Alopecia areata: Clinical perspective and an insight into pathogenesis

Journal of Dermatology

Volumn 30, Issue 4, 2003, Pages 271-289

  Sehgal, Virendra N ^a   Jain, Sanjiv ^b  

^a Sehgal Nursing Home   (India)

^b NONE

Author keywords

AA and atopy; AA and autoimmunity; AA and cell mediated immunity; AA and humoral immunity; AA and viral infection; Alopecia areata; Animal models; Clinical manifestation; Histopathology; Neurological factors; Pathogenesis; Pidemiology; Polymorphism

Indexed keywords

HLA ANTIGEN;

ALOPECIA AREATA; ATOPY; AUTOIMMUNITY; CELLULAR IMMUNITY; CLINICAL FEATURE; DISEASE ASSOCIATION; EMOTIONAL STRESS; HISTOPATHOLOGY; HUMORAL IMMUNITY; INCIDENCE; MELANOCYTE; PATHOGENESIS; PROGNOSIS; REVIEW; VIRUS INFECTION;

EID: 0037995424     PISSN: 03852407     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1346-8138.2003.tb00389.x     Document Type: Review

References (170)

1. Gollinick H, Orfenos CE: Alopecia areata pathogenesis and clinical picture, in Orfonos CE, Happle R (eds); Hair and Hair Diseases, Springer-Verlag, Berlin, 1990, p 529.
2. Safavi K: Prevalence of alopecia areata, in the First National Health and Nutrition Examination Survey (letter), Arch Dermatol, 128: 702, 1992.
3. Safavi KHH, Muller SA, Suman VJ, et al: Incidence of alopecia areata in Olmsted County, Minnesota, 1975 through 1989, Mayo Clin Proc, 70: 625-633, 1995.
4. Sabouraud R: Sur Petiologie de La pelade, Archives Dermato-Syphiligraphiques de La Clinique d'Hospital St. Louis, 1: 31, 1929.
5. Brown WH: The etiology of alopecia areata and its relationship to vitiligo and possibly scleroderma, Br J Dermatol, 41: 299, 1929.
6. Muller SA, Winkelmann RK: Alopecia areata, Arch Dermatol, 88: 290, 1963.
7. De-Waard-van-der-Spek FB, Orange AP, De Raegmaecker DM, et al: Juvenile versus maturity onset alopecia areata - A comparative retrospective clinical study, Clin Exp Dermatol, 14: 429-433, 1989.
8. Friedmann PS: Clinical and Immunologic associations of alopecia areata, Semin Dermatol, 4: 9, 1985.
9. Gip L, Loden A, Molin L: Alopecia areata: A follow up investigation of outpatient material, Acta Derm Venereol (Stockh), 49: 180-188, 1969.
10. Price V: Alopecia areata: Clinical aspects, J Invest Dermatol, 96 (suppl): 685, 1991.
11. Camacho F: Alopecia areata: Clinical features, Dermatopathology, in Camacho F, Montagna W, (eds): Trichology Diseases of the Pshilosebaceous Follicle. Aula Medical Group Madrid, 1997, p417.
12. Muralidhar S, Sharma VK, Kaur S: Ophiasis inversus: A rare pattern of alopecia areata [letter]. Pediatr Dermatol, 15: 326-327, 1998.
13. Orecchia G, Douville H, Marelli MA: Nail changes and alopecia areata, Ital Gene Rev Dermatol, 25: 179-184, 1988.
14. Mitchell A, Krull E: Alopecia areata: Pathogenesis and treatment, J Am Acad Dermatol, 11: 763-775, 1984.
15. Headington JT: The histopathology of alopecia areata (abstract), J Invest Dermatol, 96: 69s, 1991.
16. Eckert J, Church RE, Ebling FJ: The pathogenesis of alopecia areata, Br J Dermatol, 80: 203-210, 1968.
17. Whiting DA: Histopathology of alopecia areata in horizontal section of scalp biopsies, J Invest Dermatol, 104: 265-275, 1995.
18. Friedman PS: Clinical and immunologic association of alopecia areata, Semin Dermatol, 4: 9-15, 1985.
19. Pinkuo H, Alopecia: Clinicopathologic correlation, Int J Dermatol, 19: 245-253, 1980.
20. Perret C, Brocher EB, Wiesner-Menzel L, Happle R: In situ demonstration of T-cell subsets in alopecia areata, Arch Dermatol Reser, 272: 155-158, 1982.
