK, Jethwa AS. Navigating dermatology training in the United Kingdom. Indian J Dermatol Venereol Leprol 2013 May-Jun;79(3):444. DOI: skin disease by internists may have changed since then, but to http://dx.doi.org/10.4103/0378-6323.110810. our knowledge, no similar analysis has yet been performed. 4. Cancer Facts & Figures 2014 [Internet]. Atlanta, GA: American Cancer Society; 2014 [cited 2014 Jul 15]. Available from: www.cancer.org/acs/ groups/content/@research/documents/webcontent/acspc-042151.pdf. Conclusion 5. Fitzpatrick TB, Howell JB. The “missing link” in the chain of discovery of early We believe our study achieved its primary purpose, to analyze melanoma of the skin. Proc (Bayl Univ Med Cent) 2001 Oct;14(4):377. the prevalence of common dermatologic topics published in 6. Ascierto PA, Grimaldi AM, Acquavella N, et al. Future perspectives in melanoma research. Meeting report from the “Melanoma Bridge. Napoli, high-impact general medical journals. We have demonstrated December 2nd-4th 2012.” J Transl Med 2013 Jun 3;11:137. DOI: http:// that certain dermatologic topics with increased relevance to dx.doi.org/10.1186/1479-5876-11-137. internal medicine have greater numbers of publications. These 7. Hauschild A, Grob JJ, Demidov LV, et al. Dabrafenib in BRAF-mutated metastatic melanoma: a multicentre, open-label, phase 3 randomised findings are a testament to the value of these medical journals controlled trial. Lancet 2012 Jul 28;380(9839):358-65. DOI: http://dx.doi. in providing relevant yet comprehensive information to general org/10.1016/S0140-6736(12)60868-X. physicians, thus deserving the title of high-impact. v 8. Carvajal RD, Antonescu CR, Wolchok JD, et al. KIT as a therapeutic target in metastatic melanoma. JAMA 2011 Jun 8;305(22):2327-34. DOI: http://dx.doi. org/10.1001/jama.2011.746. Disclosure Statement 9. Sosman JA, Kim KB, Schuchter L, et al. Survival in BRAF V600-mutant Dr Wu received research funding from AbbVie, North Chicago, IL; advanced melanoma treated with vemurafenib. N Engl J Med 2012 Feb Amgen Inc, Thousand Oaks, CA; Coherus Biosciences, Redwood City, 23;366(8):707-14. DOI: http://dx.doi.org/10.1056/NEJMoa1112302. CA; Eli Lilly, Indianapolis, IN; Merck, Whitehouse Station, NJ; and 10. Velez NF, Wei-Passanese EX, Husni ME, Mody EA, Qureshi AA. Management of psoriasis and psoriatic arthritis in a combined dermatology and Pfizer, New York, NY, which were not directly related to this study. He rheumatology clinic. Arch Dermatol Res 2012 Jan;304(1):7-13. DOI: http:// is a consultant for AbbVie, North Chicago, IL; DUSA Pharmaceuticals dx.doi.org/10.1007/s00403-011-1172-6. Inc, Wilmington, MA; Eli Lilly, Indianapolis, IN; and Pfizer, New York, 11. Famenini S, Sako EY, Wu JJ. Effect of treating psoriasis on cardiovascular co- NY. Mr Choi and Mr Namavar have no conflicts of interest to disclose. morbidities: focus on TNF inhibitors. Am J Clin Dermatol 2014 Feb;15(1):45- No funding was received for this study. 50. DOI: http://dx.doi.org/10.1007/s40257-013-0052-6.

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 31 ORIGINAL RESEARCH & CONTRIBUTIONS Prevalence of Hypovitaminosis D and Its Association with Comorbidities of Childhood Obesity

Ronald Williams, MD, FAAP, FACP; Marsha Novick, MD; Erik Lehman, MS Perm J 2014 Fall;18(4):32-39 http://dx.doi.org/10.7812/TPP/14-016

infants and older adults, as well as people Abstract with limited sun exposure, dark skin, or Purpose: Our study sought to further delineate the prevalence of hypovitaminosis D fat malabsorption, and those who are and its relationship to comorbidities of childhood obesity. obese.5 Methods: We conducted a retrospective chart review from 155 obese children aged 5 The serum concentration of 25-hydroxy- to 19 years who attended the Penn State Children’s Hospital Pediatric Multidisciplinary vitamin D (25[OH]D) is the best indicator Weight Loss Program from November 2009 through November 2010. We determined of vitamin D status. The 25(OH)D that is the incidence of hypovitaminosis D and examined its association with comorbidities produced cutaneously or obtained from including elevated blood pressure, diabetes, acanthosis nigricans, depression, hyper- food and supplements has a fairly long lipidemia, hyperinsulinemia, and abnormal liver function test results, as well as age, circulating half-life of 15 days.6 Vitamin D sex, and geographic location. insufficiency is defined as a 25(OH)D Results: Under the latest Institute of Medicine definitions, vitamin D deficiency level of 21 to 29 ng/mL and vitamin D (< 20 ng/mL) and insufficiency (20-29 ng/mL) was present in 40% and 38% of children, deficiency as a 25(OH)D level below respectively. The prevalence of vitamin D deficiency was 27.8% in children aged 5 to 9 20 ng/mL, according to an Institute of years, 35.4% in children aged 10 to 14 years, and 50.9% of children aged 15 years or Medicine 2011 report.7 older. Older age, African-American race, winter/spring season, higher insulin level, total Since the mid-1990s, mean serum number of comorbidities, and polycystic ovary syndrome (in girls) were significantly 25(OH)D concentrations in the US have associated with vitamin D deficiency. African-American race, winter/spring season, slightly declined among males but not hyperinsulinemia, elevated systolic blood pressure, urban location, and total numbers females.8 This decline is probably caused of comorbidities were significantly associated with hypovitaminosis D (< 30 ng/mL). by reduced milk intake, inadequate sun Conclusions: Hypovitaminosis D is associated with several medical comorbidities exposure, greater use of sun protec- in obese children. Given the large percentage of children, even in our youngest age tion when outdoors, and simultaneous group, who are vitamin D deficient, obese children should be considered for routine increases in body weight.8 Obesity does vitamin D screening. not affect the skin’s capacity to synthe- size vitamin D. Rather, greater amounts Introduction obesity-related diseases, rarely seen in of subcutaneous fat sequester more of Obesity among children and adoles- children in the past, are increasingly be- the vitamin, making it less bioavailable 9 cents has continued to rise in epidemic ing diagnosed in pediatric patients; these to the body. proportions since the late 1970s. The obesity-associated conditions include Hypovitaminosis D has been consid- prevalence of obesity among children and obstructive sleep apnea, nonalcoholic ered a risk factor for glucose intolerance 10 adolescents in the US has tripled between fatty liver disease with resultant cirrho- and decreased insulin sensitivity. Serum 1976 and 2008,1 with a 2012 prevalence sis, and type 2 diabetes.3 In addition, 25(OH)D levels below 20 ng/mL have of 19.7% (females) and 17.2% (males) obesity is related to hypovitaminosis D been associated with decreased pancreatic 11 among those aged 6 to 12 years, and (vitamin D deficiency and insufficiency).4 β-cell function. It has also been found 20.4% (females) and 21.4% (males) among Vitamin D is a fat-soluble vitamin and that insulin sensitivity is as much as 60% those aged 12 to 19 years.2 Obesity rates is naturally present in only a small num- higher in individuals with serum 25(OH)D in general have plateaued since 2008, but ber of foods. Vitamin D can be added to levels of 30 ng/mL vs those with levels 11 rates for obesity Class 2 (120% of the 95th food, and it can be ingested as a dietary of 10 ng/mL. percentile or a body mass index [BMI] supplement. Vitamin D is produced en- Along with glucose intolerance, vitamin > 35 kg/m2) and Class 3 (140% of 95th dogenously when ultraviolet rays from D deficiency and insufficiency are associ- 12 percentile or BMI > 40 kg/m2) continue to sunlight strike the skin and trigger vitamin ated with obesity-related health diseases. increase.2 The obesity prevalence among D synthesis. Groups of people at risk of For instance, low vitamin D status may children is particularly alarming because vitamin D inadequacy include breastfed increase the risk of diabetes mellitus,

Ronald Williams, MD, FAAP, FACP, is a Professor of Pediatrics and Medicine at Penn State Hershey Children’s Hospital in PA. E-mail: [email protected]. Marsha Novick, MD, is an Assistant Professor of Pediatrics at Penn State Hershey Children’s Hospital in PA. E-mail: [email protected]. Erik Lehman, MS, is a Biostatistician in Public Health Services at Penn State Hershey Medical Center in PA. E-mail: [email protected].

32 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Prevalence of Hypovitaminosis D and Its Association with Comorbidities of Childhood Obesity

hypertension, cardiovascular disease,13 Children’s Hospital in Hershey, PA, and Multidisciplinary Weight Loss Program and certain types of cancer14,15 and has the association of hypovitaminosis D with from November 2009 through November been associated with greater severity of comorbidities of childhood obesity. 2010. Five children with missing or invalid critical illness.16 Vitamin D also plays a birth dates were excluded from the study, role in the liver, skeletal muscles,10 and Methods leaving 150 children for analysis. We did the immune system.10,17,18 In the present A retrospective chart review was con- not have a control group for comparison. study, we report the prevalence of vitamin ducted of 155 obese children and teenagers This multidisciplinary program has physi- D insufficiency and deficiency in obese aged 5 to 19 years who attended the Penn cians, nurses, and a dietitian who see pediatric patients at Penn State Hershey State Hershey Children’s Hospital Pediatric children and adolescents referred by their

Table 1. Associations of characteristics with vitamin D deficiency and hypovitaminosis D Vitamin D deficient, < 20 ng/mL Hypovitaminosis D, < 30 ng/mL Characteristic N Yes, n = 60 No, n = 90 p valuea Yes, n = 117 No, n = 33 p valuea Age, years (mean ± SD) 150 14.5 ± 3.1 12.7 ± 3.6 0.003 13.6 ± 3.4 12.7 ± 4.0 0.174 Age, years (%) 5-9 18 5 (27.8) 13 (72.2) 0.112 12 (66.7) 6 (33.3) 0.463 10-14 79 28 (35.4) 51 (64.6) 62 (78.5) 17 (21.5) ≥ 15 53 27 (50.9) 26 (49.1) 43 (81.1) 10 (18.9) Sex (%) Female 98 43 (43.9) 55 (56.1) 0.185 78 (79.6) 20 (20.4) 0.519 Male 52 17 (32.7) 35 (67.3) 39 (75.0) 13 (25.0) Race/ethnicity (%) White 91 23 (25.3) 68 (74.7) < 0.001 63 (69.2) 28 (30.8) 0.004 African American 29 23 (79.3) 6 (20.7) 29 (100.0) 0 (0.0) Hispanic 12 6 (50.0) 6 (50.0) 11 (91.7) 1 (8.3) Other 18 8 (44.4) 10 (55.6) 14 (77.8) 4 (22.2) Race (%) White 91 23 (25.3) 68 (74.7) < 0.001 63 (69.2) 28 (30.8) 0.003 Nonwhite 59 37 (62.7) 22 (37.3) 54 (91.5) 5 (8.5) Location (%) Rural 13 2 (15.4) 11 (84.6) 0.077 7 (53.8) 6 (46.2) 0.039 Urban 137 58 (42.3) 79 (57.7) 110 (80.3) 27 (19.7) Season (%) Winter 24 10 (41.7) 14 (58.3) 0.047 22 (91.7) 2 (8.3) 0.037 Spring 47 26 (55.3) 21 (44.7) 40 (85.1) 7 (14.9) Summer 48 13 (27.1) 35 (72.9) 36 (75.0) 12 (25.0) Fall 31 11 (35.5) 20 (64.5) 19 (61.3) 12 (38.7) Season (%) Winter/Spring 71 36 (50.7) 35 (49.3) 0.012 62 (87.3) 9 (12.7) 0.011 Summer/Fall 79 24 (30.4) 55 (69.6) 55 (69.6) 24 (30.4) Blood pressure, mm Hg Diastolic 147 65.7 ± 9.9 64.8 ± 8.5 0.536 65.7 ± 8.9 63.3 ± 9.4 0.18 Systolic 147 119.7 ± 15.6 117.0 ± 16.4 0.314 119.7 ± 16.8 112.4 ± 12.1 0.024 Heart rate, per minute 147 83.6 ± 12.8 86.7 ± 11.4 0.126 85.6 ± 12.3 84.9 ± 11.2 0.754 Lipids Total cholesterol, mg/dL 138 159.9 ± 30.9 165.1 ± 30.9 0.331 163.5 ± 29.9 161.3 ± 34.5 0.725 HDL cholesterol, mg/dL 138 39.8 ± 11.0 41.3 ± 10.6 0.405 40.8 ± 11.1 40.1 ± 9.6 0.733 LDL cholesterol, mg/dL 138 99.1 ± 25.5 102.4 ± 26.4 0.472 101.3 ± 24.5 100.4 ± 31.1 0.869 Triglycerides, mg/dL 138 109.0 ± 67.9 109.8 ± 57.8 0.94 110.0 ± 60.7 107.9 ± 67.0 0.873 AST, IU/L 131 26.1 ± 9.7 26.5 ± 9.1 0.811 26.0 ± 8.7 27.7 ± 11.3 0.388 ALT, IU/L 130 25.7 ± 21.9 25.9 ± 16.4 0.951 24.6 ± 18.4 30.1 ± 19.4 0.175

Hemoglobin A1c, % 136 5.6 ± 0.3 5.5 ± 0.3 0.233 5.5 ± 0.3 5.4 ± 0.2 0.09 Insulin, units 145 24.2 ± 20.6 14.8 ± 11.5 0.002 20.2 ± 17.6 12.8 ± 9.2 0.028 Total comorbidities, no. 150 4.1 ± 1.4 4.2 ± 1.4 0.652 4.1 ± 1.3 4.4 ± 1.7 0.396 (continued on next page)

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 33 ORIGINAL RESEARCH & CONTRIBUTIONS Prevalence of Hypovitaminosis D and Its Association with Comorbidities of Childhood Obesity

primary care provider who are obese as physician. The history included presence determine if the results were abnormal. defined by BMI. In children, obesity is of asthma, attention-deficit/hyperactivity Rural-urban commuting area code data defined as having a BMI at or above the disorder, constipation, depression, eating were used to categorize the patient’s resi- 95th percentile for age and sex. Most of disorders, gastroesophageal reflux disease, dence as either urban or rural on the basis our study population was at or above the hypertension, polycystic ovary syndrome of zip codes.19 These data were analyzed 99th percentile. [PCOS], and snoring. Pulse and blood to determine the prevalence of vitamin D Each patient underwent a complete his- pressure (BP) were measured in the of- insufficiency/deficiency and to assess for tory and physical examination, and data fice and were deemed high if above the its relationship to comorbidities. In addition from the medical history were recorded. 95th percentile for age and sex. Laboratory to those from the history, comorbidities Screening laboratory tests were ordered on values were obtained that included fast- included acanthosis nigricans, hyperlip- the basis of a full medical evaluation, which ing lipid profile, insulin, glucose, aspartate idemia, and abnormal liver function tests. included a 25(OH)D level. Parents and/or aminotransferase, alanine aminotransferase, Also assessed was the relationship between

patients provided the medical history by hemoglobin A1c (HbA1c), and 25(OH)D; vitamin D insufficiency/deficiency and the form and systematic questioning by the reference values for age were used to total number of comorbidities, insulin level,

(continued from previous page) Vitamin D deficient, < 20 ng/mL Hypovitaminosis D, < 30 ng/mL Characteristic N Yes, n = 60 No, n = 90 p valuea Yes, n = 117 No, n = 33 p valuea ADHD (%) Yes 17 7 (41.2) 10 (58.8) 0.916 14 (82.4) 3 (17.6) 0.765 No 133 53 (39.8) 80 (60.2) 103 (77.4) 30 (22.6) Acanthosis nigricans (%) Yes 89 35 (39.3) 54 (60.7) 0.839 69 (77.5) 20 (22.5) 0.866 No 61 25 (41.0) 36 (59.0) 48 (78.7) 13 (21.3) Asthma (%) Yes 24 9 (37.5) 15 (62.5) 0.785 16 (66.7) 8 (33.3) 0.149 No 126 51 (40.5) 75 (59.5) 101 (80.2) 25 (19.8) Depression (%) Yes 19 10 (52.6) 9 (47.4) 0.234 16 (84.2) 3 (15.8) 0.57 No 131 50 (38.2) 81 (61.8) 101 (77.1) 30 (22.9) Elevated systolic blood pressure (%) Yes 52 20 (38.5) 32 (61.5) 0.779 42 (80.8) 10 (19.2) 0.552 No 98 40 (40.8) 58 (59.2) 75 (76.5) 23 (23.5) GERD (%) Yes 16 5 (31.3) 11 (68.8) 0.452 12 (75.0) 4 (25.0) 1.0 No 134 55 (41.0) 79 (59.0) 105 (78.4) 29 (21.6) Hyperinsulinemia (%) Yes 61 30 (49.2) 31 (50.8) 0.056 52 (85.2) 9 (14.8) 0.074 No 84 28 (33.3) 56 (66.7) 61 (72.6) 23 (27.4) Hyperlipidemia (high total cholesterol, LDL cholesterol, or triglycerides) (%) Yes 64 19 (29.7) 45 (70.3) 0.027 47 (73.4) 17 (26.6) 0.247 No 86 41 (47.7) 45 (52.3) 70 (81.4) 16 (18.6) Hypertension (%) Yes 17 7 (41.2) 10 (58.8) 0.916 12 (70.6) 5 (29.4) 0.533 No 133 53 (39.8) 80 (60.2) 105 (78.9) 28 (21.1) PCOS (female only) (%) Yes 20 13 (65.0) 7 (35.0) 0.037 16 (80.0) 4 (20.0) 1.0 No 78 30 (38.5) 48 (61.5) 62 (79.5) 16 (20.5) Snoring (%) Yes 35 12 (34.3) 23 (65.7) 0.432 26 (74.3) 9 (25.7) 0.545 No 115 48 (41.7) 67 (58.3) 91 (79.1) 24 (20.9) a Logistic regression used for all comparisons, mean ± SD or no. (%). Boldface values indicate statistical significance. ADHD = attention-deficit/hyperactivity disorder; ALT = alanine aminotransferase; AST = aspartate aminotransferase; GERD = gastroesophageal reflux disease; HDL = high-density lipoprotein; LDL = low-density lipoprotein; PCOS = polycystic ovary syndrome; SD = standard deviation.

34 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Prevalence of Hypovitaminosis D and Its Association with Comorbidities of Childhood Obesity

sex, race, rural vs urban homestead, and tion process, but none were found to Results season of the year. None of the patients be significant to the model for either The characteristics of our study sample were taking more than 400 IU/day of outcome. The fit of the final logistic are shown in Table 1. Our population vitamin D (the recommended daily intake regression model was assessed using was 65% female, 91% urban, 61% white, of vitamin D per the American Academy the Hosmer-Lemeshow goodness-of-fit 19% African American, and 8% Hispanic. of Pediatrics20). The study was conducted test. Odds ratios were used to quantify Their most common medical comorbidi- with the permission of the Penn State the direction and magnitude of the ties included acanthosis nigricans (59%), Hershey institutional review board. association with the outcome of the hyperinsulinemia (42%), elevated systolic independent variables remaining in the BP at first visit (35%), PCOS (20%), asthma Statistical Analysis final model. (16%), attention-deficit/hyperactivity All analyses were carried out using SAS statistical software Version 9.3 (SAS Institute, Cary, NC). Descriptive statistics were generated for all variables using means, medians, and standard deviations for continuous variables and frequency tables for categorical variables. The season was defined by the laboratory date using the meteorologic definitions of the seasons by months. The outcome variables were defined in binary form for vitamin D insufficiency (< 30 ng/mL) and vitamin D deficiency (< 20 ng/mL). A bivariate analysis was performed to assess the association of these outcome variables with the various independent variables of interest using a logistic regression. This same analysis was stratified by categories: age, sex, race, and season to determine if any of the associations seen overall were manifested within 1 group more than in another. Because of a small number of children from a rural location, we were Figure 1. All season distribution of serum 25-hydroxyvitamin D levels (25[OH]D) (ng/mL). unable to stratify by location. On the basis of results of the overall bivariate analysis, a subset of clinically and statistically significant independent variables was chosen to be considered in a multivariate logistic regression for each outcome. The starting subset of variables to be considered included age, sex, race, location, season, systolic BP, insulin level, hyperlipidemia, and total comorbidities as a surrogate for the collection of individual comorbidities. Before doing any modeling, this subset of independent variables was tested for multicollinearity using variance infla- tion factor. From this subset, a final reduced set of significant independent variables was chosen for each outcome using a backward process of elimination with an inclusion criterion of p = 0.10. Two-way interactions were tested for significance between all independent variables remaining as significant in Figure 2. Distribution of serum 25-hydroxyvitamin D (25[OH]D) (ng/mL) in winter/spring the model after the backward elimina- collections.

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 35 ORIGINAL RESEARCH & CONTRIBUTIONS Prevalence of Hypovitaminosis D and Its Association with Comorbidities of Childhood Obesity

disorder (11%), gastroesophageal reflux disease (11%), constipation (7%), autism (7%), and binge eating disorder (6%). Vitamin D levels ranged from 5 to 60 ng/mL with a mean of 23 ng/mL. The prevalence of vitamin D deficiency (< 20 ng/mL) was 40% and insufficiency (20-30 ng/mL) was 38%; only 22% had a normal vitamin D level above 30 ng/mL (Figure 1). Stratifying these results by age group, 27.8% aged 5 to 9 years, 35.4% aged 10 to 14 years, and 50.9% aged 15 and older were vitamin D deficient. In bivariate analyses, older age, African- American race, winter/spring season (Figures 2 and 3), higher insulin level, hyperlipidemia (elevated total cholesterol, low-density lipoprotein, or triglycerides levels), and PCOS (female only) were significantly associated with vitamin D deficiency (Table 1). Some of these as- Figure 3. Distribution of serum 25-hydroxyvitamin D (25[OH]D) (ng/mL) in summer/fall sociations were also found with overall collections. hypovitaminosis D, including African- American race, winter/spring season, and BP; aspartate aminotransferase, alanine When the analysis was stratified by age

higher insulin level. Higher systolic BP aminotransferase, and HbA1c levels; category, sex, race, or season, several was significantly associated with hypovi- attention-deficit/hyperactivity disorder; significant associations were stronger in 1 taminosis D but not with vitamin D de- asthma; depression; gastroesophageal group than in another. For children age 10 ficiency. Urban location was significantly reflux disease; and snoring were not as- to 14 years, girls were more likely to be vita- associated with hypovitaminosis D and sociated with vitamin D deficiency or min D deficient than boys (43.4% vs 19.2%, trended toward significance for vitamin D hypovitaminosis D. p = 0.040). For children age 15 years and deficiency despite having a limited num- In the adjusted analysis, older age, non- older, a higher insulin level was significantly ber of children from rural locations. In an white race, rural location, winter/spring associated with being vitamin D deficient unadjusted comparison, the total number season, insulin, and total comorbidities (p = 0.007) or with having hypovita- of comorbidities was not associated with remained significantly associated with minosis D (p = 0.026). A stronger as- a low vitamin D level. However, when vitamin D deficiency (Table 2). These sociation was seen in female subjects controlling for all other variables in our same associations with hypovitaminosis D between urban location and vitamin D model, there was a significant association were sustained in a multivariate model deficiency (p = 0.009) or hypovitaminosis D with vitamin D deficiency, and leaning together except for older age. Elevated (p = 0.017), as well as between winter/ toward a significant association with hy- systolic BP was also associated with vita- spring season and vitamin D deficiency povitaminosis D. Sex; heart rate; diastolic min D insufficiency. (p = 0.029) or hypovitaminosis D (p = 0.013).

Table 2. Final multivariate models for vitamin D deficiency and hypovitaminosis Da Vitamin D deficient (< 20 ng/mL) Hypovitaminosis D (< 30 ng/mL) Characteristic Odds ratio (CI) p value Odds ratio (CI) p value Age (per 1-year increase) 1.24 (1.08-1.41) < 0.01 Eliminated — Sex (female vs male) Eliminated — Eliminated — Race (nonwhite vs white) 4.96 (2.01-11.71) < 0.01 4.02 (1.30-12.43) 0.02 Location (urban vs rural) 5.91 (1.03-33.81) 0.05 4.52 (1.15-17.76) 0.03 Season (winter/spring vs summer/fall) 3.69 (1.55-8.78) < 0.01 4.18 (1.57-11.12) < 0.01 Systolic blood pressure (per 1 mm Hg increase) Eliminated — 1.04 (1.01-1.07) 0.02 Insulin (per 1 µU/mL increase) 1.04 (1.01-1.07) 0.01 1.05 (1.0-1.10) 0.03 Total comorbidities (per 1 comorbidity decrease) 1.48 (1.06-2.08) 0.02 1.37 (0.99-1.92) 0.06 a All characteristics were considered for the final multivariate logistic regression model for both outcomes. The final set of variables for the model for each outcome was chosen using a backward process of elimination, and variables that were eliminated during this process are noted in the Table. Only variables with odds ratios and p values here are included in the final model. CI = confidence interval.

36 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Prevalence of Hypovitaminosis D and Its Association with Comorbidities of Childhood Obesity

Male subjects tended to have a greater as- problems. The exact reason for this is consistent observation that obesity is asso- sociation between a higher insulin level unknown, and further study in this area ciated with vitamin D deficiency.4 Insulin and vitamin D deficiency (p = 0.004) or may be warranted. levels have been shown to have seasonal hypovitaminosis D (p = 0.043). In whites, A few sex-based differences were variation with the highest levels in spring female subjects were more likely to be noted. Female subjects showed a seasonal compared with fall.25 This may explain vitamin D deficient than male subjects variation of being more likely to have low why all of the vitamin D sufficient subjects (31.7% vs 10.7%, p = 0.043), and winter/ vitamin D in winter/spring. Male subjects had normal insulin levels in the winter/ spring season had a more significant showed no seasonal variation. Male spring collection. Even with this seasonal association with both vitamin D defi- subjects showed higher mean systolic variation, 69.6% had hypovitaminosis D ciency (p = 0.038) and hypovitaminosis D BP and insulin levels as vitamin D levels and 30.4% were deficient in summer/fall (p = 0.028). There was a more pronounced dropped. This was not seen in female collections. This may lead the practitioner association between higher systolic BP subjects. Obese 10- to 14-year-old girls to consider the season with and vitamin D deficiency (p = 0.038) or are at higher risk of vitamin D deficiency borderline vitamin D results hypovitaminosis D (p = 0.021) in the sum- compared with boys the same age. The before supplementation rec- … older mer/fall seasons. exact relationship here is unknown. It may ommendations are given. children and be related to more outdoor activity for the For example, if it is fall and teenagers are Discussion boys, but this was not directly measured. the number is borderline, it most likely to The etiology of hypovitaminosis D is Race played an important factor. Afri- will likely decrease over the be vitamin D likely multifactorial because it has been can Americans had the lowest vitamin D winter/spring months. deficient … associated with several dietary factors21 as levels, with 100% being insufficient and Low vitamin D levels have [and] urban well as decreased sunlight exposure and 79.3% being deficient. Whites had much been associated with risk patients are 22 poor vitamin D intake. Our Pennsylva- lower prevalence. For those who were factors for Type 2 diabetes more likely nia prevalence of 77.8% (insufficient and vitamin D sufficient, 85% were white. mellitus (specifically insulin than rural … deficient) is less than that of a study in This is consistent with findings of previ- resistance but not HbA1c) in Texas that showed a prevalence of 92% ous studies looking at race.10,23 African obese children.21 We also of vitamin D insufficiency and deficiency Americans have skin pigmentation that found this to be true in our population, in 6- to 16-year-old obese patients,21 and reduces vitamin D production, and from as shown by its associations with overall more than 90% in 17-year-old obese teens about puberty onward, vitamin D intake BMI, hyperinsulinemia, and PCOS. Hy- in Rhode Island.9 Our study did not look is also generally below recommended perinsulinemia was particularly predictive into milk intake or specific dietary sources levels.23 It has been recently shown that in the age group 15 years and older, in of vitamin D consumption or sunlight African Americans can have lower vita- which 80% were vitamin D deficient (odds exposure. We found that nonwhite race, min D and vitamin D binding protein ratio = 10, p < 0.001). Insulin resistance is elevated systolic BP, hyperinsulinemia, levels, which may actually lead to similar also part of PCOS, and we found associa- multiple comorbidities, urban location, levels of bioavailable vitamin D compared tions with both. In another study, 72.8% and winter/spring collection of blood with whites.24 Thus, our current “normal” of women with PCOS were vitamin D samples were associated with hypovita- values for vitamin D may need to be ad- insufficient.26 minosis D. justed for this population. Further study Serum triglyceride levels and systolic Our findings suggest that older chil- in this area is needed. BPs have been linked to vitamin D defi- dren and teenagers are most likely to be We found a strong link with seasonality ciency.27 Our study overall showed that vitamin D deficient. Across age groups, in the winter and spring collections. There elevated systolic BP was predictive for urban patients are more likely than rural was a 3.7-fold greater likelihood of being hypovitaminosis D, but not deficiency. patients to be vitamin D deficient. In mul- vitamin D deficient and a 4.2-fold greater For male subjects, however, it was pre- tivariate analysis, this was still significant likelihood of having hypovitaminosis D dictive of both, with higher systolic BPs for overall hypovitaminosis D. Diet and in these seasons compared with sum- in the deficiency group. We did not find sunlight exposure probably played a role, mer and fall collections. This is probably an association with fasting triglycerides but these data were not collected. secondary to decreasing sun exposure in or cholesterol levels, but we did find an After multivariate analysis, we found a late fall into winter and poor bioavailable association with hyperlipidemia in general significant association with total number Vitamin D stores. Vitamin D is fat soluble for any elevation in total cholesterol, LDL, of comorbidities and vitamin D deficiency, and is readily stored in adipose tissue, or triglycerides levels. and the association with hypovitaminosis D and may be sequestered in a larger body It is difficult to precisely predict the almost reached statistical significance. This pool of fat of obese individuals.4 People exact amount of sunlight required to pro- may be an overall reflection of general obtain most of their vitamin D require- duce enough vitamin D for each individ- health status. Vitamin D is part of many ment from casual exposure to sunlight. It ual, and there are some health concerns physiologic pathways, and its role in has been shown that there is more than relating excessive sun exposure to skin many illnesses is still not completely 50% decreased bioavailability of cutane- cancer risks in adulthood.10 Therefore,

understood. These results may imply its ous synthesized vitamin D3 in obese adult it is important to encourage protected cumulative involvement in obesity-related subjects, and this likely accounts for the sun exposure for children and teenagers.

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 37 ORIGINAL RESEARCH & CONTRIBUTIONS Prevalence of Hypovitaminosis D and Its Association with Comorbidities of Childhood Obesity

However, this practice may translate into to causality, and insufficient to inform 2. Skinner AC, Skelton JA. Prevalence and trends 7 in obesity and severe obesity among children insufficient endogenous vitamin D pro- nutritional requirements. in the United States, 1999-2012. JAMA Pediatr duction. It is then necessary to encourage In this study, African-American race, 2014 Jun;168(6):561-6. DOI: http://dx.doi. dietary supplementation of vitamin D. winter/spring season, urban location, org/10.1001/jamapediatrics.2014.21. 3. Crocker MK, Yanovski JA. Pediatric obesity: This is needed to normalize vitamin D and higher insulin level were significantly etiology and treatment. Endocrinol Metab Clin levels and may temper insulin resistance, associated with vitamin D deficiency and North Am 2009 Sep;38(3):525-48. DOI: http:// thus possibly delaying the onset of overall hypovitaminosis D. These, along dx.doi.org/10.1016/j.ecl.2009.06.007. 4. Wortsman J, Matsuoka LY, Chen TC, Lu Type 2 diabetes mellitus (although this with elevated systolic BP, urban location, Z, Holick MF. Decreased bioavailability of has not been demonstrated). Because total number of comorbidities, and PCOS vitamin D in obesity. Am J Clin Nutr 2000 most of our patients had hypovitamino- (in female subjects only) were also associ- Sep;72(3):690-3. Erratum in: Am J Clin Nutr 2003 May;77(5):1342. sis D and vitamin D supplementation is ated with hypovitaminosis D. 5. Vitamin D [Internet]. Bethesda, MD: Office of relatively safe, the argument could be The American Academy of Pediatrics Dietary Supplements, National Institutes of made to supplement all obese children Expert Committee, regarding the assess- Health; c2014 [cited 2014 May 27]. Available from: http://ods.od.nih.gov/factsheets/list-all/ with vitamin D and forego lab testing. ment, prevention, and treatment of child VitaminD/. This, however, would not pick up the and adolescent overweight and obesity, 6. Jones G. Pharmacokinetics of vitamin D toxicity. vitamin D deficient children and would does not currently recommend assess- Am J Clin Nutr 2008 Aug;88(2):582S-586S. 29 7. Ross AC, Manson JE, Abrams SA, et al. The not adequately meet their replacement ing vitamin D status in obese children. 2011 report on dietary reference intakes for needs. In a study by Heaney et al28 of Given the large percentage of children, calcium and vitamin D from the Institute of response to oral dosing of vitamin D, it even in our youngest age group who are Medicine: what clinicians need to know. J Clin Endocrinol Metab 2011 Jan;96(1):53-8. DOI: can be extrapolated from data in men vitamin D deficient, routine screening of http://dx.doi.org/10.1210/jc.2010-2704. older than age 20 years that to raise vitamin D should be considered in obese 8. Looker AC, Pfeiffer CM, Lacher DA, the serum vitamin D concentration by children and supplementation when Schleicher RL, Picciano MF, Yetley EA. Serum 25-hydroxyvitamin D status of the US 1 ng/mL would require roughly 140 IU needed. Supplementation has been found population: 1988-1994 compared with 2000- of cholecalciferol daily. There may be helpful in patients with systemic lupus 2004. Am J Clin Nutr 2008 Dec;88(6):1519- different responses to supplementation erythematosus and hypovitaminosis D, 27. DOI: http://dx.doi.org/10.3945/ ajcn.2008.26182. based on race, with whites normaliz- as it improved inflammatory markers and 9. Harel Z, Flanagan P, Forcier M, Harel D. Low ing quicker than Hispanics or African disease activity.17 Vitamin D screening is vitamin D status among obese adolescents: Americans.9 more likely to have abnormal results with prevalence and response to treatment. J Adolesc Health 2011 May;48(5):448-52. DOI: http:// Limitations of the present study are any of the following: older age, nonwhite dx.doi.org/10.1016/j.jadohealth.2011.01.011. small sample sizes for age group com- race, elevated systolic BP, hyperinsu- 10. Alemzadeh R, Kichler J, Babar G, Calhoun parisons and from rural homes. Data on linemia, multiple comorbidities, PCOS, M. Hypovitaminosis D in obese children and adolescents: relationship with adiposity, insulin dietary vitamin D (especially milk intake), urban location, or winter/spring collection sensitivity, ethnicity, and season. Metabolism sun exposure, and sunscreen use were of blood samples. Seasonal variations of 2008 Feb;57(2):183-91. DOI: http://dx.doi. not obtained as this was a retrospective vitamin D levels should also be consid- org/10.1016/j.metabol.2007.08.023. 11. Chiu KC, Chu A, Go VL, Saad MF. study and these data were not routinely ered when recommending supplementa- Hypovitaminosis D is associated with insulin collected. In addition, data were not col- tion. Further study is needed to see if resistance and beta cell dysfunction. Am J Clin lected on parameters that could affect vitamin D supplementation will have Nutr 2004 May;79(5):820-5. 12. Holick MF. Vitamin D: importance in the insulin levels, such as amount of physical an impact on preventing further weight prevention of cancers, type 1 diabetes, heart activity, medication use, hours of sleep, gain or preventing possible comorbidi- disease, and osteoporosis. Am J Clin Nutr 2004 or a family history of diabetes and PCOS. ties such as hyperinsulinemia, diabetes, Mar;79(3):362-71. 13. Freedman DS, Dietz WH, Srinivasan SR, Our subjects were obese children from and PCOS. v Berenson GS. The relation of overweight to central Pennsylvania who were referred cardiovascular risk factors among children and adolescents: the Bogalusa Heart Study. for weight management, which may not Disclosure Statement Pediatrics 1999 Jun;103(6 Pt 1):1175-82. DOI: be representative of all obese children. The author(s) have no conflicts of interest http://dx.doi.org/10.1542/peds.103.6.1175. Despite these limitations, these results to disclose. 14. Giovannucci E, Liu Y, Rimm EB, et al. Prospective study of predictors of vitamin D status and show that there are multiple associations cancer incidence and mortality in men. J Natl for hypovitaminosis D, and these findings Acknowledgment Cancer Inst 2006 Apr 5;98(7):451-9. DOI: http:// are likely applicable to all obese children Kathleen Louden, ELS, of Louden Health dx.doi.org/10.1093/jnci/djj101. Communications provided editorial 15. Abbas S, Linseisen J, Chang-Claude J. in the US. Our study looked only at as- assistance. Dietary vitamin D and calcium intake and sociations and did not show causality. premenopausal breast cancer risk in a German case-control study. Nutr Cancer References 2007;59(1):54-61. DOI: http://dx.doi. Conclusion 1. Ogden C, Carroll M. Prevalence of obesity org/10.1080/01635580701390223. Hypovitaminosis D has many ex- among children and adolescents: United 16. McNally JD, Menon K, Chakraborty P, et al; States, trends 1963-1965 through 2007-2008 traskeletal associations, including cancer, Canadian Critical Care Trials Group. The [Internet]. Atlanta, GA: Centers for Disease association of vitamin D status with pediatric cardiovascular disease, diabetes, and Control and Prevention; 2010 Jun [cited 2014 critical illness. Pediatrics 2012 Sep;130(3): autoimmune disorders. Previous evidence May 27]. Available from: www.cdc.gov/nchs/ 429-36. DOI: http://dx.doi.org/10.1542/ data/hestat/obesity_child_07_08/obesity_ peds.2011-3059. has been inconsistent, inconclusive as child_07_08.pdf.

38 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Prevalence of Hypovitaminosis D and Its Association with Comorbidities of Childhood Obesity

17. Abou-Raya A, Abou-Raya S, Helmii M. The 21. Olson ML, Maalouf NM, Oden JD, White 27. Zhou P, Schechter C, Cai Z, Markowitz M. effect of vitamin D supplementation on PC, Hutchison MR. Vitamin D deficiency Determinants of 25(OH)D sufficiency in inflammatory and hemostatic markers and in obese children and its relationship to obese minority children: selecting outcome disease activity in patients with systemic glucose homeostasis. J Clin Endocrinol Metab measures and analytic approaches. J Pediatr lupus erythematosus: a randomized 2012 Jan;97(1):279-85. DOI: http://dx.doi. 2011 Jun;158(6):930-4.e1. DOI: http://dx.doi. placebo-controlled trial. J Rheumatol 2013 org/10.1210/jc.2011-1507. org/10.1016/j.jpeds.2010.11.034. Mar;40(3):265-72. DOI: http://dx.doi. 22. Palacios C, Gil K, Pérez CM, Joshipura K. 28. Heaney RP, Davies KM, Chen TC, Holick org/10.3899/jrheum.111594. Determinants of vitamin D status among MF, Barger-Lux MJ. Human serum 18. Science M, Maguire JL, Russell ML, Smieja M, overweight and obese Puerto Rican adults. 25-hydroxycholecalciferol response to extended Walter SD, Loeb M. Low serum 25-hydroxy- Ann Nutr Metab 2012;60(1):35-43. DOI: http:// oral dosing with cholecalciferol. Am J Clin Nutr vitamin D level and risk of upper respiratory dx.doi.org/10.1159/000335282. 2003 Jan;77(1):204-10. Erratum in: Am J Clin tract infection in children and adolescents. Clin 23. Harris SS. Vitamin D and African Americans. J Nutr 2003 Nov;78(5):1047. Infect Dis 2013 Aug;57(3):392-7. DOI: http:// Nutr 2006 Apr;136(4):1126-9. 29. Barlow SE; Expert Committee. Expert dx.doi.org/10.1093/cid/cit289. 24. Powe CE, Evans MK, Wenger J, et al. Vitamin committee recommendations regarding 19. RUCA Data [Internet]. Seattle, WA: WWAMI D-binding protein and vitamin D status of black the prevention, assessment, and treatment Rural Health Research Center; 2004 [cited 2014 Americans and white Americans. N Engl J Med of child and adolescent overweight and Jul 17]. Available from: http://depts.washington. 2013 Nov 21;369(21):1991-2000. DOI: http:// obesity: summary report. Pediatrics 2007 edu/uwruca/ruca-download.php. dx.doi.org/10.1056/NEJMoa1306357. Dec;120 Suppl 4:S164-92. DOI: http://dx.doi. 20. Wagner CL, Greer FR; American Academy of 25. Behall KM, Scholfield DJ, Hallfrisch JG, Kelsay JL, org/10.1542/peds.2007-2329C. Pediatrics Section on Breastfeeding; American Reiser S. Seasonal variation in plasma glucose Academy of Pediatrics Committee on Nutrition. and hormone levels in adult men and women. Prevention of rickets and vitamin D deficiency Am J Clin Nutr 1984 Dec;40(6 Suppl):1352-6. in infants, children, and adolescents. Pediatrics 26. Wehr E, Pilz S, Schweighofer N, et al. Asso- 2008 Nov;122(5):1142-52. DOI: http://dx.doi. ciation of hypovitaminosis D with metabolic org/10.1542/peds.2008-1862. Erratum in: disturbances in polycystic ovary syndrome. Eur J Pediatrics 2009 Jan;123(1):197. DOI: http:// Endocrinol 2009 Oct;161(4):575-82. DOI: http:// dx.doi.org/10.1542/peds.2008-3365. dx.doi.org/10.1530/EJE-09-0432.

Vitamins

It is now known that all these diseases, with the exception of pellagra, can be prevented and cured by the addition of preventive substance; the deficient substances, which are of the nature of organic bases, we will call “vitamins.”

