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Psychological Stress Perturbs Epidermal Permeability Barrier Homeostasis Implications for the Pathogenesis of Stress-Associated Skin Disorders

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Psychological Stress Perturbs Epidermal Permeability Barrier Homeostasis Implications for the Pathogenesis of Stress-Associated Skin Disorders OBSERVATION Psychological Stress Perturbs Epidermal Permeability Barrier Homeostasis Implications for the Pathogenesis of Stress-Associated Skin Disorders Amit Garg, BA; Mary-Margaret Chren, MD; Laura P. Sands, PhD; Mary S. Matsui, PhD; Kenneth D. Marenus, PhD; Kenneth R. Feingold, MD; Peter M. Elias, MD Background: A large number of skin diseases, including Results: The subjects as a group demonstrated a atopic dermatitis and psoriasis, appear to be precipitated decline in permeability barrier recovery kinetics after or exacerbated by psychological stress. Nevertheless, the barrier disruption by cellophane tape stripping, in par- specific pathogenic role of psychological stress remains un- allel with an increase in perceived psychological stress known. In 3 different murine models of psychological stress, during the higher vs the initial lower stress occasions. it was recently shown that psychological stress negatively During the follow-up, presumed lower stress period, impacts cutaneous permeability barrier function and that the subjects again displayed lower perceived psycho- coadministration of tranquilizers blocks this stress- logical stress scores and improved permeability barrier induced deterioration in barrier function. recovery kinetics, comparable to those during the initial lower stress period. Moreover, the greatest deterioration Objectives and Methods: The relationship between psy- in barrier function occurred in those subjects who dem- chological stress and epidermal permeability barrier func- onstrated the largest increases in perceived psychologi- tion was investigated in 27 medical, dental, and pharmacy cal stress. students without coexistent skin disease. Their psycho- logical state was assessed with 2 well-validated measures: Conclusion: These studies provide the first link be- the Perceived Stress Scale and the Profile of Mood States. tween psychological status and cutaneous function in hu- Barrier function was assessed simultaneously with the stress mans and suggest a new pathophysiological paradigm, measures at periods of presumed higher stress (during fi- ie, stress-induced derangements in epidermal function nal examinations) and at 2 assumed, lower stress occa- as precipitators of inflammatory dermatoses. sions (after return from winter vacation [approximately 4 weeks before final examinations] and during spring vaca- tion [approximately 4 weeks after final examinations]). Arch Dermatol. 2001;137:53-59 LTHOUGH psychological to decrease medication requirements and stress appears to be ca- to improve organ function in systemic in- pable of provoking, exac- flammatory disorders.17 erbating, and propagat- ing disease,1-3 the possible For editorial comment Acausal relationship is obscured, at least in see page 78 part, because chronic disease itself can lead to an increase in perceived stress. More- Among dermatoses, atopic dermati- From the Dermatology 18-21 22-27 (Mr Garg and Drs Chren and over, the influence of psychological stress tis, psoriasis, and a variety of other Elias), Geriatrics (Drs Chren on disease is often perceived as being ei- dermatoses are anecdotally linked to psy- and Sands), and Metabolism ther too subjective or nonquantifiable for chological stress.2,24,28-30 Psychological stress (Dr Feingold) Services, scientific assessment.4 Yet, a number of also is associated with delayed wound heal- Veterans Affairs Medical studies point to a possible pathogenic link ing in both humans31 and a murine model.32 Center, San Francisco, Calif; between psychological stress and dis- It also is widely accepted that optimal man- the Departments of ease. For example, sustained psychologi- agement of these skin conditions requires Dermatology (Drs Chren, cal stress is associated with alterations in consideration of coexistent emotional fac- Feingold, and Elias) and both humoral and cellular immune re- tors.20 Accordingly, stress-reduction tech- Medicine (Dr Feingold), 5-12 University of California, San sponses. Furthermore, there is increas- niques, such as meditation, biofeedback, and Francisco; and the Department ing evidence that psychological stress can hypnosis, may benefit some patients with 20,33-37 of Research and Development, influence the progression and survival of these disorders. Estée Lauder Inc, Melville, NY patients with cancer.8,13-16 Likewise, re- It is noteworthy that some of the most (Drs Matsui and Marenus). duced psychological stress appears both common skin disorders that are com- (REPRINTED) ARCH DERMATOL / VOL 137, JAN 2001 WWW.ARCHDERMATOL.COM 53 ©2001 