21. Todes-Taylor N, Turner R, Wood GS, et al: T-cell subpopulates in alopecia areata, J Am Acad Dermatol 11: 216-223, 1984.
22. Bergfeld WF: Alopecia: Histologic changes, Advance in Dermatol, 4: 301-322, 1989.
23. Menerger AG, Slater DN, Bleehen SS: Alopecia areata: Alterations in the low growth cycle and correlation with the follicular pathology, Br J Dermatol, 114: 333-347, 1986.
24. Tobin DJ, Fenton DA, Kendall MD: Cell degeneration in alopecia areata. An ultrastructural study, Am J Dermatopathol, 13: 248-256, 1991.
25. Hull SM, Nulbrown M, Pepall L, et al: Immunohistologic and ultrastructural of the dermal papilla and hair follicle bulb from "active" and "normal" areas of alopacea areata, J Invest Dermatol, 96: 673-681, 1991.
26. Medler VC, Buys CM: Immunohistochemical characterization of the cellular infiltrate in severe alopecia areata before and after minoxidal treatment, Dermatologia, 175 (S): 29-35, 1987.
27. Elslon DM, McCollough ML, Bergfeld WF, et al: Eosinophils in fibrous tracts and near hair bulbs: A helpful diagnostic feature of alopecia areata, J Am Acad Dermatol, 37: 101-106, 1997.
28. McDonagh AJ, Tazi-Ahnini R: Epidemiology and genetics of alopecia areata, Clin Exp Dermatol, 27: 405-409, 2002.
29. Tobin DJ, Bystryn JC: Immunity to hair follicles in alopecia areata, J Invest Dermatol, 104 (suppl): 136-145, 1995.
30. Bystryn JC, Tamesis J: Immunologic aspects of hair loss, J Invest Dermatol, 96: 885-895, 1991.
31. Tobin DJ, Oren Freicr N, Fenton DA, et al: Antibodies to hair follicles in alopecia areata, J Invest Dermatol, 102: 721-724, 1994.
32. Tobin DJ, Oren Freicr N, Bystryn JC: Autoantibodies to hair follicles in normal individuals, Arch Dermatol, 103: 395-397, 1994.
33. Paus R: Immunology of the hair follicle, in Bos JD (ed): The Skin Immune System, CRC Press Raton, Florida, 1997, pp377-398.
34. Bos JD (ed): The Skin Immune System Buca Raton, CRC press, Florida, 1997.
35. Paus R, Hofmann U, Eichmuller S, et al: Distribution and changing density of gamma-delta T cells in murine skin during the induced hair cycle, Br J Dermatol, 130: 281-289, 1994.
36. Paus R, Foitzik K, Welker R, et al: Transforming growth factor beta-receptor type I and type II expression during murine hair follicle development and cycling, J Invest Dermatol, 109: 518-526, 1997.
37. Paus R, Vanderveen C, Eichmuller S, et al: Generation and cyclic remodelling of the hair follicle immune system in mice, J Invest Dermatol, 111: 7-18, 1998.
38. Paus R: Immunology of the hair follicle, Presented at the Third International Research Workshop on Alopecia Areata, Washington DC, Nov 5, 1998.
39. Paus R, Eichmuller S, Hofmann U, et al: Expression of classical and non-classical MHC class I antigens in murine hair follicles, Br J Dermatol, 131: 177-183, 1994.
40. Paus R, Slominski A, Czarnetzki BM: Is alopecia areata an autoimmune-response against melanogenesis-related proteins, exposed by abnormal MHC class 1-expression in the anagen hair bulb?, Yale J Brt Med, 66: 541-554, 1994.
41. Westgate GE, Graggs RI, Gibson WT: Immune privileges in hair growth, J Invest Dermatol, 97: 417-420, 1991.
42. de Andrade M, Jackow CM, Dahm N, Hordinsky M, Reveille JD, Duvic M: alopecia areata in families: Association with the HLA locus, J Investig Dermatol Symp Proc, 4: 220-223, 1999.
43. Welsh EA, Clerk HH, Epstein SZ, et al: Human leukocyte antigen-DUB1*03 alleles are associated with alopecia areata, J Invest Dermatol, 103: 758-763, 1994.