— Casimir Funk, 1884-1967, Polish biochemist who is generally credited to be among the first to formulate the concept of vitamins

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 39 ORIGINAL RESEARCH & CONTRIBUTIONS A Pilot Study Comparing Anatomic Failure after Sacrocolpopexy with Absorbable or Permanent Sutures for Vaginal Mesh Attachment

Jasmine Tan-Kim, MD, MAS; Shawn A Menefee, MD; Quinn Lippmann, MD, MPH; Emily S Lukacz, MD, MAS; Karl M Luber, MD; Charles W Nager, MD Perm J 2014 Fall;18(4):40-44 http://dx.doi.org/10.7812/TPP/14-022

to the anterior longitudinal ligament overlying the sacrum at Abstract levels S1 to S2. A recent comprehensive review of sacrocol- Objectives: To describe anatomic failure rates for sacrocol- popexy and 7-year follow-up data from a randomized trial of popexy in groups receiving either delayed absorbable or perma- sacrocolpopexy with or without Burch urethropexy describe nent monofilament suture for mesh attachment to the vagina. a reoperation rate for prolapse of only 2.2% to 5.1%.2,3 Methods: We reviewed the medical records of 193 women Clinicians often use permanent suture to anchor the who underwent sacrocolpopexy with 2 different types of mesh to the vagina. Between our 2 institutions, during the sutures attaching polypropylene mesh to the vagina: delayed previous 15 years, we are aware of at least 5 cases in which absorbable sutures (median follow-up, 43 weeks) and perma- permanent monofilament suture has eroded into the bladder nent sutures (median follow-up, 106 weeks). Vaginal apical after sacrocolpopexy. These erosions presented many years failure was defined as Point C greater than or equal to half after the index surgery despite the fact that intraoperative of the total vaginal length. Anterior-posterior compartmental cystoscopic findings were noted to be normal. failures were defined as Point Ba and/or Point Bp more than Recent data suggest that permanent sutures may not be 2 0 cm. Fisher exact and c tests were used to compare failure necessary. Porcine models demonstrate that 74% of the rates. There were no documented suture erosions in the delayed final strength of tissue ingrowth into polypropylene mesh absorbable monofilament suture group during the review pe- is already achieved by 2 weeks after implantation, and riod. Two patients in the permanent suture group were found maximum strength occurs by 3 months.4 Delayed absorb- to have permanent suture in the bladder more than 30 weeks able monofilament suture (polydioxanone or polyglyconate) after the index procedure. loses 50% of its tensile strength by 4 weeks, 100% by 2 to 3 Results: Failure rates for the 45 subjects in the delayed months, and complete mass absorption by 6 to 8 months.5 In absorbable group and 148 subjects in the permanent suture a recent large series of sacrocolpopexy vaginal erosions, 3 of group were similar (4.4% vs 3.4%, p = 0.74) and not statisti- 20 erosions were suture only.6 Therefore, the use of absorb- cally different in any compartment: apical (0% vs 1.4%, p = able sutures for mesh attachment during sacrocolpopexy is 0.43), anterior (4.4% vs 2%, p = 0.38), or posterior (0% vs appealing because the risk of long-term suture exposure or 1.4%, p = 0.43). knots eroding into the bladder would likely be eliminated. Conclusions: Delayed absorbable monofilament suture ap- For these reasons, some of the surgeon authors (SAM and pears to be a reasonable alternative to permanent suture for KML) began using delayed absorbable monofilament suture mesh attachment to the vagina during sacrocolpopexy. The (polydioxanone [PDSII], Ethicon Inc, Somerville, NJ, or use of delayed absorbable suture could potentially prevent polyglyconate [Maxon], Covidien AG, Mansfield, MA) to complications of suture erosion into the bladder or vagina attach, in 2008, Type 1 polypropylene mesh to the vagina. remote from the time of surgery. The purpose of this study was to compare anatomic objective failure rates for minimally invasive sacrocol- Introduction popexy using delayed absorbable vs permanent monofila- Sacrocolpopexy is a commonly performed technique for ment suture for mesh attachment to the vagina. It was our treating apical prolapse. Abdominal sacrocolpopexy was first hypothesis that the objective failure rates would not be described by Arthure and Savage1 in 1957. The basic principles significantly different between suture types because tissue of sacrocolpopexy involve the attachment of a graft or mesh ingrowth into mesh would occur by the time the delayed to the vagina while affixing the proximal end of the mesh absorbable sutures lost their tensile strength.

Jasmine Tan-Kim, MD, MAS, is a Female Pelvic Medicine and Reconstructive Surgeon at the Kaiser Permanente San Diego Medical Center in CA. E-mail: [email protected]. Shawn A Menefee, MD, is the Division Chief in Female Pelvic Medicine and Reconstructive Surgery at the Kaiser Permanente San Diego Medical Center in CA. E-mail: [email protected]. Quinn Lippmann, MD, MPH, is a Female Pelvic Medicine and Reconstructive Surgery Fellow at the University of California, San Diego and the Kaiser Permanente San Diego Medical Center. E-mail: [email protected]. Emily S Lukacz, MD, MAS, is the Fellowship Director for Female Pelvic Medicine and Reconstructive Surgery at the University of California, San Diego. E-mail: [email protected]. Karl M Luber, MD, is a Female Pelvic Medicine and Reconstructive Surgeon at the Kaiser Permanente San Diego Medical Center in CA. E-mail: [email protected]. Charles W Nager, MD, is the Division Chief for Female Pelvic Medicine and Reconstructive Surgery at the University of California, San Diego. E-mail: [email protected].

40 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS A Pilot Study Comparing Anatomic Failure after Sacrocolpopexy with Absorbable or Permanent Sutures for Vaginal Mesh Attachment

Figure 1. Enrollment of study subjects. POP-Q = pelvic organ prolapse quantification.

Methods (polypropylene) sutures for mesh attachment to the vagina This retrospective cohort study was approved by the in- and 2) at least 1 follow-up visit with a pelvic organ prolapse stitutional review board. The study included women who quantification8 performed 12 weeks or more after surgery. underwent minimally invasive sacrocolpopexy performed at Data were extracted from the electronic medical record the 2 institutions in our fellowship training program between and hospital charts. Demographic data and baseline and November 2004 and January 2010. All subjects underwent sac- postoperative pelvic organ prolapse quantification measures rocolpopexy using either robotic-assisted laparoscopy or con- were collected from eligible subjects. Operative techniques ventional laparoscopy. Details of our operative procedure have and complications were abstracted from the hospital records. been published.7 In brief summary, our technique consisted of Postoperative follow-up visits, including pelvic organ prolapse anterior and posterior leaflets of polypropylene mesh with at quantification and the detection of suture complications, were least 6 sutures placed on each leaflet to secure the mesh to the also documented. vaginal surface. Inclusion criteria were as follows: 1) operative Our primary outcome was objective apical failure defined report documentation of delayed absorbable monofilament as Point C greater than or equal to half of the total vaginal (polydioxanone or polyglyconate) or permanent monofilament length and/or objective failure of the anterior and posterior

Table 1. Demographic data Delayed Permanent sutures, Demographic variable absorbable sutures, n = 45 n = 148 p value Mean age ± SD (years) 60 ± 9 61 ± 9 0.854a Median (range) follow-up duration, in weeks 43 (12-272) 106 (12-372) 0.007b Median (range) time to failure for primary or secondary 58 (55-61) 6 (5-181) 0.143b outcomes, in weeks Median preoperative stage of prolapse (mean) 3 (3.0) 3 (2.8) 0.002b Concomitant surgery, no. (%) Procedure for repair of pelvic organ prolapse 16 (36.0) 38 (26.0) 0.196c Anterior colporrhaphy 0 (0) 8 (5.1) 0.336c Posterior colporrhaphy 13 (29.0) 28 (18.9) 0.152c Paravaginal repair 5 (11.1) 12 (8.1) 0.534c Hysterectomy 32 (71.9) 61 (41.2) 0.001c a Student t test. b Nonparametric testing. c Chi-squared test. SD = standard deviation.

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 41 ORIGINAL RESEARCH & CONTRIBUTIONS A Pilot Study Comparing Anatomic Failure after Sacrocolpopexy with Absorbable or Permanent Sutures for Vaginal Mesh Attachment

compartments, which we defined as Point Ba and/or Point Bp No difference was seen in the objective failure rates in the more than 0 cm. We performed analysis using this definition robotic surgery group (3.4%, n = 2) vs the laparoscopic surgery of prolapse because it appears to be the most appropriate group (3.7%, n = 5). definition for surgical success. Barber et al9 suggested that Of the 7 overall subjects with anatomic failure at the hy- beyond the hymen might correlate more highly with subjec- men or beyond, 3 (43%) were asymptomatic, 3 (43%) were tive symptoms of surgical failure. This definition was used symptomatic but declined reoperation (with 1 of them using in the large randomized trial of sacrocolpopexy (Colpopexy a pessary), and 1 (14%) was scheduled for reoperation. The and Urinary Reduction Efforts, or CARE), whose results were subject planning reoperation with an anterior colporrhaphy published in 2013.3 was in the permanent suture group. The records of subjects who were determined There were no documented suture erosions in the delayed … there is to have anatomic failures were further reviewed. absorbable monofilament suture group during the review pe- Data were abstracted whether the patients re- riod. Two patients in the permanent suture group were later sufficient ported being asymptomatic, being symptomatic found to have permanent suture in the bladder. One patient tissue but declining surgery, or if they underwent presented at 47 weeks after her surgery with urinary frequency ingrowth repeated operation for prolapse. and nocturia. She was noted to have microscopic hematuria into the Chi squared tests and Fisher exact tests were and underwent cystoscopy, revealing a suture in the bladder, polypropylene used to evaluate dichotomous variables; Stu- which was removed cystoscopically. Urinary symptoms sub- mesh during dent’s t test was used for continuous, normally sequently improved. The second patient presented 32 weeks the period distributed data; and Wilcoxon rank tests were after surgery with large-volume urinary leakage, which devel- of adequate used to compare nonparametric variables. Odds oped only immediately before presentation. She was noted suture tensile ratios (ORs) and 95% confidence intervals (CIs) to have a vesicovaginal fistula with polypropylene (Prolene) strength are reported. A p value of less than 0.05 was suture and mesh visible in the bladder. Two patients were to prevent considered statistically significant. Statistical noted to have polypropylene suture in the vagina remotely analysis was performed with PASW Statistics 18 after surgery at postoperative weeks 30 and 279. failure. (IBM, Armonk, NY). Vaginal mesh erosion rates were 17% in the permanent su- ture group and 13% in the delayed absorbable suture group, Results a difference that was not statistically significant (p = 0.385). A total of 261 women underwent minimally invasive sacro- Concomitant hysterectomy was performed in 41% of the per- colpopexy at our institutions during the study period, and 74% manent suture group and 72% of the delayed absorbable suture had sufficient data to be included in the analysis (Figure 1). group (p = 0.001). There was a significant difference in the Of the 26% who were not included in the study, there were mesh erosion rate among participants receiving a concurrent no significant differences in age, parity, body mass index, or hysterectomy vs the subjects who did not undergo a hysterec- preoperative stage of prolapse between the subjects included tomy at the time of sacrocolpopexy (23% vs 10%, p = 0.014). in the analysis (data not shown). Of those included, there were no differences in mean age, median follow-up dura- Discussion tion (or range), median (or range) time to failure for primary In this preliminary analysis of the use of delayed absorb- or secondary outcomes, or rates of concomitant surgery for able monofilament suture (polydioxanone or polyglyconate) pelvic organ prolapse between the delayed absorbable and to secure polypropylene mesh to the vagina, apical failure permanent suture groups (Table 1). On nonparametric testing, rates were low, and we did not identify increases in objective the delayed absorbable group had statistically but not clini- failure rates compared with permanent monofilament suture cally worse preoperative stage compared with the permanent in patients with more than 12 weeks of follow-up. On the suture group. basis of these data and the biochemical properties of the The anatomic objective failure rates for the different su- delayed absorbable suture, we believe that there is sufficient ture groups were similar and not statistically different for the tissue ingrowth into the polypropylene mesh during the participants with at least 12 weeks of follow-up (Table 2). period of adequate suture tensile strength to prevent failure.

Table 2. Anatomic failures Delayed absorbable sutures, Permanent sutures, Odds ratio Anatomic failure n = 45, no. (%) n = 148, no. (%) (95% CI) p value Overall failure by definition 2 (4.4) 5 (3.4) 1.33 (0.25-7.10) 0.738 a Apical point (C > half of total vaginal length) 0 (0) 2 (1.4) — 0.433 a b Anterior compartment point (Ba > 0 cm) 2 (4.4) 3 (2.0) 2.2 (0.36-13.80) 0.376 Posterior compartment point (Bp > 0 cm) 0 (0) 2 (1.4)a — 0.433b a Three subjects in the permanent sutures group and 0 subjects in the delayed absorbable sutures group with simultaneous multicompartment failure. b Fisher exact test. CI = confidence interval.

42 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS A Pilot Study Comparing Anatomic Failure after Sacrocolpopexy with Absorbable or Permanent Sutures for Vaginal Mesh Attachment

The choice of sutures and mesh material used during pel- basis of a previous publication, we have determined that there vic reconstruction is an important one. In a study of sacros- is a 6-fold increase in vaginal mesh erosion when associated pinous ligament suspensions, braided polyester permanent with hysterectomy.13 We noted a significant difference in the suture had an unacceptably high rate (36%) of suture-related mesh erosion rate between patients receiving a concurrent complications such as suture erosion, persistent granulation hysterectomy (23%) and those who did not (10%). tissue, and persistent vaginal bleeding that required suture Even though our absorbable mesh group had slightly removal in 70% of cases.10 Sacrocolpopexies with expanded worse preoperative median prolapse, which should have polytetrafluoroethylene (Gore-Tex, WL Gore and Associates, biased this group to more failures, this was not observed. Flagstaff, AZ) mesh were associated with a 4-fold higher risk Most of the failures were in the anterior and posterior com- of erosion, and most clinicians have opted not to use this partments, which may not be related at all to surgical failure material in their practices.6 since these more distal compartments may not have received Permanent monofilament suture has been widely used adequate support from the sacrocolpopexy. for securing mesh to the vagina during the sacrocolpopexy The strengths of this study are its moderately large sample procedure. The rationale for the use of permanent suture size, inclusion of 74% of subjects, use of the standardized ����pel- is to secure the mesh to provide a durable repair with a vic organ prolapse quantification, a contemporaneous study theoretical lower rate of failure than that with absorbable period, and the long follow-up duration. suture. Vaginal suture erosions are often considered less Limitations of this study are primarily related to its ret- morbid than mesh erosions; however, the etiology of vaginal rospective nature and nonstandardized follow-up intervals. mesh erosion is not completely understood, especially in the This study took place at two institutions with seven differ- absence of a colpotomy. It has been postulated that if the ent surgeons performing these procedures. All surgeons are sutures that secure the mesh to the vagina traverse the full fellowship-trained urogynecologists. There was substantial thickness of the vagina, vaginal bacteria may travel along overlap in the study period, with permanent suture being used the suture to colonize the mesh.6 If this theory is true, the from 2004 to 2010, whereas the delayed absorbable suture presence of permanent suture securing the mesh to vagina was used by two of the seven surgeons from 2008 to 2010. places patients at risk of erosion, even many years after More patients in the delayed absorbable suture group had a surgery. We observed 2 permanent suture erosions into the hysterectomy at the time of surgery, and this could potentially bladder occurring more than 30 weeks after surgery. influence the results. Two different surgical modalities were There is very limited literature comparing the use of used for the sacrocolpopexy, although there was no difference monofilament absorbable suture vs permanent suture when in failure rates between the robotic and laparoscopic groups. mesh is attached to the vagina. One study by Maher et al11 A further limitation of our study is that our results were purely compared laparoscopic sacrocolpopexy with vaginal mesh- objective, and we do not have reliable subjective symptoms for reinforced repairs. The laparoscopic sacrocolpopexy subjects the anatomic success group. Subjective data were specifically (n = 53) had their mesh attached to the vagina using delayed collected from the patients if their operation failed. absorbable monofilament suture and had a 77% objective success rate after 6-month follow-up. The study did not Conclusion compare success rates for absorbable vs permanent sutures.11 We consider delayed absorbable polydioxanone or polyg- One retrospective abdominal sacrocolpopexy study compar- lyconate suture to be a reasonable alternative to permanent ing the use of braided, permanent, polyester sutures (2-0 monofilament sutures to potentially prevent complications Ethibond Excel, Ethicon, Somerville, NJ) with monofilament of suture erosion into the bladder or vagina remote from delayed absorbable (2-0 polydioxanone, Ethicon) in mesh surgery. The findings from this study should be further attachment to the vagina found that the use of monofilament confirmed in a randomized trial of delayed absorbable vs absorbable suture appeared to reduce the risk of graft-suture permanent suture. v erosion without increasing surgical failure.12 However, their study was limited by only 20% of patients having follow-up Disclosure Statement greater than 6 weeks. Our results confirm these short-term Drs Tan-Kim, Menefee, Lippmann, Luber, and Nager have no rel- results, but also confirm the durability of the delayed absorb- evant financial disclosures. Dr Lukacz is a consultant for Pfizer, Inc, a able monofilament suture technique after suture absorption. Scientific Medical Advisor for Med Edicus, and an Advisory Committee member for AMS. She receives grant support from Boston Scientific Even more bothersome and more morbid than vaginal and the National Institutes of Health. suture erosions are erosions of foreign material into the blad- der. The presence of permanent suture in the bladder many Acknowledgments years after sacrocolpopexy prompted 2 of the surgeons at our We would like to thank Emily Whitcomb, MD; Kenneth C Su, MD; institution to begin using delayed absorbable sutures for mesh and Margie A Kahn, MD, for contributing subjects to this study. attachment to the vagina. In the cases involving permanent Kathleen Louden, ELS, of Louden Health Communications provided suture in the bladder, those women had normal cystoscopy editorial assistance. results at the time of their sacrocolpopexy. We attribute the high rate of vaginal mesh erosions noted in this cohort to the References 1. Arthure HG, Savage D. Uterine prolapse and prolapse of the vaginal high rate of concomitant hysterectomy (48%) overall. On the vault treated by sacral hysteropexy. J Obstet Gynaecol Br Emp 1957

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 43 ORIGINAL RESEARCH & CONTRIBUTIONS A Pilot Study Comparing Anatomic Failure after Sacrocolpopexy with Absorbable or Permanent Sutures for Vaginal Mesh Attachment

Jun;64(3):355-60. DOI: http://dx.doi.org/10.1111/j.1471-0528.1957. 8. Bump RC, Mattiasson A, Bø K, et al. The standardization of terminology tb02652.x. of female pelvic organ prolapse and pelvic floor dysfunction. Am J Obstet 2. Diwadkar GB, Barber MD, Feiner B, Maher C, Jelovsek JE. Complication and Gynecol 1996 Jul;175(1):10-7. DOI: http://dx.doi.org/10.1016/S0002- reoperation rates after apical vaginal prolapse surgical repair: a systematic 9378(96)70243-0. review. Obstet Gynecol 2009 Feb;113(2 Pt 1):367-73. DOI: http://dx.doi. 9. Barber MD, Brubaker L, Nygaard I, et al; Pelvic Floor Disorders Network. org/10.1097/AOG.0b013e318195888d. Defining success after surgery for pelvic organ prolapse. Obstet 3. Nygaard I, Brubaker L, Zyczynski HM, et al. Long-term outcomes following Gynecol 2009 Sep;114(3):600-9. DOI: http://dx.doi.org/10.1097/ abdominal sacrocolpopexy for pelvic organ prolapse. JAMA 2013 May AOG.0b013e3181b2b1ae. 15;309(19):2016-24. DOI: http://dx.doi.org/10.1001/jama.2013.4919. 10. Toglia MR, Fagan MJ. Suture erosion rates and long-term surgical outcomes 4. Majercik S, Tsikitis V, Iannitti DA. Strength of tissue attachment to mesh in patients undergoing sacrospinous ligament suspension with braided after ventral hernia repair with synthetic composite mesh in a porcine polyester suture. Am J Obstet Gynecol 2008 May;198(5):600.e1-4. DOI: model. Surg Endosc 2006 Nov;20(11):1671-4. DOI: http://dx.doi. http://dx.doi.org/10.1016/j.ajog.2008.02.049. org/10.1007/s00464-005-0660-1. 11. Maher CF, Feiner B, DeCuyper EM, Nichlos CJ, Hickey KV, O’Rourke P. 5. Greenberg JA, Clark RM. Advances in suture material for obstetric and Laparoscopic sacral colpopexy versus total vaginal mesh for vaginal vault gynecologic surgery. Rev Obstet Gynecol 2009 Summer;2(3):146-58. prolapse: a randomized trial. Am J Obstet Gynecol 2011 Apr;204(4):360. 6. Cundiff GW, Varner E, Visco AG, et al; Pelvic Floor Disorders Network. Risk e1-7. DOI: http://dx.doi.org/10.1016/j.ajog.2010.11.016. factors for mesh/suture erosion following sacral colpopexy. Am J Obstet 12. Shepherd JP, Higdon HL 3rd, Stanford EJ, Mattox TF. Effect of suture Gynecol 2008 Dec;199(6):688.e1-5. DOI: http://dx.doi.org/10.1016/j. selection on the rate of suture or mesh erosion and surgery failure in ajog.2008.07.029. abdominal sacrocolpopexy. Female Pelvic Med Reconstr Surg 2010 7. Tan-Kim J, Menefee SA, Luber KM, Nager CW, Lukacz ES. Robotic-assisted Jul;16(4):229-33. DOI: http://dx.doi.org/10.1097/SPV.0b013e3181d683a3. and laparoscopic sacrocolpopexy: comparing operative times, costs and 13. Tan-Kim J, Menefee SA, Luber KM, Nager CW, Lukacz ES. Prevalence and outcomes. Female Pelvic Med Reconstr Surg 2011 Jan;17(1):44-9. DOI: risk factors for mesh erosion after laparoscopic-assisted sacrocolpopexy. http://dx.doi.org/10.1097/SPV.0b013e3181fa44cf. Int Urogynecol J 2011 Feb;22(2):205-12. DOI: http://dx.doi.org/10.1007/ s00192-010-1265-3.

Knowing

It is impossible to know perfectly the part, if one is not acquainted with the whole, even in a gross way (grosso modo); so it is impossible to be a good surgeon if one is not familiar with the foundations and generalizations of medicine. On the other hand, as it is impossible to know the whole perfectly if we are not acquainted in a certain measure with each of its parts, it is impossible for anyone to be a good physician who is absolutely ignorant of the art of surgery, with a knowledge of its possibilities and its limitations.

— Cyrurgia, Henri de Mondeville, 1260-1316, the “Father of French Surgery”

44 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Differences in Perceived Difficulty in Print and Online Patient Education Materials

Michael Farnsworth, MA Perm J 2014 Fall;18(4):45-50 http://dx.doi.org/10.7812/TPP/14-008

who launched many promising investi- Abstract gations of perceived difficulty, although Context: Written patient education materials frequently exceed the reading abil- not through a comparison of print and ity of the general public. Patients are often intimidated by the task of reading patient online formats. The following section education materials, perceiving the materials’ difficulty levels as prohibitive, even outlines the limitations of evaluating pa- when they do not exceed the patients’ reading abilities. It is unclear how the delivery tient education materials with readability mechanism—print or a computer screen—affects a patient’s reading experience through measures alone. Limitations of readability his/her perception of its difficulty. measures may demonstrate the promise Objective: To determine whether first-year college students perceived online or of using perceived difficulty to more print-based patient education materials as more difficult to read. effectively evaluate patient education Design: Convenience sampling of first-year college students. materials presented in both print-based Results: Some first-year college students perceived online patient education materials and online media. to be more difficult to read than print-based ones—even when the reading level of the patient education materials was similar. Demographic information about this sample’s Readability-Based high levels of digital literacy suggests that other populations might also perceive online Improvements to Patient patient education materials as more difficult to read than print-based equivalents. Pa- Education Materials tients’ perceptions of the difficulty of patient education materials influenced their ability Historically, creators of patient educa- to effectively learn from those materials. tion materials sought to lower levels of Conclusion: This article concludes with a call for more research into patients’ percep- readability, where readability was mea- tions of difficulty of patient education materials in print vs on a screen. sured by years of education necessary to comprehend a text. Levels of readability can be determined with a number of Introduction readers’ understanding of health infor- formulas, including the Simple Measure Effective patient education is a con- mation in print vs on a computer screen of Gobbledygook (SMOG), the Gun- tinuing objective in health care, and by determining whether a convenience ning Fog Index, and the Flesch-Kincaid patient education materials provided sample of first-year college students per- grade-level formula, each of which is in both print-based and online formats ceived online or print-based patient edu- recommended by the Health Literacy play important roles in this aim. Written cation materials as more difficult to read. Advisor (an interactive health literacy patient education materials (both print- The central concern of this article, then, is software tool from Health Literacy In- based and online) frequently exceed the not a matter of reading levels or penetra- novations, Bethesda, MD). SMOG is reading ability of the general public.1,2 bility of the text, but of how the delivery also recommended by the US Centers Perhaps more importantly, though, pa- mechanism interferes with or enhances a for Medicare and Medicaid Services. tients are often intimidated by the task person’s reading experience through his/ These formulas are useful as basic of reading patient education materials, her perception of its difficulty. guides for pairing patient education perceiving patient education materials’ To my knowledge, no published stud- materials with appropriate audiences difficulty levels as prohibitive, even ies have compared levels of perceived and for tracking attempts to improve the in cases where the patient education difficulty between online and print- content of patient education material. materials are not written in excessively based patient education materials. Most Understanding readability-related prob- technical language and do not exceed researchers of patient education materi- lems identifies areas of need for alter- the patients’ reading abilities.3 als have focused on readability levels native approaches to improvement of Research projects with a focus on in print media2 or online �media4,5 but patient education materials, such as patients’ perceptions of the readability have not yielded comparative analyses of perceived difficulty measures. levels of patient education materials may either print or online formats. The mea- Both print-based and online patient assist patient educators in the develop- sure of perceived difficulty has received education materials are written at read- ment of these educational materials. The comparatively little attention recently. ing grade levels that exceed the reading purpose of this study was to explore An exception is the work by Leroy et al,6 ability of most patients. A recent study of

Michael Farnsworth, MA, is a Graduate in Writing, Rhetoric, and Technical Communication from James Madison University in Harrisonburg, VA. E-mail: [email protected].

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 45 ORIGINAL RESEARCH & CONTRIBUTIONS Differences in Perceived Difficulty in Print and Online Patient Education Materials

the readability of online health literature formatting. Often, readability tests fail level grammar and term familiarity.6 found a mean reading grade level of 12.30 to incorporate considerations involv- Surface-level grammar manipulations from a sample of 352 Web sites using the ing overall passage length, individual include changes to sentence structure, readability tests SMOG, Gunning Fog, and paragraph length, as well as margin use noun phrase complexity, and function Flesch-Kincaid.5 A similar study focused and other formatting issues; however, word density. Sentence structure manipu- on readability of source material for these issues may play a major role in a lations include constructing a sentence patient education materials provided by reader’s comprehension of a document. with either an active voice or a passive private electronic health record vendors, Specifically, readability formulas are voice. Overall sentence structure can also as well as by the National Library of Medi- often difficult to apply to patient educa- change by writing the sentence with an cine.1 The study found that these vendors’ tion materials written in outline formats; extraposed subject or a sentential subject. patient education materials had reading outlines, which often depend mainly on Complex sentences often have sentential grade levels greater than the 5th through sentence fragments, do not clearly reflect subjects that contain the elements of sen- 6th grade recommendations provided by sentence length—a primary factor in tences as subject terms. For example, a the European Commission and the Health readability calculations. sentence with a sentential subject might Literacy Advisor in their codes of conduct Readability tests have entered many read “the symptoms that were observed for the readability of health information.1 domains beyond those for which they during intake were cough and fever.” The American Medical Association and the were originally created. In these ill-suited On the other hand, extraposed subjects National Institutes of Health also recom- contexts, they potentially fail to clearly use “placeholders,” such as “it,” for mended that readability levels not exceed represent the reading grade level or more complex terms or descriptions. For the 6th-grade level, and the Maine Centers actual difficulty of health information. instance, consider the sentential-subject for Disease Control and Prevention rec- However, readability tests justifiably sentence, such as “ACE inhibitors used to ommended that “consent forms be written remain a popular tool for evaluating lower blood pressure can cause fatigue.” at approximately the 6th-8th grade read- health information because they can The subject of the preceding sentence ing level, and preferably closer to the 6th rapidly provide gross approximations for could be extraposed to read: “They can grade level.”7 These studies demonstrate establishing patient education materials’ cause fatigue.” This latter form may lower that many patient education materials are difficulty, as measured through an esti- levels of perceived difficulty.6 largely inaccessible to general audiences mation of reading grade level. Function words, such as in, why, be, because they are written at higher reading or the, also affect sentence structure and, grade levels. Applying Perceived Difficulty in turn, perceived difficulty. Noun phrase Complicating the readability landscape, Measurements to Patient complexity increases as the number of the results of the various available read- Education Materials function words decreases. Finally, in- ability formulas often vary greatly. Wang Several conceptual frameworks have tuitive ease of reading decreases as the et al2 found that readability varies by up been designed to explain why patients number of function words in a sentence to five reading grade levels, depending engage in or fail to engage in a variety of decreases. Consequently, a liberal use on which readability test is applied. The health-related behaviors; these measures of function words may lower levels of SMOG formula has a standard error of attempt to account for why some patients perceived difficulty. Each of the three approximately one and one-half grade are compliant and others are not.8-10 methods described requires time com- levels, where the Flesch-Kincaid has a These frameworks examine the presence mitments and writer expertise, and thus standard error of up to two and one-half of possible impediments to successful may prove prohibitive for many attempts grade levels. Effectively, SMOG varies completion of health-related behaviors. to improve patient education materials. by up to three grade levels, or twice the One barrier to health-related behavior Term familiarity is defined by the standard error, whereas the Flesch-Kincaid is “perceived difficulty,” which impedes frequency of a term in the Google Web varies by up to five grade levels. For this patients from engaging in health-related corpus, a database of more than a trillion reason, the Journal of the Royal College of behaviors because of the belief that the words. The measure of term familiarity Physicians of Edinburgh stated, “SMOG difficulty of engaging in such behaviors is helps explain why words with fewer should be the preferred measure of read- prohibitive. Leroy et al6 state: “In the con- syllables (ie, more “readable” words) ability when evaluating consumer-orien- text of consumer education, perceived dif- are sometimes more difficult to compre- tated healthcare material.”4 These findings ficulty of the text is a barrier encountered hend.3 For example, the corpus helps demonstrate the complexities involved in by many consumers who are expected to identify why certain shorter words, such applying readability formulas to patient read text and educate themselves.” Both as apnea, are actually more difficult education materials. A potential exists the perceived and actual difficulty of pa- for most readers than longer words for underestimating and overestimating tient education materials, then, might act like obesity. Term familiarity presents patient education materials with the use as barriers to patient education by imped- a hopeful direction for improvement of either formula, but SMOG produces ing patients from obtaining knowledge of patient education materials because, more accurate approximations. about their medical condition. similar to readability, term familiarity can A related issue that can lead to varia- Levels of perceived difficulty can be be assigned by computational means tion in reported levels of readability is altered through manipulations of surface- with the use of algorithms.

46 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Differences in Perceived Difficulty in Print and Online Patient Education Materials

The current study adds to this area 2016 was 21 or younger at the time of the on pink eye, a print patient education of inquiry by evaluating whether the study.11 Therefore, these students were material on back exercises, and an on- perceived difficulty of patient education approximately 10 years younger than line patient education material on back materials is also a function of presenta- necessary for inclusion in the “digital exercises. All patient education materials tion media (eg, online or print). Acting as native” classification, as stipulated by were used in actual practice, available at a hopeful launch for future research tra- Prensky.9 Additionally, 87% of the Class either a health center or a health educa- jectories of greater scope, the following of 2016 graduated in the top third of their tion Web site. research suggests that patients may per- high school class, and 65% came from The online readings were selected from ceive online patient education materials a background with an estimated family popular search results from Google.com; to be more difficult than commensurate income of $100,000 or more annually.11 each selection occurred on the first page print-based patient education materials. Each student received patient educa- of Google search results. These patient tion materials about 2 of 4 possible topics education materials were available at Methods that are familiar in student health con- Web pages that the students accessed The purpose of this research project texts. Data were collected about 81 pairs directly. The print-based readings were was to determine whether a convenience of patient education materials. The topics physical copies provided by the JMU Stu- sample of first-year college students included the following: conjunctivitis dent Health Center (see Sidebar: Patient perceived online or print-based patient (“pink eye”); mononucleosis (“mono”); Education Materials). The SMOG test education materials as more difficult.a self-care for cuts, scrapes, and burns; was used to construct an approximately The study additionally sought to measure and back exercises. Topics were paired equivalent reading grade-level difficulty the students’ perceived difficulty level of in all possible combinations, resulting in between each set of patient education each patient education material, using a 6 survey forms, A through F. The survey materials (eg, the online and print back Likert-type scale. forms were as follows: exercises patient education materials). The research was collected at James A. “Pink Eye” and “Mono” Materials in each set varied by approxi- Madison University (JMU) in Harrison- B. “Pink Eye” and “Cuts, Scrapes, mately two reading grade levels. For burg, VA, during November 2012. This and Burns” examples of the text, see “So, You Have study was approved by the university’s C. “Pink Eye” and “Back Exercises” Mono: Taking the Next Step”12 from the institutional review board (IRB Protocol D. “Mono” and “Cuts, Scrapes, and American College Health Association and 13-0141, approved on November 8, Burns” “Mononucleosis”13 from WebMD. 2012). The sampling method was conve- E. “Mono” and “Back Exercises” The online text from WebMD on nience: participants were from 4 course F. “Cuts, Scrapes, and Burns” and mononucleosis was 2.3 grade levels low- sections of General Writing, Rhetoric, and “Back Exercises.” er than the printed brochure according Technical Communication (GWRTC) 103, Survey forms were evenly distributed to SMOG and 1.4 grades lower accord- Critical Reading and Writing. Forty-one across participants. Each topic was pre- ing to the Flesch-Kincaid measurement. students participated in the research, sented in both online and print-based On the basis of the expected standard which took place in JMU computer labo- formats. Participants received four total error for these readability measures (the ratories. Each laboratory had 21 comput- readings: two print readings and two SMOG formula has a standard error of ers with Windows 7 operating system online readings. For example, a student approximately 1.5 grade levels, and (Microsoft, Redmond, WA) available in Survey Group C received a print Flesch-Kincaid has a standard error of for student use. All students voluntarily patient education material on pink eye, up to 2.5 grade levels), this sort of varia- participated; none refused to participate. an online patient education material tion means that the texts may actually Most JMU students take GWRTC 103 during their first year of college, mean- ing that they are probably members of Patient Education Materials the Class of 2016. The Class of 2016 at Online patient education materials included: “Pinkeye (Also called: Conjunctivitis)”: JMU is composed of 4632 enrolled stu- www.nlm.nih.gov/medlineplus/pinkeye.html (from the National Institutes of Health, dents, most of whom are members of the Bethesda, MD); “Self-Care for Cuts, Scrapes, and Burns”: www.fairview.org/healthlibrary/ Millennial Generation, also referred to Article/84649 (from Fairview Health Services in Minnesota), whose content was created as Generation Y. Barring specific peti- by Krames, now Krames Staywell; “Slide Show: Back Exercises in 15 Minutes a Day”: tion for exemption, all students entering www.mayoclinic.com/health/back-pain/LB00001_D (from the Mayo Clinic’s Mayo JMU are required to take GWRTC 103, Foundation for Medical Education and Research, Rochester, MN); and “Mononucleosis which means that each group of students (Mono)”: www.webmd.com/a-to-z-guides/infectious-mononucleosis-topic-overview included a mix of academic majors from (from WebMD LLC, New York, NY). across the university. Thus, this sample Print-based patient education materials included “Conjunctivitis (‘Pink Eye’)” (from should be generally representative of University Health Center); “Self-Care for Cuts, Scrapes and Burns” (from Quality Health the university’s first-year class. Survey Care); “Back Exercises” (Brochure 7068 from Parlay International, Walnut Creek, CA); data from the JMU Office of Institutional and “So, You Have Mono: Taking the Next Step” (Brochure HS21 from the American Research shows that 83% of the Class of College Health Association, Hanover, MD).

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 47 ORIGINAL RESEARCH & CONTRIBUTIONS Differences in Perceived Difficulty in Print and Online Patient Education Materials

based patient education materials. The Table 1. Chi-square test results statistical tests were computed in the Observed, n—perceived statistics program SPSS version 21.0 Frequenciesa as more difficult Expected, n Residual (IBM SPSS, Armonk, NY). Online 43 40 −3 Print 37 40 3 a Results Test statistics The first hypothesis was analyzed Chi-square 0.450 with a χ2 test, and the second hypoth- Degrees of freedom 1 esis was analyzed with a t test. The first Asymptotic significance 0.502 hypothesis did not reflect a statistically a 1 = print; 0 = online. significant difference, whereas the sec- ond hypothesis did reflect a statistically significant finding. be almost identical reading grade levels kind of question follows: “Which was Overall, participants ranked the print- or may vary by up to approximately 3.8 easier to read: the online material on based patient education materials as less grade levels according to SMOG and ap- conjunctivitis (‘pink eye’) or the paper difficult than online patient education proximately 3.9 grade levels according material on conjunctivitis?” Three addi- materials in a test of Hypothesis 1. Across to Flesch-Kincaid. The WebMD example tional questions resulted from the other 80 difficulty rankings, participants ranked scored 4.7 for SMOG and 5.4 for Flesch- three subject matters in the respective print-based materials as less difficult in Kincaid, whereas the American College patient education materials. The results 43 cases and more difficult in 37 cases, Health Association brochure scored 7.0 for each subject matter (eg, mono, pink which did not reflect a statistically sig- for SMOG and 6.8 for Flesch-Kincaid. eye, back exercises) were combined to nificant difference (p = 0.45; Table 1). The survey was available for the find an overall ranking for print patient In the second hypothesis, participants participants at the same time they education materials and an overall reported an average ranking of 6.03, or viewed the patient education materi- ranking for online patient education “somewhat easy,” for the online patient als, so that they could refer back to materials. The generalized, two-tailed education materials, whereas they reported the readings for confirmation of their hypothesis stated the following: the an average ranking of 5.48, or “easy,” for assigned levels of difficulty. All surveys format (online or print) will produce a the print patient education materials, which were collected in Qualtrics Research statistically significant difference in the reflected a statistically significant differ- Suite survey software (Qualtrics, Salt resulting rankings. ence (p = 0.000015; Tables 2a and b). In Lake City, UT). The survey questions The second survey question asked the Likert scale, “very easy” translated to a asked the students to provide two the participant to rank the difficulty value of 7, “easy” to a value of 6, and so on. kinds of difficulty rankings of the of each type of patient education patient education materials. The first material, online and print-based, for Discussion question asked the participant to de- both subject matters. These cardinal This study is possibly the first pub- cide whether the online or print-based difficulty rankings were recorded on lished research to compare levels of education material was more difficult a seven-value Likert scale from “very perceived difficulty between online and concerning the same subject matter (eg, difficult” to “very easy.” In this case, print-based patient education materials. the subject matter “pink eye”). This the generalized, two-tailed hypothesis The findings concluded that first-year question requested an ordinal ranking stated: students will report significantly students at JMU perceive print-based pa- from the student. An example of this different rankings for online vs print- tient education materials as less difficult than online patient education materials. The students’ reports that online patient education materials were more difficult Table 2a. Results of t test: Paired-samples statistics to comprehend may be further supported Paired-samples Delivery by the observation that the online materi- statistics medium N Mean SD SEM als were written at lower reading grade Pair 1 Print 81 6.037 1.1005 0.12228 levels, as demonstrated in the SMOG Online 81 5.4815 1.37032 0.15226 and the Flesch-Kincaid measurements, SD = standard deviation; SEM = standard error of the mean. described earlier. Precisely why online patient education materials might be perceived as more dif- Table 2b. Results of t test: Paired-samples test ficult is beyond the scope of the current Paired differences project. However, hypotheses include Sample Mean SD SEM 95% CI t df p (2-tailed) distractions in online environments Pair 1 0.55556 1.08397 0.12044 0.79524 4.61 80 0.000015 (eg, advertisements or other applica- CI = confidence interval; df = degrees of freedom; SD = standard deviation; SEM = standard error of the mean. tions), the cognitive difficulties associ-

48 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Differences in Perceived Difficulty in Print and Online Patient Education Materials

ated with reading on a backlit screen, and also perceive online patient education the studied population, and use Qualtrics the processes associated with searching materials as more difficult than print or other survey software to compile and for and opening Web pages. equivalents. Larger-scale studies of analyze valuable information about the Growing consensus suggests a positive perceived difficulty rankings of patient examined patient education materials. correlation between digital literacy and education materials among additional As well, clinicians could conduct their a number of demographic and psycho- demographics or in more randomized own small-scale inquiries like social factors, which include being born settings will help to produce more the author’s own to learn more in the early 1980s or later, having at least generalizable information about the dif- about the dispositions toward Growing middle-class socioeconomic status, and ferences between print-based and online patient education materials in consensus having high levels of general literacy.9,10,14 patient education materials. various media. suggests As discussed in the “Methods” section, the The decision to group four popular As health care systems move a positive students in this study were born later than student health topics together may have toward a preventive focus correlation the 1980s, had at least middle-class socio- affected the results, in that there may and patient-centered care, between digital economic status (indicated by household be important differences between the patient education may receive literacy and … income), and had high general levels of topics. For example, the online or print increased attention. Thus, the born in the early literacy (indicated by their class standing format may have led to a larger divide in effectiveness of delivery of in high school). These characteristics sug- reported perceived difficulty concerning patient education materials 1980s or later, gest that the students likely had higher- an individual topic than is reflected by may become an increasingly having at least than-average levels of digital literacy. the pooled information that was ana- pressing concern. Although middle-class It then is reasonable to hypothesize lyzed in this study. Furthermore, student knowledge that the delivery socioeconomic that other populations that have demon- health topics, such as those examined medium affects delivery is im- status, and strably lower levels of digital literacy may here, may not be representative of other portant, knowledge of how the having high also perceive online patient education sorts of patient education materials. Sub- delivery medium affects patient levels of general materials to be more difficult than print- sequent work may wish to examine a understanding may also help literacy. based patient education materials. This wide range of health topics individually patient educators better create claim presents reasons for further inquiry and with relevant populations to better and distribute patient educa- into differences in perceived difficulty understand, in each case, whether patient tion materials. In particular, investigators between print and online patient educa- perception of difficulty is influenced by might attempt to understand why online tion materials among other populations, presentation media. patient education materials are perceived perhaps while tentatively maintaining Finally, it may be argued that because as more difficult. the hypothesis that most user groups will mononucleosis may sometimes be Additionally, a content analysis of perceive online patient education materi- associated with promiscuity—a poten- current online patient education materi- als to be more difficult than print-based tially charged topic—health information als’ use of best practices in Web writing patient education materials. seekers may experience additional dif- and Web design may highlight important Future studies may confirm that most ficulties when learning about this topic. differences between writing designed for populations perceive online patient Conversely, a topic that does not invoke online and print-based contexts. These education materials as more difficult. similar emotional responses, such as and other possible factors deserve atten- Health educators may then wish to di- back exercises designed to help stave tion to better understand why online pa- rect patients toward print-based patient off back pain, may not include similar tient education materials are perceived as education materials before they consult impediments to learning. more difficult, should that tentative con- online patient education materials, and clusion receive further confirmation. v they might approach online patient Conclusion education materials with caution despite This research presents a starting point a The author had access to this population while the growing availability of online patient for future research on the influence of in pursuit of a master’s degree at James Madison University in the Writing, Rhetoric, and Technical education materials. the delivery medium on the perceived Communication Department, where he focused on The current study did have some limi- difficulty of patient education materi- medical writing, communication, and rhetoric. tations. It dealt with a limited population: als. Larger-scale studies with more first-year students at JMU. The sample randomized samples may more conclu- Disclosure Statement size was also small. This study offers sively demonstrate that online patient The author(s) have no conflict of interest starting points and directions for future education materials are more difficult to to disclose. research and does not provide immedi- comprehend. This study underscores the ately generalizable knowledge. topic’s importance and offers a model for Acknowledgment The author wishes to thank Cathryn Molloy, However, despite the shortcomings a relatively easy-to-follow protocol. That PhD, for her continual support during this of the convenience sample, the popula- is, other researchers might select random- project. tion’s potentially high levels of digital ized samples from relevant populations, Kathleen Louden, ELS, of Louden Health literacy suggest that populations with choose patient education materials for Communications provided editorial lower levels of digital literacy may examination that cover topics relevant to assistance.