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/02/2021 SUBJECTS AND METHODS recovery kinetics are not affected by sex or race,48 no sub- jects were excluded based on these criteria. EXPERIMENTAL SUBJECTS AND STUDY DESIGN We assessed permeability barrier function in parallel with completion of 2 standard self-report inventories for Twenty-seven students who were randomly chosen from psychological stress at 3 occasions: (1) an initial period of a larger group of students attending the University of Cali- presumed lower stress (LS1), ie, shortly after return from fornia, San Francisco, School of Medicine, Pharmacy, or winter vacation (January 1999); (2) a period of presumed Dentistry provided informed consent to participate as paid higher stress (HS), approximately 4 weeks later, during fi- volunteers in a study on the effects of psychological stress nal examination week (February 1999); and (3) a recur- on permeability barrier function in normal skin. The study rent period of presumed lower stress (LS2), approxi- subjects, who ranged in age from 23 to 27 years (mean age, mately 4 weeks after the HS period, shortly after return from 24.4 years), represented a broad cross section of their re- spring vacation. Because of scheduling difficulties, only a spective student bodies. limited number of students (n=17) were available for re- examination at the LS2 period. These students did not dif- Characteristics No. (%) of Subjects fer from the group as a whole, as examined during the other School 2 periods. Because of prolonged cold weather during the Medical 14 (52) winter of 1999, both outdoor temperatures and humidity Pharmacy 7 (26) levels remained comparable in San Francisco, from Janu- Dental 6 (22) ary through mid-March 1999. Sex M 6 (22) PSYCHOLOGICAL STRESS ASSAYS F 21 (78) Ethnicity The extent of perceived psychological stress and related White 12 (44) Asian 9 (33) anxiety were assessed using 2 self-report measures: the Hispanic 3 (11) Profile of Mood States (POMS) and the Perceived Stress Scale Other 2 (7) (PSS). The POMS is a 65-point, descriptive rating scale African American 1 (4) that identifies and assesses transient fluctuations in mood state.49 The POMS consists of 6 individual subscales: Ten- The subjects were in good health and free of preexisting sion-Anxiety, Depression-Dejection, Anger-Hostility, Vigor- primary skin disease, and none was receiving sedatives, an- Activity, Fatigue-Inertia, and Confusion-Bewilderment. The tidepressants, psychotherapy, or exogenous steroid hor- total score of the POMS, referred to as total mood distur- mones (however, 12 of the 21 women were taking oral bance, represents a summation of the 6 subscale scores. In contraceptives). Since prior studies showed that barrier contrast, the PSS is a 14-item scale that assesses global monly associated with increased psychological stress, eg, ings point to a potential pathogenic link between psy- psoriasis, eczema, and healing wounds,38 are character- chological stress, permeability barrier homeostasis, and ized by defective cutaneous permeability barrier func- the induction, exacerbation, and propagation of inflam- tion. For example, even the apparently uninvolved skin matory skin disorders. of patients with atopic dermatitis demonstrates in- creased transepidermal water loss (TEWL), and barrier RESULTS function deteriorates still further in involved skin sites.39,40 Psoriatic lesions also display abnormalities in TEWL,41,42 PERCEIVED STRESS DURING and the severity of lesional phenotype in psoriasis cor- THE DIFFERENT PERIODS relates directly with the extent of the barrier abnormal- ity.43 Recent studies suggest that a barrier abnormality, Psychological stress levels and permeability barrier func- coupled with epidermal injury, provokes or sustains these tion were assessed first in all 27 subjects shortly after their cutaneous disorders through activation of an epidermal return from winter vacation, the LS1 period. To test the initiated cytokine cascade.44,45 hypothesis that the perceived psychological stress of ex- Our laboratory has explored the potential patho- aminations results in decompensation of permeability bar- genic link between psychological stress and permeabil- rier homeostasis, we reevaluated the same parameters in ity barrier homeostasis. In 3 different murine models of the same subjects 6 weeks later, ie, during final exami- psychological stress, Denda et al46,47 recently demon- nation week, the HS period. During the HS period, the strated defects in barrier function that were reversed by subjects as a group perceived a significant increase in psy- the systemic coadministration of anxiolytic agents. In the chological stress relative to the LS1 period on both the present study, we assessed whether increased levels of POMS and the PSS (Figure 1; P,.001 and P,.05 for psychological stress in medical, dental, and pharmacy stu- the POMS and the PSS, respectively). Moreover, the in-
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