44. Duvic M, Welsh EA, Jacrow C, et al: Analysis of HLA-D Locus alleles in alopecia areata patients and families, J Invest Dermatol, 104: 55-65, 1995.
45. Hsoi J, Murphy Gf, Egan CL, et al: Regulation of 'Langerhans' cells function by nerves containing calcitonin gene-related peptide, Nature, 363: 159-163, 1993.
46. Rauch J, Lundeberg T, Brodda-Jansen G, et al: Potent anti-inflammatory action of calcitonin gene-related peptide, Biochem Biophy Res Commun, 180: 1429-1435, 1993.
47. Vanderbank AA, Autoimmune disease: Promising emerging therapies, J Invest Dermatol, 104: 10s-11s, 1995.
48. Mims CA: Alopecia in mice infected with murine cytomegalovines (MCMV), Br J Esp Path, 66: 655-662, 1985.
49. Ulmer R, Cho R, Duvic M: Analysis of p53 expression in psoriasis by immuno-peroxidase staining, Clin Res, 1: 774A, 1993.
50. Skinner R 13 Ji, light WH, Bale GF: Alopecia areata and the presence of cytomegalovirus DNA, JAMA, 273: 1419-1420, 1998.
51. Jackow C, Puffer N, Hordineky M, et al: Alopecia areata and cytomegalovirus infection in twins. Genes versus environment, J Am Acad Dermatol, 38: 418-425, 1998.
52. Tosti A, La Placa M, Placucci F, et al: No correlation between cytomegalovirus and alopecia areata, J Invest Dermatol, 107: 443, 1996.
53. Szafer F, Price VH, Oksenberg JR, et al: T-cell receptor repertoire V2 in alopecia areata, J Invest Dermatol, 104: 225-245, 1995.
54. Larsen CG, Anderson AO, Oppenheim JJ, et al: Production of interleukin 8 by human dermal fibroblasts and keratinocytes in response to interleukin 17 tumour necrosis factor, Immunol, 68: 31-39, 1989.
55. Baggiolini M, Walz A, Kunkel SL: Neutrophil activating peptide-1/interleukin-8, a novel cytokine that activates neutrophils, J Clin Invest, 84: 1045-1049, 1989.
56. Kupper TS, Kent M, Pravin Kumar S, et al: Production of IL-6 by keratinocytes: Implication for epidermal inflammation and immunity, Ann NY Acad Sci, 557: 454-465, 1990.
57. Kupper TS, Birchall N, Mc Guire JS, et al: Induction of GM-CSF gene expression by interleukin-1 in human keratinocytes, Clin Res, 35: 581, 1987.
58. Callard RE: Cytokine Regulation of B-cell growth and development, Br Med Bull, 45: 371-388, 1984.
59. Feldmann M, Londei M, Hawarth C: T cells and lymphokines, Br Med Bull, 45: 361-370, 1989.
60. Balkwill FR: Tumour necrosis factor, Br Med Bull, x45: 389-407, 1989.
61. Fiero W, Beyaer R, Brouckeurt P, et al: Gene cloning and structure-function relationship of cytokines such as TNF and interleukins, Immunal Lett, 16: 219-226, 1987.
62. Dustin MI, Rothlein R, Bhan AK, et al: Induction of IL-1 and interferon, tissue distribution, biochemistry, and function of a natural adherence molecule (ICAM-1), J Immunol, 137: 245-254, 1986.
63. Pober JS, Gimbrone MA, Lapierre LA, et al: Overlapping patterns of activation of human endothelial cells by interleukin-1, tumour necrosis factor and immune interferon, J Immunol, 137: 1893-1896, 1986.
64. Bevilacqua MP, Stengelin S, Gimbrone MA, et al: Endothelial leukocyte adhesion molecule 1: An inducible receptor for neutrophils related to complement regulatory proteins and lectins, Science, 243: 1160-1165, 1989.
65. Dustin ML, Singer KH, Tuck Dt, et al: Adhesion of T-lymphocytes to epidermal keratinocytes is regulated by interferon and is mediated by intracellular adhesion molecule 1 (ICAM-1), J Exp Med, 167: 1323-1340, 1988.