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 49 ORIGINAL RESEARCH & CONTRIBUTIONS Differences in Perceived Difficulty in Print and Online Patient Education Materials

References Dec;36(4):173-89. DOI: http://dx.doi.org/10.31 9. Prensky M. Digital natives, digital immigrants. 1. Stossel LM, Segar N, Gliatto P, Fallar R, Karani 09/17538157.2010.542529. On the Horizon 2001 Oct;9(5):1-6. R. Readability of patient education materials 5. Janz NK, Becker MH. The Health Belief 10. Selber SA. Multiliteracies for a digital age. available at the point of care. J Gen Intern Med Model: a decade later. Health Educ Q Carbondale, IL: SIU Press; 2004. 2012 Sep;27(9):1165-70. DOI: http://dx.doi. 1984 Spring;11(1):1-47. DOI: http://dx.doi. 11. James Madison University, Student Affairs and org/10.1007/s11606-012-2046-0. org/10.1177/109019818401100101. University Planning. First-year survey [Internet]. 2. Wang LW, Miller MJ, Schmitt MR, Wen FK. 6. Leroy G, Helmreich S, Cowie JR. The influence Student Development Newsi 2012 Oct [cited Assessing readability formula differences of text characteristics on perceived and actual 2014 Apr 14];35(1):1. Available from: www. with written health information materials: difficulty of health information. Int J Med jmu.edu/ie/Surveys/FirstYear2012.pdf. application, results, and recommendations. Res Inform 2010 Jun;79(6):438-49. DOI: http:// 12. So you have mono: taking the next step Social Adm Pharm 2013 Sep-Oct;9(5):503-16. dx.doi.org/10.1016/j.ijmedinf.2010.02.002. [brochure HS21]. Hanover, MD: American DOI: http://dx.doi.org/10.1016/j. 7. Suggestions on improving the readability of a College Health Association; 2012. sapharm.2012.05.009. consent form [Internet]. Augusta, ME: Maine 13. Mononucleosis (mono) [Internet]. New York, 3. Fitzsimmons PR, Michael BD, Hulley JL, Center for Disease Control and Prevention; NY: WebMD; updated 2011 Jul 28 [cited 2014 Scott GO. A readability assessment of online updated 2014 Aug 11 [cited 2014 Aug 11]. Apr 16]. Available from: www.webmd.com/a- Parkinson’s disease information. J R Coll Available from: www.maine.gov/dhhs/mecdc/ to-z-guides/infectious-mononucleosis-topic- Physicians Edinb 2010 Dec;40(4):292-6. DOI: irb/irb08.htm. overview. http://dx.doi.org/10.4997/JRCPE.2010.401. 8. Leu DJ. The new literacies of online reading 14. Hayles NK. How we think: digital media and 4. McInnes N, Haglund BJ. Readability of online comprehension: expanding the literacy and contemporary technogenesis. Chicago, IL: health information: implications for health learning curriculum. Journal of Adolescent University of Chicago Press; 2012.� literacy. Inform Health Soc Care 2011 and Adult Literacy 2011 Sep;55(1):5-14. DOI: http://dx.doi.org/10.1598/JAAL.55.1.1.

So They Understand

Use familiar words—words that your readers will understand, and not words they will have to look up. No advice is more elementary, and no advice is more difficult to accept. When we feel an impulse to use a marvelously exotic word, let us lie down until the impulse goes away.

— James J Kilpatrick, 1920-2010, American columnist and grammarian

50 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 SOUL OF THE HEALER

Morning Mist photograph

Brad Christian McDowell, MD

This photograph was taken at sunrise on Long Lake in Rocky Mountain National Park in Colorado.

Dr McDowell is a Plastic Surgeon at the Denver Medical Office in CO. More of his photography can be viewed online at: www.DiversityofVision.com.

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 51 ORIGINAL RESEARCH & CONTRIBUTIONS

Special Report Behavior Medicine Specialist

Phillip Tuso, MD, FACP, FASN Perm J 2014 Fall;18(4):52-57 http://dx.doi.org/10.7812/TPP/14-035

Introduction Abstract Total Health is a vision for the future of health care. Total Health Total Health is a vision for the future and a strategy to prevent means health of mind (behavior health), body (physical health), preventable disease, save lives, and make health care more af- and spirit. Total Health includes investing in the determinants of fordable. Total Health means health of mind (behavior health) health by leveraging nonmedical impacts as a catalyst for public and health of body (physical health). To achieve Total Health health and primary care integration. In addition, the current model we need healthy people in healthy communities. A behavior of behavior and physical health care is better than treating either medicine specialist is a psychologist who works in the medical alone but is not sufficient to promote deeper healing of underly- home with the primary care physician instead of in the Mental ing trauma. The goal of Total Health is to treat the entire person Health Department with a psychiatrist. and to have a deep understanding of how a patient’s emotional The key to achieving Total Health will be to transform our history and community may contribute to disease.1 current health care system from a focus on treating disease To achieve Total Health we will need healthy people in to a focus on preventing disease. This transformation will healthy communities and a system to make lives better. We hope require complex behavior change interventions and services to make lives better by 1) measuring vital signs of health, 2) not usually provided in the medical home. The behavior promoting healthy behaviors, 3) monitoring and treating disease, medicine specialist will bring the knowledge and experience 4) spreading leading practices, and 5) creating healthy environ- used to treat mental illness into the medical home to help ments with our community partners. Best practices, spread to the primary care physician improve the care of all patients the communities we serve, will make health care more afford- in the medical home. able, prevent preventable diseases, and save lives.2 The key to The behavior medicine specialist will help improve out- achieving our goal of Total Health is behavior change of people comes in synergy with the primary care physician by universal and behavior change of communities (Figure 1). screening of high-risk diseases, stepped care protocols, and Primary care practice has adopted a generalist approach in efficient use of all resources available to care for patients in the which physicians are trained in the medical model and in solu- medical home (health education classes, wellness coaches, tions to problems that typically involve advice, medical inter- and online social networking lifestyle management programs). ventions, medications, or a referral to a specialist. Appointment These interventions should increase patient satisfaction, times are designed to maximize access and decrease appoint- increase access to specialty care (psychiatry), and help us ment demand. However, we know many patients have behavior achieve Total Health. health needs whose symptoms may exacerbate, complicate, or masquerade a physical condition. In addition, the co-occurrence of a behavior health issue may prevent a front-line physician’s ability to effectively treat or prevent chronic diseases such as obesity, diabetes, or coronary artery disease. Additionally, owing to current appointment time constraints, physicians often do not have the time or the skill set to effectively manage change in patients with behavior health needs. The future focus of health care will be on wellness and in- tegrated care in a medical home. The National Committee for Quality Assurance3 has defined criteria for a medical home to be a clinic that include standards that apply to disease and case management activities that are beneficial to both physical and mental health. These criteria include patient registries, case man- agement, evidence-based guidelines, self-management support, and access to specialists. If these standards are applied, then quality outcomes and cost of care should improve.4 Cost-effective care will depend on our ability to prevent dis- eases such as diabetes through early detection and treatment. Figure 1. Total Health and the behavior medicine specialist. The key to a successful wellness program will be the ability to

Phillip Tuso, MD, FACP, FASN, is the Care Management Institute Physician Lead for Total Health. E-mail: [email protected].

52 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Behavior Medicine Specialist

engage patients in behavior that may prevent illness or disease. Table 1. Behavior medicine specialist compared with mental health The science of behavior change is complex. Most patients are specialist overwhelmed with what is prescribed by physicians and the Dimensions Behavior medicine specialist Mental health specialist media. But many people lack the knowledge, skills, and con- fidence to practice the health behaviors that will improve their Model of Care Population-based consultation Patient-based specialty focus physical and mental health. Patient engagement to improve Primary customer Primary care physician Patient health care outcomes may require the expertise and resources Direct report(s) Primary care physician Psychiatrist of a psychologist trained in behavior change who can work side Psychiatrist by side with the physician in the medical home. Team structure Primary care team member Mental health team member This journey to holistic health will start when patients come Location Primary care clinic Mental health clinic to see their physician and continue when they access health care Goal(s) Measure vital signs of total health Resolve patient’s mental services in their community. The key to achieving Total Health Promote healthy behaviors health issues in the future may be integrating behavior health services into Monitor and treat disease the medical home. In this model, healthy people will be able to Spread leading practice receive physical health services and behavior health services in Create healthy environments the clinic where they see their primary care physician. Currently with our community partners most physicians focus on physical illness and refer patients to specialty behavior medicine for behavior health treatment. To be more effective and to obtain behavior change interventions effectiveness. In the medical home, the physician is respon- to help the physician manage chronic diseases, primary care sible for the care of all patients. physicians may benefit from integrating a psychologist called a The tools a psychologist acquires to treat mental illness may behavior medicine specialist (BMS) into the medical home where be applied to treat physical health conditions. In this way, the they provide direct patient care. primary care physician, the BMS, and the patient work together as a health care team with the common goal of preventing and Behavior Medicine Specialist treating chronic diseases in a healthy medical home. By establish- The BMS concept is not new. Large health care systems ing a role in primary care, BMS providers gain direct access to across the country, including the Department of Defense, patients and physicians. The Healthy People 2020 Mental Health have added behavior change specialists into the medical goal is to improve mental health through prevention and by home.5 Traditionally, the BMS is a psychologist who works ensuring access to appropriate, quality mental health services. side by side with all members of the health care team to One of their strategies to achieve this goal is to increase the enhance effective preventive and clinical care for all patients. proportion of primary care facilities that provide mental health The BMS role in primary care is different from his or her treatment onsite.6,7 role in a mental health clinic (Table 1). As a member of the primary care team, the BMS mainly focuses on helping the Measuring Vital Signs of Health primary care physician make lives better. As stated above, we Measuring vital signs of health will help the BMS and the can make lives better by 1) measuring vital signs of health, medical home team identify patients who will benefit from 2) promoting healthy behaviors, 3) monitoring and treat- upstream behavior change interventions before a disease pro- ing disease, 4) spreading leading practices, and 5) creating gresses to a more serious level of care. Although consensus on healthy environments with our community partners. The BMS vital signs of health has not been determined, some that may consults with the entire team but serves as a link between make the list are shown in the Sidebar: Proposed Vital Signs of the patient and the physician (primary care physician and Total Health. Vital signs of health should include measurements the psychiatrist) and helps these providers to increase their around healthy eating and active living as these have been shown to help improve biometrics or risk factors for health like 8 Proposed Vital Signs of Total Health blood pressure, cholesterol, and body mass index. Tobacco is a well-documented vital sign for health, and lowering tobacco Healthy eating and active living smoking rates may be the single most important intervention • Number of servings of fruits and vegetables consumed per day we can do to save lives and reduce health care costs.9,10 Finally, • Number of minutes of physical activity per day mental health screening will be a very important means to help Biometrics identify and treat patients with anxiety and depression. A new • Body mass index tool called the Treatment Progress Indicator measures anxiety, • Blood pressure depression, and functional status.11 This tool can be used to moni- • Low-density lipid cholesterol level tor an individual patient’s therapy and response to interventions • Fasting blood sugar level while seeing how care provided by one provider compares with • Tobacco use care provided by many providers. This type of report could be Mental Health used to identify and spread best practices. Once vital signs of • Anxiety health are agreed on, programs can be developed that promote • Depression healthy behaviors and improve health care outcomes. • Functional status

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Promoting Healthy Behaviors with kidney disease). To accomplish these goals, the BMS and The BMS is a culturally competent psychologist who provides physician must agree on a common strategy for management treatment for a wide variety of mental health, psychosocial, of patients with behavior health issues. An example of this motivational, and medical concerns, including management of model of care is known as stepped care.28 anxiety,12 pain,13,14 depression,15-17 substance abuse, smoking The BMS will help facilitate systemic change within a pri- cessation,18 insomnia,19 diabetes,20 medication adherence,21 and mary care population to improve measurable outcomes. The psychological trauma.22 The BMS also provides support and BMS typically collaborates with physicians as a consultant to management for patients with severe and persistent mental develop treatment plans and monitor patient progress. The BMS illness and tends to be familiar with psychopharmacologic is needed in primary care clinics because research has shown interventions.23 The BMS coordinates care of mental illness that approximately half of all mental health care services are with the primary care physician and psychiatrists, which may provided solely by primary care providers.29 Furthermore, pri- decrease the need to refer patients to a psychiatrist, reducing mary care practitioners prescribe about 70% of all psychotropic overall cost of care,24 and alleviating the stigma of patients medications and 80% of antidepressants.30 Another reason to seen in the mental health clinic.25 Randomized controlled trials integrate the BMS into the medical home is that chronic disease show that disease management models using care managers can contribute to behavior health dysfunction, and behavior are both clinically effective and cost-effective. Meta-analyses health dysfunction can contribute to chronic disease. An ex- indicate that there is a cost offset of 20% to 40% for primary ample is depression, which can coexist in diabetes, coronary care patients who receive behavior health services. Notably, artery disease, obesity, and chronic pain. Studies have shown fewer hospitalizations result in significant cost reductions for effective treatment of depression in primary care clinics can patients with chronic physical illness and those with psychi- improve quality of life and measurable outcomes31 and may atric diagnoses.26 improve treatment adherence in chronic disease.32 In stepped care, patients who do not improve through the Monitoring and Treating Disease usual course of care will move to the next level of care where Finally, the BMS may help primary care physicians differenti- the intensity of service is customized according to the patient’s ate symptoms from disease and prevent unnecessary tests and response. This may include cognitive behavior therapy or psy- referral to specialists. Even though mind-body relationships chotherapy. The key is to use a viable model and to have a may seem obvious, physical health problems may be masked strong, positive connection between provider and patient that by psychosocial concerns. Physicians are trained to deal with occurs in a timely manner and over an appropriate period. diseases, and they often must evaluate symptoms that are not Likewise, a patient who no longer needs a higher level of associated with a disease. treatment can step down to a milder intervention. An example A retrospective 3-year study of 1000 patients in a general of stepped care is shown in Table 2. To diagnose a behavior medical clinic setting provided a comprehensive picture of health issue, primary care providers often use evidence-based symptoms in the outpatient setting. The investigators identified behavior health screening tools. One such screening tool is the 14 common symptoms: chest pain, fatigue, dizziness, head- Patient Health Questionnaire (PHQ-9) that is used to identify ache, edema, back pain, dyspnea, insomnia, abdominal pain, adults with depression.33 This nine-item questionnaire can be numbness, impotence, weight loss, cough, and constipation. quickly completed, usually in one to two minutes. They found that 38% of the patients reported at least one of Ideally, the physician confirms the depressive symptomol- these symptoms, but an organic cause for the symptoms was ogy and then uses brief intervention algorithms for treatment. found only 16% of the time. Ten percent of the symptoms Many medical homes have begun to integrate the screening were believed to be psychological in origin and 74% were of of depression as a routine practice in caring for patients unknown cause.27 with chronic illnesses. This process may begin with a brief As the physician focuses on helping his or her population two-question screening, using the first two questions of the achieve their health care goals, the BMS helps the physician by PHQ-9. Patients with depression, as determined by answers to advising on the best way to successfully change the behavior the PHQ-9 tool, may need different types of care on the basis of a single patient and a population of patients (eg, diabetics of the severity of their illness. Patients with mild depression

Table 2. Stepped care for depression Stepped care Step One Step Two Step Three Step Four Depression Mild Moderate Moderate-Severe Severe PHQ-9 score 1-9 10-14 15-19 > 20 Intervention Very-low-intensity intervention Low-intensity intervention High-intensity intervention Very-high-intensity intervention Health education classes Cognitive behavioral Group therapy, brief One-on-one therapy, intensive therapy psychotherapeutic interventions outpatient and inpatient programs Wellness coaching Care management Care management Care management PHQ-9 = Patient Health Questionnaire-9.

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(PHQ-9 score, 1-9) may need only mild intervention whereas a communities. In addition, the BMS will have the ability to track patient with severe depression (PHQ-9 score, > 20) may need referrals, services, visits, and program enrollment. Outcome- significant intervention. Stepped care protocols can be used to based reporting will have the potential to demonstrate com- help patients understand the different options of care available munity and individual patient results. This program will help to them according to the severity of their illness. Stepped care the BMS to identify community care gaps and best practices. may include referrals to wellness coaches, online programs, Many communities have a plethora of support or community resources not provided in the medical home and social services, but locating these resources The disease (eg, faith-based counseling). can be time-consuming and frustrating. This new management Historically, subjective evaluations were used to determine program can be incorporated into stepped care as model of the when a patient’s condition had improved. Since it is hard to part of a comprehensive care plan that includes standardize outcomes and set goals for subjective measurable referrals for required services. The coordination of future will outcomes, it is also hard to determine when a patient could be social services with clinical services should result be a system repatriated back to the primary care physician and to identify in a significant increase in patient compliance and of care and and to share best practices in care. As a result, access to be- improved outcomes. interventions havior health has been a challenge at a time when it appears designed demand for behavior health service has been increasing. In Discussion to optimize the future, physicians and the BMS will use objective tools to Since the 1980s, research has improved our wellness and help manage behavior health conditions much like primary care ability to recognize, to diagnose, and to treat actually prevent physicians use objective measures to manage chronic disease chronic disease. In fact, many studies have found disease. such as diabetes, high blood pressure, and obesity. correlations between physical and behavior health-related problems. Individuals with serious Spreading Leading Practices physical health problems often have comorbid behavior health Healthy people and medical homes will be the foundation to problems.34 In addition, it is estimated that as many as 70% a healthy community. Self-management tools will help individu- of primary care visits stem from behavior health issues.35 For als understand what they need to do to be healthy. To achieve these reasons it makes sense at this time to integrate the BMS Total Health in the future, we will need healthy communities into the primary care clinics and medical homes. Deliver- to maintain health. Because patients spend very little time in ing behavior health services in primary care can help to 1) the medical home, our communities need to be healthy to sup- minimize the stigma and delay of seeing a behavior health port work being done by healthy people and healthy medical specialist in another building, 2) increase opportunities to homes. Healthy communities will help people thrive where improve overall health care outcomes, and 3) improve access they live, learn, work, play, and pray. To accomplish this goal to psychiatry services. healthy people and medical homes will need to interact with The disease management model of the future will be a healthy communities. The BMS is an important team member system of care and interventions designed to optimize well- coming into primary care clinics. The BMS will help stimulate ness and actually prevent disease. Effective implementation of change in our communities by identifying and sharing best this concept will reduce the overall cost of care and disease practices while also identifying gaps in care. burden. Prevention is forever a part of disorder management. Key to this shift in our paradigm will be a use of BMS-directed Creating Healthy Environments self-management tools needed to be healthy and thrive. This Another key responsibility of the BMS will be to integrate will involve developing Web-based tools to help people the patient with community resources. Every day thousands measure their biometrics and behavior health index as well of our patients require assistance from our clinical social as tools to help them meet their biometric and behavior workers and other staff members for basic necessities like goals. Web-based programs will be interlinked with the BMS food, housing, transportation, medications, dental services, and the medical home. The final part of this strategy is link- and support groups. And every day organizations in our local ing the care of patients to community resources. This last communities assist us to help our patients by providing these strategy will be more difficult because it will involve Kaiser needed services. Currently there is no organized systematic Permanente partnering with key community leaders to align Web-based approach to locate these services that also allows resources to help both the patient and the communities to for community organizations to see the services previously achieve Total Health. accessed by a patient. In addition, there is currently no ob- Finally, in addition to universal screening for vital signs of jective way to know if a service provided to a community health, there should also be an awareness of an alternative improves health care outcomes. paradigm that emphasizes a focus on health and protective fac- In the future, the BMS will have access to Web-based tors as opposed to a focus on problems and risk factors.36,37 A resources (wellness resource locators) to help match up a recent article looked at estimated deaths attributable to social particular patient need with a specific community resource factors in the US. Results showed that approximately 245,000 where people live, learn, work, play, and pray (Figure 1). The deaths in the US in 2000 were attributable to low education, BMS will have the ability to locate and interact quickly and 176,000 to racial segregation, 162,000 to low social support, effectively with all appropriate services in the local healthy 133,000 to individual-level poverty, 119,000 to income inequal-

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ity, and 39,000 to area-level poverty. The authors concluded 7. Healthy People 2020: mental health and mental disorders: objectives [Internet]. Washington, DC: US Department of Health and Human Services; that the estimated number of deaths attributable to social updated 2014 Jul 28 [cited 2014 Jul 28]. Available from: www.healthypeople. factors in the US is comparable with the number attributed to gov/2020/topicsobjectives2020/objectiveslist.aspx?topicId=28. pathophysiologic and behavior causes. Therefore, regarding 8. Ellsworth DL, Croft DT Jr, Weyandt J, et al. Intensive cardiovascular risk reduction induces sustainable changes in expression of genes improving the Total Health of populations, social factors may and pathways important to vascular function. Circ Cardiovasc play a role in determining why certain populations are not Genet 2014 Apr 1;7(2):151-60. DOI: http://dx.doi.org/10.1161/ meeting their vital signs of health outcomes goals.38 For this CIRCGENETICS.113.000121. 9. Smoking & tobacco use: quitting smoking [Internet]. Atlanta, GA: reason, behavior health clinics that address social issues along Centers for Disease Control and Prevention; updated 2014 Jun 13 [cited with behavior health issues have been established into medi- 2014 Jul 24]. Available from: www.cdc.gov/tobacco/data_statistics/ cal settings at Northwestern Memorial Hospital (www.nmh. fact_sheets/cessation/quitting/index.htm?utm_source=feedburner&utm_ medium=feed&utm_campaign=Feed%3A+CdcSmokingAndTobaccoUseFa org/nm/bluhm-specialists-cardiac-behavioral-medicine) and ctSheets+(CDC+-+Smoking+and+Tobacco+Use+-+Fact+Sheets). Boston Children’s Hospital (www.childrenshospital.org/centers- 10. The health consequences of smoking—50 years of progress: a report and-services/behavioral-medicine-clinic-program/overview). of the Surgeon General [Internet]. Atlanta, GA: US Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Chronic Disease Prevention and Conclusion Health Promotion, Office on Smoking and Health; 2014 [cited 2014 In population-based care, the entire population is the target. Jun 5]. Available from: www.surgeongeneral.gov/library/reports/50- years-of-progress/. Our strategy should be to use a “wide net” approach aimed at 11. Tuso PJ. Treatment progress indicator: application of a new assessment serving the entire primary care population with emphasis on tool to objectively monitor the therapeutic progress of patients with prevention and improving outcomes with effective accountable depression, anxiety, or behavioral health impairment. Perm J 2014 Summer;18(3):55-9. DOI: http://dx.doi.org/10.7812/TPP/13-091. interventions. By going upstream in care, health care clinics 12. Generalized anxiety disorder and panic disorder (with or without may dramatically improve health care outcomes while reduc- agoraphobia) in adults: management in primary, secondary and community ing cost of care. For example, the BMS may help to introduce care [Internet]. London, UK: National Institute for Health and Care Excellence; 2011 Jan [cited 2014 Jul 24]. Available from: http://guidance. trauma and stress reduction education to help everyone better nice.org.uk/CG113. understand the relationships between illness and wellness. It 13. Moore JE, Von Korff M, Cherkin D, Saunders K, Lorig K. A randomized is important to recognize that the current health care environ- trial of a cognitive-behavioral program for enhancing back pain self care in a primary care setting. Pain 2000 Nov;88(2):145-53. DOI: http://dx.doi. ment is promoting and rewarding quality improvement and the org/10.1016/S0304-3959(00)00314-6. concept of the patient-centered medical home. Medical groups 14. Ahles TA, Wasson JH, Seville JL, et al. A controlled trial of methods for that want to grow will need to focus on disease prevention to managing pain in primary care patients with or without co-occurring psychological problems. Ann Fam Med 2006 Jul-Aug;4(4):341-50. DOI: lower health care costs. To accomplish this goal, health care http://dx.doi.org/10.1370/afm.527. leaders will need to work closely with community leaders to 15. Katon W, Von Korff M, Lin E, et al. Collaborative management to create healthy environments. v achieve treatment guidelines. Impact on depression in primary care. JAMA 1995 Apr 5;273(13):1026-31. DOI: http://dx.doi.org/10.1001/ jama.1995.03520370068039. Disclosure Statement 16. Simon GE, Katon W, Rutter C, et al. Impact of improved depression The author(s) have no conflicts of interest to disclose. treatment in primary care on daily functioning and disability. Psychol Med 1998 May;28(3):693-701. DOI: http://dx.doi.org/10.1017/ S0033291798006588. Acknowledgment 17. Robinson P, Bush T, Von Korff M, et al. Primary care use of cognitive Mary Corrado, ELS, provided editorial assistance. behavioral techniques with depressed patients. J Fam Pract 1995 Apr;40(4):352-7. 18. Fiore MC, Jaén CR, Baker B, et al. Treating tobacco use and dependence: References 2008 update [Internet]. Rockville, MD: US Deptartment of Health and 1. Felitti VJ, Anda RF, Nordenberg D, et al. Relationship of childhood abuse Human Services; 2008 May [cited 2014 Jul 28]. Available from: http:// and household dysfunction to many of the leading causes of death bphc.hrsa.gov/buckets/treatingtobacco.pdf. in adults: The Adverse Childhood Experiences (ACE) Study. Am J Prev 19. Goodie JL, Isler WC, Hunter C, Peterson AL. Using behavioral health Med 1998 May;14(4):245-58. DOI: http://dx.doi.org/10.1016/S0749- consultants to treat insomnia in primary care: a clinical case series. 3797(98)00017-8. J Clin Psychol 2009 Mar;65(3):294-304. DOI: http://dx.doi.org/10.1002/ 2 Tuso P. Physician update: total health. Perm J 2014 Spring;18(2):58-63. jclp.20548. DOI: http://dx.doi.org/10.7812/TPP/13-120. 20. Ridgeway NA, Harvill DR, Harvill LM, Falin TM, Forester GM, Gose OD. 3. Standards and Guidelines for Physician Practice Connections—Patient- Improved control of type 2 diabetes mellitus: a practical education/behavior Centered Medical Home (PPC-PCMH) [Internet]. Washington, DC: modification program in a primary care clinic. South Med J 1999 Jul;92(7): National Committee for Quality Assurance; 2008 [cited 2014 Jul 24]. 667-72. DOI: http://dx.doi.org/10.1097/00007611-199907000-00004. Available from: www.ncqa.org/Portals/0/Programs/Recognition/PCMH_ 21. Craven MA, Bland R. Better practices in collaborative mental health care: Overview_Apr01.pdf. an analysis of the evidence base. Can J Psychiatry 2006 May;51(6 Suppl 1): 4. Hunter CL, Goodie JL. Operational and clinical components for integrated- 7S-72S. collaborative behavioral healthcare in the patient-centered medical home. 22. Schnurr PP, Friedman MJ, Engel CC, et al. Cognitive behavioral therapy Fam Syst Health 2010 Dec;28(4):308-21. DOI: http://dx.doi.org/10.1037/ for posttraumatic stress disorder in women: a randomized controlled a0021761. trial. JAMA 2007 Feb 28;297(8):820-30. DOI: http://dx.doi.org/10.1001/ 5. Talen MR, Valeras AB. Integrated behavioral health in primary care: evaluating jama.297.8.820. the evidence, identifying the essentials. New York, NY: Springer New York; 23. Wolf NJ, Hopko DR. Psychosocial and pharmacological interventions for 2013 Jun 18. DOI: http://dx.doi.org/10.1007/978-1-4614-6889-9. depressed adults in primary care: a critical review. Clin Psychol Rev 2008 6. Healthy People 2020: Mental health and mental disorders: overview Jan;28(1):131-61. DOI: http://dx.doi.org/10.1016/j.cpr.2007.04.004. [Internet]. Washington, DC: US Department of Health and Human 24. Schulberg HC, Raue PJ, Rollman BL. The effectiveness of psychotherapy Services; updated 2014 Jul 28 [cited 2014 Jul 28]. Available from: in treating depressive disorders in primary care practice: clinical and cost www.healthypeople.gov/2020/topicsobjectives2020/overview. perspectives. Gen Hosp Psychiatry 2002 Jul-Aug;24(4):203-12. DOI: http:// aspx?topicid=28. dx.doi.org/10.1016/S0163-8343(02)00175-5.

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25. Mak WW, Poon CY, Pun LY, Cheung SF. Meta-analysis of stigma and BMJ 2006 Feb 4;332(7536):259-63. DOI: http://dx.doi.org/10.1136/ mental health. Soc Sci Med 2007 Jul;65(2):245-61. DOI: http://dx.doi. bmj.38683.710255.BE. org/10.1016/j.socscimed.2007.03.015. 32. Dunbar-Jacob J, Mortimer-Stephens MK. Treatment adherence in chronic 26. Blount A, Schoenbaum M, Kathol R, et al. The economics of behavioral disease. J Clin Epidemiol 2001 Dec;54 Suppl 1:S57-60. DOI: http://dx.doi. health services in medical settings: a summary of the evidence. Prof org/10.1016/S0895-4356(01)00457-7. Psychol Res Pr 2007;38(3):290-7. DOI: http://dx.doi.org/10.1037/0735- 33. Kroenke K, Spitzer RL, Williams JB. The PHQ-9: validity of a brief 7028.38.3.290. depression severity measure. J Gen Intern Med 2001 Sep;16(9):606-13. 27. Kroenke K, Mangelsdorff AD. Common symptoms in ambulatory DOI: http://dx.doi.org/10.1046/j.1525-1497.2001.016009606.x. care: incidence, evaluation, therapy, and outcome. Am J Med 1989 34. Kessler RC, Chiu WT, Demler O, Merikangas KR, Walters EE. Prevalence, Mar;86(3):262-6. DOI: http://dx.doi.org/10.1016/0002-9343(89)90293-3. severity, and comorbidity of 12-month DSM-IV disorders in the National 28. van Straten A, Seekles W, van‘t Veer-Tazelaar NJ, Beekman AT, Cuijpers P. Comorbidity Survey Replication. Arch Gen Psychiatry 2005 Jun;62(6):617-27. Stepped care for depression in primary care: what should be offered and DOI: http://dx.doi.org/10.1001/archpsyc.62.6.617. how? Med J Aust 2010 Jun 7;192(11 Suppl):S36-9. 35. Robinson P, Reiter J. Behavioral consultation and primary care: a 29. Narrow WE, Regier DA, Rae DS, Manderscheid RW, Locke BZ. Use of guide to integrating services. New York, NY: Springer; 2006 Dec 29. services by persons with mental and addictive disorders. Findings from 36. Antonovsky A. Social class, life expectancy and overall mortality. Milbank the National Institute of Mental Health Epidemiologic Catchment Area Mem Fund Q 1967 Apr;45(2):31-73. DOI: http://dx.doi.org/10.2307/3348839. Program. Arch Gen Psychiatry 1993 Feb;50(2):95-107. DOI: http://dx.doi. 37. Antonovsky A. Unraveling the mystery of health: how people manage org/10.1001/archpsyc.1993.01820140017002. stress and stay well. San Francisco, CA: Jossey-Bass Publishers; 1987. 30. Beardsley RS, Gardocki GJ, Larson DB, Hidalgo J. Prescribing of 38. Galea S, Tracy M, Hoggatt KJ, Dimaggio C, Karpati A. Estimated deaths psychotropic medication by primary care physicians and psychiatrists. Arch attributable to social factors in the United States. Am J Public Health 2011 Gen Psychiatry 1998 Dec;45(12):1117-9. DOI: http://dx.doi.org/10.1001/ Aug;101(8):1456-65. DOI: http://dx.doi.org/10.2105/AJPH.2010.300086. archpsyc.1988.01800360065009. 31. Hunkeler EM, Katon W, Tang L, et al. Long term outcomes from the IMPACT randomized trial for depressed elderly patients in primary care.

Trinity

Man is a trinity composed of three elements: the body, the heart, and the mind. To each of these elements corresponds some need. The satisfaction of these needs, in full measure, constitutes the science of life and assures the greatest sum of happiness, which we can enjoy.

— Joseph-François Malgaigne, 1806-1865, French surgeon and medical historian

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 57 ORIGINAL RESEARCH & CONTRIBUTIONS Special Report Mindful Mood Balance: A Case Report of Web-Based Treatment of Residual Depressive Symptoms

Jennifer Felder, MA; Sona Dimidjian, PhD; Arne Beck, PhD; Jennifer M Boggs, MSW; Zindel Segal, PhD Perm J 2014 Fall;18(4):58-62 http://dx.doi.org/10.7812/TPP/14-019 Editor’s note: Please see related article on page 4. and didactic eLearning modules that use Abstract text, video, interactive programs, and re- Residual depressive symptoms are associated with increased risk for relapse and flection questions. Between weekly Web impaired functioning. Although there is no definitive treatment for residual depressive sessions, skill consolidation is developed symptoms, Mindfulness-Based Cognitive Therapy has been shown to be effective, but from daily home practice of session access is limited. Mindful Mood Balance (MMB), a Web-based adaptation of Mind- content, including mindfulness medita- fulness-Based Cognitive Therapy, was designed to address this care gap. In this case tion. Program support with a master’s study, we describe a composite case that is representative of the course of intervention level clinical psychology doctoral stu- with MMB and its implementation in a large integrated delivery system. Specifically, dent who was part of the MMB research we describe the content of each of eight weekly sessions, and the self-management team was available via phone, e-mail, skills developed by participating in this program. MMB may be a cost-effective and or text messaging and was intended to scalable option in primary care for increasing access to treatments for patients with facilitate engagement with MMB as well residual depressive symptoms. as to troubleshoot barriers to complet- ing weekly sessions and home practice. Introduction effective when sequenced with pharma- MMB patients were invited to contact the Patients treated for depression who cotherapy for treating RDS.11,12 However, support person with any questions or continue to experience residual de- access to MBCT groups is limited owing challenges. Furthermore, the MMB sup- pressive symptoms (RDS) may be at to a lack of trained clinicians as well as port person contacted patients who had increased risk for relapse1 and impaired to other barriers impeding dissemination not logged on to the program in a week. long-term functioning.2 RDS are highly of psychological treatments for mood Qualitative data provided by MMB prevalent, with research showing that disorders.13,14 patients during a study exit interview 90% of individuals who remit from de- Previous research has demonstrated suggest that the MMB program is feasible pression experience RDS up to 1 year the efficacy of Web-based cognitive and acceptable.18 An open trial examina- later.3 Although there is no definitive behavioral approaches for preventing tion of MMB demonstrated that patients treatment for RDS, the most common depressive relapse among individuals significantly improved in depressive approach is antidepressant or psycho- in partially remitted patients15 and the severity, which was sustained over six therapeutic monotherapy. Sequenced, feasibility of Web-based mindfulness pro- months; improved on proximal mark- phase-specific approaches4 are less com- grams.16,17 Mindful Mood Balance (MMB) ers of relapse such as rumination and monly observed in practice but show (Dimidjian S, Beck A, Felder JN, Boggs mindfulness; and engaged with program increased effectiveness for treating RDS J, Gallop R, Segal ZV, unpublished data, sessions and daily mindfulness practice. compared with monotherapy. These ap- 2014) is an eight-session self-guided, MMB also was associated with significant proaches usually involve treating patients Web-based program that incorporates the reduction in RDS severity compared to remission with pharmacotherapy and core content of in-person MBCT. MMB with the quasi-experimental propensity- then providing psychotherapy for RDS. aims, in part, to address the care gap for matched control group (Dimidjian S, Mindfulness-Based Cognitive Therapy patients with RDS. Consistent with MBCT, Beck A, Felder JN, Boggs J, Gallop R, (MBCT) has a strong evidence base MMB targets RDS by teaching specific Segal ZV, unpublished data, 2014). Al- for prevention of depressive relapse5-10 emotion regulation and depression self- though informative at the group level, among recurrently depressed patients management skills. In each session, skill these reports provide limited detail about and has recently been shown to be acquisition is enabled via experiential both the nature of the MMB intervention

Jennifer Felder, MA, is a Doctoral Candidate in the Psychology and Neuroscience Department at the University of Colorado Boulder. E-mail: [email protected]. Sona Dimidjian, PhD, is an Associate Professor in Psychology and Neuroscience at the University of Colorado Boulder. E-mail: [email protected]. Arne Beck, PhD, is the Director for Quality Improvement and Strategic Research at the Kaiser Permanente Institute for Health Research in Denver, CO. E-mail: [email protected]. Jennifer M Boggs, MSW, is a Doctoral Candidate in the Health Services Research Program at University of Colorado Denver: School of Public Health and a Project Coordinator at the Kaiser Permanente Institute for Health Research in Denver, CO. E-mail: [email protected]. Zindel Segal, PhD, is a Distinguished Professor of Psychology in Mood Disorders at the University of Toronto in Ontario, Canada. E-mail: [email protected].

58 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Mindful Mood Balance: A Case Report of Web-Based Treatment of Residual Depressive Symptoms

and the specific experiences of patients guided by the Sequenced Treatment mindfulness practice, mindful eating, as they complete the program curricu- Alternatives to Relieve Depression algo- during which she was encouraged to lum. Such information may be valuable rithm for sequential pharmacotherapy.20 direct her attention first to the sensations for primary care physicians considering When the patient continued to experi- of sight, texture, smell, sound, and taste MMB as an option for patients with ence symptoms of insomnia, anhedonia, of eating a raisin. For all audio record- RDS either following or combined with guilt, and functional impairment, her ings, the patient chose to download maintenance pharmacotherapy.19 The physician referred her to the study for the recording as an mp3 file to save aim of this case study is to describe a augmentation because no in-person on her phone, which she found more composite case that is representative of MBCT group was available. The patient convenient than logging on to the pro- the course of intervention with MMB and reported that she was interested in MMB gram to listen to recordings. She often its implementation in a large integrated because she was an “introvert” and the listened to the recordings while traveling delivery system. opportunity to access treatment at home on the bus to work. After this practice appealed to her more than attending a and all others, the participant answered Case Report group with other patients. reflection questions in a text box. These Patient Identification questions asked about what she noticed This report describes a composite case Patient Use of Mindful during the practice and how she thought that is representative of the course of Mood Balance the practice related to preventing de- intervention with MMB and its imple- See Table 1 for a brief description of pression and staying well. The patient mentation with patients referred from the objectives for each MMB session. In reported that this was a helpful way to primary care clinics in a large integrated the first session of MMB, titled “Finding concretize what she had experienced delivery system. The composite case is Your Place Beyond Blue,” the partici- in the practice and that it was useful to based on the experiences of patients pant started by watching an introduc- be able to return to her notes later. The enrolled in an open trial study of MMB tory video from one of the two MMB session ended with a video of one of who were recruited via physician refer- facilitators that is featured throughout the MMB facilitators discussing the home ral and informational materials made the program. She responded to a list practice for the week. available in clinics. All participants of difficulties she hoped MMB would In session 2, “The Body Scan,” the in the open trial study of MMB had a help, such as “being caught in my mind” patient watched a “welcome back” history of major depressive disorder and “taking things too personally,” and video and was provided brief instruc- and therefore were at elevated risk for viewed video clips of participants from tions about how to prepare for her first depressive relapse. RDS were not an eli- an in-person MBCT group discussing formal meditation practice. The patient gibility criterion for the open trial study, their experience with the MBCT pro- participated in a 30-minute body scan but the composite case described in this gram. The primary focus in this session practice, during which she moved her case report experienced RDS. was differentiating between “automatic attention to specific foci in her body. Before participation in the MMB pro- pilot,” described as acting without After the practice, she was invited gram, the patient, a woman in her late awareness, and mindfulness. These to describe what she noticed during 40s, was treated for her third episode concepts were conveyed through text, her body scan and to reflect on how of major depression by her primary care illustrations, videos, and mindfulness intentional deployment of attention physician. Antidepressant medication practices. For example, the patient contrasted to automatic pilot. She was was prescribed (citalopram, 40 mg/day), streamed an audio recording of her first also presented with a list of videos of

Table 1. Mindful Mood Balance session objectives # Session topic Session objectives 1 Finding Your Place What is mindfulness; recognizing automatic patterns of reactivity associated with sad mood; integrating brief Beyond Blue informal mindfulness practice into daily life. 2 The Body Scan Paying attention to specific regions in the body to develop a foundation of mindfulness skill; identifying links between interpretations of interpersonal events and emotional responses. 3 The Breath Increasing awareness of how often the mind is busy/scattered. 4 Exploring the Landscape Recognizing experiential avoidance; practicing ways to stay present and attentive in the face of difficulty; of Depression identifying depression’s early warning signs. 5 Facing Difficulties Using mindful awareness as the first step in responding effectively to difficult experiences; increasing awareness of the experience of emotions in the body. 6 Thoughts Are Not Facts Learning to “de-center” from difficult thoughts; recognizing one’s personal patterns of recurring thoughts. 7 Building Your Plan of Action Identifying activities that improve or deteriorate mood; developing action plans to implement during periods of high risk; using mindfulness practice explicitly to guide taking action. 8 Supporting Your Practice Emphasizing the importance of regular self-care routines; reinforcing links between mindfulness practices, n the World well-being, and mood balance.

