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Transmission of Human Papillomavirus in Heterosexual Couples Brenda Y

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Transmission of Human Papillomavirus in Heterosexual Couples Brenda Y RESEARCH Transmission of Human Papillomavirus in Heterosexual Couples Brenda Y. Hernandez,* Lynne R. Wilkens,* Xuemei Zhu,* Pamela Thompson,* Katharine McDuffi e,* Yurii B. Shvetsov,* Lori E. Kamemoto,† Jeffrey Killeen,‡ Lily Ning,* and Marc T. Goodman* CME ACTIVITY Medscape, LLC is pleased to provide online continuing medical education (CME) for this journal article, allowing clinicians the opportunity to earn CME credit. Medscape, LLC is accredited by the Accreditation Council for Continuing Medical Education (ACCME) to provide CME for physicians. Medscape, LLC designates this educational activity for a maximum of 1.0 AMA PRA Category 1 Credits™. Physicians should only claim credit commensurate with the extent of their participation in the activity. All other clinicians completing this activity will be issued a certifi - cate of participation. To participate in this journal CME activity: (1) review the learning objectives and author disclosures; (2) study the education content; (3) take the post-test and/or complete the evaluation at http://www.medscape.com/cme/eid; (4) view/print certifi cate. Learning Objectives Upon completion of this activity, participants will be able to: • Identify the most common baseline human papillomavirus (HPV) status of couples • Specify the most common mode of transmission of HPV between couples • Describe the role of anatomic sites in the transmission of HPV • Identify behavioral factors associated with the transmission of HPV Editor D. Peter Drotman, MD, Editor-in-Chief, Emerging Infectious Diseases. Disclosure: D. Peter Drotman, MD, has disclosed no relevant fi nancial relationships. CME Author Charles P. Vega, MD, Associate Professor; Residency Director, Department of Family Medicine, University of California, Irvine, California, USA. Disclosure: Charles P. Vega, MD, has disclosed that he has served as an advisor or consultant to Novartis, Inc. Authors Disclosures: Brenda Y. Hernandez, PhD, MPH; Lynne R. Wilkens, DrPH; Xuemei Zhu, MD; Pamela Thompson, MPH; Katharine McDuffi e, BS; Yurii B. Shvetsov, PhD; Jeffrey Killeen, MD; Lily Ning, MD; and Marc T. Goodman, PhD, MPH, have disclosed no relevant fi nancial relationships. Lori E. Kamemoto, MD, MPH, has disclosed that she has received grants for clinical research from GlaxoSmithKline, and is on the speakers’ bureau for Merck. We examined the transmission of human papillomavirus ervical cancer remains a major source of illness and (HPV) in 25 heterosexual, monogamous couples (25 men, Cdeath among women globally, and infection with on- 25 women), followed up over an average of 7.5 months. A cogenic human papillomaviruses (HPVs) is its principal total of 53 heterosexual transmission events were observed cause (1,2). Men are assumed to be the main reservoirs of among 16 couples (14 male-to-female and 39 female-to- genital HPV infection for women, although comparatively male). Sexual transmission involved 13 different oncogenic little is known about the natural history of HPV in men. and nononcogenic HPV types; 8% were vaccine-covered types transmitted between partners. The overall rate of HPV A limited number of cross-sectional and case-control transmission from the penis to the cervix was 4.9/100 per- studies have evaluated genotype-specifi c HPV concor- son-months, which was substantially lower than that from dance in male-female couples (3–7). There are, however, the cervix to the penis (17.4/100 person-months). Trans- no empirical data on the heterosexual transmission of HPV. mission between the hands and genitals, as well as ap- Our investigation evaluates the transmission of HPV in a parent self-inoculation events (primarily in men), were also cohort of male-female sexual partners. observed. Couples who transmitted HPV were more sexu- ally active and used condoms less frequently. These results Methods have implications for HPV prevention and control strategies, including the targeting of prophylactic vaccines. Study Participants *University of Hawaii, Manoa, Hawaii, USA; †University of Hawaii The study was conducted at the University Health Ser- John A. Burns School of Medicine, Honolulu, Hawaii, USA; and vices of the University of Hawaii at Manoa from February ‡Kapi’olani Medical Center for Women and Children, Honolulu 2005 through November 2006. Promotional efforts includ- 888 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 14, No. 6, June 2008 Transmission of HPV in Couples ed fl yers and email invitations, which were part of larger Statistical Analysis ongoing studies of HPV. The study was approved by the The main objective of the statistical analysis was to Committee on Human Studies of the University of Hawaii. evaluate HPV transmission between partners. Each type- All study participants provided written informed consent. specifi c HPV infection was assigned a status of transmitted