66. Bashom TY, Nickloff BJ, Merigan TC, et al: Recombinant gamma interferon induces HLA-DR expression on cultured human keratinocytes, J Invest Dermatol, 83: 88-90, 1988.
67. Mac Donald-Hull S, Nutbrown M, Pepall L, et al: Immunohistologic and ultra-structural comparison of the dermal papilla and hair follicle bulb from 'active' and 'normal' 'areas' of alopecia areata, J Invest Dermatol, 96: 673-681, 1991.
68. Tarlow JK, Clay FE, Cork MJ, et al: Severity of alopecia areata is associated with a polymorphism in the interleukin-1 receptor antagonist gene, J Invest Dermatol, 103: 387, 1991.
69. Barahamani N, de Andrade M, Slusser J, Zhang Q, Duvic M: Interleukin-1 receptor antagonist allele 2 and familial alopecia areata, J Invest Dermatol, 118: 335-337, 2002.
70. Cork MJ, Tarlow JK, Clay FE, et al: Alleles of the interleukin-1 receptor antagonist as a genetic severity factor in alopecia areata, J Invest Dermatol, 104: 158-165, 1995.
71. Philpott MP, Sanders DA, Bowes J, et al: Effect of interleukins, colony stimulating factors, and tumour necrosis factor on human hair follicle growth in vitro, A possible role for interleukin-1 and tumour necrosis factor in alopecia areata, Br J Dermatol, 135: 942-948, 1995.
72. Bodemer C, Peuchmaur M, Fraitaig S, et al: Role of cytotoxic T cells in chronic alopecia areata, J Inverst Dermatol, 114: 112-116, 2000.
73. Nicklin MJ, Weith A, Duff GW: A physical map of the region encompassing the human interleukin-1 alpha, interleukin-1 beta, and interleukin-1 receptor antagonist genes, Genomics, 19: 382-384, 1994.
74. Di Giovine FS, Takhish E, Blakemore AIF, et al: Single base polymorphism at-511 in the human interleukin-1 beta gene, Hum Mol genet, 1: 352, 1994.
75. Di Giovine FS, Cork MJ, Crane A, et al: Novel genetic association of an IL-1 gene variation at +3953 with IL-1 protein production and psoriasis, Cytokine, 7: 606, 1995.
76. Mc Dowell TL, Symons JA, Ploski R, et al: A genetic association between juvenile rheumatoid arthritis and novel interleukin-1 alpha polymorphism, Arthritis Rheum, 38: 221-228, 1995.
77. Tarlow JK, Blakemore AIF, Leonard A, et al: Polymorphism in human IL-1 receptors antagonist gene intron 2 is due to variable number of an 86 bp tandem repeat, Human genet, 91: 403-404, 1995.
78. Kinato U, Reunala T, Karvonen J, et al: HLA-B 12 in alopecia areata, Arch Dermatol, 13: 17-16, 1977.
79. Hachom-Zadeh S, Brautbar C, Cohen C, et al: HLA and alopecia areata in Jerusalem, Tissue Antigen, 18: 71-74, 1981.
80. Bjorleman PJ, Safer MA, Binroui B, et al: Structure of the human class I histocompatability antigen, HLA-A2, Nature, 329: 506, 1987.
81. Kuntz BM, Selzle D, Braun-Falco O, et al: HLA antigens in alopecia areata, Arch Dermatol, 113: 1717, 1977.
82. Valsecchi R, Vicari O, Frigeni A, et al: Familial alopecia areata - Genetic susceptibility or coincidence?, Acta Derm Venereol (Stockh), 65: 175-177, 1984.
83. Frentz G, Thorpson K, Jakobson BK, et al: HLADR4 in alopecia areata (Letter), J Am Acad Dermatol, 14: 129, 1986.
84. Mikesell JF, Bergfeld WF, Braun WE: HLA-DR antigens in alopecia areata, Cleve Clin Q, 53: 189-191, 1986.
85. Orecchia G, Cuccia Belvedrere SM, Martinetti M, et al: Human leukocyte antigen region involvement in the genetic predisposition to alopecia areata, Dermatologica, 175: 10-14, 1987.
86. Odum N, Morling N, Georgsen J, et al: HLA-DR antigens in patients with alopecia areata, Tissue Antigen, 35: 114-117, 1990.