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the group participants responding to to complete the Body Scan each day and ment. She also reported greater aware- the same questions. The patient found that she was looking forward to having a ness of the patterns of her thoughts and it reassuring that group members expe- briefer meditation option. Additionally, emotions and an ability to notice that rienced many of the same challenges she responded to an e-mail check-in they ebb and flow. She described mo- as she did during the practice, such as from the program support person to ments when she was able to stand back feeling sleepy, or judging herself when let her know that she was struggling to a bit from her thoughts and emotions her mind wandered from the practice to complete the daily home practice. The instead of reacting to them, and say, thinking about what to make for dinner program support person explained that “Oh, there’s sadness again, and think- that night. Next, the patient completed home practice is often difficult for pro- ing I am inadequate. Interesting that I an exercise that highlighted the gram participants, especially in the first am feeling that.” She contrasted this to relationship between thoughts few sessions of the program. Together, times in the past where she would in- MMB aims to and feelings. She listened to a the patient and program support person stead say, “I can’t handle this! I’m never help patients scenario in which she imagined identified some ideas to support her going to feel better!” and her thoughts move from seeing a friend, waving at the practice, including adding her practice would spiral out of control from there, a pattern friend, and getting no response. time to her calendar to protect the time, worsening her mood. of getting The patient generated interpre- recruiting her spouse’s assistance with In session 6, “Thoughts Are Not “sucked tations, such as “she’s mad at childcare during her practice times, and Facts,” she learned how emotions into” me” or “she didn’t notice me,” adopting a compassionate attitude with affect thoughts—for example, by see- and resulting emotions, includ- herself when unexpected challenges ing the world “through rose-colored negative ing sadness or feeling neutral. arose. She also experimented with glasses” when happy and as “the glass thoughts This practice was reinforced completing the longer practices on the half empty” when sad. This session de- and with a home practice assign- weekends and briefer practices during scribed mindful attention as a first step emotions ment that involved noting one busy workdays. in responding to difficulties. An anima- to stepping pleasant event each day and In session 4, “Exploring the Land- tion of four doors illustrated potential back the accompanying thoughts, scape of Depression,” the patient options for when she notices negative from and feelings, and sensations. The learned that understanding depres- thoughts, emotions, or sensations. The observing following week, the patient sion is a vital step in learning how first door, “re-entry,” was described as them. reported that she enjoyed to recognize it and to prevent it from the door to take when simply bring- bringing her attention to pleas- gathering momentum. The patient ing awareness to a difficulty makes it ant events because she noticed interacted with a “playlist” of negative less troubling. The “body door” invited things she would usually miss, and it automatic thoughts frequently reported her to attend to the ways in which dif- helped her stay present in the moment by individuals with depression and, ficult emotions and experiences can of her experiences. She planned to she created a personalized playlist of show up as physical sensations. The continue this practice, although it was thoughts that accompany her depres- “thought door” suggested bringing not assigned for home practice again. sive episodes, such as “I’m a loser.” She fine-tuned awareness to observing her Session 3, “The Breath,” began with a noticed that the mindfulness practices negative thoughts versus getting pulled video of a group leader describing the increased her ability to observe the into them. The “door of skillful action” breath as another door to awareness. presence of these thoughts without get- highlighted that mindful awareness of The patient reported feeling connected ting pulled into disputing them. difficult experiences does not require to the MMB facilitators, whom she de- Over sessions 5 and 6, the patient passivity. Instead, sometimes it is im- scribed as warm and compassionate. practiced applying her mindfulness portant to take action in ways that bring In this session, the patient listened to skills to face painful thoughts, emo- a sense of pleasure, nourishment, or an audio recording of a sitting medita- tions, and bodily sensations as they accomplishment. The patient reported tion practice. She noted the physical arose throughout the day. Session 5, to the program support person that she sensations that were present during “Facing Difficulties,” cultivated this was surprised to notice that sometimes her practice and how busy her mind practice in several ways, including a a 3MBS was all she needed to deal with was. The patient participated in 2 ad- sitting meditation during which she difficulties, such as a disagreement with ditional mindfulness practices, including invited a difficulty into the practice, the a coworker. Other times, taking a bath, a mindful stretching exercise and a brief presentation of a poem, and the use folding laundry, or watching a favorite breathing practice called the 3-Minute of the 3MBS in reaction to a negative movie at the end of a tough workday Breathing Space (3MBS). The 3MBS was event. At first, the patient reported to was needed. described as a “mini-meditation” to be the program support person that she In sessions 7 (“Building Your Plan of used at any point during the day and was concerned that focusing on nega- Action”) and 8 (“Supporting Your Prac- as a first step in dealing with difficult tive events might hasten the onset of tice in the World”), the patient reflected situations. While reviewing the previ- depression. Over time, she found that on actions she could take to look after ous week’s home practice, the patient they actually helped her feel prepared herself in the areas of energy, pleasure, noted that it was difficult to make time to deal with negative events in the mo- and mastery. She identified her personal

60 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Mindful Mood Balance: A Case Report of Web-Based Treatment of Residual Depressive Symptoms

relapse signatures and wrote a letter connection with the learning context; MMB can be easily sequenced with on- to herself to catalog the strategies she these include both the videotaped group going antidepressant treatment, it may learned in the program. Specific activi- participants and group facilitators and the be a cost-effective and scalable option ties she included as part of her wellness access to a phone coach. As described in primary care for increasing access to plan were as follows: “Call your sister in the composite case here, patients comprehensive care for RDS. v if you notice your mood is starting to often find their personal concerns, drop,” “Do one nice thing for yourself questions, and challenges during the Disclosure Statement each day like buying a magazine you’ll practices reflected in the experiences This research was supported by a National enjoy reading during lunch,” or “Make of members of the videotaped group. Institutes of Mental Health Grant #R34 plans to go for dinner after work with This both is validating and provides an 087723. The author(s) have no other conflicts of interest to disclose. a friend.” The patient kept her wellness opportunity to learn via modeling from plan in a file on her computer to revisit how others coped with the challenge. Acknowledgment easily and reviewed it with her spouse The live phone coach also augments such Mary Corrado, ELS, provided editorial so he could support her wellness plan. asynchronous support through provid- assistance. The patient reported really enjoying the ing concrete feedback about technical practical suggestions in the last three questions and troubleshooting challenges References sessions of the program. with the home practice. Future research 1. Paykel ES, Ramana R, Cooper Z, Hayhurst H, Kerr J, Barocka A. Residual symptoms after The patient logged on to the program may seek to establish the appropriate partial remission: an important outcome in 73 times in 61 days over the course of training threshold for the program sup- depression. Psychol Med 1995 Nov;25(6):1171- completing the 8 sessions of MMB. In port person. For example, could trained 80. DOI: http://dx.doi.org/10.1017/ S0033291700033146. addition to online completion of each health educators be effective in this 2. Kennedy N, Paykel ES. Residual symptoms at weekly program session, the patient role? Finally, the program includes an remission from depression: impact on long-term logged on to submit logs that recorded anonymous forum to post questions and outcome. J Affect Disord 2004 Jun;80(2-3):135- 44. DOI: http://dx.doi.org/10.1016/S0165- the frequency and duration of each daily receive responses from the group facili- 0327(03)00054-5. home practice assignment. The patient tators; although not all patients use this 3. Nierenberg AA, Husain MM, Trivedi MH, et al. submitted 38 daily home practice logs, feature, it represents an additional option Residual symptoms after remission of major depressive disorder with citalopram and risk of and reported completing brief informal for patients to receive program support. relapse: a STAR*D report. Psychol Med 2010 mindfulness practices 54 times (194 min- RDS represent an important inter- Jan;40(1):41-50. DOI: http://dx.doi.org/10.1017/ utes) and formal meditation practices 32 vention target to prevent relapse for S0033291709006011. 4. Fava GA, Ruini C, Belaise C. The concept of times (755 minutes) over the course of at-risk individuals following treatment recovery in major depression. Psychol Med 9 weeks. The program support person for acute depression. Physicians may 2007 Mar;37(3):307-17. DOI: http://dx.doi. provided an average of 55 minutes of find that MMB is a useful clinical adjunct org/10.1017/S0033291706008981. 5. Kuyken W, Byford S, Taylor RS, et al. phone, e-mail, and text support time per for RDS that could be used sequentially Mindfulness-based cognitive therapy to prevent patient over the 9 weeks of enrollment. with pharmacotherapy. Physicians might relapse in recurrent depression. J Consult Clin elect to refer patients who have been Psychol 2008 Dec;76(6):966-78. DOI: http:// dx.doi.org/10.1037/a0013786. Discussion treated either pharmacologically or with 6. Segal ZV, Bieling P, Young T, et al. Antidepres- This case study, based on a composite psychotherapy for an acute episode of sant monotherapy vs sequential pharmaco- of representative experiences of patients major depression and who are showing therapy and mindfulness-based cognitive therapy, or placebo, for relapse prophylaxis who have completed the MMB program, signs of treatment response, or patients in recurrent depression. Arch Gen Psychiatry describes the specific learning goals, with residual symptoms. 2010 Dec;67(12):1256-64. DOI: http://dx.doi. interventions, and trajectory of patients At present there are insufficient org/10.1001/archgenpsychiatry.2010.168. 7. Bondolfi G, Jermann F, der Linden MV, et who use MMB as a component of a data to indicate which patients would al. Depression relapse prophylaxis with treatment approach to RDS. The case be most suited for MMB, but an open Mindfulness-Based Cognitive Therapy: 18 replication and extension in the Swiss study illustrates that skills are learned trial described elsewhere indicated a health care system. J Affect Disord 2010 over the course of the program that relationship between the number of May;122(3):224-31. DOI: http://dx.doi. focus on new ways of relating to nega- sessions completed and the amount org/10.1016/j.jad.2009.07.007. 8. Godfrin KA, van Heeringen C. The effects of tive thoughts, emotions, and sensations. of benefit experienced. The question mindfulness-based cognitive therapy on recur- MMB aims to help patients move from of suitability merits further study. One rence of depressive episodes, mental health and a pattern of getting “sucked into” nega- possibility is the MMB might be viewed quality of life: a randomized controlled study. Behav Res Ther 2010 Aug;48(8):738-46. DOI: tive thoughts and emotions to stepping positively by patients for whom in- http://dx.doi.org/10.1016/j.brat.2010.04.006. back from and observing them. Both the person MBCT is not available, for those 9. Ma SH, Teasdale JD. Mindfulness-based mindfulness meditation and the cogni- who cannot travel regularly or do not cognitive therapy for depression: replication and exploration of differential relapse tive and behavioral techniques support feel comfortable attending in-person prevention effects. J Consult Clin Psychol this important learning. groups or individual psychotherapy, 2004 Feb;72(1):31-40. DOI: http://dx.doi. Additionally, the MMB program in- or for those who would prefer non- org/10.1037/0022-006X.72.1.31. 10. Teasdale JD, Segal ZV, Williams JM, Ridgeway cludes key elements that are designed pharmacologic options to long-term VA, Soulsby JM, Lau MA. Prevention of relapse/ to strengthen a sense of interpersonal depression care management. Because recurrence in major depression by mindfulness-

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based cognitive therapy. J Consult Clin Psychol linking epidemiologic data to practice. Psychiatr 18. Boggs JM, Beck A, Felder JN, Dimidjian S, 2000 Aug;68(4):615-23. DOI: http://dx.doi. Serv 2009 Nov;60(11):1540-2. DOI: http:// Metcalf CA, Segal ZV. Web-based intervention org/10.1037/0022-006X.68.4.615. dx.doi.org/10.1176/appi.ps.60.11.1540. in mindfulness meditation for reducing residual 11. Kingston T, Dooley B, Bates A, Lawlor E, 15. Holländare F, Johnsson S, Randestad M, et al. depressive symptoms and relapse prophylaxis: a Malone K. Mindfulness-based cognitive therapy Randomized trial of Internet-based relapse qualitative study. J Med Internet Res 2014 Mar for residual depressive symptoms. Psychol prevention for partially remitted depression. 24;16(3):e87. DOI: http://dx.doi.org/10.2196/ Psychother 2007 Jun;80(Pt 2):193-203. DOI: Acta Psychiatr Scand 2011 Oct;124(4):285- jmir.3129. http://dx.doi.org/10.1348/147608306X116016. 94. DOI: http://dx.doi.org/10.1111/j.1600- 19. Guidi J, Fava GA, Fava M, Papakostas GI. 12. Geschwind N, Peeters F, Huibers M, van Os 0447.2011.01698.x. Efficacy of the sequential integration of J, Wichers M. Efficacy of mindfulness-based 16. Morledge TJ, Allexandre D, Fox E, et al. psychotherapy and pharmacotherapy in cognitive therapy in relation to prior history of Feasibility of an online mindfulness program for major depressive disorder: a preliminary meta- depression: randomised controlled trial. Br J stress management­—a randomized, controlled analysis. Psychol Med 2011 Feb;41(2):321- Psychiatry 2012 Oct;201(4):320-5. DOI: http:// trial. Ann Behav Med 2013 Oct;46(2):137-48. 31. DOI: http://dx.doi.org/10.1017/ dx.doi.org/10.1192/bjp.bp.111.104851. DOI: http://dx.doi.org/10.1007/s12160-013- S0033291710000826. 13. Butler M, Kane RL, McAlpine D, et al. 9490-x. 20. Trivedi MH, Kleiber BA. Algorithm for the Integration of mental health/substance abuse 17. Cavanagh K, Strauss C, Cicconi F, Griffiths N, treatment of chronic depression. J Clin and primary care. Evid Rep Technol Assess (Full Wyper A, Jones F. A randomised controlled trial Psychiatry 2001;62 Suppl 6:22-9. Rep) 2008 Nov;(173):1-362. of a brief online mindfulness-based intervention. 14. Patten SB, Meadows GM. Population-based Behav Res Ther 2013 Sep;51(9):573-8. DOI: service planning for implementation of MBCT: http://dx.doi.org/10.1016/j.brat.2013.06.003.

The Storm of Murk

The madness of depression is … the antithesis of violence. It is a storm indeed, but a storm of murk. Soon evident are the slowed-down responses, near paralysis, psychic energy throttled back close to zero. Ultimately, the body is affected and feels sapped, drained.

— Darkness Visible, William Styron, 1925-2006, American novelist and essayist

62 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 SOUL OF THE HEALER

Moose Antlers of Eielson photograph

Sally J Cullen, MD, MS

This photograph was taken in Denali National Park in Alaska. Our national parks �preserve some of our country’s most magnificent natural wonders, and we are incredibly fortunate to have them.

After more than 32 years practicing medicine, Dr Cullen retired in 2012 as Assistant Chief of Pediatrics at Kaiser Permanente Folsom in CA. She is passionate about protecting national parks and public spaces and uses photography to encourage others to celebrate our natural world. More of her photography can be viewed at: www.myparkphotos.com/property/SallyCullen.html.

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 63 ORIGINAL RESEARCH & CONTRIBUTIONS Special Report Thinking about Thinking and Emotion: The Metacognitive Approach to the Medical Humanities that Integrates the Humanities with the Basic and Clinical Sciences

Quentin G Eichbaum, MD, PhD, MPH, MFA, MMHC, FCAP Perm J 2014 Fall;18(4):64-75 http://dx.doi.org/10.7812/TPP/14-027

Abstract Medicine, Nashville, TN, has moved away emotion, and the importance of cognitive Medical knowledge in recent decades from the traditional conception of the medi- monitoring and emotional regulation. has grown prodigiously and has outstripped cal humanities as “the arts,” composed In the group setting, students also gain the capacity of the human brain to absorb of art, music, and literature, toward an a sense of perspective of their thinking and understand it all. This burgeoning of approach that integrates the humanities patterns and emotions in relation to those knowledge has created a dilemma for med- with the basic and clinical sciences, based of their peers. Perspective taking and mind- ical educators. We can no longer expect on metacognition. This metacognitive ap- fulness engender tolerance and empathy, students to continue memorizing this large proach to the humanities, described in which ultimately serves as a platform for body of increasingly complex knowledge. this article, has three goals: 1) to develop working collaboratively in teams as medi- Instead, our efforts should be redirected at students as flexible thinkers and agile cal professionals. Students become aware developing in students a competency as learners and to provide them with essential of the social context in which thinking and flexible thinkers and agile learners so they cognitive and emotional skills for navigat- learning occur, and this further shapes their can adeptly deal with new knowledge, ing medical complexity and uncertainty; 2) professional identity. Thinking, learning, and complexity, and uncertainty in a rapidly to elicit in students empathy and tolerance interacting in the group setting ultimately changing world. Such a competency would by making them aware of the immense di- induces a shift from self-preoccupation and entail not only cognitive but also emotional versity in human cognition (and emotion); an individualistic approach to knowledge skills essential for the holistic development and 3) to integrate the humanities with the toward an appreciation of collective cogni- of their professional identity. This article basic and clinical sciences. tion and empathy towards others. will argue that metacognition—“thinking Through this metacognitive approach, In this article, I describe the metacogni- about thinking (and emotion)”—offers the students come to understand their patterns tive approach to the medical humanities at most viable path toward developing this of cognition and emotions, and in the group Vanderbilt University School of Medicine competency. setting, they learn to mindfully calibrate and how it is designed to develop students The overwhelming volume of medi- their thinking and emotions. They gain a as agile learners and flexible thinkers with cal knowledge has driven some medical humbling appreciation of the fallibility of the mindful capacity for cognitive and schools to reduce the time allocated in their the human mind/brain and how cognitive emotional monitoring and regulation. curricula to the “soft-option” humanities as biases and misperceptions can lead to Thinking and learning in the group setting they tend to consider them an expendable medical error. They come to appreciate the of the colloquium ultimately also fosters “luxury.” Vanderbilt University School of complex interplay between cognition and the student’s professional identity.

Introduction thinking (and emotion)”—offers the most viable path toward In a rapidly changing world of increased complexity, developing this competency. In this article, I describe the medical educators should direct efforts at developing in metacognitive approach to the medical humanities at Vander- students a competency as flexible thinkers and agile learn- bilt University School of Medicine (VSUM), Nashville, TN, and ers with the capacity for navigating this complexity and its how it is designed to develop students as agile learners and contingent uncertainties. Such a competency would entail flexible thinkers with the mindful capacity for cognitive and not only cognitive but also emotional skills essential for the emotional monitoring and regulation. Thinking and learning holistic development of the students’ professional identity. in the group setting of the colloquium ultimately also fosters This article will argue that metacognition—“thinking about the student’s professional identity.

Quentin G Eichbaum, MD, PhD, MPH, MFA, MMHC, FCAP, is an Associate Professor of Medical Education, Associate Professor of Pathology, Microbiology, and Immunology, a Course Director, and Clinical Fellowship Program Director at Vanderbilt University School of Medicine in Nashville, TN. E-mail: [email protected].

64 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Thinking aboutabout Thinking Thinking and and Emotion: Emotion: The The Metacognitive Metacognitive Approach Approach to the to Medicalthe Medical Humanities Humanities that Integrates the Humanities with the Basic and Clinical Sciences that Integrates the Humanities with the Basic and Clinical Sciences

The Conundrum of the of professionalism. For these reasons, we at VUSM view Humanities in Medical Education metacognition as the foundation of the colloquium and as an The germane role of the humanities in medical education emerging competency that students should begin developing remains a topic of ongoing controversy. As the volume and early in their medical education. complexity of medical knowledge continues to surge, some educators may view the humanities as an expendable luxury Structure and Rationale and reduce the time in the medical curriculum allocated to of the College Colloquium these disciplines. Others may see a vital role for the humanities I developed and innovated the College Colloquium in a more in eliciting and nurturing in students the essential Hippocratic comprehensive form at a previous medical school and adapted qualities of caring and empathy. The humanities are frequently it at VUSM as a course consistent with the goals of its new taught in medical schools to provide a rehumanizing coun- curriculum (Curriculum 2.0 introduced in 2013). Curriculum 2.0 terbalance to the burdensome weight of scientific knowledge at VUSM was designed in part to cope with the rapid growth that students must memorize to pass their examinations, or as in medical knowledge and complexity that can no longer be Bleakley1 says: “as compensation for an overdose of science.” comprehensively accommodated in the curriculum, and instead Be this as it may, the humanities and sciences are usually still to provide students with a more individualized and customized taught in medical schools and universities as “silo” disciplines. approach to their education. Curriculum 2.0 at VUSM reduces Separating the sciences and humanities into what Snow2 the basic science component of the traditional US medical famously called “the two cultures” has, however, created a curriculum from 2 years to about 15 months in length, and false dichotomy in knowledge. shifts the bulk of the clinical clerkships from third year to the The College Colloquium at VUSM seeks to integrate the second year of the curriculum. The third and fourth years are sciences and humanities into a unified tapestry of knowledge. devised as an individualized learning plan in which students The colloquium is based on the premise that there are not can tailor their education in the direction of their choice of “two cultures” but only a single “culture” of knowledge that is medical specialty. The goal of the colloquium is to develop mediated through cognition and the human brain. The intel- students to be more agile learners and flexible thinkers. In lectual framework of the colloquium has its foundations in place of traditional rote memorization, students are taught metacognition, a higher order of human cognition that is less to become competent conceptual thinkers and to develop a formally referred to as “thinking about thinking.”3-5 Thinking scientific and holistic understanding of how the mind works. and metacognition, or thinking about thinking (and emo- The colloquium is situated in the 4 “colleges” that comprise tion), happen in the brain, the physical manifestation of the the “learning communities.” mind, which is the epicenter of our cognitive processes, our These “college” learning communities are designed to pro- consciousness, as well as our sense of morality.a6 However, vide an environment in which students can interact in smaller modern neuroscience now disputes whether the brain and groups, in a trusting space among peers and mentors, to hone mind are separate entities (a discussion beyond the scope of their thinking and emotional skills and in which they can also this article). Panksepp and Biven, in their landmark book The develop and nurture their professional identity. Two college Archaeology of Mind: Neuroevolutionary Origins of Human mentors oversee each college and serve as advisors to the Emotions, write that “modern neuroscience … has revealed students in their college and as facilitators during discussions that it is no longer useful to distinguish between the mind in the colloquium. In the college community, students learn and the brain, although we surely must distinguish between to trust one another and to develop their cognitive, emotional, types of minds and types of brains.”7p8 and collaborative skills as medical professionals. With the ongoing increase in knowledge, medical education The College Colloquium meets for two to two-and-a-half will be impelled to abandon the clichéd fire hose image of hours each week. The first half hour is devoted to a “context filling students with factual information toward a competency- talk,” a short talk delivered to the class by the course directors based approach that develops students into agile learners or associated faculty experts. The context talks are designed and flexible thinkers. Students possessing this competency to provide a context around the required readings by placing will have a deeply enhanced understanding of how the the week’s colloquium topic in a broader learning and intel- mind works.8 They will come to have a keen sense of what lectual framework, and by posing challenging questions for they know and do not know, be more adept at navigating discussion in the ensuing within-college discussions. Rather complexity and dealing with uncertainty, and they will be than leaving the context of learning implicit, the context talks more skilled at asking the “right” questions. Moreover, with situate the colloquium topics in the setting of their scientific and a sense of their own cognitive fallibility and of the brain as sociocultural/ethical interrelationships. The role of the expert a fallible biologic organ, such students will likely be more teacher is not to provide answers, but to be challenging and circumspect and humble about their learned knowledge. to open up exploratory avenues for students to navigate in the They will be mindful of the context and the social setting participatory and trusting setting of their colleges. of their learning, and (as will be argued) will also be more After the talk, students break up into their separate colleges to adept at regulating their own emotions. Such cognitive skills, discuss the assigned readings and possibly questions triggered monitoring, and mindfulness will have a positive impact on by the context talk. The colloquium as a course starts with foun- their well-being as well as their ethical sensibility and sense dational readings and discussions on topics in metacognition

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 65 ORIGINAL RESEARCH & CONTRIBUTIONS Thinking about Thinking and Emotion: The Metacognitive ApproachThinking to the about Medical Thinking Humanities and Emotion: that Integrates The Metacognitive the Humanities Approach with the toBasic the andMedical Clinical Humanities Sciences that Integrates the Humanities with the Basic and Clinical Sciences

and critical thinking, and in subsequent semesters proceeds Selected Readings in Meta/Neurocognition to topics in professionalism, medical ethics, leadership, and Assigned in the College Colloquium at health care systems. (See Sidebar: Selected Readings in Meta/ Vanderbilt University School of Medicine Neurocognition Assigned in the College Colloquium at VUSM, which presents examples of the kinds of readings prescribed Books for the foundational colloquia on metacognition.) • Schulz K. Being Wrong: Adventures in the Margin of Error. New For promoting open communication and for generating a York, NY: Harper Collins; 2010. sense of community, the seating arrangement of the student • Quirk ME. Intuition and Metacognition in Medical Education: Keys (and mentor) participants in the colloquium is important. The to Developing Expertise. New York, NY: Springer; 2006. students sit together with their mentors in a circle facing each • Montgomery K. How Doctors Think: Clinical Judgment and the other across an open space. (No electronic devices or social me- Practice of Medicine. Oxford, UK: Oxford University Press; 2006. dia are allowed.) The college mentors facilitate the discussions. • Siegel D. The Mindful Brain. New York, NY: WW Norton; 2007. Students are required to submit and to disseminate a carefully • Hall S. Wisdom: From Philosophy to Neuroscience. New York, considered question on each of the week’s readings to the col- NY: Knopf; 2010. lege the evening before each colloquium, to drive discussions • Doidge N. The Brain That Changes Itself. New York, NY: Penguin and to give the student practice in formulating creative questions. Books; 2007. Most medical humanities courses in the US, it appears, are • Kahneman D. Thinking Fast and Slow. New York, NY: Farrar, Straus not summatively assessed, and many are not even required and Giroux; 2011. courses. This is fairly well known among directors of medi- • Churchland P. Braintrust: What Neuroscience Tells Us about cal humanities programs and is also frequently discussed at Morality. New York, NY: Knopf; 2010. conferences on medicine humanities, such as the Project to • Taylor JB. My Stroke of Insight: A Brain Scientist’s Personal Journey. Rebalance and Integrate Medical Education (PRIME) con- New York, NY: Viking; 2006. ference in 2012. Requiring attendance and assessing such • Berns G. Iconoclast: A Neuroscientist Reveals How to Think courses, it is commonly thought, may further alienate students. Differently. Boston, MA: Harvard Business Review Press; 2010. Paradoxically, however, such tentativeness may compound • Colvin G. Talent is Overrated: What Really Separates World-Class the perception of the humanities as being a soft option and Performers from Everybody Else. New York, NY: Penguin; 2008. inferior to the basic science courses. Like the science courses • Ramachandran VS. The Tell-Tale Brain: A Neuroscientist’s Quest at VUSM, the colloquium is a required, fully assessed, and for What Makes Us Human. New York, NY: WW Norton; 2011. evaluated course. Rather than having a separate examination, • Spiro H, Peschel E, Curnen MGM, St James D. Empathy and the essay-style questions from the colloquium are integrated into Practice of Medicine. New Haven, CT: Yale University Press; 1993. the science end-block examinations. The questions are aimed • Damasio A. Self Comes to Mind: Constructing the Conscious at assessing whether students have intellectually integrated Brain. New York, NY: Vintage Books; 2012. and assimilated the context (rather than just the content) of the readings into their own thinking and can communicate Articles their thinking clearly. As attributed to William Osler, who • Gladwell M. Most likely to succeed: how do we hire when we spoke of absorbing readings: “It is much simpler to buy books can’t tell who’s right for the job? [Internet]. New York, NY: The than to read them and easier to read them than to absorb New Yorker; 2008 Dec 15 [cited 2014 Jul 31]:[about 15 p]. their contents.” Available from: www.newyorker.com/magazine/2008/12/15/ most-likely-to-succeed-2. The Meta/Neurocognitive Approach • Gladwell M. The talent myth: are smart people overrated? [In- Integration of the Humanities ternet]. New York, NY: The New Yorker; 2002 Jul 22 [cited 2014 with the Basic and Clinical Sciences Jul 31]:[about 7 p]. Available from: www.newyorker.com/maga- The overemphasis on factual knowledge in medical educa- zine/2002/07/22/the-talent-myth. tion has a stifling effect on learning and thinking. Philosopher • Tierney J. Do you suffer from decision fatigue? [Internet]. New York, Nussbaum insists that education should teach us not to be NY: The New York Times; 2011 Aug 17 [cited 2014 Jul 31]:[about just passive assimilators of facts but to be expert thinkers: 10 p]. Available from: www.nytimes.com/2011/08/21/magazine/ “[E]ducation is not just about the passive assimilation of do-you-suffer-from-decision-fatigue.html?pagewanted=all. facts and cultural traditions, but about challenging the mind • Lucey C, Souba W. The problem with the problem of profession- to become active, competent, and thoughtfully critical in a alism. Acad Med 2010 Jun;85(6):1018-24. DOI: http://dx.doi. complex world.”9p18 org/10.1097/ACM.0b013e3181dbe51f. Medical students and trainees have a tendency to overempha- • Charon R. The patient-physician relationship. Narrative medicine: size and value the importance of factual knowledge. Many seem a model for empathy, reflection, profession, and trust. JAMA to consider a sound command of factual medical knowledge as 2001 Oct 17;286(15):1897-902. DOI: http://dx.doi.org/10.1001/ the hallmark of the outstanding physician. From this perspec- jama.286.15.1897. tive, students may perceive the humanities as subjective or a • Epstein RM, Siegel DJ, Silberman J. Self-monitoring in clinical prac- soft option compared with the objective sciences and therefore tice: a challenge for medical educators. J Contin Educ Health Prof may relegate the humanities to an inferior standing. 2008 Winter;28(1):5-13. DOI: http://dx.doi.org/10.1002/chp.149.

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The lopsidedness between the sciences and the humanities in that cognition and emotions are processed along separate the medical curriculum is antithetical to the notion of medicine noninteracting pathways in the brain.7 Instead, there is a major as both a science and an art, and runs counter to a culture of interplay between cognition and emotions, and neither can be producing well-rounded empathetic physicians. Bleakley et al understood in isolation. Neurobiologist Damasio argues that argues that the humanities have a vital role to play in the pro- “when emotion is entirely left out of the reasoning picture cess of learning the medical sciences: “[W]e see potential for … reason turns out to be even more flawed than when emo- learning medicine as imaginative and aesthetic science where tion plays bad tricks on our decisions.”14pxii Cognition affects medical humanities is reformulated as the process or perspec- emotion, and emotions in turn shape cognitive processes tive that creates the conditions of possibility for such learning such as perception, memory, learning, and decision making. of science to occur.”10p200 In medicine, we have underestimated the complex interplay Analogously, just as the humanities can have a vital role in between cognition and emotion in effective decision mak- creating the conditions for the effective learning of science, ing and how this interplay underlies a sizable component of so too can the rigors of the scientific method be brought to medical error.7,15-17 enlighten the humanities. For example, investigators have The metacognitive approach of the colloquium therefore used medical imaging to study how the brain processes stories encompasses the study of not only cognition but also the and literature. Research shows that a group of neurons in the emotions. At VUSM, we examine the complex interconnections brain known as mirror neurons are involved in the processing between cognition and emotion with a focus on the role of of stories. These neurons also play a role in empathy. One emotions in the lives of patients and physicians. Thus, the therefore sees that the sciences and humanities are part of an metacognitive approach enhances not only students’ think- integral field of human knowledge. Harvard biologist Wilson11 ing and learning skills but also develops their professional refers to this integration of human knowledge as “consilience.”b identity by including topics that affect the students’ emotional The colloquium aims to redress this curricular imbalance lives, such as emotional regulation, coping and resilience, and between the sciences and humanities. The metacognitive empathy. Specific sessions in the colloquium are devoted to approach—increasingly informed through neuroscience— each of these and additional similar topics. provides the intellectual framework and focusing lens for integrating the sciences and humanities. The colloquium runs Metacognition, Neuroscience, … there is a in parallel each week with the science curriculum allowing for and Cognitive Fallibility major interplay a bidirectional integration of subject matter between the col- The study of metacognition has traditionally between cognition loquium and science courses. For example, course content on fallen under the disciplines of philosophy and and emotions, the genetics of breast cancer may be included in a colloquium psychology. Advances in neuroscience and and neither can session, “How We Perceive,” to illustrate pitfalls in perception neuroimaging have more recently shed light on be understood that can occur in reading a diagnostic mammogram. A science the biology of brain function during a variety of in isolation. … In course on genetics conducted in parallel might include content specific cognitive tasks, transforming the field of medicine, we have from the colloquium about the ethics of genetic diagnosis metacognition into neurocognition. Many of the and/or a discussion on how the mind navigates the kinds of topics and required readings in the colloquium underestimated the cognitive complexity seen in genetics, such as the problems therefore derive from writings and research complex interplay this complexity might pose for effective thinking and learning in neurocognition. We at VUSM thus term this between cognition or the uncertainties entailed in genetic complexity that may emerging fieldmeta/neurocognition. A selection and emotion in result in mistakes and medical error. of readings is shown in the Sidebar: Selected effective decision The colloquium challenges the notion of the “two cultures” Readings in Meta/Neurocognition Assigned in making and how as separate cultures and instead attempts to integrate the the College Colloquium at Vanderbilt University this interplay humanities and sciences into a unified medical curriculum. School of Medicine. underlies a sizable 12 Kulasegaram et al recently suggested that “cognitive science” Modern neurobiology is providing the impetus component of (“cognitive activity occurring within learners”) should serve for unifying previously disparate fields of knowl- medical error. as the vehicle for integrating the basic and clinical sciences. edge. In The Marketplace of Ideas, Menand18 of The metacognitive approach, especially as informed by Harvard University suggests: modern neuroscience, provides the most tenable approach The most important intellectual development in the acad- to breaking down silos of knowledge in medicine and sci- emy in the 21st century has to do with the relationship be- ence, and to integrating the humanities and sciences in the tween the life sciences—particularly neurobiology, genetics, medical curriculum. and psychology—to the fields outside the natural sciences, such as philosophy, economics, and literary studies.18p19 Metacognition as an Interplay Neurobiology is integrating the sciences and humanities. of Cognition and Emotion Fields of investigation previously falling mostly in the realm Quirk definesmetacognition as “the ability to think about of philosophy and psychology, such as perception, learning, one’s thinking and feelings and to predict what others are and decision making, we can now examine using the rigor- thinking.”13p4 A substantial body of literature from the neurosci- ous methods of science.11 To some, this reductionism may ences and cognitive sciences has challenged the assumption be unappealing, but as Wilson11 forcefully argues in his book

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Consilience: The Unity of Knowledge, science can actually enhance our appreciation of the humanities. As a further Deliberate Practice 1 manifestation of how the metacognitive approach integrates This term was coined by Ericsson et al in an article titled the humanities with the basic and clinical sciences, students “The Role of Deliberate Practice in the Acquisition of Expert in the colloquium will simultaneously in the curriculum learn Performance” to describe “expert performance as the end about brain anatomy and function as well as neuroscience result of individuals’ prolonged efforts to improve performance and pathology. while negotiating motivational and external constraints. In most Through the study of neurocognition, students become domains of expertise, individuals begin in their childhood a aware that the brain does not record reality like a camera. regimen of effortful activities (deliberate practice) designed to Instead, it constructs models of the world that are sufficiently optimize improvement. Individual differences, even among elite effective for survival. As neuroscientist Eagleman states: performers, are closely related to assessed amounts of deliberate One of the most pervasive mistakes is to believe that our practice. Many characteristics once believed to reflect innate visual system gives a faithful representation of what is “out talent are actually the result of intense practice extended for a there” in the same way that a movie camera would.19p24 minimum of 10 [years].” … [B]rains reach out into the world and actively extract the type of information they need.19p30 Reference 1. Ericsson KA, Krampe, RT, Tesch-Römer C. The role of deliberate The brain doesn’t need a full model of the world because practice in the acquisition of expert performance. Psychol Rev it merely needs to figure out, on the fly, where to look, and 1993 Jul;100(3):363-406. DOI: http://dx.doi.org/10.1037/0033- when.19p27 295X.100.3.363. Colloquium sessions on perception, learning, decision mak- ing, and medical error impress on students the brain’s cogni- tive fallibility and proneness to error. Such an awareness of the ristics and biases. Students learn to distinguish “straight” brain’s cognitive fallibility is generally humbling. It instills in from “crooked” thinking, how to recognize the multifarious student learners a mindfulness about their own potential for forms of cognitive bias, and how the quality of their thinking being “wrong”19 about their beliefs, their perspectives on the has an impact on medical error and the effective practice world, and their decisions. For many students, this realization of medicine. Included in the readings for these sessions are is initially unsettling. They begin to worry about their own seminal works by Kahneman,23 Kahneman and Tversky,24 potential for medical error as they progress to their clinical Gardner,25 and de Bono,26 as well as physician-authors, such years. This realization, however, also impresses on them the as Groopman15 and Montgomery,16 who discuss how physi- relevance to their education of the colloquium’s metacognitive cians think and the kinds of cognitive errors physicians make. approach and the importance of mindfulness and ongoing Besides critical thinking, students are also taught about cognitive and emotional monitoring. the uses and abuses of intelligence testing.27 The colloquium emphasizes that intelligence is not a monolithic human at- Critical Thinking, Cognitive Flexibility, tribute but that there are “multiple intelligences” as described Learning Agility, and Mindfulness in Gardner’s25 Frames of Mind: The Theory of Multiple Intel- Critical Thinking and the Shape of Thought ligences. Having excelled in college examinations and in stan- Medical students in general are academic high achievers, dardized tests, medical students frequently hold a monolithic having scored at the top of their class in college examinations view of intelligence—the fast and analytical type that Gardner and in medical school admission tests. Yet they are generally terms analytical intelligence. They are surprised but often not trained as critical thinkers. Critical thinking as a discipline also encouraged to learn about Gardner’s other equally valid is seldom taught in US schools and colleges. Kuhn,21 in her forms of intelligence that include kinesthetic, music, linguistic, book Education for Thinking, writes: intrapersonal, and interpersonal intelligences. Many students are unable to give evidence of more than Students in the colloquium also discuss the pros and cons a superficial understanding of the concepts and relation- of group thinking and, in small groups, engage in exercises ships that are fundamental to the subjects they have studied in creative thinking. One such creative thinking exercise is … [I]t is possible to finish 12 or 13 years of public school de Bono’s26 “six thinking hats,” in which individuals in small education in the United States without developing much groups assume different thinking roles according to the color competence as a thinker. of the hat they are given to wear. Critical thinking is defined by Paul and Elder22 as “the art As a further example of integration between the humani- of analyzing and evaluating thinking with a view to improving ties and sciences, specific colloquium sessions focus on the it.” In the colloquium, we emphasize the “deliberate practice” biology of the brain and how specific neuropathologies can (see Sidebar: Deliberate Practice) of critical thinking both shape patterns of thinking. For instance, we assign readings as an intrinsically important skill, and to emphasize that the on how brain stroke can distort thinking and personal identity humanities are no less rigorous as intellectual disciplines (eg, Taylor,28 My Stroke of Insight); the effects of Alzheimer than the sciences. disease on memory and identity; and the biologic correlates Sessions on critical thinking include topics on the pitfalls of autism and other mental disorders. In addition, we explore of logic and the analysis of various forms of cognitive heu- the biologic basis of imagination and how imagination drives

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creative thinking.29 The objective of these colloquia is to under new or first time conditions.” To function effectively in make students aware that thinking emanates from a biologic a world of uncertainty and complex medical knowledge, the organ, the brain, an organ that is fallible and prone to its own physician of the future will, we at VSUM postulate, need to pathologies, as with all biologic organs. have the capacity for “cognitive flexibility” and be an “agile These colloquia thus serve to make students aware that learner.” These skills are therefore deliberately cultivated and thinking cannot be taken for granted but is the product of a nurtured in the colloquium. fallible biologic organ. Thinking as a “product” or emanation The discussion format of the colloquium encourages stu- of the brain is constrained, and our thought processes are dents to learn from the perspectives of their peers and men- subject to error. In medicine, this translates more specifically tors, and to integrate this learning into their own experience. into medical error—a topic further explored in dedicated The course impels students to develop the flexibility to adapt colloquium sessions. In view of these biologic constraints on their own thinking and perspectives to the particular contexts cognition, it becomes evident to students that a higher order (see Sidebar: Mobile Mind). of thinking to cultivate is “cognitive flexibility.” Cognitive flexibility includes such mental attributes as the Cognitive Flexibility and Learning Agility capacity to see the world from different perspectives and the The concept of cognitive flexibility has been well studied, capacity to be sufficiently flexible to change one’s mind. It although there is no consensus on a precise definition. Den- entails the ability to recognize one’s cognitive biases and to nis and Vander Wal30 suggest a general definition that entails see how the subjectiveness of one’s beliefs can obfuscate clear as a core component “the ability to switch cognitive sets to thinking. Cognitive flexibility is also an inherent quality of adapt to changing environmental stimuli.” The authors de- agile learning that the colloquium promotes as an emerging veloped an instrument, the Cognitive Flexibility Inventory, competency in medical education. which is designed to measure three components of cognitive As a consequence of the battery of tests medical students flexibility: “1) the tendency to perceive difficult situations as have taken, they may tend to overvalue factual knowledge controllable; 2) the ability to perceive multiple alternative over the nuanced, conditional, and contextual processes of explanations for life occurrences and human behavior; and thinking. Students in the colloquium may be perturbed to 3) the ability to generate multiple alternative solutions to dif- learn that “facts” are not immutable but that medical knowl- ficult situations.” Dennis and Vander Wal30 use this inventory edge churns over and changes, and its veracity is constantly to determine cognitive flexibility as a coping mechanism to reevaluated. Robinson32 showed that medical knowledge assess the ability of individuals to “successfully challenge doubles every 5 years and that approximately 90% of medical and replace maladaptive thoughts with more balanced and information becomes worthless and of little value in about adaptive thinking.”30p242-3 10 years from the date of publication. In the colloquium, we use cognitive flexibility to determine The emphasis in medical education on factual information how rigidly students adhere to their beliefs and/or precon- is misguided and can constrain cognitive flexibility and sup- ceived notions and ideas, as well as their capacity to gain press curiosity. In her acclaimed essay, “Curiosity,” Fitzgerald new insights and willingness to change their mind. We have suggests how the weight of factual knowledge in medical applied the Cognitive Flexibility Inventory to assess and moni- education can stifle student curiosity: “Medical education itself tor whether students change in their capacity to think more suppresses the expression of curiosity, emphasizing examin- flexibly and adaptively (see the later section, Evaluation of able facts rather than more ineffable thought processes in the College Colloquium). order to provide reproducible experiences for students.”33p71 An analogous term, learning agility, pertaining to flexibility Mindfulness and Mindful Learning in learning, was coined by Lombardo and Eichinger31 to con- The colloquium seeks to amend this static approach to note the “the willingness and ability to learn from experience, knowledge. Instead, we encourage students to be flexible, and subsequently apply that learning to perform successfully skeptical, and curious. To this end, a key attribute cultivated in the colloquium is mindfulness. Siegel has defined mindful- ness “in its most general sense [as being] about waking up Mobile Mind from a life on automatic and being sensitive to novelty in our 34p5 Berger uses a similar term, mobile mind, which Quirk1 everyday experiences.” paraphrases as a “skill set that involves respecting/embracing Students in the colloquium discuss readings on mindful- 34-36 multiple human values and orientations—even those that are ness in medicine and the qualities of mindful learning. In different from one’s own.” contrast to the learning of static facts and absolutes, mindful Berger (quoted in Quirk1) uses the term mobile mind to con- learning encompasses the ability to think in terms of condi- note the metacognitive concept that entails “a … cosmopolitan tions and contexts. In his book, The Mindful Brain, Siegel way of thinking—broad-mindedness, or an openness to envi- describes this difference between mindful learning and the ronment around us, including a sensitivity to differences and learning of factual knowledge as follows: respect for others.” When our minds lock onto something as being absolute, it enters our memory stores in a very different form from the Reference way it would were we to be tentative about the contexts and 1. Quirk M. Intuition and metacognition in medical education: keys to devel- conditions in which what we just learned might apply. … oping expertise. New York, NY: Springer Publishing Company, Inc; 2006.