Eligible participants were at least 18 years of age, English- or not transmitted by time period and anatomic site. For speaking, not currently pregnant, and in a monogamous re- some statistics, the penis anatomic site was further divided lationship with the index partner. into foreskin, glans, shaft, and urine, which is a proxy for urethral infection. HPV in female urine, which has dem- Specimen Collection onstrated type-specifi c concordance with cervical measure- Couples attended concurrent study visits at 2-month ments (17), was considered to be a proxy for cervical and intervals. Trained clinicians collected exfoliated cell sam- other lower genital tract infections. Therefore, cervix and ples for HPV DNA detection. For men, separate genital urine were combined as 1 anatomic site. When there were specimens from the penis glans/corona, penis shaft, scro- >1 possible source sites, sites were grouped and evaluated tum, and inner foreskin (uncircumcised men) were col- as 1 transmission event. When there were >2 destination lected by using textured paper and a saline-moistened sites, each was counted as a separate transmission event. swab (8,9). Anal canal specimens were collected by using Partner transmission was defi ned as the presence of a saline-moistened swab. A cytobrush was used to collect a specifi c HPV genotype at an anatomic site in 1 partner oral specimens (buccal cavity, tongue). Specimens from and its absence in all sites of the other partner at a given the dominant hand (palm, fi ngertips, under the fi nger- visit, along with the presence of this HPV type in the un- nails) were collected by using a saline-moistened swab. affected partner at the subsequent visit. Auto-inoculation Participants self-collected fi rst-catch urine samples (30 was defi ned as the presence of a particular HPV type at an mL) at the clinic. Using latex gloves, men collected se- anatomic site in 1 partner and its absence in all sites of the men specimens at home during masturbation within 24 other partner at a given visit, and the presence of this HPV hours of each visit. type in a different anatomic site in the affected partner at For women, a cervical cytology (Papanicolaou [Pap]) the subsequent visit. An event was defi ned as self-inocula- smear was collected, and a swab and cytobrush were used tion only after possible transmission from the partner was to consecutively sample the ectocervix and endocervix, ruled out, i.e., when the partner was negative for the HPV including the transformation zone. The same methods genotype at prior and concurrent visits. used for collection of anal, oral, hand, and urine speci- The rate of HPV transmission was calculated as the mens from men were used for collection of specimens number of HPV type-specifi c transmission events divided from women. by the number of person-months of exposure × 100 and expressed as the rate per 100 person-months. Exact confi - HPV DNA Testing and Genotyping dence intervals (CIs) for transmission rates were calculated DNA was extracted from specimens by using com- by assuming a Poisson distribution for the number of events mercial reagents (QIAGEN, Valencia, CA, USA). The (18). Person-months of exposure for each HPV infection by PCR used PGMY09/PGMY11 primers to amplify a 450-bp anatomic site were computed based on the period of time be- region of the L1 HPV genome (10). Amplifi cation of the tween successive visits. When HPV was detected at a given human β-globin gene was included as an internal control visit and HPV type was absent at the successive visit, the for sample suffi ciency. HPV-positive specimens were sub- exposure period was estimated at half of the visit interval. sequently genotyped by using commercial reagents (Roche Comparisons between couples by transmission status were Molecular Systems Inc., Branchburg, NJ, USA) originating made by using the t test, χ2 statistic, and linear rank statistic. from a prototype line blot assay (11). The assay detects 37 different HPV types, including oncogenic/probable onco- Results genic types (HPV 16, 18, 26, 31, 33, 35, 39, 45, 51, 52, 53, 56, 58, 59, 66, 68, 73, 82, and IS39, a subtype of HPV 82), Study Participants nononcogenic types (HPV 6, 11, 40, 42, 54, 61, 70, 72, 81, Thirty-eight couples (38 men, 38 women) were en- and CP6108, also known as candidate HPV 89), and types rolled. Six couples left the study, including 2 whose rela- with undetermined risk status (HPV 55, 62, 64, 67, 69, 71, tionships ended. The present analysis focuses on 25 couples 83, and 84) (12,13). This PCR-based assay has demonstrat- with at least 2 visits. Couples were followed up at ≈2-month ed a high degree of sensitivity and reproducibility (14–16). intervals over an average of 7.5 months. HPV testing and genotyping procedures have been given in The mean age was 28 years (range 18–59 years) for detail previously (9). men and 26 years (range 18–57 years) for women. Partici- pants comprised Caucasians (52%), Asians (8%), Pacifi c Emerging Infectious Diseases • www.cdc.gov/eid • Vol.
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