87. Horling N, Frentz G, Fugger L, et al: DNA polymorphism of HLA class II gene in alopecia areata, Disease Marker, 9: 35, 1991.
88. Zheng L, Weetman AP, Triedmann PS, et al: HLA association with alopecia areata, Tissue Antigen, 38: 89, 1991.
89. Duvic M, Hordinsky MK, Tredler VC, et al: HLA-D locus association in alopecia areata, Arch Dermatol, 127: 64-68, 1991.
90. Colombe BW, Price VH, Knoury EL, et al: HLA class I antigen association helps to define two types of alopecia areata, J Am Acad Dermatol, 33: 757-764, 1995.
91. Kavak A, Baykal C, Ozarmagan G, et al: HLA in alopecia areata, Int J Dermatol, 39: 589-592, 2000.
92. Ikeda T: A new classfication of alopecia areata, Dermatologica, 131: 421, 1965.
93. Penders AJM: Alopecia areata and atopy, Dermatologica, 156: 306-308, 1978.
94. Young E, Bruns HM, Berrens L: Alopecia areata and atopy, Dermatologica, 156: 306-308, 1978.
95. Shellow WV, Edwards JE, Koo JY: Profile of alopecia areata: A questionnaire analysis of patients and family, Int J Dermatol, 31: 186-189, 1992.
96. Cookson WOCM, Young RP, Sandford AJ, et al: Maternal inheritance of atopic IgE responsiveness on chromosome 11q, Lancet, 340: 381-384, 1992.
97. CERI) on chromosome 11q, Lancet, 341: 332-334, 1993.
98. Bergfeld WF, Tam RC, Remzi BK: Alopecia areata and thyroid disease, Presented as a poster at the Third International Research Workshop on Alopecia Areata, Washington DC, Nov. 5, 1998.
99. Hordinsky M: Alopecia areata and atopy, Presented at the 53rd Annual Meeting of the American Academy of Dermatology, New Orleans, Feb. 4-9, 1995.
100. Stankler Bewsher PD: Chronic mucocutaneous candidiasis, endocrine deficiency and alopecia areata, Br J Dermatol, 86: 238-245, 1972.
101. Boni R, Trueb RM, Wuthrich B: Alopecia areata in a patient with candidiasis-endocrinopathy syndrome, Dermatology, 191: 68-71, 1995.
102. Cunliffe WJ, Hall R, Newell DJ, et al: Alopecia areata, thyroid disease and autoimmunity, Br J Dermatol, 81: 877-881, 1969.
103. Wong SJ, Shohat T, Vadheim C, et al: Increased risk of type-1 (insulin dependent) diabetes in relatives of patients with alopecia areata, Am J Med Genet, 51: 234, 1994,
104. Tan RS: Ulcerative colitis, myaesthenia gravis, atypical lichen planus, alopecia areata, vitiligo, Proc K Soc Med, 67: 195, 1974.
105. Brenner W, Diem E, Gschnart F: Coincidence of vitiligo alopecia, onychodystrophy, localized scleroderma and lichen planus, Dermatologica, 159: 356-360, 1979.
106. Werth VP, White WL, Sanchez MR, et al: Incidence of alopecia areata in lupus erythematosus, Arch Dermatol, 128: 368-371, 1992.
107. Friedmann PS: Alopecia areata and autoimmunity, Br J Dermatol, 105: 153-157, 1981.
108. Cunliffe WJ, Hall R, Stevenson CJ: Vitiligo, thyroid disease and autoimmunity, Br J Dermatol, 80: 135-139, 1968.
109. Kern F, Hoffmann WH, Hambrick GW, et al: Alopecia areata. Immunologic studies and treatment with prednisone, Arch Dermatol, 107: 407, 1973.
110. Kockak Altintas AG, Gulv, Dumon S: Bilateral keratoconus associated with Hashimoto's disease, alopecia areata and atopic keratoconjunctivitis, Eur J Ophthalmol, 9: 130-133, 1999.
111. Sharma VK, Sialy R, Kumar B, et al: Evaluation of thyroid function in north Indians with alopecia areata: Response to intravenous infection of 100 microgram thyrotopin releasing hormone (TRH), J Dermatol, 26: 339-342, 1999.
112. Faergemann J: Lichen sclerosus et atrophicus generalisato, alopecia areata, and polymyalgia rheumatica found in the same patient, Cutis, 23: 757-758, 1979.