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[We] can take a “fact” and create a rapidly accessible node said, a danger of individuals rigidly adhering to their own of neural firing patterns … but with conditional statement, perspectives, is “Every man takes the limits of his own field of that neural nodal point must have far more intricately estab- vision for the limits of the world.” A premise of the colloquium lished connections for it to meet the criteria for inclusion into is that students and trainees will function more effectively in the scaffold of knowledge. … [T]he conditional presentation teams if they develop the capacity to view social contexts and of mindful learning engages a more complex set of neural medical situations from different perspectives. This ability to associations, making it accessible in the future for retrieval hold different and contrasting perspectives is an attribute of in more flexible and adaptive ways.33p232-3 metacognitive capacity and skill.c Mindfulness and mindful learning are antidotes to the ab- The colloquium exposes students to the variegated perspec- solutes of factual learning and serve to sustain curiosity and tives of their mentors and peers.d In addition, students receive cognitive flexibility. It would seem intrinsically valuable for ongoing explicit or implicit feedback on their own views and physicians to cultivate these attributes of mind to effectively behaviors during colloquium sessions. The thoughts, opinions, navigate the immense complexity of medical knowledge and beliefs they express are further validated or negated in and the associated uncertainty in diagnosing and treating varying degrees by their college peers. Students will inevitably patients. The dynamism and flexibility associated with con- compare their perspectives with those of their peers and quite ditional, mindful learning in contrast to the rote learning of likely modulate or recalibrate their perspectives. (As argued factual knowledge trains physicians to know what they do later in the Mindfulness, Self-Monitoring, and Emotional not know, to ask the right questions, and ultimately to make Regulation section, this change in perspective also ultimately better-informed decisions. leads to behavior modification and emotional self-regulation.) Quirk refers to this capacity as “collective perspective taking” Professionalism and Professional Identity and associates this capacity with emotional self-regulation: Medical educators have tended to view professionalism as An essential capability of professionalism is acceptance of being driven primarily by particular behaviors. As a result, one’s role and regulation of role-related behaviors within the the focus on improving professionalism in medical schools group. … Collective perspective-taking and self-regulation has been on identifying undesirable behaviors with the aim capabilities are often how high-profile professions are judged of eliminating these behaviors. Quirk13p82 points out that this “from the outside” by the public.13p85-6 focus on defining and evaluating behaviors associated with Collective perspective taking instills in students a respect for professionalism “does not adequately ensure the depth of the views and opinions of their peers and others (see Sidebar: understanding necessary to deal with the new professional Mobile Mind). In the colloquium, we encourage students to challenges for generations of physicians to come.” Whether engage in vigorous debate and to disagree with each other this approach has been effective yet is doubtful because in a respectful manner. The term we use in the colloquium unprofessional behavior in medicine has not appreciably is respectful disagreement. Allowing students the intellec- declined over the years. tual and emotional space to respectfully disagree with each Professionalism in medical schools is frequently ap- other’s ideas and beliefs is essential for critical and creative proached in a manner that is static and prescriptive. thinking and is important in their development as medical Collective What is needed instead is a dynamic mindset that is professionals. In medical practice, these future physicians perspective aimed at understanding the root causes of behavior will find themselves disagreeing with colleagues, coworkers, taking instills and that encourages behavioral self-monitoring, reflec- and patients. Students therefore need to develop the skill to in students tion, and emotional regulation. Wear and Castellani37 disagree in a professional and respectful manner and to cali- a respect for propose a dynamic view of professionalism and sug- brate their thinking against the thinking of their colleagues. the views and gest that professionalism should be viewed not as a opinions of series of isolated behaviors or personality character Professionalism: Identity and Leadership their peers traits but instead as “an ongoing self-reflective process Disagreeing with one’s peers and going against the group and others involving habits of thinking, feeling, and acting.” can take courage. This topic is explored in the colloquium. The understanding of professionalism has been In a session on “How We Perceive/Misperceive” we assign (see Sidebar: problematic in part because of our incomplete under- readings by neuroscientist Berns,39p83-105 in which he describes Mobile Mind). standing of the scientific underpinnings of behavior. imaging experiments based on the well-known findings of Neurocognition offers a unique opportunity to under- Solomon Asch in the 1950s. These studies showed how in- stand the specific drivers of human behavior more accurately dividuals, rather than disagreeing with the group about their and scientifically, and it provides a more methodical and own valid perceptions, will change their mind and adopt an humanistic approach to modifying unprofessional behavior. incorrect perception to conform with the group opinion and allay their fears of opposing and being ostracized from the Professionalism: Respectful group. Challenging a group takes courage, a core quality of Disagreement and Perspective Taking leadership. A leader would do best knowing when to conform As individuals, we each hold differing perspectives of the with, and when to challenge, the group.e40 Understanding, world. As German philosopher Arthur Schopenhauer38 famously through neurocognition, the origins of the fear associated with

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challenging the group can be empowering to the individual feedback from others can be a major impetus for behavior and works to diffuse such fears associated with courageous modification, but it is nonetheless usually sporadic and can leadership. Thus, the neurocognitive approach of the col- also be misconstrued. For this reason, self-monitoring is an loquium is ultimately also an education in leadership. Such essential skill for effective behavior modification. Epstein et al group skills are central to working in medical teams and to defineself-monitoring as “an ability to attend, moment to mo- the student’s developing professional identity. ment, to our actions; curiosity to examine the effects of those actions; and willingness to use those observations to improve Cognitive Diversity, Empathy, behavior patterns and patterns of thinking in the future.”41p5 Mindfulness, and Emotional Regulation Self-monitoring is, however, also susceptible to misjudg- Cognitive Diversity and Empathy ment. As Epstein et al write in their seminal article, “Self-Moni- A major objective of the colloquium is to make students toring in Clinical Practice: A Challenge for Medical Educators”: aware of the immense diversity in human cognition (or cogni- [Self-assessment] requires the ability to distinguish high tive “wiring”). The realization of such diversity triggers a mind quality data from imagination and projection. The task is shift in the individual’s self-centeredness toward an other- difficult because the mind is ultimately both the object and centeredness, leading to a deepening in tolerance and empathy. the instrument of assessment, and our mental processes In her book Not for Profit: Why Democracy Needs the embed idealization directly within our self perceptions.41p6 Humanities, philosopher Nussbaum suggests how essential Nonetheless, Epstein et al41 suggest that self-monitoring to the humanities is this ability to view the world from the provides a solution to the problem of integrating internal and perspective of a “person different from oneself”: external data to assess personal performance and improve Citizens cannot relate well to the complex world around learning. It enables physicians and trainees to follow and as- them by factual knowledge and logic alone. … [W]hat we sess their own learning and mental processes for the purpose can call the narrative imagination … means the ability to of improving clinical practice. think what it might be like to be in the shoes of a person The deliberate practice of mindfulness that is nurtured and different from oneself, to be an intelligent reader of that explored through readings in the colloquium is one of the person’s story, and to understand the emotions and wishes main vehicles through which students accomplish such self- and desires that someone so placed might have. The culti- monitoring. Through mindful practice, as Epstein42 describes vation of sympathy has been a key part of the best modern it, students learn to self-regulate their emotions by bringing to ideas of democratic education.9p95-6 consciousness their deeply held values and knowledge, and A key function of the metacognitive approach to the humani- then integrating these with new information and perspectives.f ties is therefore to help students relate to the world through the Self-monitoring and emotional regulation are also essential eyes, emotions, and perspectives of others. This capacity elicits components of the resilience that physicians may need to and nurtures in medical students the essential professional sustain them through the uncertainties and emotional vicis- quality of empathy. Students often remark on how their per- situdes of medical practice. spectives change during the colloquium, rendering them more David and Congleton coined the term emotional agility to tolerant to alternate viewpoints and empathic toward others. describe “the ability to manage one’s thoughts and feelings … in a mindful, value-driven and productive way … in a Mindfulness, Self-Monitoring, complex, fast-changing knowledge economy.”43p89 The authors and Emotional Regulation expound this concept in the setting of business leadership Students in the colloquium receive from their peers and to describe the ability to apply effective inner strategies to mentors direct and indirect feedback on the views and opinions mindfully control negative thoughts and feelings that “sap they express in discussions, and on their general conduct. Such important cognitive resources” during meetings and man- agement experiences. For purposes of the colloquium, the term provides a helpful link with the concepts of cognitive Narrative Medicine flexibility and learning agility (discussed earlier) to suggest Rita Charon, MD, PhD, is a major proponent and one of the again how metacognition encompasses the capacity to moni- pioneers of narrative medicine, a field she helped consolidate tor both cognition and emotion. Of note, Flavell4 does not through her seminal work, Narrative Medicine: Honoring the use the terms emotional regulation and emotional agility but Stories of Illness.1 Charon distinguishes between “nonnarrative suggests a similar notion when he writes about “monitoring of knowledge” and “narrative knowledge” as follows: “Nonnarra- … memory, comprehension and other cognitive enterprises.” tive knowledge attempts to illuminate the universal by transcend- ing the particular; narrative knowledge, by looking closely at Narrative Medicine: A Metacognitive Tool individual human beings grappling with the conditions of life, for Eliciting and Nurturing Empathy attempts to illuminate the universals of the human condition by We introduce the topic of narrative medicine early in the revealing the particular.”1p9 colloquium to emphasize that medicine is not just about science but that the medical narrative is also important (and patients’ Reference “stories matter”). Many students are perplexed, and some are 1. Charon R. Narrative medicine: honoring the stories of illness. Oxford, irked, to hear that the patient’s “story” can at times have a United Kingdom: Oxford University Press; 2006.

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higher diagnostic value than test results in attaining a clinical stimulates parts of the brain such as mirror neurons that are diagnosis. How can a subjective “story” pose a challenge to implicated in the empathic response. Reading literary narrative a lifesaving medical “fact”? (See Sidebar: Narrative Medicine.) that delves into the lives of its characters and describes the These sessions apprise students of the importance of the complex social interactions between individuals can serve to patient’s “story,” which may contain critical clues to effective simulate empathic responses in the reader.45 A rigorous study diagnosis. The goal is to develop the student’s narra- published in Science recently demonstrated that reading liter- tive competence, which Charon44 defines as “the abil- ary fiction (compared with nonfiction and nonliterary fiction) Similar to the ity to acknowledge, absorb, interpret, and act on the evoked a measurable empathetic response in readers.46 These recent scientific stories and plights of others.” In the colloquium, we studies, moreover, demonstrate how the scientific method can finding that discuss a wide range of medical narratives (fictional shed light on how the brain processes literature, a humanistic reading literary and nonfictional) to give students a sense of narra- discipline. Such studies again demonstrate how the sciences and fiction can elicit tive structure and to further develop their narrative humanities should not be viewed as “silo” disciplines (“two cul- in the reader competence. This competence is further reinforced tures”) but as part of a unified field of human knowledge. Such an empathic through the personal narratives from medical practice a view validates the approach for integrating the humanities that students hear from their mentors, and through with the clinical and basic sciences in the medical curriculum. response, their own reflective writing (see Reflective Writing: A evidence Tool for Emotional Regulation and Professionalization). Reflective Writing: A Tool for Emotional suggests the Students are often intrigued that listening carefully to Regulation and Professionalization act of writing patients’ stories and developing their narrative com- We view the “deliberate practice” of writing personal and personal petence can have clinical and therapeutic relevance critical reflections as an integral component of the metacogni- reflections and should not be regarded as an inefficient use of tive approach (see Sidebar: Deliberate Practice). Similar to the can have time in clinical practice. recent scientific finding that reading literary fiction can elicit neurocognitive Narrative medicine is also viewed as a vehicle for in the reader an empathic response, evidence suggests the benefits. eliciting and nurturing student empathy. Medical hu- act of writing personal reflections can have neurocognitive manities courses generally include literature for this benefits.47-49 We view the writing of personal reflections also as implicit purpose of humanizing students and nurturing a way of connecting students with their inner voice and with empathy. More recently, neuroscience has shed light on how their innate empathy. Shapiro et al50 argue that writing personal literature, and specifically the act of reading literary narrative, reflections increases provider well-being, which includes the may be implicated in eliciting empathy. Neuroimaging stud- enhancement of “emotional equilibrium, self-healing and re- ies have recently shown that the act of reading literary fiction ducing isolation/restoring a sense of community” (see Sidebar: Two Phases of Reflective Writing). The reflective writing assignments in the colloquium are Two Phases of Reflective Writing usually about a personal experience related to medicine, for Shapiro et al distinguish two phases of reflective writing: the instance, the experience of a medical error that occurred dur- writing phase and the group reading and discussion phase. The ing the student’s own care or that of a close friend or family writing phase is “individual and solitary, consisting of personal member. However, we also assign critical reflections that reflection and creation. … [I]ntrospection and imagination guide include topics on the ethics of specific clinical scenarios as a learners from loss of certainty to reclaiming a personal voice.”1 way of integrating the clinical sciences into the colloquium. In the first two years of the College Colloquium, reflective We have developed a specific writing format called APCL writing involves only the writing phase. These reflections are (Analysis, Perspectives, Critique, Learning) that jump-starts held confidentially between students and their college mentors the creative writing process. The “Perspectives” section of this who provide formative feedback. We consider confidentiality reflective writing format is in keeping with the colloquium essential for the following reasons: 1) to give the students the notion of “perspective taking” (discussed in the section, Profes- space to find their “voice” without the potential anxiety of hav- sionalism: Respectful Disagreement and Perspective Taking). ing to read their reflections to the group and 2) to nurture trust The deliberate practice of writing personal reflections thus between students and mentors, which is important for molding reinforces other metacognitive components of the colloquium. the identity of the learning communities. Only in later years of medical school, after students have had more contact with Evaluation of the College Colloquium patients, do they move to the reading and discussion phase Students express a high level of satisfaction with the College discussed by Shapiro et al: “where sharing one’s writing results Colloquium. Results of an extensive (required) course evalua- in acknowledging vulnerability, risk-taking, and self-disclosure. tion demonstrate that 80% to 90% of students rated the College Listening to others’ writing becomes an exercise in mindfulness Colloquium as good to excellent. In particular, students valued and presence, including witnessing suffering and confusion hearing the perspectives of their peers in colloquium sessions experienced by others.”1p231 and frequently commented on how this had caused them to reevaluate their own perspectives and beliefs. In addition, Reference they valued hearing the “stories” of peers and mentors, and 1. Shapiro J, Kasman D, Shafer A. Words and wards: a model of reflective they commented on the trust that developed in their college writing and its uses in medical education. J Med Humanit 2006 Win- ter;27(4):231-44. DOI: http://dx.doi.org/10.1007/s10912-006-9020-y.

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over the course of the colloquium. Students valued the general Some have suggested that the metacognitive approach may clinical experience of their mentors and the willingness of be too abstract and premature for first-year medical students. In their mentors to share their personal experiences from medical the context of the personalized curriculum being implemented practice. The colloquium has therefore functioned as a true at VUSM, this approach seems to us highly appropriate for learning community. educating the physician of the future. Quirk concludes his The following are examples of some of the de-identified treatise on Intuition and Metacognition in Medical Education positive comments taken from the course evaluations: with the following emphatic statement: • “Colloquium provides a welcome change from the rigorous The personalized curriculum that is the hallmark of the science we learn and provokes interesting and relevant dis- new paradigm begins in the first year of medical school with cussion. The assignments … challenge our class in important the establishment of an infrastructure for thinking that will areas that are often overlooked in medical and premedical impact learning, practice and teaching. New evaluation curricula.” strategies must focus on the achievement of metacognitive • “The readings were great. I saved many for future reference as well as cognitive benchmarks and capabilities.13p133 v and shared them with friends and family.” • “I loved colloquium discussions. I have always walked a Neuroethicist Harris argues that our understanding of the world, of human well-being in the world, and the ethics for maximizing such well-being, away with having heard a new perspective that I hadn’t should derive not from philosophy but from the scientific study of the considered before.” brain: “Whatever can be known about maximizing well-being of conscious creatures—which … is the only thing we can reasonably value—must at Application of the Cognitive Flexibility Inventory, an in- some point translate into facts about brains and their interaction with the strument for determining student’s cognitive flexibility (as world at large.”6p11 mentioned earlier), showed that most students enhanced their b Wilson argues that this unification of knowledge is being spurred by the cognitive neurosciences: “As late as the 1970s most scientists thought the inventory score during colloquium. This indicated that they had concept of mind a topic best left to philosophers. Now the issue has been learned to think more adaptively, to perceive problems from joined where it belongs, at the juncture of biology and psychology. … The multiple perspectives, and to generate alternative solutions to cutting edge of the endeavors is cognitive neuroscience.”11p99 c Siegel considers the connection between multiple perspectives and complex situations. These pilot surveys suggest that the col- metacognition, as follows: “Embracing multiple perspectives has the quality loquium is achieving one of its major objectives of enhancing of a metacognitive skill. In the study of how we come to think about students’ cognitive flexibility. thinking, there are acquired capacities called representational ‘diversity’ and ‘change’ that enable individuals to sense that each of us may have a different perspective, and that even the viewpoint we have at one time may change Conclusion in the future. In this metacognitive view we can then see perspective as not In the setting of learning communities, the VUSM College only a changing frame of reference but also one that needs to be considered in viewing the situationally embedded meaning of knowledge.”34p242 Colloquium presents an innovative approach to teaching the d Flavell4 refers to the “personal category” of metacognition as “thinking humanities in medical school. Instead of viewing the humani- about cognitive differences within people, cognitive differences between ties as separate and isolated from the sciences, the colloquium people and cognitive similarities among all people.” He views this capacity as one of the “universal properties of human cognition.” seeks to integrate these intellectual domains (the “two cultures”) e Ringleb and Rock describe this dilemma as follows: “[B]eing a good group into a unified medical curriculum. Starting with a foundation in member involves an awareness of one’s thinking, feelings, behavior, and meta/neurocognition, the colloquium aims to train students not emotions with the ability to alter any one of those to satisfy group standards or expectations. … Once the circuitry [of the brain] senses that the individual’s only in critical thinking but also more broadly to engender the actions have or may violate group standards and that other group members qualities of cognitive flexibility and mindfulness as well as the are evaluating them negatively, the individual needs the self regulatory ability 40p372 capacities for cognitive and emotional monitoring and regula- to rectify the situation and re-establish or maintain group status.” f “Mindful practitioners use a variety of means to enhance their ability to tion. These qualities, coupled with an awareness in students engage in moment-to-moment self-monitoring, bring to consciousness their of the immense breadth of human cognitive diversity, serve tacit personal knowledge and deeply held values, use peripheral vision and subsidiary awareness to become aware of new information and perspectives, to elicit and nurture tolerance and empathy, which are core and adopt curiosity in both ordinary and novel situations.”42p833 attributes of the “good” physician. Bleakley and Bligh contend the following: Disclosure Statement Learning is largely a meta-process concerning legitimate The author(s) have no conflicts of interest to disclose. access to situated (context-linked) and distributed knowing. This is not to deny the value of one’s own store of knowledge, Acknowledgments but to place this in the wider and more pressing context The author wishes to sincerely thank the following individuals for of learning how to learn or how to access knowledge.51p80 kindly reviewing the manuscript at different stages of its preparation: Metacognition is such a “meta-process” that takes account Brian D Hodges, MD, PhD; Tom Janisse, MD; Jennie Ariail, PhD; of this broader continuum of learning to include how we learn Donald Moore, PhD; and Regina Russell MEd, MA. and access knowledge, as well as the context and social set- Kathleen Louden, ELS, of Louden Health Communications provided editorial assistance. ting of such learning. The metacognitive approach at VUSM is deliberately situated in the social setting of the colleges References (as described earlier) so that students come to appreciate the 1. Bleakley A. Broadening conceptions of learning in medical education: the participatory and peer context of learning, in contrast to the message from teamworking. Med Educ 2006 Feb;40(2):150-7. DOI: http:// individualistic acquisition of knowledge that mostly occurs in dx.doi.org/10.1111/j.1365-2929.2005.02371.x. 2. Snow CP. The two cultures. Cambridge, United Kingdom: Cambridge Uni- their basic and clinical science courses. versity Press; 1998.

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3. Flavell JH. Metacognitive aspects of problem solving. In: Resnick LB, editor. 15. Groopman J. How doctors think. New York, NY: Springer; 2007. The nature of intelligence. Oxford, United Kingdom: Lawrence Erlbaum 16. Montgomery K. How doctors think: clinical judgement and the practice of Associates; 1976 Aug. p 231-5. medicine. Oxford, United Kingdom: Oxford University Press; 2005 Nov. 4. Flavell JH. Metacognition and cognitive monitoring: a new area of cog- 17. Ofri D. What doctors feel: how emotions affect the practice of medicine. nitive-developmental inquiry. Am Psychol 1979 Oct;34(10):906-11. DOI: Boston, MA: Beacon Press; 2013. http://dx.doi.org/10.1037/0003-066X.34.10.906. 18. Menand L. The marketplace of ideas: reform and resistance in the American 5. Resnick LB, editor. The nature of intelligence. Oxford, United Kingdom: university. New York, NY: WW Norton & Company, Inc; 2010. Routledge; 1976 Jun. 19. Eagleman D. Incognito: the secret lives of the brain. New York, NY: 6. Harris S. The moral landscape: how science can determine human values. Pantheon Books; 2010 May 31. New York, NY: Free Press; 2011 Sep. 20. Schulz K. Being wrong: adventures in the margin of error. New York, NY: 7. Panksepp J, Biven L. The archaeology of mind: neuroevolutionary origins HarperCollins Publishers; 2010. of human emotions. 1st ed. New York, NY: WW Norton & Company, Inc; 21. Kuhn D. Education for thinking. Cambridge, MA: Harvard University 2012. p xxvii. Press; 2008. 8. Pinker S. How the mind works. New York, NY: WW Norton & Company, 22. Paul R, Elder L. Critical thinking: tools for taking charge of your learning Inc; 1997. and your life. 1st ed. Upper Saddle River, NJ: Prentice Hall; 2001. 9. Nussbaum MC. Not for profit: why democracy needs the humanities. 23. Kahneman D. Thinking, fast and slow. New York, NY: Farrar, Straus and Princeton, NJ: Princeton University Press; 2010. Giroux; 2011. 10. Bleakley A. Broadening conceptions of learning in medical education: the 24. Kahneman D, Tversky A. Choices, values, and frames. Am Psychol 1984 message from teamworking. Med Educ 2006 Feb;40(2):150-7. DOI: http:// Apr;39(4):341-50. DOI: http://dx.doi.org/10.1037/0003-066X.39.4.341. dx.doi.org/10.1111/j.1365-2929.2005.02371.x. 25. Gardner H. Frames of mind: the theory of multiple intelligences. 1st ed. 11. Wilson EO. Consilience: the unity of knowledge. New York, NY: Vintage New York, NY: Basic Books; 1983. Books; 1999 Apr. 26. de Bono E. Six thinking hats. 2nd ed. New York, NY: Back Bay Books; 1999. 12. Kulasegaram KM, Martimianakis MA, Mylopoulos M, Whitehead CR, 27. Gould SJ. The mismeasure of man. Revised & expanded ed. New York, NY: Woods NN. Cognition before curriculum: rethinking the integration of basic WW Norton & Company, Inc; 1996. science and clinical learning. Acad Med 2013 Oct;88(10):1578-85. DOI: 28. Taylor JB. My stroke of insight: a brain scientist’s personal journey. Lrg ed. http://dx.doi.org/10.1097/ACM.0b013e3182a45def. New York, NY: Large Print Press; 2006. 13. Quirk M. Intuition and metacognition in medical education: keys to 29. Doidge N. The brain that changes itself: stories of personal triumph developing expertise. New York, NY: Springer Publishing Company, Inc; 2006. from the frontiers of brain science. New York, NY: Penguin Group, 14. Damasio A. Descartes’ error: emotion, reason, and the human brain. New Inc; 2007. York, NY: Penguin Books; 2005.

Glossary

Cognitive diversity: A term indicating liberately”) and proactively designed to term refers to one’s ability to think about the immense differences in brain function improve performance, entailing focused one’s thinking and emotions and, to some and cognitive “wiring” that exists between attention to detail and ongoing feedback extent, predict what others are thinking individuals. It has been estimated that the (often with a teacher’s or coach’s help). and feeling. Flavell also uses another term, human brain contains some 100 billion Deliberate practice may be undertaken metacognitive knowledge, to describe neurons with trillions of synapses intercon- in intellectual domains such as chess or knowledge that “consists primarily of necting these neurons. These connections learning a language, in music, in business- knowledge or beliefs about what factors or are unique to each brain, resulting in an related activities, or in physical activities variables act and interact in what ways to immense diversity in the way we think such as sports. affect the course and outcome of cognitive and respond to the world. Moreover, these Emotional agility: A mindful, values- enterprises.”6p907 connections are constantly forming and driven, and productive way of managing Meta/neurocognition: I use these terms reforming, resulting in enormous plasticity one’s thoughts and feelings.3 interchangeably to indicate how the field that furthers increases this diversity. Emotional regulation: The ability to of metacognition is increasingly being Cognitive flexibility: The ability to regulate changes in one’s emotions, control informed by scientific findings in neurosci- switch cognitive sets in order to adapt to negative thoughts, and respond appropri- ence and neurocognition. changing environmental stimuli.1 Cognitive ately to a given context, and to modulate Mindful learning: A concept originally flexibility would determine how adaptively excitement, fear, and detachment in the proposed by Langer7-9 in which “learning is individuals can let go of preconceived face of challenge. offered in a conditional format rather than and untenable ideas and beliefs, and their Learning agility: The willingness and as a series of absolute truths. … [Mindful willingness to change their mind as new ability to learn from experience and learning] consists of an openness to nov- insights are gained. subsequently apply that learning to per- elty; alertness to distinction; sensitivity to Colloquium: Meaning “talking together” form successfully under new or first-time different contexts; [and] implicit, if not ex- from the Latin co + loquare. conditions.4 plicit, awareness of multiple perspectives; Deliberate practice: A concept ad- Metacognition: Flavell5 initially defined and orientation to the present.” vanced by Ericsson and colleagues,2 this term as “one’s knowledge concerning Mindfulness: Mindfulness in its most referring to a form of practice that is not one’s own cognitive processes and products general sense is “about waking up from a just routinely repetitive but carefully (“de- or anything related.” More broadly, the life on automatic, and being sensitive to

74 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ORIGINAL RESEARCH & CONTRIBUTIONS Thinking aboutabout Thinking Thinking and and Emotion: Emotion: The The Metacognitive Metacognitive Approach Approach to the to Medicalthe Medical Humanities Humanities that Integrates the Humanities with the Basic and Clinical Sciences that Integrates the Humanities with the Basic and Clinical Sciences

30. Dennis JP, Vander Wal JS. The cognitive flexibility inventory: instrument 42. Epstein RM. Mindful practice. JAMA 1999 Sep 1;282(9):833-9. development and estimates of reliability and validity. Cognit Ther Res 2010 DOI: http://dx.doi.org/10.001/jama.282.9.833. Jun;34(3):241-53. DOI: http://dx.doi.org/10.1007/s10608-009-9276-4. 43. David S, Congleton C. Emotional agility. Harv Bus Rev 2013 31. Lombardo MM, Eichinger RW. High potentials as high learners. Hum Resour Nov;91(11):125-7. Manage 2000 Winter;39(4):321-9. 44. Charon R. The patient-physician relationship. Narrative medicine: a 32. Robinson A. What smart students know: maximum grades. Optimum model for empathy, reflection, profession, and trust. JAMA 2001 Oct learning. Minimum time. 1st ed. New York, NY: Three Rivers Press; 17;286(15):1897-902. DOI: http://dx.doi.org/10.1001/jama.286.15.1897. 1993. 45. Mar RA. The neural bases of social cognition and story comprehension. 33. Fitzgerald FT. Curiosity. Ann Intern Med 1999 Jan 5;130(1):70-2. DOI: Ann Rev Psychol 2011;62:103-34. DOI: http://dx.doi.org/10.1146/annurev- http://dx.doi.org/10.7326/0003-4819-130-1-199901050-00015. psych-120709-145406. 34. Siegel DJ. The mindful brain: reflection and attunement in the cultivation 46. Kidd DC, Castano E. Reading literary fiction improves theory of mind. of well-being. New York, NY: WW Norton & Company, Inc; 2007. Science 2013 Oct 18;342(6156):377-80. DOI: http://dx.doi.org/10.1126/ 35. Langer EJ. Mindfulness. Reading, MA: Addison-Wesley; 1989. science.1239918. 36. Langer EJ. The power of mindful learning. Reading, MA: Addison-Wesley; 47. Pennebaker JW. Writing about emotional experiences as a therapeutic 1997. process. Psychol Sci 1997 May;8(3):162-6. DOI: http://dx.doi. 37. Wear D, Castellani B. The development of professionalism: curriculum org/10.1111/j.1467-9280.1997.tb00403.x. matters. Acad Med 2000 Jun;75(6):602-11. DOI: http://dx.doi. 48. Schön DA. The reflective practitioner: how professionals think in action. org/10.1097/00001888-200006000-00009. New York, NY: Basic Books; 1983. 38. Schopenhauer A. Studies in pessimism. New York, NY: Cosimo, Inc; 2007. 49. Schön DA. Educating the reflective practitioner: toward a new design for 39. Berns G. Iconoclast: what neuroscience reveals about how they think teaching and learning in the professions. 1st ed. San Francisco, CA: Jossey- differently. Watertown, MA: Harvard Business Press; 2008. Bass; 1987. p xvii. 40. Ringleb AH, Rock D. Teaching leadership with the brain in mind: leadership 50. Shapiro J, Kasman D, Shafer A. Words and wards: a model of reflective and neuroscience at CIMBA. In: Snook SA, Nohria N, Khurana R. The writing and its uses in medical education. J Med Humanit 2006 handbook for teaching leadership: knowing, doing, and being. Thousand Winter;27(4):231-44. DOI: http://dx.doi.org/10.1007/s10912-006-9020-y. Oaks, CA: Sage Publications; 2012. p 369-86. 51. Bleakley A, Bligh J. Looking forward-looking back: aspects 41. Epstein RM, Siegel DJ, Silberman J. Self-monitoring in clinical practice: of the contemporary debate about teaching and learning a challenge for medical educators. J Contin Educ Health Prof 2008 medicine. Med Teach 2007 Mar;29(2-3):79-82. DOI: http://dx.doi. Winter;28(1):5-13. DOI: http://dx.doi.org/10.1002/chp.149. org/10.1080/01421590701206780.

novelty in our everyday experiences.”10 Professional identity: The values, com- 1993 Jul;100(3):363-406. DOI: http://dx.doi. (Mindfulness in medicine should be dis- org/10.1037/0033-295X.100.3.363. mitments, responsibilities, and particular 3. David S, Congleton C. Emotional agility. Harv tinguished from mindfulness as a form of contextual behaviors that members of a Bus Rev 2013 Nov;91(11):125-7. meditation that entails an “emptying of profession share at the level of the self 4. Lombardo MM, Eichinger RW. High potentials the mind.”) as high learners. Hum Resour Manage 2000 and the group, and that creates a sense Winter;39(4):321-9. Mindful practice: Epstein et al define of belonging to the same group. From a 5. Flavell JH. Metacognitive aspects of problem mindful practice as the “conscious and metacognitive perspective, Quirk defines solving. In: Resnick LB, editor. The nature of in- intentional attentiveness to the present telligence. Oxford, United Kingdom: Lawrence professional identity as “collective meta- Erlbaum Associates; 1976 Aug. p 231-5. situation—the raw sensations, thoughts, cognition [that] significantly influences 6. Flavell JH. Metacognition and cognitive moni- and emotions as well as the interpretations, professional behavior ... [and that] requires toring: a new area of cognitive-developmental judgments, and heuristics that one applies inquiry. Am Psychol 1979 Oct;34(10):906-11. the capabilities to reflect on, assess, and DOI: http://dx.doi.org/10.1037/0003- 11p9 to a particular situation.” modify one’s values, attitudes and behavior 066X.34.10.906. Perspective taking: “A metacognitive in relation to those of the profession.”12p83 7. Langer EJ. Mindfulness. Reading, MA: Addison- Wesley; 1989. capability that demands thinking about Self-monitoring: The “ability to attend, 8. Langer EJ. The power of mindful learning. another’s thoughts and feelings. … Expert moment to moment, to our actions; curios- Reading, MA: Addison-Wesley; 1997. perspective-takers control their inter- ity to examine the effects of those actions; 9. Langer EJ. Mindful learning. Current personal interactions and relationships and willingness to use those observations Directions in Psychological Science, 2000 Dec;9(6):220-23. through mastery of empathy, patient educa- to improve behavior patterns and patterns 10. Siegel DJ. The mindful brain: reflection and at- tion, and negotiation.”12p32 of thinking in the future.”11p5 tunement in the cultivation of well-being. New Professionalism: Professionalism in York, NY: WW Norton & Company, Inc; 2007. 11. Epstein RM, Siegel DJ, Silberman J. Self- medical education may be viewed as a References monitoring in clinical practice: a challenge for competency entailing such attributes and 1. Dennis JP, Vander Wal JS. The cognitive flex- medical educators. J Contin Educ Health Prof behaviors as responsibility, accountability, ibility inventory: instrument development and 2008 Winter;28(1):5-13. DOI: http://dx.doi. estimates of reliability and validity. Cognit Ther org/10.1002/chp.149. honesty, and caring, as well as the appropri- Res 2010 Jun;34(3):241-53. DOI: http://dx.doi. 12. Quirk M. Intuition and metacognition in medi- ate and ethical application of knowledge, org/10.1007/s10608-009-9276-4. cal education: keys to developing expertise. in the relationship between doctor and 2. Ericsson KA, Krampe, RT, Tesch-Römer C. New York, NY: Springer Publishing Company, The role of deliberate practice in the acqui- Inc; 2006. patient. sition of expert performance. Psychol Rev

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 75 REVIEW ARTICLE A Business Case for Tele-Intensive Care Units

Alberto Coustasse, DrPH, MD, MBA, MPH; Stacie Deslich, MA, MS; Deanna Bailey, MS; Alesia Hairston, MS; David Paul, DDS, PhD Perm J 2014 Fall;18(4):76-84 http://dx.doi.org/10.7812/TPP/14-004

monitoring to sites with high levels of Abstract need via private, dedicated telecommu- Objectives: A tele-intensive care unit (tele-ICU) uses telemedicine in an intensive nications lines.9 Networks of audiovisual care unit (ICU) setting, applying technology to provide care to critically ill patients by communication and computer systems off-site clinical resources. The purpose of this review was to examine the implementation, link hospital ICUs to intensivists and adoption, and utilization of tele-ICU systems by hospitals to determine their efficiency other critical care professionals, who and efficacy as identified by cost savings and patient outcomes. are able to access patient data such as Methods: This literature review examined a large number of studies of implementa- medical records, to conduct remote real- tion of tele-ICU systems in hospitals. time monitoring of vital signs or chronic Results: The evidence supporting cost savings was mixed. Implementation of a tele- conditions, or to facilitate staff interactions ICU system was associated with cost savings, shorter lengths of stay, and decreased via video, phone, or online computer. mortality. However, two studies suggested increased hospital cost after implementa- Video cameras located on the ceiling of tion of tele-ICUs is initially expensive but eventually results in cost savings and better an ICU patient room are situated to allow clinical outcomes. telemedicine practitioners to observe Conclusions: Intensivists working these systems are able to more effectively treat ICU equipment and monitors in the patient’s patients, providing better clinical outcomes for patients at lower costs compared with room. Cameras often have an alert sys- hospitals without a tele-ICU. tem to announce that the tele-ICU staff is in visual contact to share observations Introduction about $67 billion annually, with mortality and care recommendations with bedside Telemedicine is the use of medical rates ranging from 10% to 28%, or ap- caregivers.10 These devices and elements information exchanged from one site to proximately 540,000 deaths each year.6-8 are vital to the successful application of another via electronic communications to Tele-ICUs may be effective by de- tele-ICUs. As has been noted, without improve a patient’s clinical health status. creasing costs, decreasing ICU length appropriate electronic medical records Telemedicine includes a growing variety of stay (LOS), decreasing medication er- and clinical decision support systems, or of applications and services using two- rors, and increasing patient safety when lacking patient-related data and informa- way video, smart phones, wireless tools, adopted and implemented in hospitals. tion, clinicians may make inappropriate and other forms of telecommunications Two distinct types of tele-ICU have been treatment recommendations.11 technology.1 A tele-intensive care unit identified. The decentralized tele-ICU is Studies have demonstrated both clini- (tele-ICU) involves the use of telemedi- a medical facility or multiple medical fa- cal and economic benefits associated cine in an intensive care unit (ICU), using cilities that can be accessed from remote with adoption of tele-ICUs, including technology to assist in providing care for sites such as office, home, or mobile. decreased mortality rate, decreased fre- critically ill patients by off-site clinical There is no distinct tele-ICU; rather there quency of ICU complications, decreased resources.2 is a process of care having multiple sites ICU LOS and decreased ICU costs after a In the US, more than 4 million patients of access to the patient, with intensivists 16-week implementation of technology- are admitted to ICUs each year; treatment monitoring the patients. A centralized tele- enabled remote care.12-14 Additionally, it of these critically ill patients has been ICU program is often the tele-ICU system has been found that tele-ICU use can estimated to account for 30% of costs of choice. In the centralized system, one decrease medication errors and improve of acute care hospitals.3,4 Patient safety central ICU provides intensive care via patient safety.11 A meta-analysis of non- concerns persist in the ICU, and serious telemedicine and remote monitoring to severity-adjusted data from 11 studies medication errors account for 78% of all several satellite ICUs. confirmed these results and found the errors in the ICU.5 Hospital costs for criti- In the tele-ICU model, the tele-ICU is decrease of ICU mortality and ICU LOS, cally ill patients have been estimated to be a definable entity providing continuous as well as hospital mortality and hospital

Alberto Coustasse, DrPH, MD, MBA, MPH, is an Associate Professor of Management, Marketing, and Management Information Systems at Marshall University in Charleston, WV. E-mail: [email protected]. Stacie Deslich, MA, MS, is an Alumna of the Health Care Administration Program at Marshall University in Charleston, WV. E-mail: [email protected]. Deanna Bailey, MS, is an Alumna of the Health Care Administration Program at Marshall University in Charleston, WV. E-mail: [email protected]. Alesia Hairston, MS, is an Alumna of the Health Care Administration Program at Marshall University in Charleston, WV. E-mail: [email protected]. David Paul, DDS, PhD, is an Associate Professor of Marketing and Health Care Management at the Leon Hess Business School at Monmouth University in West Long Beach, NJ. E-mail: [email protected].

76 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 REVIEW ARTICLE A Business Case for Tele-Intensive Care Units

LOS to be statistically significant.15 These outcomes are particularly important be- cause studies that reported results on the basis of both severity-adjusted data and non-severity-adjusted data have found that the level of statistical significance of these outcome variables when using non- severity-adjusted data was higher than when using severity-adjusted data.16,17 These findings indicate that the benefits of tele-ICU implementation reach all populations of patients, regardless of Figure 1. Research framework. severity of illness. ICU = intensive care unit. It has been estimated that full imple- mentation of the tele-ICU standard in community hospitals could prevent be- frequently have such complex medical prescribing technologies, thus supporting tween 5400 and 13,400 deaths and could and/or surgical conditions, intensive care its internal validity.25-27 potentially save $5.4 billion annually.18,19 provided via a tele-ICU system can pro- The review was conducted in stages, One of the main barriers to adoption of vide this care and decrease hospital cost.23 including: 1) determining the search strat- tele-ICUs has been adoption and imple- The purpose of this review was to egy and establishing inclusion and exclu- mentation cost: the cost of construction, examine the implementation, adoption, sion criteria, 2) literature analysis, and 3) installation, and training. The “command and utilization of tele-ICU systems by extracting and categorizing the findings. center” for a tele-ICU system has been es- hospitals to determine their efficiency and timated to cost between $2 and $5 million, efficacy as identified by cost savings and Step 1: Determining the Search with each additional tele-ICU added to the patient outcomes. Strategy and Establishing system costing $250,000.20 Such substan- Inclusion and Exclusion Criteria tial financial outlays can be a challenge Methods When executing the search, the fol- for hospitals and health systems that lack The methods employed for this study lowing terms were used: “tele-ICU” or significant financial funds or borrowing were a literature review and a review of “telemedicine ICU” or “virtual ICU” and capacity, especially with annual operat- case studies. The research approach for “cost” or “benefits.” A mix of databases ing costs of about $2 million, including the examination of the promotion factors and online sources were used to com- maintenance costs, licenses, staffing ex- and barriers to adoption of tele-ICUs was pile a set of references covering both penses, and additional upgrades.21 If the customized to this study following the academic peer-reviewed research and tele-ICU system is not fully compatible conceptual framework used by Yao et al24 practitioner literature. It was believed that with the hardware or software systems (Figure 1). Figure 1 depicts the process of this approach would help create the most of the physical ICU, additional software, IT adoption in health care, in this case, the comprehensive and up-to-date review. hardware, and infrastructure may be re- tele-ICU. To research how tele-ICU can The following electronic databases and quired, which would require additional help improve health care practices in the sources were used: PubMed, Academic cost to the hospital. ICU, it is first necessary to recognize the Search Premier, Science Direct, ProQuest, Regardless of the need for upgrades, existing problems in the ICU and issues and Google Scholar. The Web sites of the staff must overcome additional barri- that drive and impede adoption of this Society of Critical Care Medicine and the ers such as computer issues, including technology by the hospital industry; then American Telemedicine Association also difficulty logging on, short battery life, different applications can be identified to were searched. frequent rebooting, and other technical solve or partially unravel these challenges. issues with computers or software. Some By analyzing the literature, the benefits Step 2: Literature Analysis of the possible solutions for these prob- and barriers of tele-ICU utilization in The literature review yielded 76 sourc- lems include ensuring computers remain health care can be identified (Figure 1). es, which were assessed for information plugged in, confirming that passwords The use of this framework in the current pertaining to this research project. Given are able to be used in multiple programs, study is appropriate because the focus the technology- and enterprise-oriented and providing information technology of this study, as in that by Yao et al,24 is nature of the current study, literature was (IT) assistance by phone and on-site as to show how new technologies and IT selected for review on the basis of finan- required.22 systems can be applied to health care cial, technological, and organizational Although tele-ICUs are expensive to settings to enhance the care of patients. impacts. References were reviewed and implement, with startup costs between In addition, this conceptual approach has determined to have satisfied the inclusion $50,000 and $100,000 per bed, the benefits been successfully replicated in previous criteria if the material provided accurate of tele-ICU utilization may far outweigh studies, including adoption of tele-ICU, ra- information about the tele-ICU with a those costs for ICUs. Because ICU patients diofrequency identification, and electronic particular focus on benefits and barriers

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to its implementation. Only articles that VISICU to be approximately 20% of the patient turnover resulting from decreased were written in English were included for software costs, or about $300,000 for 100 LOS.34 Table 2 displays the findings of the review. Given the rapid changes in tech- beds.30 Staffing costs depended on hours patient cost reduction of $2150 per stay nology, studies that were published be- in use and level of additional staff in the based on reduced patient expenses and fore 2001 were excluded from the search. off-site center; typical staffing scenarios increased ICU capacity as well. added approximately $1 to $2 million per The centralized model has allowed Step 3: Literature Categorization year per 100 beds covered.31 optimization of time and services of In the third step, selected academic intensivists without the requirement of articles and practitioner health IT sources Brief Case Study 1: staffing intensivists at multiple locations. were analyzed, and relevant categories Sentara Healthcare The availability of intensivists in a single were identified. The findings are presented Sentara Healthcare in Norfolk, VA, was location also has given patients the op- in the subsequent sections using the cat- the nation’s first health system to establish portunity to stay in location, instead of egories of cost of telemedicine technology a tele-ICU program in 2000 through the traveling and being transferred to a dif- in the ICU and several case studies. The use vendor VISICU (now Philips VISICU).32 ferent hospital.35 As of 2010, more than 1 of brief case studies was thought to illus- Implementation of the tele-ICU at Sentara million ICU patients had been cared for trate real cases of tele-ICU implementation. Norfolk General Hospital and Sentara using the strategy of frequent reassess- Hampton General Hospital took 5 months ment, alert-prompted evaluation, and Results and cost more than $1 million. In 2002, rapid response to clinical needs.34 How Tele-ICUs Sentara reported a reduction in hospital Can Be Cost-Effective mortality of 26%, with a 17% decrease in Brief Case Study 2: According to the leading tele-ICU sys- ICU LOS (Table 1).33 University of Massachusetts tems vendor, Philips VISICU in Baltimore, Findings from an independent evalu- Memorial Medical Center MD, tele-ICU implementation costs ranged ation by Cap Gemini Ernst & Young, The University of Massachusetts Memo- from about $50,000 to $100,000 per bed, London, United Kingdom, suggested a rial Medical Center in Worcester, MA, and the cost of equipping 100 beds was $2 million tele-ICU cost that was offset installed a tele-ICU command center in approximately $3 to $5 million.28,29 Annual by $3 million in net savings annually.33 2005 and extended the tele-ICU coverage operating costs (eg, overhead, mainte- It reported extra revenue, approximately to 2 Massachusetts community hospitals in nance, staffing) were estimated by Philips $460,000 per month, because of increased 2007 and 2008. Over 3 years, 1 tele-ICU

Table 1. Tele-intensive care unit cases studied, implementation costs, and outcomes Implementation costs Institution Setting (US dollars) Major results/outcomes Sentara Healthcare Sentara Healthcare,a academic tertiary care 1 million Decreased ICU LOS by 17%; decreased medical center with 5 ICUs, 103 critical care beds hospital mortality by 26.4%33,36 New England Healthcare University of Massachusetts Memorial Medical 7.12 million Decreased ICU LOS (from 13.3 to 9.8 Institute and Massachusetts Center, academic hospital with 5 adult ICUs, days); decreased mortality from 13.6% to Technology Collaborative 130 beds, 7000 ICU patients 11.8%; recovered costs of implementation; lowered rates of complications36 Resurrection Health Care Community hospitals with 14 ICUs, 182 critical 7 million 6 months after implementation: 38% care beds decrease in ICU LOS, approximately 37,38 Pre- and postimplementation design; $3 million in cost savings preimplementation: n = 2034 patients; postimplementation: n = 2134 a Includes both Sentara Norfolk General Hospital and Sentara Hampton General Hospital. ICU = intensive care unit; LOS = length of stay.

Table 2. Sentara Healthcare and Resurrection Health Care tele-intensive care unit implementation savings Cost of implementation Hospital (US dollars) Outcomes Cost saving Sentara Healthcare 1 million Reduction in mortality by 27%; Reduced patient cost of $2150; average case (savings from 2002 to 2010) decreased LOS of 17% contribution margina increased by 55.6%33,36 Resurrection Health Care 7 million Decreased LOS of 38% 7% reduction in blood transfusions ($11,200 in savings); (savings from 2007 to 2011) estimated total cost savings of $11.5 million37,38 a Average case contribution margin is the selling price per unit minus cost per unit. Contribution represents the portion of sales revenue that is not consumed by variable costs and so contributes to the coverage of fixed costs. LOS = length of stay.

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Figure 2. University of Massachusetts Memorial Medical Center: one-time costs for tele-intensive care unit implementation, 2010.36 ICU = intensive care unit; Misc = miscellaneous.

command center extended coverage to cine into its 14 ICUs in 2007. The tele-ICU reported, including $11,200 from a 7% 9 adult ICUs covering 116 ICU beds in command center in Resurrection’s Holy reduction in blood transfusions. The hos- central Massachusetts.36 Family Medical Center (now Presence pital found a 38% decrease in ICU LOS in Figure 2 shows the initial expenses of Holy Family Medical Center) promoted 6 months, which totaled to approximately implementation of a tele-ICU at the medi- proactive intervention, including trended $3 million in savings (Table 2). cal center. The total operating costs of alerts, which showed incremental changes Resurrection Health Care leadership $7.12 million also required an increment in such factors as blood pressure, oxygen wanted to know how the system was of annual operating cost of $3.15 mil- levels, and drip rates.37 going to prove its return on investment lion. Licensing and implementation fees In the first 6 months after installation on the $7 million spent to set up all 14 accounted for 34% of the total expenses. in 2007, a cost savings of $3 million was ICU systems simultaneously. In 2011, it Tele-ICU equipment costs and support center and servers accounted for $1.1 million and $1.19 million, respectively (Figure 2). Figure 3 shows the operating costs and the continuous ongoing costs for the tele- ICU. The main ongoing cost was clinical salaries and benefits accounting for 72% or $2.27 million, followed by nonclinical salaries at 20% or $630,000 (Figure 3). The centralized tele-ICU program has been one of the most beneficial programs to the medical center. The positive net revenue produced a rapid payback such that total costs of implementation were recovered within 1 year.36

Brief Case Study 3: Resurrection Health Care Covering 7 acute care hospitals and a long-term care facility, Resurrection Figure 3. University of Massachusetts Memorial Medical Center ongoing operating Health Care in Des Plaines, IL (now part costs, 2010.36 of Presence Health), introduced telemedi- ICU = intensive care unit; MD = physician; NP = nurse practitioner; PA = physician assistant.

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was reported that it had a $387,000 fi- case increased from $13,029 to $19,324 or greater increased from 23% to 70%, and nancial benefit: tele-ICU support for ICU after tele-ICU installation.39 central line placements increased from patients across the health care system Costs per patient for hospitals in- 33% to 50%.53 Higher rates of ICU staff resulted in 9000 ICU days saved, for an creased, but the patient out-of-pocket adherence to critical care best practices, estimated cost savings of $11.5 million. expenses remained the same, causing the reduction of ICU LOS, and improved Also, it was reported that the reengineer- hospitals to need to find some way to ab- patient care were found in several stud- ing of the existing tele-ICU infrastructure sorb the financial losses of tele-ICU imple- ies (Table 5). Quality improvement and was expanded to support telestroke, mentation. Average ICU hospital cost per patient care have been improved by the telepsychiatry, telemedicine with skilled patient was $20,231 in the pretest period implementation of the tele-ICU by increas- nursing facilities, and sepsis management and $25,846 in the posttest period, which ing the use of evidence-based protocols initiatives.38 was financially and statistically significant for sepsis, ventilator-associated pneumo- (Table 4). Overall, the installation of the nia, and blood transfusion (Table 5).67-70 Brief Case Study 4: tele-ICU programs in the 6 ICUs was as- In 2013, Kumar et al71 combined a Six Intensive Care Units sociated with higher costs not attributable systematic review with cost data from the in Five Large Hospitals to medical inflation. These researchers did implementation of a tele-ICU program in A study by Franzini et al39 was con- note that sicker patients exhibited lower 7 ICUs (74 beds) in the Veterans Health ducted to determine the costs and mortality; thus ICUs with high volumes of Administration to measure the cost of tele- cost-effectiveness of 6 ICUs in 5 large severely ill patients may gain more finan- ICU programs. According to the authors, hospitals in the Gulf Coast region after cial benefit with the utilization of tele-ICU it was estimated that the first-year costs of the installation of a tele-ICU program. technology. The researchers also noted implementation ranged between $70,000 The sample included 4142 patients in the that about two-thirds of ICU physicians in and $87,000 per ICU bed. The Veterans 6 different ICUs: 2034 patients were from the study chose only minimal participation Health Administration also projected cost the pretest period and 2108 were from in the tele-ICU intervention. for staffing and operating the monitoring the posttest period. Table 3 shows the site for the first year as $3300 or 27% of ICU average daily cost before and after Positive Outcomes of total cost. The researchers also reported the tele-ICUs were implemented. The Tele-ICU Implementation that tele-ICU studies with vendor asso- average daily costs and costs per case in- In terms of effectiveness, the literature ciation presented cost savings of $2600 creased in all 6 ICUs after implementation on tele-ICUs demonstrated improved to $3000 per patient, whereas studies (posttest period) from the period before hospital financial performance, improved without vendor association suggested implementation of the tele-ICU (pretest ICU financial performance, improved increased hospital cost after implemen- period). Overall, the daily average ICU teamwork climate and safety climate, tation. Hospital cost per patient ranged cost increased from $2851 to $3653, or and improved patient care (Table 5).40-66 from a reduction of $3000 to an increase a 28% increase after tele-ICUs were in- A tele-ICU program enhanced compliance of $5600.71 stalled, which was statistically significant. to evidence-based practice bundles for se- Two hospitals experienced cost increases vere sepsis. Between January 1, 2006, and Discussion greater than 30% (Table 3).39 December 31, 2008, antibiotic administra- This research study has examined The floor daily average costs increased tion increased from 55% to 74%, serum potential benefits of implementing a 16%, from $1451 to $1687, after tele-ICUs lactate measurement increased from 50% centralized tele-ICU system. The evidence were installed. The overall ICU costs per to 66%, the initial fluid bolus of 20 mL/kg supporting cost savings is mixed. The

Table 3. Average daily costs (US dollars) before and after tele-ICU installation in six intensive care units in 201039 Costs Overall ICU 1 ICU 2 ICU 3 ICU 4 ICU 5 ICU 6 Before tele-ICU period 2851 2586 3647 4248 3155 2355 2370 After tele-ICU period 3653 3272 4307 4252 4131 3275 2746 Change (%) 802 (28) 686 (27) 660 (18) 4 (0) 976 (31) 920 (39) 376 (16) ICU = intensive care unit.

Table 4. Intensive care unit costs per case (US dollars) before and after tele-ICU installation in six intensive care units in 201039 Costs Overall ICU 1 ICU 2 ICU 3 ICU 4 ICU 5 ICU 6 Before tele-ICU period 13,029 7422 12,912 26,296 8770 13,328 15,167 After tele-ICU period 19,324 10,797 18,519 33,594 19,002 15,392 18,947 Change (%) 6295 (48) 3374 (45) 5608 (43) 7298 (28) 10,232 (117) 2065 (15) 3780 (25) Average cost: before tele-ICU 20,231 period vs after tele-ICU period vs 25,846 ICU = intensive care unit.

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Table 5. Studies addressing tele-ICU implementation and utilization Author, year Study design Outcome Aaronson et al, 200640 Literature review Higher rates of ICU staff adherence to critical care best practices Badawi et al, 201041 Pre/posttest of tele-ICU implementation Higher rates of ICU staff adherence to critical care best practices Badawi and Shemmeri, 200642 Pre/posttest of tele-ICU implementation Higher rates of ICU staff adherence to critical care best practices Berenson et al, 200931 Literature review Improved patient care Breslow et al, 200412 Pre/posttest of tele-ICU implementation across several Improved hospital financial performance, improved ICU financial hospitals performance, improved patient care Chu-Weininger et al, 201043 Pre/posttest of tele-ICU implementation and utilization Improved teamwork and/or safety climate in 3 ICUs Coletti et al, 200844 Cross-sectional survey of residents in ICU Improved teamwork and/or safety climate and tele-ICUs Dickhaus, 200645 Pre/posttest of tele-ICU implementation and utilization Lower ICU LOS in a multistate hospital system Giessel and Leedom, 200746 Pre/posttest of tele-ICU implementation and utilization Higher rates of ICU staff adherence to critical care best practices Groves et al, 200813 Literature review Lower ICU LOS Howell et al, 200747 Pre/posttest of tele-ICU implementation and utilization Lower ICU LOS Howell et al, 200848 Pre/posttest of tele-ICU implementation and utilization Lower ICU LOS Ikeda et al, 200967 Pre/posttest of tele-ICU implementation and utilization Lower ICU LOS Kohl et al, 200749 Pre/posttest of tele-ICU implementation and utilization Lower ICU LOS Kohl et al, 200750 Pre/posttest of tele-ICU implementation and utilization Improved ICU financial performance, lower ICU LOS Kohl et al, 201216 Pre/posttest of tele-ICU implementation and utilization Lower ICU LOS Kumar et al, 201351 Literature review Improved ICU financial performance Khunlertkit and Carayon, 201311 Qualitative study with semistructured interview Improved ICU staff adherence to evidence-based protocols for of tele-ICU staff sepsis, ventilator-associated pneumonia, and blood transfusion Lilly et al, 201117 Pre/posttest of tele-ICU implementation and utilization Higher rates of ICU staff adherence to critical care best practices, lower ICU LOS, improved patient care Mora et al, 200752 Survey of residents practicing in tele-ICUs Improved patient care Norman et al, 200953 Literature review and meta-analysis Improved ICU financial performance Patel et al, 200754 Pre/posttest of tele-ICU implementation and utilization Higher rates of ICU staff adherence to critical care best practices, of 6 tele-ICUs lower ICU LOS Rincon et al, 200755 Pre/posttest of tele-ICU utilization in prevention Higher rates of ICU staff adherence to critical care best practices: of sepsis • Antibiotic administration increased from 55% to 74% • Serum lactate measurement increased from 50% to 66% • Central line placements increased from 33% to 50% Scales et al, 201156 Literature review Higher rates of ICU staff adherence to critical care best practices Thomas et al, 200757 Pre/posttest of tele-ICU implementation and utilization Improved teamwork and/or safety climate Vespa et al, 200758 Pre/posttest of tele-ICU implementation and utilization Improved ICU financial performance, lower ICU LOS, improved patient care Wilcox and Adhikari, 201215 Meta-analysis of 11 studies Lower ICU LOS Willmitch et al, 201259 Pre/posttest of tele-ICU implementation and utilization Lower ICU LOS over 3 years Youn, 200660 Literature review and meta-analysis Higher rates of ICU staff adherence to critical care best practices Young et al, 201161 Meta-analysis of 11 studies Lower ICU LOS Zawada et al, 200662 Survey of physicians practicing in remote areas using Higher rates of ICU staff adherence to critical care best practices, tele-ICU lower ICU LOS Zawada et al, 200763 Pre/posttest of tele-ICU implementation and utilization Improved ICU financial performance, lower ICU LOS Zawada et al, 200864 Pre/posttest of tele-ICU implementation and utilization in Higher rates of ICU staff adherence to critical care best practices, a rural health care system improved ICU financial performance Zawada and Herr, 200865 Pre/posttest of tele-ICU implementation and utilization Improved patient care Zawada et al, 200966 Pre/posttest of tele-ICU implementation and utilization Improved hospital financial performance ICU = intensive care unit; LOS = length of stay.

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hospitals in the first three cases expe- across 8 states, supporting decreasing to produce organizational change, with rienced some benefit in terms of cost mortality and shorter LOS with increased clinical and nonclinical ICU staff becom- reduction, a decreased ICU LOS, or an cost savings for the hospitals implement- ing more efficient and effective, and to overall improved efficiency. ing the tele-ICU programs. decrease ICU LOS, hospital costs, and The return on investment for hospitals Overall, hospitals have few research ICU mortality. v implementing a tele-ICU system depends findings to help guide them when making on how the system is used, as well as the a decision about whether to adopt and Disclosure Statement number of patients the hospital ICU treats. to use a tele-ICU program. The findings The author(s) have no conflicts of interest If a hospital system wants to use a tele-ICU of this literature search suggest that the to disclose. system for safety reasons or to make their implementation of a centralized tele-ICU workforce more efficient, the tele-ICU is system can be cost-effective and can result Acknowledgment a tool that could help. Another benefit in more efficient use of the hospital’s ICU Katheleen Louden, ELS, of Louden Health Communications provided editorial of tele-ICU implementation has been an staff, improvement in the quality of care assistance. expansion of markets; the tele-ICU allows provided, and a financial positive impact health care facilities to take care of more by the reduction of ICU LOS. References patients, which decreases geographic barri- There were several limitations of this 1. What is telemedicine? [Internet]. Washington, ers and allows the provision of ICU services study review. Many articles documented DC: The American Telemedicine Association; c2012 [cited 2014 Feb 19]. Available from: into previously inaccessible markets, such the benefits of tele-ICUs but contained www.americantelemed.org/learn/what-is- as those in rural areas. limited data on the actual financial sav- telemedicine. In hospital tele-ICU systems examined ings or cost of implementing a tele-ICU. 2. Aust MP. Intensive care unit telemedicine. Am J 39 72 Crit Care 2012 Jan;21(1):34. DOI: http://dx.doi. by Franzini et al and Morrison et al, Other articles had cost data about the org/10.4037/ajcc2012416. hospital costs rose after implementation. savings but did not have data on how 3. ICU outcomes (mortality and length of stay) Both studies noted that costs associated much ICUs were costing them before a methods, data collection tool and data [Internet]. San Francisco, CA: Philip R Lee with physicians choosing a low or nonexis- tele-ICU implementation. In addition, the Institute for Health Policy Studies, University of tent involvement with tele-intensivists rose excessively high fees presented may be California, San Francisco; 2012 [cited 2014 Apr more quickly than those costs associated peculiar to the location and hospital size, 21]. Available from: http://healthpolicy.ucsf.edu/ content/icu-outcomes. with physicians choosing a higher level of and so may not be as large elsewhere. This 4. Wenham T, Pittard A. Intensive care unit tele-intensivist involvement. Additionally, study also was limited by restrictions in environment. Continuing Education in Franzini et al39 noted that the tele-ICU the search strategy used, and publication Anaesthesia, Critical Care & Pain 2009 Dec;9(6):178-83. DOI: http://dx.doi. system used in their study was not fully and researcher’s bias may have limited the org/10.1093/bjaceaccp/mkp036. integrated with the hospitals’ electronic availability and quality of the research iden- 5. Rothschild JM, Landrigan CP, Cronin JW, et al. health record system, which may also have tified for review. Additionally, the review The Critical Care Safety Study: the incidence and nature of adverse events and serious contributed to increased cost. was limited to hospital organizations in medical errors in intensive care. Crit Care Med The LOS decreased because intensiv- the US, thus excluding many international 2005 Aug;33(8):1694-700. DOI: http://dx.doi. ists had more time to spend with the providers of tele-ICU care. org/10.1097/01.CCM.0000171609.91035.BD. 6. Angus DC, Barnato AE, Linde-Zwirble WT, et al; patient and were able to provide adequate The implication of this study is that Robert Wood Johnson Foundation ICU End-Of- intensive care. Franzini et al39 and Mor- the implementation of tele-ICU systems Life Peer Group. Use of intensive care at the end 72 of life in the United States: an epidemiologic rison et al noticed patients were being can be cost-effective and can improve study. Crit Care Med 2004 Mar;32(3):638- served more effectively than before the patient outcomes. Future research should 43. DOI: http://dx.doi.org/10.1097/01. implementation of a tele-ICU system. examine the results attributable to the CCM.0000114816.62331.08. 7. Kersten AE, Milbrandt EB, Rahim MT, et al. How The large range of hospital costs per implementation of a tele-ICU. A meta- big is critical care in the US? Crit Care Med bed reported by Kumar et al71 stresses analysis should be performed to have a 2003;31(Suppl):A8. that each health care institution must do more precise measurement of the effects 8. Mayr VD, Dünser MW, Greil V, et al. Causes of death and determinants of outcome in critically a careful cost-benefit analysis and should (ie, cost and savings) of the implementa- ill patients. Crit Care 2006;10(6):R154. DOI: include vendors in the implementation tion of a tele-ICU in practice. Other areas http://dx.doi.org/10.1186/cc5086. process from the beginning. Many hospi- for study include how tele-ICUs affect 9. Reynolds HN, Bander J, McCarthy M. Different systems and formats for tele-ICU coverage: tals have demonstrated that a strong tele- different types of ICUs such as surgical designing a tele-ICU system to optimize ICU program can find payback in about vs nonsurgical ICUs, including tele-ICU functionality and investment. Crit Care Nurs Q a year, according to the New England vs a 24/7 in-house pulmonary model, and 2012 Oct-Dec;35(4):364-77. DOI: http://dx.doi. org/10.1097/CNQ.0b013e318266bc26. Healthcare Institute (now the Network whether similar findings can be achieved 10. Myers MA, Reed KD. The virtual ICU (vICU): for Excellence in Health Innovation) in in small and rural hospitals. a new dimension for critical care nursing Cambridge, MA.36 In another study, with practice. Crit Care Nurs Clin North Am 2008 Dec;20(4):435-9. DOI: http://dx.doi. 10,000 patients, Advanced ICU Care in Conclusion org/10.1016/j.ccell.2008.08.003. St Louis, MO, achieved a 40% reduction Although mixed results were found in 11. Khunlertkit A, Carayon P. Contributions of of mortality and a 25% reduction of ICU the literature in terms of cost savings, the tele-intensive care unit (Tele-ICU) technology 73 to quality of care and patient safety. J Crit Care LOS. This finding concurred also with a findings suggest that the implementation 2013 Jun;28(3):315.e1-12. DOI: http://dx.doi. study by Lilly et al74,75 of 28,000 patients of tele-ICU systems have the potential org/10.1016/j.jcrc.2012.10.005.

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12. Breslow MJ, Rosenfeld BA, Doerfler M, 26. Coustasse A, Tomblin S, Slack C. Impact intensive care unit program in 6 intensive care et al. Effect of a multiple-site intensive of radio-frequency identification (RFID) units in a large health care system. J Crit Care care unit telemedicine program on clinical technologies on the hospital supply chain: a 2011 Jun:26(3):329.e1-6. DOI: http://dx.doi. and economic outcomes: an alternative literature review. Perspect Health Inf Manag org/10.1016/j.jcrc.2010.12.004. paradigm for intensivist staffing. Crit Care 2013 Oct 1;10:1d. 40. Aaronson ML, Zawada ET Jr, Herr P; Avera Med 2004 Jan;32(1):31-8. DOI: http://dx.doi. 27. Porterfield A, Engelbert K, Coustasse A. ICU Research Group. Role of a telemedicine org/10.1097/01.CCM.0000104204.61296.41. Electronic prescribing: improving the efficiency intensive care unit program (TISP) on glycemic 13. Groves RH Jr, Holcomb BW Jr, Smith ML. and accuracy of prescribing in the ambulatory control (GC) in seriously ill patients in a Intensive care telemedicine: evaluating a care setting. Perspect Health Inf Manag 2014 rural health system [abstract]. Chest 2006 model for proactive remote monitoring and Apr 1;11:1g. Oct;130(4_MeetingAbstracts):226S. DOI: intervention in the critical care setting. Stud 28. Goran SF. A second set of eyes: an introduction http://dx.doi.org/10.1378/chest.130.4_ Health Technol Inform 2008;131:131-46. to Tele-ICU. Crit Care Nurse 2010 Aug;30(4):46- MeetingAbstracts.226S-a. 14. Rosenfeld BA, Dorman T, Breslow MJ, et al. 55. DOI: http://dx.doi.org/10.4037/ccn2010283. 41. Badawi O, Breslow M, Jaber H, Hassan E. Trends Intensive care unit telemedicine: alternate 29. Becker C. Remote control. 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patient care value from remote telemonitoring 60. Youn BA. ICU process improvement: using 67. Ikeda D, Hayatdavoudi S, Winchell J, Rincon T, in a medical intensive care unit [abstract]. Chest telemedicine to enhance compliance Yee A. The impact of using a standard protocol 2007 Oct;132(4_MeetingAbstracts):443a. and documentation for the ventilator for the surviving sepsis 6 and 24 hr bundles DOI: http://dx.doi.org/10.1378/chest.132.4_ bundle [abstract]. Chest 2006 Oct;130(4_ in septic patients on total ICU risk adjusted MeetingAbstracts.443a. MeetingAbstracts):226S. DOI: http:// mortality [abstract]. Crit Care Med 2006 53. Norman V, French R, Hassan E, et al. Effect dx.doi.org/10.1378/chest.130.4_ Dec;34(Abstract suppl 12):A108. of a telemedicine facilitated program on ICU MeetingAbstracts.226S-c. 68. Ries M. Tele-ICU: a new paradigm in critical length of stay (LOS) and financial performance 61. Young LB, Chan PS, Lu X, Nallamothu BK, care. Int Anesthesiol Clin 2009 Winter;47(1): [abstract]. Crit Care Med 2009 Dec;37(12 Sasson C, Cram PM. Impact of telemedicine 153-70. DOI: http://dx.doi.org/10.1097/ Suppl):A2. DOI: http://dx.doi.org/10.1097/01. intensive care unit coverage on patient AIA.0b013e3181950078. ccm.0000365439.11849.a2. outcomes: a systematic review and meta- 69. Groves RH Jr, Holcomb BW Jr, Smith ML. 54. Patel B, Kao L, Thomas E, Campos T. Improving analysis. Arch Intern Med 2011 Mar Intensive care telemedicine: evaluating a compliance with surviving sepsis campaign 28;171(6):498-506. DOI: http://dx.doi. model for proactive remote monitoring and guidelines via remote electronic ICU monitoring org/10.1001/archinternmed.2011.61. intervention in the critical care setting. Stud [abstract]. Crit Care Med 2007 Dec;35(12 62. Zawada ET Jr, Aaronson ML, Herr P, Erickson Health Technol Inform 2008;131:131-46. Suppl):A275. DOI: http://dx.doi.org/10.1097/01. DK; Avera ICU Research Group. Relationship 70. Ploetz JM, Badawi O, Rosenfeld BA. Adoption ccm.0000301049.77714.a1. between levels of consultative management rate of blood transfusion evidence in 55. Rincon T, Bourke G, Ikeda D, Seiver A. Screening and outcomes in a telemedicine intensivist the intensive care unit [abstract]. Chest for severe sepsis: an incidence analysis staffing program (TISP) in a rural health 2008;135(4_MeetingAbstracts):p60004. [abstract]. Crit Care Med 2007 Dec;35(12 system [abstract]. Chest 2006 Oct;130(4_ DOI: http://dx.doi/org/10.1378/chest.134.4_ Suppl):A257. DOI: http://dx.doi.org/10.1097/01. MeetingAbstracts):226S. DOI: http:// MeetingAbstracts.p60004. ccm.0000301049.77714.a1. dx.doi.org/10.1378/chest.130.4_ 71. Kumar G, Falk D, Bonello R, Kahn JM, 56. Scales DC, Dainty K, Hales B, et al. A MeetingAbstracts.226S-b. Perencevich E, Cram P. The costs of critical care multifaceted intervention for quality 63. Zawada ET, Herr P, Erickson D, Hitt J. Financial telemedicine programs: a systematic review and improvement in a network of intensive care benefit of a tele-intensivist program to a analysis. Chest 2013 Jan;143(1):19-29. DOI: units: a cluster randomized trial. JAMA 2011 rural health system [abstract]. Chest 2007 http://dx.doi.org/10.1378/chest.11.3031. Jan 26;305(4):363-72. DOI: http://dx.doi. Oct;132(4_MeetingAbstracts):444. DOI: 72. Morrison JL, Cai Q, Davis N, et al. Clinical and org/10.1001/jama.2010.2000. http://dx.doi.org/10.1378/chest.132.4_ economic outcomes of the electronic intensive 57. Thomas EJ, Chu-Weininger MYL, Lucke J, MeetingAbstracts.444. care unit: results from two community hospitals. Wueste L, Weavind L, Mazabob J. The impact 64. Zawada ET, Herr P, Lindgren L. Clinical Crit Care Med 2010;38(1):2-8. DOI: http:// of a tele-ICU on provider attitudes about and fiscal impact of a rural tele-intensivist dx.doi.org/10.1097/CCM.0b013e3181b78fa8. teamwork and safety climate [abstract]. Crit staffing program on transfer of patients from 73. Gorman MJ. Driving best practices with tele- Care Med 2007 Dec;35(12 Suppl):A145. their community to a tertiary care hospital ICU [Internet]. Chicago, IL: National Association DOI: http://dx.doi.org/10.1097/01. [abstract]. Crit Care Med 2008 Dec;36(12 for Healthcare Quality; 2012 [cited 2014 ccm.0000301049.77714.a1. Suppl):A86. DOI: http://dx.doi.org/10.1097/01. April 24]. Available from: www.nahq.org/ 58. Vespa PM, Miller C, Hu X, Nenov V, Buxey ccm.0000341823.62097.1d. annualconference/2012/401-404.html. F, Martin NA. Intensive care unit robotic 65. Zawada ET, Herr P. ICU telemedicine improves 74. Lilly CM, Thomas EJ. Tele-ICU: experience telepresence facilitates rapid physician care to rural hospitals reducing costly transports to date. J Intensive Care Med 2010 Jan- response to unstable patients and decreased [abstract]. Crit Care Med 2008 Dec;36(12 Feb;25(1):16-22. DOI: http://dx.doi. cost in neurointensive care. 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DOI: http://dx.doi. org/10.1001/jama.2011.697.

Structure and Ability

The tasks assigned [to the physician] … are determined primarily by the social and economic structure of society and by the technical and scientific means available to medicine at the time.

— Medicine and Human Welfare, Henry E Sigerist, 1891-1957, Swiss medical historian

84 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 CASE STUDY Vasal Injury During Inguinal Herniorrhaphy: A Case Report and Review of the Literature

Lawrence Flechner, MD, PhD; James Smith, MD, MS; Patrick Treseler, MD, PhD; John Maa MD Perm J 2014 Fall;18(4):85-88 http://dx.doi.org/10.7812/TPP/14-073

Case Study Abstract A 28-year-old man with a history of An injury to the vas deferens during inguinal herniorrhaphy from possible tether- pelvic fracture sought urologic evalu- ing of the vas has not, to our knowledge, previously been described in the surgical ation because of erectile dysfunction literature. We report a case of iatrogenic injury of the vas deferens that occurred dur- and the desire to conceive a child. His ing elective hernia repair in a 28-year-old man who had previously sustained blunt medical and surgical history was notable trauma to the abdomen and pelvis. for a pedestrian vs auto accident in 2005, in which he sustained fractures of the pelvis and right femur (Figure 1), and a Introduction cord—consisting of the vas deferens, partial urethral disruption. He required Inguinal herniorrhaphy is among the vessels, nerves, lymphatics, and tunica an emergency exploratory laparotomy, most common surgical procedures per- albuginea—is often involved in inguinal with a temporary colostomy because 1 formed in the US. An inguinal hernia hernias, particularly of the indirect vari- of a rectal laceration, and external fixa- develops from a weakness in either ety. Yet reports of injury to the spermatic tion of his pelvic and femoral fractures. the abdominal wall fascia at the Hes- cord and its contents are rare. We herein The urethral injury was treated with selbach triangle or the internal inguinal report a case of vas deferens injury dur- temporary Foley catheterization and a ring. Any adjacent abdominal contents ing inguinal herniorrhaphy in a patient suprapubic cystostomy tube, after which may be contained in or adherent to who had previously sustained extensive normal voiding function eventually an inguinal hernia sac. The spermatic abdominal and pelvic trauma. returned. After an initially unsuccess- ful attempt at colonic reanastomosis, the colostomy was later reversed. The patient’s medical history was otherwise unremarkable; he did not use prescrip- tion medications or smoke tobacco. He could obtain erections using phospho- diesterase Type 5 inhibitor therapy, suggesting a vasculogenic cause of his erectile dysfunction. He opted to at- tempt conception with his partner by natural means. His urologic evaluation at our insti- tution took place four years after his accident. At this time, a moderate right inguinal hernia was identified, prompt- ing referral to the General Surgery Ser- vice. The hernia caused discomfort but was easily reducible, without evidence of incarceration or obstruction. The pa- tient’s pelvic surface anatomy was heav- ily scarred from the prior external fixator Figure 1. Axial computed tomographic scan of pelvis revealing diastasis and hetero- placement. After an extensive discussion, topic ossification superior to symphysis pubis adjacent to right inguinal canal. the patient decided to undergo surgical

Lawrence Flechner, MD, PhD, is a Urologist at the Urology Institute of the South Bay, Torrance in CA. E-mail: [email protected] Smith, MD, MS, is an Assistant Professor in Urology and Obstetrics, Gynecology, and Reproductive Sciences at the University of California, San Francisco. E-mail: [email protected]. Patrick Treseler, MD, PhD, is a Professor of Pathology at the University of California, San Francisco. E-mail: [email protected]. John Maa, MD, is the Immediate Past President of the Northern California Chapter of the American College of Surgeons and a General Surgeon at Marin General Hospital in CA. E-mail: [email protected].

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 85 CASE STUDY Vasal Injury During Inguinal Herniorrhaphy: A Case Report and Review of the Literature

repair of the hernia with polypropylene metal clip was placed just lateral to the The stricture was identified, excised, mesh. An open approach was selected, anastomosis to facilitate possible future and reconstructed by vasovasostomy given the patient’s history of abdominal- localization. A Lichtenstein tension-free (Figure 3). pelvic surgery. mesh herniorrhaphy was performed to The patient had an uncomplicated re- At the time of herniorrhaphy, exten- repair the direct hernia, and the wound covery, and subsequent semen analysis sive scarring was noted in the subcuta- was closed. findings 1 month and 4 months after sur- neous and fascial layers, possibly result- The patient’s postoperative recovery gery were equivalent to his preoperative ing from previous pelvic hemorrhage. was uncomplicated. Pathologic evalu- values. After 2 attempts at intrauterine The inguinal canal was exposed, and the ation of a segment of the vas did not insemination, the patient and his wife iliohypogastric and ilioinguinal nerves demonstrate ischemic changes or other were able to successfully conceive a and the spermatic cord were identi- underlying abnormalities (Figure 2). child spontaneously. fied. A 5-cm-diameter direct hernia sac A postoperative semen analysis re- was identified medial to the epigastric vealed a low-normal sperm count of Discussion vessels. The cord and hernia sac were 20 million/mL with motility and mor- We believe that this case represents densely adherent but could be sepa- phologic characteristics within normal a novel and previously undescribed rated, after which the spermatic cord limits. Although the status of the vasal mechanism of injury to the vas deferens was encircled using a Penrose drain. repair was unknown at the time of that during open inguinal herniorrhaphy, in During retraction of the cord en masse analysis, these findings suggested that the setting of extensive scarring result- to expose the pubic tubercle and floor the contralateral vas was patent and ing from prior pelvic surgery. To deter- of the inguinal canal, an audible snap functional, and likely would enable the mine whether there is a precedent for was heard. Careful inspection revealed patient to conceive a child. However, he this scenario in the medical literature, that the vas deferens had fractured, pos- underwent another urologic evaluation we searched the MEDLINE electronic sibly because of extensive scarring and after 9 months of failing to achieve a database for English-language articles lack of mobility of the vas in particular. pregnancy with his spouse. He chose by using the following key words: vas, An intraoperative urologic consulta- to undergo vasography with contrast hernia, injury, pelvis, scar. No reports tion indicated that the vas was firm and medium delivered by hemivasotomy were identified. attenuated. The proximal and distal proximal to the prior anastomotic site. An iatrogenic injury to the vas deferens vasal ends were identified and were The contrast agent did not pass beyond during adult open inguinal herniorrha- incised to expose fresh tissue in prepara- the level of the inguinal canal, saline phy is rare.2 Mechanisms of vasal injury tion for primary end-to-end anastomo- injection revealed obstruction, and a include partial or complete transection, sis. The vas was approximated using 5 2-0 nylon suture did not pass the region fracture, thermal or crush injury, com- interrupted 7-0 polypropylene (Prolene) of the inguinal canal, thus indicating pression, and excessive tension from a sutures in a tension-free manner. A vasal obstruction at the anastomotic site. foreign body such as mesh, leading to obstruction and ischemia.2-6 Injury to the vas deferens is thought to occur when it is adherent to the hernia sac.7,8 Although difficult to prove, chronic ischemia from our patient’s earlier pelvic vascular in- jury might have contributed to inherent weakness of the tissue, predisposing it to fracture despite careful handling of the cord. Furthermore, although the vasal injury may contribute to obstruction as a source of azoospermia, results of his physical examination demonstrated mild atrophy of the right testicle, suggest- ing that blood supply may have been compromised during one of his prior operations. At the time of surgery, we hypoth- esized that either scar tissue was tether- ing the testicle and vas or that chronic ischemia contributed to the vasal injury and abnormal texture of the vas. Typi- cally, the testicle can be delivered into Figure 2. Cross-section of unremarkable vas deferens (hematoxylin-eosin stain, original the inguinal canal with gentle traction, magnification 100×). but in this case, the testicle was immobile

86 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 CASE STUDY Vasal Injury During Inguinal Herniorrhaphy: A Case Report and Review of the Literature

nent location of the vas and gonadal vessels must be noted when placing the mesh, especially during bilateral herni- orrhaphy. Longer-term follow-up of the fertility of young men who undergo bi- lateral laparoscopic hernia repair should be considered. Special consideration should be made when obtaining preoperative consent for inguinal herniorrhaphy from men of childrearing age who have sustained previous pelvic trauma. In our case, an intraoperative alternative would have been to ligate the vas, with the expecta- tion that if the contralateral vas were patent, the patient’s fertility would not be dramatically altered. We recognized, however, that the history of pelvic trauma might have predisposed the contralateral vas to ischemia or nonfunction, and to infertility if a repair had not been at- Figure 3. Intraoperative photograph of reconstructed vas deferens via vasovasostomy. tempted. However, for patients who no longer wish to father children, the option of simple ligation of the vas deferens and the vas fractured into two segments. a cohort of 472 patients who underwent or unilateral orchiectomy could also be The absence of chronic ischemic findings vasovasostomy or epididymovasostomy considered. in the pathologic evaluation of the vas indicated that 30 of the injuries were In the months after our patient’s led us to conclude that scarring from caused by inguinal herniorrhaphy.9 Ten vas deferens injury, he and his wife the pelvic fracture and tethering of the of these were adult cases, supporting were initially unsuccessful in achieving testicle placed the vas on traction and the argument that vasal injury is under- spontaneous pregnancy. No symptoms resulted in the abnormal texture. reported after childhood. One reason for of scrotal edema or pain developed, or The true incidence of vas deferens this underreporting may be that diagnosis any other suggestion of an obstruction injury during open hernia repair in adult of injury might be learned only from ab- of the vas deferens. He thus chose to men is likely underreported. This under- normal findings of semen analysis, a test undergo a repeated procedure to assess reporting probably reflects that small obtained primarily for fertility evaluation. the patency of the initial repair and to injuries may be unrecognized intraopera- Additionally, perhaps because of delayed increase the likelihood to conceive a tively, that improper mesh placement is diagnosis, treatment outcomes for vasal child spontaneously. difficult to appreciate,4 and that postsur- injury repair are poor. Compared with gical symptoms are often absent. In the vasectomy reversal, microsurgical repair Conclusion most common scenario, an unrecognized of iatrogenic vasal injury was associated To our knowledge, this is the first injury is revealed only years later in the with a reduced success rate, longer- report of an unusual vas deferens injury evaluation of subfertile or azoospermic length vasal defects, impaired blood during open inguinal herniorrhaphy in a men who underwent hernia repair during supply, and longer duration of obstruc- patient with a history of extensive pelvic childhood.7,9-11 Unlike in adults, inguinal tion.9 Yet in our patient, the relatively surgery. For patients with a history of hernia repair in children is the most com- brief duration of obstruction suggests pelvic trauma who are being considered mon cause of injury to the vas deferens,9 a more favorable outcome. Because a for herniorrhaphy, our case suggests that which is more delicate and attenuated in microscopic repair of the vas requires there is a modestly increased risk of iatro- infants. Early reports suggested that vasal additional expertise and equipment, the genic injury to spermatic cord structures. injury occurs in 0.8% to 2% of pediatric urgent nature of the intraoperative con- Although an open approach is preferred, hernia cases.11 However, an incidence sult at the time of injury precluded this it does not preclude the possibility of as high as 26.7% has been reported in approach initially in our patient. injury. Intraoperatively, extra care should subfertile men with vasal obstruction.7 The advent of laparoscopic inguinal be taken during mobilization of the cord There should be a high index of sus- herniorrhaphy has potentially increased structures to prevent excess traction. If an picion for iatrogenic vasal injury in azo- the risk of vasal injury, given the precari- injury is identified, urologic consultation ospermic patients who have undergone ous location of the abdominal vas and is indicated, and a primary reanastomosis bilateral inguinal herniorrhaphy.11,12 A gonadal vessels as they converge onto should be attempted, preferably with the review of 34 iatrogenic vasal injuries from the internal inguinal ring.10,13 The promi- aid of a surgical microscope. A metal clip

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 87 CASE STUDY Vasal Injury During Inguinal Herniorrhaphy: A Case Report and Review of the Literature

placed adjacent to the site of repair may 3. Thapa PB, Maharjan DK, Pudasaini S, Sharma 1998 Jan;159(1):139-41. DOI: http://dx.doi. facilitate future procedures for repeated SK. Inguinal vasal obstruction following org/10.1016/S0022-5347(01)64036-9. polypropylene mesh repair. JNMA J Nepal Med 10. Ridgway PF, Shah J, Darzi AW. Male genital reconstruction if necessary. Finally, follow- Assoc 2009 Apr-Jun;48(174):168-9. tract injuries after contemporary inguinal hernia up semen analyses may help guide fertility 4. Shin D, Lipshultz LI, Goldstein M, et al. repair. BJU Int 2002 Aug;90(3):272-6. DOI: v Herniorrhaphy with polypropylene mesh http://dx.doi.org/10.1046/j.1464-410X. evaluation. causing inguinal vasal obstruction: a preventable 2002.02844.x. cause of obstructive azoospermia. Ann Surg 11. Lynn HB, Johnson WW. Inguinal Disclosure Statement 2005 Apr;241(4):553-8. DOI: http://dx.doi. herniorrhaphy in children. A critical The author(s) have no conflicts of interest org/10.1097/01.sla.0000157318.13975.2a. analysis of 1,000 cases. Arch Surg 1961 5. Meacham RB. From androlog. Potential for vasal Oct;83:573-9. DOI: http://dx.doi.org/10.1001/ to disclose. occlusion among men after hernia repair using archsurg.1961.01300160085010. mesh. J Androl 2002 Nov-Dec;23(6):759-61. 12. Weber CH. Successful restoration of fertility Acknowledgments 6. Valenti G, Baldassarre E, Torino G. Vas twenty-nine years after bilateral vasal injury The authors would like to thank Pamela deferens obstruction due to fibrosis after plug in infancy. Urology 1986 Oct;28(4):299- hernioplasty. Am Surg 2006 Feb;72(2):137-8. 300. DOI: http://dx.doi.org/10.1016/0090- Derish, MA, of the University of California, 7. Matsuda T, Muguruma K, Hiura Y, Okuno H, 4295(86)90010-5. San Francisco Department of Surgery Shichiri Y, Yoshida O. Seminal tract obstruction 13. Parelkar SV, Oak S, Gupta R, et al. Laparoscopic Publications Office for editorial assistance. caused by childhood inguinal herniorrhaphy: inguinal hernia repair in the pediatric age Kathleen Louden, ELS, of Louden Health results of microsurgical reanastomosis. J Urol group—experience with 437 children. J Pediatr Communications provided editorial 1998 Mar;159(3):837-40. DOI: http://dx.doi. Surg 2010 Apr;45(4):789-92. DOI: http://dx.doi. assistance. org/10.1016/S0022-5347(01)63747-9. org/10.1016/j.jpedsurg.2009.08.007. 8. Steigman CK, Sotelo-Avila C, Weber TR. The incidence of spermatic cord structures References in inguinal hernia sacs from male children. 1. Jenkins JT, O’Dwyer PJ. Inguinal hernias. BMJ Am J Surg Pathol 1999 Aug;23(8):880-5. 2008 Feb 2;336(7638):269-72. DOI: http:// DOI: http://dx.doi.org/10.1097/00000478- dx.doi.org/10.1136/bmj.39450.428275.AD. 199908000-00004. 2. Pollak R, Nyhus LM. Complications of 9. Sheynkin YR, Hendin BN, Schlegel PN, groin hernia repair. Surg Clin North Am Goldstein M. Microsurgical repair of 1983;63(6):1363-71. iatrogenic injury to the vas deferens. J Urol

Bassini’s Technique

This method reconstructs the inguinal canal as it is physiologically, with two rings, one abdominal, the other subcutaneous; and with two walls, one posterior and the other anterior, between which the spermatic cord passes obliquely.