113. Anderson L: Alopecia areata: A clinical study, Br Med J, 4691: 1250, 1950.
114. Main RA, Robbie RB, Gay ES, et al: Smooth muscle antibodies and alopecia areata, Br J Dermatol, 92: 389-393, 1975.
115. Calver NS, Macdonald Hull SP, Parkin SM, et al: Autoantibodies in alopecia areata, Br J Dermatol, 127: 432, 1992.
116. Calver NS, Randal VA, Parkin SM, et al: Alopecia areata serum inhibits the growth of normal dermal papilla cells, J Invest Dermatol, 1101: 475, 1993.
117. Randall VA, Macdonald Hull SP, Nutbrown M, et al: Is the dermal papilla a primary target in alopecia areata?, J Invest Dermatol, 104: 75-85, 1995.
118. Tobin DJ, Orentreich N, Fenton DA, et al: Autoantibodies to hair follicles in alopecia areata, J Invest Dermatol, 102: 721-724, 1994.
119. Tobin DJ, Hann SK, Song MS, et al: Hair follicle structures targeted by antibodies in patients with alopecia areata, Arch Dermatol, 133: 57-61, 1997.
120. Tobin DJ, Sundberg JP, King LE, et al: Autoantibodies to hair follicles in C3H/HeJ mice with alopecia areata like hair loss, J Invest Dermatol, 109: 329-333, 1997.
121. Friedmann PS: Decreased lymphocyte reactivity and autoimmunity in alopecia areata, Br J Dermatol, 105: 145-152, 1981.
122. Majewski, BBJ, Koh MS, Taylor DR, et al: Increased ratio of helper to suppressor T-cells in alopecia areata, Br J Dermatol, 110: 171-175, 1984.
123. Hordinsky MK, Hallgren H, Nelson D: Suppressor cell number and function in alopecia areata. Arch Dermatol, 120: 188-195, 1984.
124. Brown AC, Olkouski ZL, McLaren JR: Thymus lymphocytes of the peripheral blood in patients with alopecia areata, Arch Dermatol, 113: 688, 1977.
125. Valsecchi R, Bontempelli M, Vicari O, et al: Peripheral T-cell subsets in patients with alopecia areata in different clinical phases, Dermatologica, 171: 170-174, 1985.
126. Imai R, Miura J, Takamori K, et al: Increased HLA-DR+ T-lymphocyte population in peripheral blood of alopecia areata, Clin Exp Dermatol, 16: 176-180, 1991.
127. Valsecchi R, Imberti G, Martino D, et al: Alopecia areata and interleukin-2 receptor, Dermatology, 184: 126-128, 1992.
128. Perret C, Wiesner-Menzel L, Happle R: Immunohistochemical analysis of T-cell subset in peribulbar and intrabulbar infiltrates of alopecia areata, Acta Derm Venereol, 64: 26-30, 1984.
129. Wiesner-Menzel L, Happle R: Intrabulbar and peribulbar accumulation of dendritic 67 OKT6-positive cells in alopecia areata, Arch Dermatol Res, 276: 333-334, 1984.
130. Kalish RS, Johnson KL, Hordmsky MK: Alopecia areata: Autoreactive T-cell are variably enriched in scalp lesion relative to peripheral blood, Arch Dermatol, 128: 1072-1077, 1992.
131. Gilhar A, Pillai T, Assay B, et al: Failure of passive transfer of serum from patients with alopecia areata and alopecia universalis to inhibit hair growth in transplant of human scalp skin grafted onto nude mice, Br J Dermatol, 126: 166-171, 1992.
132. Gilhar A, Ulmann Y, Berkutzki T, et al: Autoimmune hair loss (alopecia areata) transferred by T-lymphocytes to human explants on SCID mice, J Clin Invest, 101: 62-67, 1998.
133. Mims CA: Alopecia in mice infected with murine cytomegalovirus (MCMVC), Br J Exp Pathol, 66: 655-662, 1985.
134. Cerimes PE, Martin J, Wojdoni A: A potential role for viral infections in the pathogenesis of vitiligo as assessed by the polymerase chain reaction. American Dermatological Association Inc., 114 Annual Meeting. White Sulphur Springs, West Virginia, May 27-June 1, 1994.