— Attività di Congresso Associazone Medicina di Italia, Edoardo Bassini, MD, 1844-1924, Italian surgeon

88 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 credits available for this article — see page 96.

EDITORIAL Healthy Behavior Change in Practical Settings

Scott Young, MD Perm J 2014 Fall;18(4):89-92 http://dx.doi.org/10.7812/TPP/14-018

their change-related goals using support, Abstract advice, affirmation, and empathetic con- The core principle of implementing healthy behavior change is making the healthy versation. These stages include engaging choice the easy choice. Putting this motto into practice requires us to remove the barri- with patients to help build rapport, focus- ers that individuals face when trying to live a healthy lifestyle. It is important to look at ing patients on the changes they want to the bigger picture when helping our patients reach optimal health, looking closely at make while offering advice and support, exercise levels and home life. Environmental factors can cause strain and present chal- evoking the tools and desires they pos- lenges for people trying to develop and maintain good health. At the Care Management sess within them to effect change, and Institute and at Kaiser Permanente, we are making strides to change default behaviors planning to implement the goals and so optimal lifestyles become the norm, rather than the exception. next steps patients identified through the encounter.1 Supporting my patients’ The Healthy Choice hypertension, I’m going to care about awareness about their current behavior At the Care Management Institute, we aspects of their daily lives that prevent patterns, helping them become aware of pride ourselves on the work we do to them from exercising healthier practices. the skills they already have, and respect- “make the right thing easy to do.” One I care about their environment—where ing any initial resistance will be crucial to of the key tenets of putting this motto they live, what they eat during the day, conducting a positive conversation. into practice is removing the barriers that and how many hours they spend sitting make it difficult for us as an organization each day. I care about whether there’s Healthy Lifestyle Changes to initiate change—and a big part of that a grocery store in their neighborhoods Traditionally, the ability to achieve is looking at the whole picture. We’re not where they can access fresh fruits and total good health has been dependent on just trying to solve problems; we’re trying vegetables. The things I care about when an individual’s willingness to implement to identify the sources of the problems so I’m meeting with my patients look a lot change in his or her everyday life. Behav- that we can make necessary adjustments different from the list of questions that ioral design ultimately helps people find early on, and with greater success. pops up in the EHR. Yet these factors useful tools and tactics for making healthy The same principles apply on an are equally, if not more, important than lifestyle changes. It also helps determine individual level. As a family practice anything else when I’m looking at the how able and ready a person is to make a physician, when I am sitting across from causes of my patients’ medical conditions. change, and what triggers are most likely patients with high blood pressure, there to instigate that change. At times, if I’m are a number of questions I must ask. A Positive Conversation unable to motivate my patients to change, Their electronic health records (EHRs) Once I have a better understanding I might need to enlist the expertise of prompt me with certain information about of the total picture of my patients, there others on my team and provide a referral. their family histories and body mass in- is a second set of considerations I must What kind of resources or outside referrals dexes and even remind me to measure examine. Will my patients make the will be beneficial in helping my patients exercise as a vital sign. However, there lifestyle and behavior changes needed to accomplish their goals? I may need to are so many more elements that I want to positively affect their health? Yes, I can go beyond the exam room and look to examine, beyond what the medical record tell them to eat better and exercise more, what the community can offer. There can show me. To be successful in making but if they work two jobs and don’t have may be diet- and exercise-tracking apps, my patients their healthiest selves, I need access to a grocery store in their neighbor- free nutritional and wellness counseling, to have effective and constructive con- hoods, they’re going to have a tough time cooking classes, sports clubs, and even versations before providing any advice. with this. At this point, I might think back community or church groups that could to the motivational interviewing training help my patients to make positive lifestyle Behaviors and Social Practice I received and think about how to frame changes once they leave my exam room. Our EHR system doesn’t necessarily the conversation with patients in the most For individuals to sustain healthy life- prompt us to look at behaviors and social constructive way. Motivational interview- style changes, we must make the healthy factors that may be obstacles to achiev- ing involves four stages of dialogue to choice the easy choice. Something as ing optimal health. For my patients with help orient patients toward success with simple as having well-lit and well-main-

Scott Young, MD, is the Associate Executive Director of Clinical Care and Innovation and the Senior Medical Director and Executive Director of the Care Management Institute. E-mail: [email protected].

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 89 EDITORIAL Healthy Behavior Change in Practical Settings

Figure 1. The Behavior Change Pathway. Reprinted with permission from Kaiser Permanente.

tained stairwells in office buildings, hav- the Motivational Interviewing Toolkit: there has been a dramatic increase in ing weekly walking meetings, or including www.kphealtheducation.org; however, obesity in the US.2 According to the Cen- healthy food choices at lunchtime meet- there are many ways to approach behav- ters for Disease Control and Prevention, ings can make the difference for someone ior change conversations with patients. 35.7% of US adults and approximately to implement healthy habits. Discussions about behavior change help 17%—or 12.5 million—of children and individuals understand healthy living in the adolescents aged 2 to 19 years are obese.3 Behavior Change context of preexisting goals they may have Obesity can lead to more serious chronic Conversations and to view overall health as a community diseases such as heart disease and dia- However, to sustain healthy lifestyle issue, rather than as a medical condition. betes. Obesity is a problem that begins changes, we must address them not by affecting communities and eventually only in communities but also in clinical Unhealthy Habits spreads to a national level. Awareness settings. Clinicians and physicians are The prevalent and growing obesity campaigns such as HBO’s The Weight a crucial element to bridging the gap epidemic in the US initially stemmed, in of the Nation (developed in partnership between individuals knowing what needs part, from negative systematic change. with Kaiser Permanente) are attempting to change and actually implementing New communities today are frequently to reach individuals in their communities those lifestyle changes. Physicians are designed around unhealthy habits: Sub- and warn them of the severe and adverse in a position to help educate patients urban housing developments require effects of being overweight or obese. about the importance of healthy behavior people to drive to everyday destinations, The Centers for Disease Control and change and to guide them to resources and fast food restaurants make unhealthy Prevention also reports, through the that may aid them in living healthier lives. food the most convenient option. This Diabetes Prevention Program national Training in motivational interviewing is has created an unmet need for system- study, that intensive lifestyle change and one useful tool that can aid clinicians atic changes in the opposite direction— intervention can prevent diabetes caused to have productive conversations about changes that will help us to climb out of by obesity. The multicenter clinical re- behavior change with their patients. One the unhealthy routine and to redesign for search study aimed to discover whether resource used in Northern California is optimal default behaviors. Since 1994, modest (5% to 7%) weight loss through

90 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 EDITORIAL Healthy Behavior Change in Practical Settings

dietary changes and increased physical everyday routines. First, we must deter- physician’s office and the individual’s activity (150 minutes/week) could pre- mine what changes each individual is experience in the community (Figure 1). vent or delay the onset of type 2 diabetes willing to make. Then we must simplify Because healthy behavior change be- in study participants. The Diabetes Pre- these changes and guide patients through gins at home, it’s important for primary vention Program ultimately found that how to monitor their actions against an care physicians to connect and engage participants who lost a modest amount of overall goal. We also must be aware that patients on a personal level and to deter- weight through dietary changes and in- some patients may be initially resistant mine what matters the most to patients creased physical activity sharply reduced to change. Instead of challenging this and what changes they are willing to their chances of developing diabetes.4 resistance, we should respect it and make, so we can ultimately set them up Since Kaiser Permanente’s (KP’s) in- encourage patients to drive toward their for success in sustaining those changes. ception, the importance of prevention own goal-oriented solutions. It’s equally important to reinforce ongo- has always influenced our work and our Karen J Coleman, PhD, research ing successes once individuals do imple- values, and we have remained on the scientist at the KP Southern California ment healthy habits in their everyday leading edge. Healthcare Effectiveness Department of Research and Evaluation lives. Again, personal behavior is a major Data and Information Set (HEDIS) data and lead author of the study examining contributor to overall health. show that KP’s Georgia and Southern exercise as a vital sign, stated, “Given that One way to engage individuals in im- California Regions are ranked first and health care providers have contact with proving their health is to show them how second, respectively, in the nation for the majority of Americans, they have a healthy behavior changes can be major adult body mass index screening, with unique opportunity to encourage physi- contributors to preventing or delaying other KP Regions not far behind.5 cal activity among their patients through the onset of disease or personal injury. an assessment and brief counseling.”7 Health care leaders are increasingly rec- Exercise as Vital Sign She added, “embedding questions about ognizing healthy behaviors as factors in Last year, we determined the valid- physical activity in the electronic medical the improvement of overall health. For ity of asking our patients how many record provides an opportunity to counsel example, studies indicate that there is a minutes per week they exercise and millions of patients during routine medical clear link between good emotional health recording this number as a vital sign. care regarding the importance of physical and healthier behaviors. This was a progressive step toward activity for health.” 7 In 1994, KP created the bone den- achieving optimal behavior design in a sity screening program for osteoporosis clinical setting, and toward achieving to- Prescribing Success prevention in Southern California. As tal good health. It was also our first foray To focus on total health at a personal part of this innovative initiative, we into creating a clinical measure that level with individuals, it is important to identified members with a higher risk determines how a patient’s lifestyle can enlist the clinical community to help of osteoporosis, and we performed directly translate into the prevention of us prescribe success, rather than just bone density screenings on this popula- the leading causes of death in our coun- prescribing medical interventions. A tion. We were also able to recommend try. According to a KP study published crucial question to ask ourselves is, “As calcium supplements, exercise, and in the journal Medicine and Science in a physician, am I equipped to prescribe other lifestyle changes that could help Sports and Exercise, establishing a sys- success for my patient?” Although we, prevent fractures later on. By 2002, the tematic method for recording patients’ as physicians, have a role to play in the fully integrated Healthy Bones program physical activity in their EHRs ultimately continued health of our patients, barri- was in place at all Medical Centers in helps clinicians better treat and counsel ers to achieving this goal are inevitable. the organization’s Southern California patients about their lifestyles.6 We must incorporate behavior change Region. Since then, the Healthy Bones as part of the total health framework program has reduced the number of Healthy Habits that physicians advocate and model for fragility fractures among Southern Cali- Although recognizing exercise as a their patients and that individuals imple- fornia members by 15%. The program has vital sign is a step in the right direction ment in their lives and communities. As expanded to all KP Regions.8 for healthy behavior change, there is still an integrated health care system, we This is just one example of how early work to be done. Addressing exercise should aim to change the course of how intervention combined with lifestyle and as a vital sign certainly opens the door to approach and encourage healthier behavior change successfully altered to a larger conversation about healthy behaviors to prevent disease, as well as the course of health history for a sig- habits, but what keeps us from fully en- consider what fundamental elements en- nificant number of our members with gaging with our patients is the fact that courage people to change their behavior, the potential for bone disease. With this we don’t completely understand how to and sustain that change, understanding example in mind, it seems logical that, measure environmental determinants, that personal behavior is a major con- as a delivery system, we should consider or how to talk to patients about them. tributor to overall health. our role in addressing intensive lifestyle We must find a way to effectively relate As the behavior change pyramid change to prevent other diseases such to each patient individually to ascertain suggests, it is crucial to bridge the gap as diabetes, cardiovascular disease, and how they can fit healthy habits into their between the medical model of the lung disease.

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 91 EDITORIAL Healthy Behavior Change in Practical Settings

Mood and Sleep of Illinois at Chicago School of Public References Health, and colleagues.12 In addition, by 1. Miller WR, Rollnick S. Motivational interviewing: Increased physical activity can directly Helping people change. 3rd ed. New York, NY: and positively affect mood in individuals examining television analytics data, the Guildford Press; 2012. who experience depression. Physical ac- researchers found that teens’ exposure 2. Fryar CD, Carroll MD, Ogden CL. NCHS health to food ads increased by 9.3%. e-stat: Prevalence of overweight, obesity, tivity has been examined as an adjunctive and extreme obesity among adults: United treatment strategy for major depressive “Teens’ exposure to food-related TV States, trends 1960-1962 through 2009-2010 disorder.9 This type of evidence can help advertising has continued to increase [Internet]. Atlanta, GA: Centers for Disease Control and Prevention; 2012 Sep 13 [cited patients see the positive effects of physical steadily since 2003, reaching almost 16 2014 Jul 28]. Available from: www.cdc.gov/ activity on not only their weight and blood ads per day in 2011,” the authors wrote nchs/data/hestat/obesity_adult_09_10/obesity_ pressure, but also on more se- in the American Journal of Preventative adult_09_10.htm. 3. Ogden CL, Carroll MD, Kit BK, Flegal KM. rious emotional issues, such as Medicine.12 Challenges such as the adver- Increased physical Prevalence of obesity in the United States, depression and anxiety. tising of unhealthy habits are an inherent 2009–2010. NCHS Data Brief No. 82 activity can directly Similarly, lack of sleep problem for individual communities— [Internet]. Hyattsville, MD: National Center and positively for Health Statistics; 2012 Jan [cited 2014 Jun has been directly linked which makes it more crucial for physi- 2]. Available from: www.cdc.gov/nchs/data/ affect mood to obesity. According to a cians to connect with individuals, better databriefs/db82.pdf. in individuals new University of California, understand where they come from and 4. Knowler WC1, Barrett-Connor E, Fowler SE, et al; Diabetes Prevention Program who experience Berkeley study, something the challenges they face, and effectively Research Group. Reduction in the incidence depression. as simple as getting a good motivate them to change their lifestyles. of Type 2 diabetes with lifestyle intervention or metformin. N Engl J Med 2002 Feb Physical activity night’s sleep could be a habit 7;346(6):393-403. DOI: http://dx.doi. has been examined that directly affects an indi- Invest in People org/10.1056/NEJMoa012512. 10 as an adjunctive vidual’s weight. The study in Community 5. 2013 Reports (2012 Performance Year). HEDIS found that not only did sleep- In the end, for the medical community, [Internet]. Washington, DC: National Committee treatment for Quality Assurance; c2012 [last reviewed deprived individuals crave including KP, to be successful in helping strategy for 2014 Apr 2; cited 2014 Jun 2]. Available from: unhealthy choices, but their individuals implement healthy behavior http://store.ncqa.org/index.php/performance- major depressive measurement.html. brain behaved differently as change, it is crucial to approach preven- disorder. 6. Coleman KJ, Ngor E, Reynolds K, et al. well. Ultimately, the brain tion in a different way. To ultimately Initial validation of an exercise “vital sign” in impairment that occurs when produce good health, we must make electronic medical records. Med Sci Sports Exerc 2012 Nov;44(11):2071-6. DOI: http://dx.doi. sleep deprivation occurs leads to un- investments in the personal lives of our org/10.1249/MSS.0b013e3182630ec1. healthy food choices and can eventually patients­—understanding the communi- 7. Kaiser Permanente study finds efforts to cause obesity. However, on the other ties they live in and what intersection establish exercise as a vital sign prove valid [press release; Internet]. Oakland, CA: Kaiser side of the coin, this means that getting is needed between the clinical system Permanente; 2012 Oct 17 [cited 2014 Jul 28]. enough sleep is a factor that can help and changes that are easily supported by Available from: http://share.kaiserpermanente. promote weight loss in overweight pa- communities. As a health care system, org/article/kaiser-permanente-study-finds- efforts-to-establish-exercise-as-a-vital-sign- tients, as long as we can share relevant we know that there is no more impor- prove-valid/. information with them and engage them tant relationship than the one between 8. Bone health: a lifelong challenge [press release; to implement this healthy change.10,11 physician and patient. We have reached Internet]. Pasadena, CA: Kaiser Permanente; 2013 May 2 [cited 2014 Jun 2]. Available from: a point where we have an opportunity to http://xnet.kp.org/newscenter/pressreleases/ Advertising Unhealthy Habits help the primary care system prescribe scal/2013/050213-osteoporosis-month.html. Some environmental factors such success among individuals, empowering 9. Kaiser Permanente Care Management Institute. Diagnosis and treatment of depression as television advertising are beyond them to restore and maintain healthy in adults: 2012 clinical practice guideline individual control, making it even lifestyles, and we have tools available to [Internet]. Rockville, MD: National Guideline help us guide the necessary conversations Clearinghouse, Agency for Healthcare Research more difficult to break unhealthy hab- and Quality; 2012 Jun [cited 2014 Jun 2]. its. Furthermore, advertisements also to effect change. Recognizing exercise Available from: www.guideline.gov/content. become a contributing factor to poor as a vital sign is one step forward in this aspx?id=39432. process, and we will continue to engage 10. Greer SM, Goldstein AN, Walker MP. The impact eating choices, creating a vicious cycle of sleep deprivation on food desire in the of bad behavior that is difficult to break. physicians and patients to ultimately human brain. Nat Commun 2013;4:2259. DOI: Advertisements are a telling example of change the way healthy behavior change http://dx.doi.org/10.1038/ncomms3259. is approached and perceived. v 11. Anwar Y. Sleep deprivation linked to junk food environmental factors that individuals cravings [Internet]. Berkeley, CA: UC Berkeley face in their daily lives that they cannot News Center; 2013 Aug 6. Available from: change or control. Television marketing Disclosure Statement http://newscenter.berkeley.edu/2013/08/06/ poor-sleep-junk-food/. increased by 8.3% for children ages 2 to The author(s) have no conflicts of interest to disclose. 12. Powell LM, Harris JL, Fox T. Food marketing 5 years and by 4.7% for children ages 6 expenditures aimed at youth: Putting the to 11 years from 2009 to 2011, reversing numbers in context. Am J Prev Med 2013 Oct;45(4):453-61. DOI: http://dx.doi. declines in previous years, according Acknowledgment Leslie E Parker, ELS, provided editorial org/10.1016/j.amepre.2013.06.003. to Lisa Powell, PhD, of the University assistance.

92 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 LETTERS Narratives In Medical Education: The Next Steps

[Letter]. Perm J 2014 Fall;18(4):93 http://dx.doi.org/10.7812/TPP/14-106

Re: Johna S, Woodward B, Patel S. What can we learn from narratives in medical education? Perm J 2014 Spring;18(2):92-4. DOI: http://dx.doi.org/10.7812/TPP/13-166.

Dear Editor, Johna et al1 have offered an intriguing insight into reflective nar- ratives written by medical learners. Although their study was small, Response to Dr Walsh they have succeeded in getting the learners to reflect on their prac- tice, to express such reflections in a written narrative, and to express We read with interest and enthusiasm the letter written by positive feelings about the experience. It will be interesting to see Kieran Walsh, MD, in reference to narratives in medical educa- where their further research leads. tion. Dr Walsh raises some important questions and concerns, to The first challenge in this field is that of taking a great idea, in most of which we have no clear answers. Like other educators, this case reflective written narratives, and rolling it out to a wider we face many challenges in teaching and evaluating domains of group. Problems start to occur when reflection is made compulsory, Accreditation Council for Graduate Medical Education (ACGME) which in itself sounds like an oxymoron. In the United Kingdom, core competencies. many continuing professional development bodies require learners Reflective writing through narratives, at least in our opinion, is to reflect on every learning activity that they undertake. When you just another tool that can be added to the armamentarium of the have to write 50 reflections on 50 hours of learning, what should be educator. We agree that there are several challenges associated with a life-affirming activity becomes a life-draining one. Learners repeat the use of narratives; fostering a culture of self-introspection rather the same reflections or worse sometimes copy what they think is the than mandating it is just one. Measuring its effectiveness toward “right answer” from another source. Reflection can be encouraged; achieving competence is another one. Our experience, as of yet, reflective practice skills can be nurtured; a culture of reflecting on has not been validated. We took our research a step further when practice and on learning can be engendered, but reflection should we conducted a prospective, randomized, cross-over study among not become a tick-box exercise. Another challenge is developing family medicine residents not previously exposed to this tool. Only a system of assessment of reflective practice: the first test is to -as 19 residents (convenience sample) were randomized in two arms, sess whether reflection has occurred or not—this is a simple binary an intervention group (n = 9) and a control group (n = 10). Our choice for the assessor. However, assessing the quality of reflection intervention was to introduce the learners to sample narratives that is more challenging. But this has been done—sometimes in quite were analyzed with the help of the senior author. The events that challenging domains. For example, Moon et al2 have analyzed reflec- were reflective of the ACGME core competencies were highlighted. tive narratives to assess the ethical reasoning of pediatric residents. Although we could not demonstrate a difference, post hoc analysis In their case too, the study was small and required substantial and showed some very interesting findings that we will consider in expert input—however, feasibility was demonstrated. Assessment is our future research. The study is pending publication in one of vital: it drives learning, and it is incumbent on medical educators to the journals focusing on education and curricula development. ensure that assessment motivates the learners in the right way and Perhaps as important, if not more important than the use of moves them in the right direction—that is, so that they engage in real narratives in teaching ACGME core competencies, is the fact that and meaningful reflection on their practice and that such reflection such narratives were the mirror reflecting what happens in our ultimately has an impact on their practice and their patients. teaching environment day in and day out. Some of what we learned was very telling. Negative role modeling, unethical behavior, poor Yours Sincerely, professionalism, and living examples of the hidden curriculum were Kieran Walsh, MD, FRCPI just some examples. Reflective writing gave us an opportunity to Clinical Director of BMJ Learning enforce positive behaviors and mediate negative ones through BMJ Learning, London, UK structured faculty development programs. We thank Dr Walsh for his insight. We remain optimistic about the use of narratives, and we hope that our future research will References help us prove our point. 1. Johna S, Woodward B, Patel S. What can we learn from narratives in medical education? Perm J 2014 Spring;18(2):92-4. DOI: http://dx.doi.org/10.7812/ TPP/13-166. Sincerely, 2. Moon M, Taylor HA, McDonald EL, Hughes MT, Beach MC, Carrese JA. Analyzing Samir Johna, MD; Brandon Woodward, MD; Sunal Patel, MD reflective narratives to assess the ethical reasoning of pediatric residents. Narrat Inq Arrowhead Regional/Kaiser Fontana General Surgery Bioeth 2013 Fall;3(2):165-74. DOI: http://dx.doi.org/10.1353/nib.2013.0034. Residency Program

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 93 LETTERS Plant-Based Diets in Crohn’s Disease

[Letter]. Perm J 2014 Fall;18(4):94 http://dx.doi.org/10.7812/TPP/14-117

Re: Tuso PJ, Ismail MH, Ha BP, Bartolotto C. Nutritional update for physicians: plant-based diets. Perm J 2013 Spring;17(2):61-6. DOI: http://dx.doi.org/10.7812/TPP/12-085.

Dear Editor, There are a lot of papers on plant-based diets by researchers, nutritionists, References or specialists in the fields, but there is a paucity of comprehensive review for 1. Tuso PJ, Ismail MH, Ha BP, Bartolotto C. Nutritional update for physicians: plant-based diets. Perm J 2013 Spring;17(2):61-6. DOI: physicians. Therefore, we enjoyed greatly the article, “Nutritional update for physi- http://dx.doi.org/10.7812/TPP/12-085. cians: plant-based diets.” Tuso et al1 recommend a plant-based diet to all patients, 2. Takagi S, Utsunomiya K, Kuriyama S, et al. Effectiveness of an especially those with hypertension, diabetes, cardiovascular disease, or obesity. ‘half elemental diet’ as maintenance therapy for Crohn’s disease: a randomized-controlled trial. Aliment Pharmacol Ther 2006 We want to comment on our experience of a plant-based diet in treating Crohn’s Nov 1;24(9):1333-40. DOI: http://dx.doi.org/10.1111/j.1365- disease (CD). Symptoms of CD subside easily with total parenteral nutrition or 2036.2006.03120.x. total enteral nutrition. But CD is well known to flare up after the resumption of 3. Sandborn WJ, Löfberg R, Feagan BG, Hanauer SB, Campieri M, Greenberg GR. Budesonide for maintenance of remission in meals. Therefore, meals per se are thought to cause gut inflammation. Takagi et patients with Crohn’s disease in medically induced remission: al2 named their therapy “half elemental diet.” Generally, the more the amount a predetermined pooled analysis of four randomized, double- blind, placebo-controlled trials. Am J Gastroenterol 2005 of the elemental diet, the less the relapse rate is. Consequently, about half of Aug;100(8):1780-7. DOI: http://dx.doi.org/10.1111/j.1572- the daily energy is provided by an elemental diet, which is a standard regi- 0241.2005.41992.x. men in quiescent CD in Japan.2 Relapse rates with an “elemental diet” occur at 4. Hirakawa H, Fukuda Y, Tanida N, Hosomi M, Shimoyama T. Home 2 elemental enteral hyperalimentation (HEEH) for the maintenance the rate of 27% at one year, whereas the control group rate is 60% to 70% in of remission in patients with Crohn’s disease. Gastroenterol Jpn the studies by Takagi et al2 and Sandborn et al.3 When more than 30 kcal/kg 1993 Jun;28(3):379-84. ideal body weight/day of elemental diet is given, the remission rate at 1 year 5. Chiba M, Abe T, Tsuda H, et al. Lifestyle-related disease in Crohn’s 4 disease: relapse prevention by a semi-vegetarian diet. World J is about 95%. However, increasing the amount of elemental diet decreases the Gastroenterol 2010 May 28;16(20):2484-95. DOI: http://dx.doi. quality of life. We regard CD as a lifestyle-related disease mainly mediated by org/10.3748/wjg.v16.i20.2484. Westernized diets, which tend to cause dysbiosis in gut microflora.5 Namely, the 6. Chiba M, Tsuda H, Abe T, Sugawara T, Morikawa Y. Missing 6 environmental factor in inflammatory bowel disease: greatest environmental factor in CD is diet-associated gut microflora. A design diet-associated gut microflora. Inflamm Bowel Dis 2011 for increasing beneficial bacteria led us to a semivegetarian diet (SVD): lacto- Aug;17(8):E82-3. DOI: http://dx.doi.org/10.1002/ibd.21745. ovo-vegetarian with fish once a week and meat once every two weeks.5 SVD 7. Colombel JF, Sandborn WJ, Reinisch W, et al; SONIC Study Group. Infliximab, azathioprine, or combination therapy for Crohn’s and infliximab induction therapy were initiated simultaneously. Patients were disease. N Engl J Med 2010 Apr 15;362(15):1383-95. DOI: http:// admitted until completion of standard induction therapy of infliximab. Patients dx.doi.org/10.1056/NEJMoa0904492. were advised to continue the SVD after discharge. Relapse rates at 1 year and 8. Chiba M, Akashi T, Ando H, Matsuhashi T, Kato J. Three Japanese cases of inflammatory bowel disease associated with 2 years were 0% and 8% in patients on SVD and 33% and 75% in patients on left-sided colonic diverticulosis: its implication. Inflamm Bowel an omnivorous diet. These results were obtained in the absence of scheduled Dis 2005 Oct;11(10):952-4. DOI: http://dx.doi.org/10.1097/01. infliximab maintenance therapy or immunosuppressive agents,5 and they are MIB.0000183427.41587.92. 7 9. Chiba M, Ono I, Wakamatsu H, Wada I, Suzuki K. Diffuse far better than the scheduled infliximab maintenance therapy. SVD is provided gastroduodenitis associated with ulcerative colitis: treatment by during hospitalization and is recommended not only in CD but also in other infliximab. Dig Endosc 2013 Nov;25(6):622-5. DOI: http://dx.doi. intestinal diseases including ulcerative colitis8-10 and cytomegalovirus enteritis.11 org/10.1111/j.1443-1661.2012.01398.x. 1 10. Chiba M, Tsuda H, Tsuda S, Komatsu M, Horie Y, Ohnishi As Tuso et al pointed out, current diseases are a reflection of our lifestyle, H. Normalization of serum alkaline phosphatase in primary particularly a Westernized diet, in wealthy nations.12 Diet reviews recommend sclerosing cholangitis associated with ulcerative colitis. Health plant-based diets to treat and prevent a variety of common diseases. Inflammatory 2014 Apr;6(10):969-74. DOI: http://dx.doi.org/10.4236/ health.2014.610122. bowel disease (IBD) is not an exception. However, evidence level of our study 11. Chiba M, Tsuda H, Sugawara T, Ono I. Medical cure for life- is not enough to make gastroenterologists appreciate the efficacy of a plant- threatening severe cytomegalovirus enteritis in a 71-year-old man. based diet in IBD. Clinical studies providing high levels of evidence showing the Clin J Gastroenterol 2012 May;5(3):210-5. DOI: http://dx.doi. v org/10.1007/s12328-012-0305-6. efficacy of a plant-based diet in IBD is eagerly awaited. 12. Zoetendal EG, de Vos WM. Effect of diet on the intestinal microbiota and its activity. Curr Opin Gastroenterol Yours sincerely, 2014 Mar;30(2):189-95. DOI: http://dx.doi.org/10.1097/ MOG.0000000000000048. Mitsuro Chiba, MD Hideo Ohno, MD Hajime Ishii, MD Masafumi Komatsu, MD Division of Gastroenterology, Akita City Hospital, Akita City, Japan

94 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 BOOK REVIEW The Doctor Crisis by Jack Cochran, MD, and Charles Kenney

Review by Edward Ellison, MD Perm J 2014 Fall;18(4):95 http://dx.doi.org/10.7812/TPP/14-123

In their book, The Doctor Crisis, Jack Cochran, MD, and experiences and challenges as the Executive Charles Kenney send a clear and compelling message to physi- Director, President, and Chairman of the Board cians and health care executives seeking to heal a health care of the Colorado Permanente Medical Group. system in need: to fix the health care crisis, we must first fix Each story demonstrates the challenges of the doctor crisis. health care and what remarkable things can Many physicians today are struggling under the burden of be achieved when we are at our very best. increased regulatory pressures, reduced reimbursements, and Cochran also outlines his leadership learn- bureaucracy, all of which have contributed to levels of physician ing journey, which includes practical leader- burnout of epic proportion. And yet, according to the authors, ship tips and practices that have played a engaging physicians not only as healers, but as partners and critical role in his development and in that leaders, creates a path forward that heals the system from the of other physician leaders. Included among inside out. them are the importance of active listening, Cochran states, “We can’t legislate our way out of the problem. engaging and valuing physicians, and setting We must learn our way out of the problem. Improved quality will clear expectations. He discusses the impact 1p20 2 ultimately be the most powerful force for controlling costs.” key learnings from the book Play to Win New York, NY: Public Affairs; Engaging physicians, Cochran and Kenney state, would be that had on the transformation of the Colorado 2014 powerful force to mobilize for change. Permanente Medical Group. Cochran believes ISBN-13: 978-1-61039-443-7 Physicians by their very nature want to do what is right and that committing to the preservation and en- Hardbound: 216 pages best for their patients. And although physicians are often weighed hancement of physician careers frees physi- $ 23.99 down by the many challenges they face today, by addressing cians to focus on optimizing the patient care what holds them back, helping them to grow and to lead, they experience and streamlining the care process. in turn will improve the health care system. I strongly recommend The Doctor Crisis to physicians and As Cochran states with such clarity, “… physicians must step up to every leader in health care. Health care, at its heart, is a and solve the health care crisis. We must be part of the solution; team sport. Success lies in bringing together all the compas- we must be creative and bold and stand up for our patients.”1p55 sionate, dedicated professionals who care for patients. Phy- In making their case, Cochran and Kenney create an eloquent sicians have always played a critical role as leaders of our juxtaposition of data, biography, and leadership philosophy. The health care teams. By the very nature of their positions, they authors weave together stories of success and failure within the set the tone in every setting, influence every system, and are health care system, revealing its strengths and weaknesses. They looked to by others as leaders. While asking them to engage, note the relentless challenges negatively affecting the morale of to value, and to listen to others, we also need to engage, to hundreds of thousands of physicians who want nothing more value, and to listen to them. than to “put their patients first, every step in the care process, The Doctor Crisis is a valuable read for anyone seeking every time.”1p1 to understand the essential role physicians play in creating With a keen knack for storytelling, Cochran and Kenney tell solutions for care delivery, and as a result, their critical in- powerful stories that touch our heads and our hearts: from open- volvement in making health care in the US all that we need ing the book with the inspiring story of a young boy with a cleft it to be. v lip who convinced his anxious father to allow him to undergo reparative surgery, to the harrowing account of 22 surgeons and References a large multidisciplinary team representing the best that medicine 1. Cochran J, Kenney C. The doctor crisis. New York, NY: Public Affairs; 2014. 2. Wilson L, Wilson H, Blanchard K. Play to win! Choosing growth over fear in has to offer as they operate on conjoined twins, to Cochran’s work and life. Austin, TX: Bard Press; 2004.

Edward Ellison, MD, is the Executive Medical Director and Chairman of the Board of the Southern California Permanente Medical Group. E-mail: [email protected].

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 95 Physicians may earn up to 1 AMA PRA Category 1 Credit™ per article for reading and analyzing the designated CME articles published in each edition of TPJ. Each edition has four articles available for review. Other clinicians for whom CME is acceptable in meeting educational requirements may report up to four hours of participation. Please return (fax or mail to the This form is also available online: www.thepermanentejournal.org address listed on the bottom of this form) to The Permanente Journal by December 30, 2014. Forms may also be completed and submitted online at: www.thepermanentejournal.org. You must complete all sections to receive credit. (Completed forms will be accepted until December 2015. Acknowledgment will be mailed within 2 months after receipt of form.) To earn CME for reading each article designated for AMA PRA Category 1 Credit, you must: CME Evaluation Program • Score at least 50% in the post-test • Complete the evaluation and provide your contact information

Section A. Article 1. (page 4) Mindfulness-Based Stress Reduction in an Integrated Care Delivery System: Article 3. (page 21) Impact of Implementing Glycated Hemoglobin Testing for Identification One-Year Impacts on Patient-Centered Outcomes and Health Care Utilization of Dysglycemia in Youth Which of the following core skills is not taught in Mindfulness-Based Stress Reduction? The following American Diabetes Association recommendations for children are true except: a. understanding of attitudes, perceptions, and unskillful thought patterns a. screening at age 10 with any 2 risk factors as discussed in the study b. understanding and modulating one’s reaction to stressors b. Body mass index (BMI) ≥ 85th percentile for age and sex with no other risk factors c. recognizing pleasant and unpleasant emotions, thoughts, and sensations c. BMI ≥ 85th percentile for age and sex with any 2 risk factors d. meditation d. onset of puberty with any 2 risk factors Which of the patient-reported outcomes showed negative changes at 1 year, compared The following are the main findings of the study except: to 8 weeks following the Mindfulness-Based Stress Reduction intervention? a. glycated hemoglobin testing was more common in 2012 a. mental composite score b. the proportion of patients identified as at-risk for diabetes by either test (fasting plasma glucose b. bodily pain or glycated hemoglobin) increased significantly in both sites from 2009 to 2012 c. self-efficacy c. a significantly larger proportion of females were identified in 2012 in both sites d. depression d. the mean age for youth at risk for diabetes increased significantly between 2009 and 2012

Article 2. (page 10) Improving Appropriate Use of Pulmonary Computed Tomography Angiography by Article 4. (page 89) Healthy Behavior Change in Practical Settings Increasing the Serum D-Dimer Threshold and Assessing Clinical Probability Motivational interviewing involves which 4 stages of dialogue? Based on the results of the three PIOPED trials, what should be the minimum prevalence a. assessing, level-setting, supporting, and motivating of acute pulmonary embolism among patients undergoing evaluation for pulmonary embolism? b. empathizing, balancing, orienting, and activating a. 5% c. engaging, focusing, evoking, and planning b. 10% d. understanding, rationalizing, processing, and materializing c. 15% The Bone Density Screening Program is an example of how combining early intervention with d. 20% ______and ______can significantly alter the course of health history for patients. e. 30% a. exercise and wellness coaching Which of the following statements is true: b. lifestyle and behavior change a. the prevalence of acute pulmonary embolism in patients with a D-dimer < 1.0 ug/mL is no greater c. supplemental vitamins and physical therapy than the coincidental pulmonary embolism rate seen on computed tomography scans of the chest d. diet and health education b. all patients with low clinical risk for pulmonary embolism should have their D-dimer level checked c. patients with intermediate clinical risk for pulmonary embolism do not need to have their D-dimer level checked d. patients with both high clinical risk and D-dimer level > 1.0 ug/mL should be treated for pulmo- nary embolism Please return completed form by December 30, 2014 e. raising the D-dimer threshold to 1.0 ug/mL does not increase the prevalence of pulmonary embolism seen on pulmonary computed tomography angiographs

Section B. Section C. Referring to the CME articles, how likely is it that you will implement this learning to improve your practice What other changes, if any, do you plan to make in your practice as within the next 3 months? a result of reading these articles?

Objective 1 Objective 2 Objective 3 Integrate learned Lead in further developing “Patient- Implement changes and ______Key knowledge and Centered Care” activities by acquiring apply updates in services and 5 = highly likely ______4 = likely increase competence/ new skills and methods to overcome practice/policy guidelines, confidence to support barriers, improve physician/patient incorporate systems and 3 = unsure ______2 = unlikely improvement and relationships, better identify diagnosis quality improvements, and 1 = highly unlikely change in specific and treatment of clinical conditions, effectively utilize evidence- 0 = I already did this practices, behaviors, as well as, efficiently stratify health based medicine to produce and performance. needs of varying patient populations. better patient outcomes. Section D. (Please print)

Name ______Article 1 5 4 3 2 1 0 5 4 3 2 1 0 5 4 3 2 1 0 Physician Non-Physician Article 2 5 4 3 2 1 0 5 4 3 2 1 0 5 4 3 2 1 0 Title ______Article 3 5 4 3 2 1 0 5 4 3 2 1 0 5 4 3 2 1 0

Article 4 5 4 3 2 1 0 5 4 3 2 1 0 5 4 3 2 1 0 E-mail ______

Address ______

The Kaiser Permanente National CME Program is accredited by the Mail or fax completed form to: ______Accreditation Council for Continuing Medical Education (ACCME) to provide The Permanente Journal continuing medical education for physicians. 500 NE Multnomah St, Suite 100 Signature ______The Kaiser Permanente National CME Program designates this journal-based Portland, Oregon 97232 CME activity for 4 AMA PRA Category 1 Credits™. Physicians should claim Phone: 503-813-3286 Date ______only the credit commensurate with the extent of their participation in the activity. Fax: 503-813-2348

96 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ONLINE ONLY CASE STUDY Reverse Pseudohyperkalemia in a Patient with Chronic Lymphocytic Leukemia

Taurino Avelar, MD Perm J 2014 Fall;18(4):e150-e152 http://dx.doi.org/10.7812/TPP/14-084

to have been confirmed. On the basis of the elevated plasma Abstract potassium level, the patient was subsequently referred to the A man, age 78 years, with a history of chronic lymphocytic Emergency Department for treatment. leukemia presented to clinic for evaluation of a cough. On Upon arrival, the patient’s repeat plasma potassium was further evaluation, he was noted to have an elevated potassium 8.1 mEq/L. Electrocardiogram did not demonstrate peaked T level. This case report highlights the importance of distinguishing waves, loss of P waves, prolonged QRS intervals, or evidence cases of true hyperkalemia from pseudohyperkalemia and of high-grade block. He was treated with intravenous calcium reverse pseudohyperkalemia. gluconate, intravenous insulin, and oral sodium polystyrene sulfonate. Plasma potassium remained elevated at 8.1 mEq/L. A repeat electrocardiogram showed no change. With the excep- Introduction tion of the cough and toe pain, he continued to be asymptom- Hyperkalemia can be challenging to manage. Differentiating atic despite the persistently elevated plasma potassium, and true hyperkalemia from pseudohyperkalemia is often difficult. he denied any weakness, fatigue, or palpitations. Given the A less well-known condition that is thus challenging to identify apparent lack of improvement in potassium despite medical is reverse pseudohyperkalemia. Here, I present an unusual treatment, the decision was to proceed with emergent dialysis. case of reverse pseudohyperkalemia in an elderly man with a After partial dialysis, the possibility of reverse pseudohy- history of chronic lymphocytic leukemia (CLL). perkalemia was considered. Potassium was rechecked, both the plasma and serum potassium, which were 7.9 mEq/L and Case Report 4.4 mEq/L, respectively. Given the patient’s history, hemody- A man, age 78 years, with a history of CLL (not currently namic stability, and lack of electrocardiogram findings and the on treatment), chronic kidney disease 3A, coronary artery fact that he was without improvement despite hemodialysis, disease, and hypertension was initially seen in clinic report- it was suspected that the plasma potassium results did not ing two days of coughing. He also reported one day of toe represent the true in vivo potassium levels. Hemodialysis was pain but was otherwise asymptomatic. There were no recent subsequently discontinued, and repeat testing 4 hours later changes to his home medications, which included amlodipine, demonstrated similar results. The patient’s serum potassium atenolol, aspirin, and pravastatin. Notably, he was not on an was 4.4 mEq/L and 4.6 mEq/L on the day of discharge. angiotensin-converting-enzyme inhibitor or an angiotensin re- ceptor blocker, despite a history of coronary artery disease. Vital Discussion signs were within normal limits, and physical examination was Hyperkalemia is a life-threatening electrolyte abnormality unremarkable. Given his history of CLL, tumor lysis syndrome that requires prompt diagnosis and treatment. In treating hyper- leading to gout was suspected. He was further evaluated, and kalemia, physicians have multiple therapeutic options at their laboratory results were significant for leukocytosis, 206 × 103 disposal. In the case above, hemodialysis was felt to be an ap- cells/μL (95% lymphocytes) (normal 4.0 to 10.0 × 103 cells/μL); propriate intervention because the patient’s plasma potassium plasma potassium, 8.4 mEq/L (nonhemolyzed; normal 3.5 to level was not responding to medical management for severe 5.0 mEq/L); calcium, 8.4 mg/dL (normal 9.0 to 10.5 mg/dL); hyperkalemia, a justifiable reason for emergent hemodialysis. phosphorus, 4.7 mg/dL (normal 3.0 to 4.5 mg/dL); uric acid, Unfortunately, the inability to determine the patient’s true po- 10.6 mg/dL (normal 2.5 to 8.0 mg/dL); and glucose, 91 mg/dL tassium level resulted in the implementation of interventions (normal 70 to 100 mg/dL). Results were also significant for that could have led to significant morbidity and mortality. It blood urea nitrogen, 36 mg/dL (normal 8.0 to 20 mg/dL); cre- was only after further clinical laboratory investigation that the atinine, 1.4 mg/dL (normal 0.7 to 1.3 mg/dL); and glomerular true potassium level was identified (Table 1). Because there are filtration rate of 49 mL/min/1.73 m2. The patient’s baseline various causes for falsely elevated potassium measurements, creatinine was 1.3 mg/dL, with a glomerular filtration rate of understanding the scenarios in which they may occur is crucial 53 mL/min/1.73 m2. Given the profound leukocytosis, hyper- to a clinician’s decision making.1 The challenges in identifying kalemia, and hyperuricemia, tumor lysis syndrome seemed this abnormality demand further discussion.

Taurino Avelar, MD, is an Internist at the Los Angeles Medical Center in CA. E-mail: [email protected].

e150 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 CASE STUDY Reverse Pseudohyperkalemia in a Patient with Chronic Lymphocytic Leukemia

been attempts to define pseudohyperkalemia as a difference Table 1. Differential diagnosis of hyperkalemia between serum and plasma potassium concentration of more Condition Serum K Plasma K than 0.4 mEq/L when the samples are obtained at the same Hyperkalemia High High time, remain at room temperature, and are tested within an Pseudohyperkalemia Falsely High Normal hour of collection.9,10 Given the implications of basing medical Reverse Pseudohyperkalemia Normal Falsely High decisions on falsely elevated levels, measuring potassium from K = potassium. plasma continues to be the preferred method. In the case of reverse pseudohyperkalemia, the opposite is seen: plasma potassium is noted to be higher than serum po- Potassium is normally measured from a sample of either tassium. It is a phenomenon that has been reported in patients plasma or serum. A sample of plasma is collected in a tube that with CLL.10-13 The mechanism of this phenomenon is yet to be contains heparin to serve as the anticoagulant (although it can clearly characterized, but several observations have been made. also be collected with other additives, such as ethylenediamine One possibility is increased sensitivity to heparin-mediated tetra-acetic acid [EDTA] and citrate), whereas serum is collected cell membrane damage during processing and centrifugation in a tube that does not contain heparin or the other additives. in the context of hematologic malignancy.10,11 In one study, In the clotting process, platelets undergo aggregation and de- the degree of increase in potassium was directly related to the granulation while also releasing potassium.2,3 As a result, serum amount of heparin contained within the tube into which the potassium is higher (0.36 ± 18 mEq/L) compared with a sample sample was collected.12 Mechanical stressors have also been collected in plasma.4 This has also been noted in patients with implicated. Pneumatic tube transportation systems may lead to significant erythrocytosis and leukocytosis.5-8 Such abnormalities falsely elevated plasma potassium levels.14 These findings are can lead to what is known as pseudohyperkalemia, which is not surprising given that the cells in patients with CLL are both a phenomenon observed in vitro where the measured serum fragile, and thus more susceptible to lysis, and more numerous, potassium is elevated and the plasma potassium is normal. In which can lead to significant abnormal laboratory results that addition to these patient-related causes, there are additional may not otherwise be appreciated. This patient had a history factors that can lead to this abnormality (Table 2). There have of CLL with extreme leukocytosis, and the samples had been collected in heparin-containing tubes and transported via a pneumatic tube transportation system. No tested sample was Table 2. Causes of pseudohyperkalemia transported manually for comparison. Factors Examples There are ways laboratories may promptly identify cases of Mechanical Prolonged tourniquet use reverse pseudohyperkalemia. Consideration may be given to Fist clenching testing serum potassium if the plasma potassium is elevated Traumatic venipuncture or probing in the context of leukocytosis. In addition, serum testing may Inappropriate needle diameter include evaluating potassium in patients with CLL. Such testing may lead to prompt recognition of reverse pseudohyperka- Excessive force with syringe draws lemia. On further chart review, it was noted that the patient Diameter mismatch of catheter, tube adapter device, and needle had not previously been started on an angiotensin-converting- enzyme inhibitor or an angiotensin receptor blocker because Pneumatic tube transport/unpadded canisters of previously elevated potassium levels, further highlighting Specimen processing (vigorous mixing, excessive centrifugal force, prolonged fixed angle the importance of making the diagnosis. centrifugation or recentrifugation of gel separator Because of its cardiotoxic potential, hyperkalemia is a tubes) potentially fatal electrolyte abnormality. The ability to dif- Chemical Incomplete drying of ethanol containing antiseptics ferentiate true hyperkalemia from pseudohyperkalemia and before venipuncture reverse pseudohyperkalemia is crucial for determining the Temperature Specimens not stored at 15 ºC -25ºC appropriate interventions. The necessary treatments can only Time Delayed processing be determined by taking into account the clinical history, Patient related Acute respiratory alkalosis hemodynamics, appropriate clinical laboratory investigation, Thrombocytosis and echocardiogram findings. v Erythrocytosis Leukocytosis/WBC neoplasms Disclosure Statement The author(s) have no conflicts of interest to disclose. Postsplenectomy state Familial pseudohyperkalemia Acknowledgment Contaminants Potassium-containing IV fluids Leslie Parker, ELS, provided editorial assistance. Tube additives containing potassium salts Miscellaneous Plasma reference ranges References Mislabeling 1. Asirvatham JR, Moses V, Bjornson L. Errors in potassium measurement: a laboratory perspective for the clinician. N Am J Med Sci 2013 Apr;5(4):255-9. IV = intravenous; WBC = white blood cell. DOI: http://dx.doi.org/10.4103/1947-2714.110426.

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 e151 CASE STUDY Reverse Pseudohyperkalemia in a Patient with Chronic Lymphocytic Leukemia

2. Ifudu O, Markell MS, Friedman EA. Unrecognized pseudohyperkalemia as 9. Sevatos N, Theodossiades G, Archimandritis AJ. Pseudohyperkalemia a cause of elevated potassium in patients with renal disease. Am J Nephrol in serum: a new insight into an old phenomenon. Clin Med Res 2008 1992;12(1-2):102-4. DOI: http://dx.doi.org/10.1159/000168425. May;6(1):30-2. DOI: http:/dx.doi.org/10.3121/cmr.2008.739. 3. Sevastos N, Theodossiades G, Efstathiou S, Papatheodoridis GV, Manesis E, 10. Singh PJ, Zawada ET, Santella RN. A case of ‘reverse’ pseudohyperkalemia. Archimandritis AJ. Pseudohyperkalemia in serum: the phenomenon and its Miner Electrolyte Metab 1997;23(1):58-61. clinical magnitude. J Lab Clin Med 2006 Mar;147(3):139-44. DOI: http:// 11. Abraham B, Fakhar I, Tikaria A, et al. Reverse pseudohyperkalemia in a dx.doi.org/10.1016/j.lab.2005.11.008. leukemic patient. Clin Chem 2008 Feb;54(2):449-51. DOI: http:/dx.doi. 4. Nijsten MW, de Smet BJ, Dofferhoff AS. Pseudohyperkalemia and plate- org/10.1373/clinchem.2007.095216. let counts. N Engl J Med 1991 Oct 10;325(15):1107. DOI: http://dx.doi. 12. Meng QH, Krahn J. Reverse pseudohyperkalemia in heparin plasma org/10.1056/NEJM199110103251515. samples from a patient with chronic lymphocytic leukemia. Clin Bio- 5. Fukasawa H, Furuya R, Kato A, et al. Pseudohyperkalemia occurring in a pa- chem 2011 Jun;44(8-9):728-30. DOI: http:/dx.doi.org/10.1016/j.clinbio- tient with chronic renal failure and polycythemia vera without severe leuko- chem.2011.03.026. cytosis or thrombocytosis. Clin Nephrol 2002 Dec;58(6):451-4. DOI: http:// 13. Garwicz D, Karlman M. Early recognition of reverse pseudohyperkalemia dx.doi.org/10.5414/CNP58451. in heparin plasma samples during leukemic hyperleukocytosis can prevent 6. Kintzel PE, Scott WL. Pseudohyperkalemia in a patient with chronic lym- iatrogenic hypokalemia. Clin Biochem 2012 Dec;45(18):1700-2. DOI: http:/ phoblastic leukemia and tumor lysis syndrome. J Oncol Pharm Pract 2012 dx.doi.org/10.1016/j.clinbiochem.2012.07.104. Dec;18(4):432-5. DOI: http://dx.doi.org/10.1177/1078155211429885. 14. Kellerman PS, Thornbery JM. Pseudohyperkalemia due to pneumatic tube 7. Bellevue R, Dosik H, Spergel G, Gussoff BD. Pseudohyperkalemia and ex- transport in a leukemic patient. Am J Kidney Dis 2005 Oct;46(4):746-8. treme leukocytosis. J Lab Clin Med 1975 Apr;85(4):660-4. DOI: http:/dx.doi.org/10.1053/j.ajkd.2005.06.005. 8. Ruddy KJ, Wu D, Brown JR. Pseudohyperkalemia in chronic lymphocyt- ic leukemia. J Clin Oncol 2008 Jun 1;26(16):2781-2. DOI: http:/dx.doi. org/10.1200/JCO.2008.16.3014.

e152 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ONLINE ONLY CASE STUDY An Incidental Discovery of Low-Grade Appendiceal Mucinous Neoplasm

Aaysha Kapila, MD; Jennifer Phemister, MD; Pranav Patel, MD; Chakradhar M Reddy, MD; Ravindra Murthy, MD; Mark F Young, MD Perm J 2014 Fall;18(4):e153-e154 http://dx.doi.org/10.7812/TPP/14-077

A 65-year-old man with a history of hyperplastic polyps underwent a surveil- lance colonoscopy, which revealed a large, smooth cystic bulge at the appen- dicular orifice (Figure 1). Subsequently, a computed tomography (CT) of the abdomen with contrast revealed an ap- pendiceal mucocele measuring 13.3 x 4.5 cm (Figures 2a and 2b). Because of the abnormal imaging findings, an elec- tive laparoscopic appendectomy and cecectomy was performed with minimal spillage. A gross specimen measuring Figure 2a (left) and 2b (right). Computed tomography (coronal [2a] and transverse [2b]) with 9 cm in length and 3 cm in diameter was contrast, demonstrating a large appendix with diffuse wall thickening indicative of appendiceal collected with the appendiceal lumen, mucocele neoplasm. which was filled with yellow mucoid material. Histopathologic evaluation of the appendix revealed a low-grade ap- and 12 months, and a colonoscopy at 1 colon cancer, peritoneal sarcomatosis, pendiceal mucinous neoplasm (LAMN)-I year after surgery. peritoneal mesothelioma, disseminated (Figure 3). The patient had an uneventful On endoscopic visualization of this peritoneal fungal infections, pseudomyx- recovery and was doing well at the time 65-year-old patient, lipoma or mucocele oma peritonei, or retroperitoneal cyst.1,3 of writing. Repeat CT of the abdomen were considered the differentials. On the LAMN is divided into two major classes. and pelvis was scheduled at 6 months basis of the CT of the abdomen and of the LAMN-I is found in a younger group of endoscopy, we considered LAMN, with patients, with the tumor confined to the the rare possibility of pseudomyoma and appendix lumen.4 LAMN-I is rarely pro- peritoneal metastasis. gressive, so a “wait-and-watch” policy is LAMN is a rare entity with an incidence recommended with measurement of tu- ranging from 0.2% to 0.7% of all excised mor markers, CT of the abdomen and pel- appendixes.1 Approximately 25% to 50% vis at six months, and an annual work-up.4 of LAMN are incidental findings with LAMN-II is usually found in older patients, the initial discovery during radiologic or with mucin and/or neoplastic epithelium endoscopic examinations, or during sur- in the submucosa, the intestinal wall, or gery.2 Initial presentation can range from in the area around the appendix with asymptomatic to right lower quadrant or without perforation.1,4 Recommended abdominal pain or a palpable abdominal treatment for LAMN-II includes hyperther- mass. Initial clinical differentials include mic intraperitoneal chemotherapy, pro- acute appendicitis, diverticulitis, ovarian phylactic cytoreductive surgery, greater Figure 1. Colonoscopy image showing a large cystic lesion at the appendicular mass (in women), large cecal mass, peri- omentectomy and splenectomy, left up- orifice. toneal carcinomatosis originating from per quadrant peritonectomy, right upper

Aaysha Kapila, MD, is an Internist at East Tennessee State University in Johnson City. E-mail: [email protected]. Jennifer Phemister, MD, is an Internist at East Tennessee State University in Johnson City. E-mail: [email protected]. Pranav Patel, MD, is a Gastroenterologist at East Tennessee State University in Johnson City. E-mail: [email protected]. Chakradhar M Reddy, MD, is a Gastroenterologist at East Tennessee State University in Johnson City. E-mail: [email protected]. Ravindra Murthy, MD, is a Gastroenterologist at the James H Quillen Veterans Affairs Medical Center in Johnson City, TN. E-mail: [email protected]. Mark F Young, MD, is a Gastroenterologist at East Tennessee State University in Johnson City. E-mail: [email protected].

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 e153 CASE STUDY An Incidental Discovery of Low-Grade Appendiceal Mucinous Neoplasm

Disclosure Statement The author(s) have no conflicts of interest to disclose.

Acknowledgements The authors are thankful to Elizabeth Arze, MD, from the Department of Pathology at East Tennessee State University in Johnson City, TN, and to Rowena Velilla, MD, from the James H Quillen Veterans Affairs Medical Center in Johnson City, TN, for providing the histopathologic images.

References 1. Chua TC, Moran BJ, Sugarbaker PH, et al. Early- and long-term outcome data of pa- tients with pseudomyxoma peritonei from appendiceal origin treated by a strategy of cytoreductive surgery and hyperthermic intra- peritoneal chemotherapy. J Clin Oncol 2012 Jul 10;30(20):2449-56. DOI: http://dx.doi. org/10.1200/JCO.2011.39.7166. Figure 3. Histopathologic image (10x magnification) demonstrating villiform mucinous 2. Rojnoveanu G, Ghidirim G, Mishin I, Vozian M, epithelium, glandular epithelium with tall columnar mucinous cells, and pseudostrati- Mishina A. Preoperatively diagnosed mucocele fied nuclei at the base. of the appendix. Chirurgia (Bucur) 2014 May- Jun;109(3):416-20. quadrant peritonectomy, lesser omentec- ment of ovary and peritoneum, whereas 3. Sugarbaker PH. Surgical responsibilities in the management of peritoneal carcinomatosis. J tomy with cholecystectomy, pelvic peri- others believe that each tumor has an Surg Oncol 2010 Jun 15;101(8):713-24. DOI: tonectomy with rectosigmoid resection, independent origin.5 The topic continues http://dx.doi.org/10.1002/jso.21484. and anterectomy with a more aggressive to be debated. Since intact mucoceles are 4. McDonald JR, O’Dwyer ST, Rout S, et al. Classi- fication of and cytoreductive surgery for low- 3,5 follow-up. In women with concomitant benign, the worst outcomes are perfora- grade appendiceal mucinous neoplasms. Br J peritoneum, ovarian, or appendix tumors, tion or spillage of the mucoceles into the Surg 2012 Jul;99(7):987-92. DOI: http://dx.doi. many authors believe that the appendix is peritoneal cavity, causing pseudomyxoma org/10.1002/bjs.8739. 5. Misdraji J. Appendiceal mucinous neoplasms: 3 the primary site with secondary involve- peritonei to develop. v controversial issues. Arch Pathol Lab Med 2010 Jun;134(6):864-70.

e154 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 ONLINE ONLY CASE STUDY Latrodectus Envenomation in Greece

Garyfallia Nikolaos Antoniou, MSc; Dimitrios Iliopoulos, PhD; Rania Kalkouni, MD; Sofia Iliopoulou, MSc; Giorgos Rigakos, MD; Agoritsa Baka, MD Perm J 2014 Fall;18(4):e155-e158 http://dx.doi.org/10.7812/TPP/14-028

large, shiny, black abdomen with a red-orange hourglass or Abstract spot on the ventral abdomen. However, they can have variation During the summer period 2011-2012, seven widow spider in color and markings.3 Latrodectus tredecimguttatus is black in bites in Greece were reported to the Hellenic Center for Disease color, similar to most other Latrodectus species, and is identi- Control and Prevention. Widow spiders (in the genus Latrodectus) fied by the 13 spots found on its dorsal abdomen. These spots are found all over the world, including Europe, Asia, Africa, are usually red in color but may also be yellow or orange. It Australia, and the US. Alpha-latrotoxin (main mammalian toxin) is otherwise similar to other species in the genus Latrodectus. causes the toxic effects observed in humans. Victims should The male L tredecimguttatus is smaller, brown, and incapable receive timely medical care to avoid suffering. Latrodectus bites of envenomating humans. The female sometimes eats the male are very rarely fatal. during or after copulation. Webs are irregular, low-lying, and All the patients reported having an insect bite 30 minutes commonly seen in dark environments such as garages, barns, to 2 hours before they arrived at the Emergency Department outhouses, and foliage.4 Generally, Latrodectus bite if they are of the local hospital. Severe muscle cramps, weakness, disturbed, so people should take care when reaching into dark tremor, abdominal pain, and increased levels of creatinine areas to avoid spider bites. phosphokinase were present in all patients. The Emergency Alpha-latrotoxin is the main mammalian toxin found in the Operation Center of the Hellenic Center for Disease Control Latrodectus venom, with predominantly neurologic and auto- and Prevention was informed immediately in all cases. An- nomic effects. The toxin opens presynaptic cation channels, tivenin was administered to four patients upon the request causing a massive influx of calcium and increased release of of their physicians. multiple neurotransmitters (primarily acetylcholine). This results All patients recovered fully. It is essential that health care in excess stimulation of motor endplates with resultant clinical workers recognize early the symptoms and signs of Latrodectus manifestations. bites to provide the necessary care. The management of mild to No deaths caused by Latrodectus envenomation have been moderate Latrodectus envenomations is primarily supportive. reported to the American Association of Poison Control Centers Hospitalization and possibly antivenin should be reserved for since its first annual report in 1983 until 2004.5 Deaths caused patients exhibiting serious systemic symptoms or inadequate by Latrodectus bites were reported in Spain (2001),6 Greece pain control. The most important thing for all of these patients (2003),7 and Albania (2006).8 is early pain relief. The spiders that bit the Greek victims during the summer period 2011-2012 were not caught, so it was not possible for Introduction the physicians to identify whether they were Latrodectus bites. The spider genus Latrodectus, commonly called “widow However, the patients’ symptoms were indicative of bites from spider,” is found all over the world, including Europe, Asia, Latrodectus as determined by medical personnel and supported Africa, Australia, North America, and South America. The genus by the positive response to the antivenin, which the Hellenic includes the black widow spider common in North America: L Poison Information Centre and the medical staff agreed was mactans.1 The term widow spider is used because not all spe- indicated. The antivenin used (Aracmyn Plus; Instituto Bioclon; cies in the genus Latrodectus are black. There are other widow Mexico City, Mexico) possesses the necessary mix of antibod- spiders including the brown widow (Latrodectus geometricus), ies to neutralize the various toxic components found in spider the red-legged widow (Latrodectus bishopi), the redback venom. It is produced by the antibodies developed by horses spider (Latrodectus hasselti), the button spider (Latrodectus that are immunized with Latrodectus venom.9 indistinctus), Latrodectus variolus, and Latrodectus hesperus. Symptoms of spider envenomation (latrodectism) may include Latrodectus tredecimguttatus is found in Europe (including initial localized reaction at the bite site, generally trivial, which Greece) and South America.2 The adult female L mactans is may go unnoticed. Commonly, the bite is described as a pinch approximately 2 cm in length and is easily identified by its or pinprick; however, infants may present with unexplained

Garyfallia Nikolaos Antoniou, MSc, is an Epidemiological Nurse in the Emergency Operation Center at the Hellenic Center for Disease Control and Prevention in Athens, Greece. E-mail: [email protected]. Dimitrios Iliopoulos, PhD, is an Epidemiological Dentist in the Emergency Operation Center at the Hellenic Center for Disease Control and Prevention in Athens, Greece. E-mail: [email protected]. Rania Kalkouni, MD, is an Epidemiologist in the Epidemiological Surveillance Department at the Hellenic Center for Disease Control and Prevention in Athens, Greece. E-mail: [email protected]. Sofia Iliopoulou, MSc, is an Epidemiologist in the Emergency Operation Center at the Hellenic Center for Disease Control and Prevention in Athens, Greece. E-mail: [email protected]. Giorgos Rigakos, MD, is an epidemiologist in the Emergency Operation Center at the Hellenic Center for Disease Control and Prevention in Athens, Greece. E-mail: [email protected]. Agoritsa Baka, MD, is an Epidemiologist in the Emergency Operation Center at the Hellenic Center for Disease Control and Prevention in Athens, Greece. E-mail: [email protected].

The Permanente Journal/ Fall 2014/ Volume 18 No. 4 e155 CASE STUDY Latrodectus Envenomation in Greece

crying.10 Tiny fang marks may be visible, and local effects are Latrodectus envenomations may be managed with opioid usually limited to a small circle of redness, localized diaphoresis, analgesics and sedative-hypnotics.11 Antivenin administration and/or induration around the immediate bite site. A central red- may be indicated for patients who have severe envenomation dened fang puncture site surrounded by an area of blanching with pain refractory to these measures. Antivenin administra- and an outer halo of redness is described as having a target tion results in resolution of most symptoms half an hour after appearance. Systemic symptoms begin within about one hour administration most of the time, and it has been shown to de- and may last for a few days. crease the need for hospitalization.9 Calcium gluconate, though Abdominal rigidity after the bite may mimic an acute abdo- historically a treatment, has been shown to be less effective men regarding the symptom’s intensity.4 It is not a true surgical than benzodiazepines combined with opioids.11 Hospitalization emergency. Neurologic effects, including mild weakness, fas- and possibly antivenin administration should be reserved for ciculations, and ptosis, have been described as well. Latrodectus patients exhibiting serious systemic symptoms or inadequate facies, characterized by spasm of facial muscles, edematous pain control. High-risk factors include age older than 60 years, eyelids, and lacrimation, may occur. This can be mistaken for an severe envenomation, pediatric patient, or history of hyperten- allergic reaction. Pain in the chest, back, and extremity muscles, sion and coronary artery disease. depending on the bite site, may occur. Respiratory symptoms Latrodectism can be easily confused with steatodism. including chest pain/tightness, shortness of breath, grunting and Steatodism is the envenomation caused by the spider species respiratory distress, bronchorrhea, and pulmonary edema have Steatoda. Steatoda resemble Latrodectus in size and physical been described in Europe and South Africa.4 Other reported form, owing to being members of the same family (Theridiidae). symptoms include nausea, vomiting, headache, numbness, Although the bite of Steatoda spiders is not as serious as that of agitation, irritability, and priapism.4 true widow spiders, several of these spiders do have medically

Table 1. Cases of Latrodectus envenomation Demographics Clinical symptoms and findings Level of Age, Cardiovascular Respiratory Other reported white blood Sex years Pain system symptoms symptoms CPK CRP cells Other Treatment Male 24 Acute ECG: incomplete right Tachypnea, Sweating, Elevated Elevated Elevated Elevated Antivenin abdominal pain bundle branch block pulmonary salivation, troponine edema priapism (1.6 ng/mL) Male 66 Severe pain in Increased systolic Dyspnea Slightly Elevated Elevated Impaired Oxygen the legs at the pressure (200 mm Hg), elevated (20,000/μL) renal (venturi mask bite point, acute signs of cardiac downturn function 30%), diuretic abdomen (pain, were present without the (creatinine and morphine, flatulence) final manifestation 1.4-1.6) antivenin Male 64 Severe pain Mild Sweating Pethidine at the dorsal tachypnea surface of the right foot at the bite area, back pain Female 70 Generalized Mild hypertension Metabolic Opioid muscle pain to (155/90 mm Hg) acidosis analgesics back, chest, (pH: 7.23) and abdomen Male 49 Intense pain at Increased blood pressure Local swelling Elevated Mild Oxygen, opioid the area of bite (180 mm Hg) at the bite area (1423 leukocytosis analgesics, (inner surface U/L) calcium of the arm), and beta- extension of adrenergic pain to the chest blockers, and abdomen antivenin Female 4 Intense pain at Local swelling Mild Oxygen, opioid the area of bite at the bite area leukocytosis analgesics Male 21 Severe pain Myocarditisaugmentation General anxiety Mild Elevated Oxygen, in the legs, in T-wave amplitude leukocytosis cardiac opioid thoracic pain in leads V3 through enzymes analgesics, V6 without reciprocal troponin antivenin changes (1.1 ng/mL) CPK = creatinine phosphokinase; CRP = C-reactive protein; ECG = electrocardiogram.

e156 The Permanente Journal/ Fall 2014/ Volume 18 No. 4 CASE STUDY Latrodectus Envenomation in Greece

significant bites. Their bites cause symptoms that have been contacted the Emergency Operations Center of the Hellenic described as a very minor Latrodectus bite. Use of Latrodectus Center for Disease Control and Prevention to request the anti- antivenin has been shown effective in treating steatodism.12 venin Aracmyn Plus, two vials of which were sent immediately. The first dose of antivenin was administered while the patient Case Presentations was sedated, and the second dose was administered while se- All patients reported having an insect bite 30 minutes to 2 dation was interrupted. Half an hour after the administration of hours before they arrived at the Emergency Department (ED) the second dose of antivenin, the patient’s respiratory function of the local hospital. The bite area looked like 2 small holes. significantly improved. Severe pain at the bite area, acute abdomen, severe muscle On the second day of hospitalization in the ICU, the patient cramps, weakness, and mild leukocytosis were present in most was extubated. For his ventilation, a venturi mask was used. patients. Respiratory symptoms including chest pain/tightness Initially, the patient’s pulse increased during effort, but this im- and tachypnea were present in 3 of them. Other reported proved by the third day of hospitalization. Cardiovascular and symptoms were hypertension, sweating, priapism, elevated pulmonary systems were in good condition, and he suffered creatinine phosphokinase (CPK), elevated C-reactive protein mild fever. CPK and amylase were declining; whereas CRP was (CRP), pulmonary edema, dyspnea, elevated troponin levels, increasing. The white blood cells decreased by 21,000/mL. (On and metabolic acidosis. the first day of hospitalization, antibiotics were administered to It is interesting that two young males (first and seventh cases) avoid possible local bacterial infection.) manifested cardiac toxicity. The first patient’s electrocardiogram During the third day of hospitalization, CPK, CRP, and amy- (ECG) showed incomplete right bundle branch block, and he lase remained elevated, whereas transaminases were normal suffered elevated troponin levels; whereas the ECG of the sev- (morning). In the afternoon, CPK increased significantly (4-digit enth patient showed augmentation T-wave amplitude in leads number); amylase was declining. White blood cells declined to V3 through V6 without reciprocal changes; he also had elevated 17,000/mL. Twenty-four hours later, CPK was on a downward troponin levels. Detailed information about each patient’s symp- trend, owing to increasing hydration and diuresis. Amylase and toms may be found in Table 1. transaminases were increased. The patient’s overall health condi- The antivenin (Aracmyn Plus) was administered to 4 patients tion was quite good, so he was moved from the ICU to the Internal upon the request of their physicians because of the severity of Medicine Department of the hospital for further observation. their situation or the presence of underlying diseases. One or 2 On the sixth day of hospitalization, the patient was discharged vials were administered to patients. The clinical improvement with complete recovery. of the patients occurred after half an hour of the antivenin ad- ministration. Per the manufacturer, antivenin dose varies from Discussion 1 to 5 vials depending on severity of symptoms. The antivenin In cases of Latrodectus envenomation, it is essential that health Aracmyn Plus has completed human Phase 3 trials. Aracmyn care practitioners recognize the signs and symptoms of enven- Plus is an equine-origin Fab2 product and is considered to be omation as quickly as possible to begin the best care of patients. less likely to trigger an allergic reaction.9 One vial of the anti- To diagnose a Latrodectus envenomation, it is important for venin is mixed with 50 mL normal saline and is administered the physician to see the suspected spider. If this is not possible, intravenously within 30 minutes.9 Latrodectus bites are diagnosed through a bit of detective work. All patients were administered opioid analgesics for the relief Evidence of the classic “target” lesion can aid the diagnosis. Ad- of their intense pain, which is the mainstay of therapy. Readers ditionally, other subtle findings on physical examination can be can find more information about patients’ cures in Table 1. We helpful. Physicians often must diagnose Latrodectus bites by ask- specifically describe here the case of the first victim, who suf- ing patients about the onset of symptoms, how they discovered fered the most severe clinical signs. their bites, and whether they saw the spider. Patient A. A man age 24 years came to the ED of our general Latrodectus bites are distinctive. The site of a bite develops a hospital. The patient was sweating, with acute abdominal pain, pale central area with surrounding erythema; often fang marks salivation, priapism, palpitations, and reduced blood saturation. will be visible.4 There will probably also be some swelling and The ECG showed incomplete right bundle branch block and redness at the area of the bite. elevated troponin levels (1.6 ng/mL). CPK and amylase levels In the case presented here, the spider was not available were elevated as well. CRP was normal, and the absolute value for identification, so the diagnosis was made by the clinical of white blood cells was 28,000/μL. and laboratory findings that are reported extensively in Table The patient reported experiencing intense back pain while 1. The victims of Latrodectus bites in Greece experienced he was sleeping, which was severe enough to wake him. After the typical symptoms of the venomous spider bite. These a few minutes, the symptoms appeared. On the basis of the symptoms were more severe than those caused by steatodism. symptoms and the statements and descriptions of the spider by Thus, physicians determined the identity of the insect that the patient, it was determined that the patient was bitten by L caused the bite and the type of the envenomation. The first tredecimguttatus, one of the European species of Latrodectus. case, described here, was the most severe compared with During his hospitalization in the ED, the patient suffered the others reported. It is interesting that the first and the last pulmonary edema. He was intubated, sedated, and transferred case reported (two young men) had positive troponins, ECG to the intensive care unit (ICU) of the hospital. ICU physicians manifestations indicating that they suffered cardiac toxicity.

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The elevated CPK levels in the other patients more likely Conclusion originated in the skeletal muscle. It is very important that health care practitioners recognize Antivenin use appears justified in severe envenomation. It the symptoms and signs of Latrodectus to provide immediate is available and effective, but it is often withheld because of care to Latrodectus bite victims. The management of mild to fear of acute hypersensitivity reactions. Because of these con- moderate Latrodectus envenomations is primarily supportive. cerns about acute hypersensitivity reactions, physicians must Hospitalization and possibly antivenin administration should be weigh the benefits of treating with antivenin for a condition reserved for patients exhibiting serious systemic symptoms or with limited mortality.13 This is a subject of intense debate inadequate pain control. Physicians should know that high-risk within the toxicology community. This controversy stems from factors include age older than 60 years, severe envenomation, a single reported case of fatal hypersensitivity related to spi- pediatric patient, or history of hypertension and coronary ar- der antivenin administration.11 Generally, antivenin provides tery disease. People who report these factors should receive rapid symptomatic improvement—mainly rapid pain relief—as antivenin as soon as possible to avoid suffering envenomation demonstrated in the cases presented here. complications (eg, cardiovascular collapse). Finally, the most Calcium therapy was once considered to be an antidote for important goal for all patients is early pain relief. v Latrodectus envenomation.14 Calcium was thought to stabilize nerve membrane permeability, resulting in decreased neu- Disclosure Statement rotransmitter release. Although this effect was demonstrated The author(s) have no conflicts of interest to disclose. in vitro and reported in some early clinical series, subsequent experience has not shown effectiveness. Therefore, calcium Acknowledgment therapy has lost favor in the medical toxicology community.11,14 Mary Corrado, ELS, provided editorial assistance. The traditional therapies for Latrodectus envenomation are aimed at providing symptomatic relief while venom ef- References fects resolve. Therapies include primarily opioid analgesics 1. Garb JE, González A, Gillespie RG. The black widow spider genus Latro- dectus (Araneae: Theridiidae): phylogeny, biogeography, and invasion his- and muscle relaxants. In the majority of moderate to severe tory. Mol Phylogenet Evol 2004 Jun;31(3):1127-42. DOI: http://dx.doi. Latrodectus envenomation, patients treated with antivenin org/10.1016/j.ympev.2003.10.012. experienced a much shorter duration of symptoms and were 2. Martindale C, Newlands G. The widow spiders: a complex of species. S Afr J Sci 1982:78(2):78-9. less likely to be admitted to the hospital than those who did 3. Bush SP. Widow spider envenomation medication [Internet]. New York, NY: not receive antivenin. Relief of symptoms occurred within an Medscape, WebMD, LLC; c2014 [updated 2012 Jun 5; cited 2014 Jun 3]. average of 31 minutes of antivenin infusion.9,11 Administration Available from: http://emedicine.medscape.com/article/772196-medication. 4. Bryan P. Black widow spider envenomation. Utox Update 2002;4(3):1-3. of antivenin even late in the course of envenomation has 5. Watson WA, Litovitz TL, Klein-Schwartz W, et al. 2003 annual report of the been reported to be effective. Multiple allergies, asthma, or American Association of Poison Control Centers Toxic Exposure Surveillance past reactions to equine-based products should be consid- System. Am J Emerg Med 2004 Sep;22(5):335-404. DOI: http://dx.doi. org/10.1016/j.ajem.2004.06.001. ered contraindications. Antivenin therapy is recommended 6. González Valverde FM, Gómez Ramos MJ, Menarguez Pina F, Vázquez Ro- in cases of envenomation during pregnancy because of the jas JL. [Fatal latrodectism in an elderly man]. [Article in Spanish]. Med Clin risk of venom-induced abortion or other possible harm to (Barc) 2001 Sep 22;117(8):319. 15 7. Pneumatikos IA, Galiatsou E, Goe D, Kitsakos A, Nakos G, Vougiouklakis TG. the fetus, although the risk is not known. Furthermore, it Acute fatal toxic myocarditis after black widow spider envenomation. Ann is not known whether Latrodectus antivenin passes into the Emerg Med 2003 Jan;41(1):158. DOI: http://dx.doi.org/10.1067/mem.2003.32. breast milk. Although most medications pass into breast milk 8. Hoxha R. Two Albanians die from black widow spider bites. BMJ 2006 Aug in small amounts, many of them may be used safely while 5;333(7562):278. DOI: http://dx.doi.org/10.1136/bmj.333.7562.278-a. 9. Osweiler GD, Hovda LR, Brutlag AG, Lee JA, editors. Blackwell’s five-minute breastfeeding. veterinary consult: clinical companion: small animal toxicology. Ames, IA: Regarding the incidents in Greece, hospitalization was Blackwell Publishing Ltd; 2011. reserved for all patients, and antivenin was reserved for 10. Bush SP, Thomas TL, Chin ES. Envenomations in children. Pediatr Emerg Med Rep 1997;2:1-12. patients exhibiting serious systemic symptoms or inadequate 11. Clark RF, Wethern-Kestner S, Vance MV, Gerkin R. Clinical presentation and pain control. All the patients who were administered the an- treatment of black widow spider envenomation: a review of 163 cases. Ann tivenin required hospitalization, but none of them suffered an Emerg Med 1992 Jul;21(7):782-7. DOI: http://dx.doi.org/10.1016/S0196- 0644(05)81021-2. allergic reaction. Four of seven symptomatic patients suffering 12. Graudins A, Gunja N, Broady KW, Nicholson GM. Clinical and in vitro evi- Latrodectus envenomation were administered antivenin, and dence for the efficacy of Australian red-back spider (Latrodectus hasselti) rapid resolution of symptoms was observed within about half antivenom in the treatment of envenomation by a Cupboard spider (Steato- da grossa). Toxicon 2002 Jun;40(6):767-75. DOI: http://dx.doi.org/10.1016/ an hour after the administration. These cases demonstrate the S0041-0101(01)00280-X. safe and effective use of Latrodectus antivenin. Antivenin is 13. Hahn IH, Lewin NA. Arthropods. In: Flomenbaum NE, Goldfrank LR, Hoff- an important treatment for Latrodectus envenomation but has man RS, Howland MA, Lewin NA, Nelson LS, editors. Goldfrank’s toxicolog- ic emergencies. 8th ed. New York, NY: McGraw-Hill Companies, Inc; 2006. been less successful than those for snake envenomation, with p 1603-22. concerns about their effectiveness for latrodectism.11 14. Gilbert EW, Stewart CM. Effective treatment of arachnidism by calcium salts: a preliminary report. Am J Med Sci 1935 Apr;189(4):532-6. 15. Bernstein JN. Antivenom (scorpion and spider). In: Flomenbaum NE, Gold- frank LR, Hoffman RS, Howland MA, Lewin NA, Nelson LS, editors. Gold- frank’s toxicologic emergencies. 8th ed. New York, N�Y: McGraw-Hill Com- panies, Inc; 2006. p 1623-8.

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The size Paperback: 272 pages single cohort design evaluated an 8-week and composition of the population $15.99 MBSR program for 38 Kaiser Permanente of youth identified with diabetes was Colorado members with chronic pain, not affected. chronic illness, or stress-related problems. 29 Most Common Dermatologic Topics Repeated measures analyzed at 8 weeks Published in Five High-Impact and 1 year showed significant improve- General Medical Journals, 1970-2012: ments in self-reported mental and physical Melanoma, Psoriasis, Herpes Simplex, function, pain, psychological symptoms, Herpes Zoster, and Acne. and self-efficacy, but not in work produc- Handbook of Anesthesia, Backlit Aspens Young M Choi; Aram A Namavar, MS; 5th edition tivity. There were also significant decreases Jashin J Wu, MD Near Monitor Pass, at 1 year for visits to: primary care, spe- John J Nagelhout, Karen L Plaus California 2012 Internists frequently diagnose herpes cialty care, and the Emergency Depart- ISBN-10: 145571125X by Stuart Hahn, MD simplex, herpes zoster, and acne, which ment, and for hospital admissions. ISBN-13: 978-1455711253 This photograph of a are also common dermatologic topics beautifully lit aspen 10 Improving Appropriate Use of published. The authors conducted an Philadelphia, PA: Saunders; 2013 grove in autumn was Pulmonary Computed Tomography independent search of the Thomson Paperback: 864 pages taken in the Sierra Angiography by Increasing the Serum Reuters’ Science Citation Index for $70.95 Nevada Mountains near D-Dimer Threshold and Assessing common dermatologic topics, limited to the border of California Clinical Probability. Sydney Char; the period 1970 to 2012. The five most and Nevada. Hyo-Chun Yoon, MD, PhD common dermatologic topics published in five high-impact general medical journals Dr Hahn retired from The Permanente A retrospective review was conducted of all patients undergoing pulmonary com- were melanoma, psoriasis, herpes simplex, Medical Group in 2010. He has been seri- herpes zoster, and acne. ously exploring photography since 2000 puted tomography angiogram during 2 and has an interest in both wildlife and separate 12-month intervals: 1 before the 32 Prevalence of Hypovitaminosis D and landscape photography. For further infor- implementation of an increased D-dimer Its Association with Comorbidities of mation about his artwork, Dr Hahn can threshold and recommendation for formal Childhood Obesity. Ronald Williams, Luck Just Happens clinical probability assessment, and the be contacted at: [email protected]. MD, FAAP, FACP; Marsha Novick, MD; Paul Crane ANNOUNCEMENT: other after regional implementation. The Erik Lehman, MS prevalence of pulmonary embolism de- ISBN-10: 1479798290 ISBN-13: 978-1479798292 tected by computed tomography angiog- We conducted a retrospective chart CME Credits Now Available for Reviewers raphy increased from 4.7% to 11.7%, but review from 155 obese children aged Bloomington, IN: XLibris; 2013 only 4% of patients had a formal clinical 5 to 19 years who attended the Penn Paperback; 182 pages probability assessment recorded in their State Children’s Hospital Pediatric $19.99 electronic medical record. Multidisciplinary Weight Loss Program from November 2009 through November The Permanente Journal is happy to announce 16 Testing for Meningitis in Children with 2010. Under the latest Institute the availability of Continuing Medical Education Bronchiolitis. Michael Stefanski, MD, of Medicine definitions, vitamin D credits for completing manuscript reviews for 93 LETTERS TO THE EDITOR MPH; Ronald Williams, MD, FAAP, deficiency (< 20 ng/mL) and insufficiency FACP; George McSherry, MD; Joseph (20-29 ng/mL) was present in 40% The Permanente Journal. Physicians are now eligible 95 BOOK REVIEWS Geskey, DO, MBA and 38% of children, respectively. African-American race, winter/spring to receive up to 15 AMA PRA Category 1 Credits 96 CME EVALUATION FORM The authors present a retrospective, case-control study of hospitalized infants season, hyperinsulinemia, elevated Crush Step 1: The Ultimate per year (3 AMA PRA Category 1 Credits per systolic blood pressure, urban location, USMLE Step 1 Review younger than age one year diagnosed manuscript). With this change, we have launched with viral bronchiolitis who underwent and total numbers of comorbidities were significantly associated with Theodore X O’Connell, lumbar puncture as part of an evaluation Ryan A Pedigo, Thomas E Blair our new For Reviewers home page on our Web site: for meningitis. The presence of apnea, hypovitaminosis D (< 30 ng/mL). Obese ISBN-10: 1455756210 cyanosis, meningeal signs, positive urine children should be considered for routine www.thepermanentejournal.org/reviewers.html. ISBN-13: 978-1455756216 culture results, and young age were fac- vitamin D screening. tors found to be preliminarily associated Philadelphia, PA: Saunders; 2013 Paperback: 680 pages The Permanente Journal with the performance of a lumbar punc- ture in the setting of bronchiolitis. Young $37.75 500 NE Multnomah St, Suite 100 age was the only significant clinical factor The Portland, Oregon 97232 found after multivariable regression; no www.thepermanentejournal.org other demographic, clinical, laboratory, PermanenteJournal or radiologic variables were found to be ISSN 1552-5767 significant.

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