135. Skinner RB, Jr, Light WH, Bale GF: Alopecia areata and the presence of cytomegalovirus DNA, JAMA, 273: 1419-1420, 1995.
136. Skinner RB Jr, Light WH, Leonardi to, Bale F, Rosenberg EW: A molecular approach to alopecia areata, J Invest Dermatol, 104: 35-45, 1995.
137. Jackow C, Puffer N, Hordinsky M, et al: Alopecia areata and cytomegalovirus infection in twins: Genes versus environment?, J Am Acad Dermatol, 38: 418-425, 1998.
138. Tosti A, Gentilomi G, Venturoli S: In correlation between cytomegalovirus and alopecia areata, J Invest Dermatol, 107: 43, 1996.
139. Garcia-Hernandez MJ, Torres MJ, Palomares JC, et al: No evidence of cytomegalovirus DNA in alopecia areata (letter), J Invest Dermatol, 110: 185, 1998.
140. Mc Elwee KJ, Boggess D, Burgett B, et al: Murine cytomegalovirus is not associated with alopecia areata in C3H/HeJ mice (letter), J Invest Dermatol, 110: 986-987, 1998.
141. Mac Alpine J: Is alopecia areata psychomatic? A psychiatric study, Br J Dermatol, 70: 117, 1958.
142. Piemi GI: Life events and alopecia areata, Psychother Psychosom, 41: 48-52, 1984.
143. Colon EA: Lifetime prevalence of psychiatric disorders in patients with alopecia areata, Compr Psyciatry, 32: 245-251, 1991.
144. Van der Steen P, Tranpe H, Happle R, et al: The genetic risk of alopecia areata in first degree relations of affected patients, Acta Derm Venereol (Stock), 72: 373-375, 1992.
145. Liakopoulo M, Alifierati T, Katideniou A, et al: Children with alopecia areata: Psychiatric symptomatology and life events, J Am Acad Child Adol Psych, 36: 678-684, 1997.
146. MacDonald Hull S, Nutbrown M, Pepall L, et al: Immunohistologic and ultrastructural comparison of dermal papilla and hair follicle bulb from active and normal areas of alopecia areata, J Invest Dermatol, 96: 673-681, 1991.
147. Nutbrown M, Susan P, MacDonald Hull S, et al: Abnormalities in the uitra-structure of melanocytes and outer root sheath of clinically normal hair follicles from alopecia areata scalps, J Invest Dermatol, 104: 125-135, 1995.
148. Tobin DJ, Fenton DA, Kendall MD: Ultra-structural observations on the hair bulb melanocytes and melanosomes in acute alopecia areata, J Invest Dermatol, 94: 803-807, 1990.
149. Hsoi J, Murphy GF, Egan CL, et al: Regulation of Langerhans cell function by nerves containing calcitonin gene-related peptide, Nature, 363: 159-163, 1993.
150. Hordinsky M, Lorimer S, Word S: Innervation and vasculature of the normal human and alopecia areata hair follicle: An immuno-histochemical and laser scanning contocal microscope study, in Proceedings of the First Tricontinental Meeting of Hair Research Societies, Brussles, Belgium, 1995.
151. Hordinsky M, Kennedy W, Wendelschafer-Gabb G, et al: Structure and function of cutaneous nerves in alopecia areata, J Invest Dermatol, 104: 285-295, 1995.
152. Raud J, Lundeberg T, Brodda-Jansen G, et al: Potent anti-inflammatory action of calcitonin generelated peptide. Biochem Biophys Res, Commun, 180: 1429-1435, 1991.
153. Paus R, Heinzelmann T, Schultz IC-D, et al: Hair growth induction by substance P, Lab Invest, 71: 134-140, 1994.
154. Oliver R, Jahoda CAB, Home KA, et al: The DEBR rate model for alopecia areata, J Invest Dermatol, 96: 97s, 1993.
155. McElwee KJ, Tobin DJ, Bystryn JC, et al: Alopecia areata: An autoimmune disease?, Exp Dermatol, 8: 371-379, 1999.
156. Freyshmidt-Paul P, Sundberg JP, Happle R, et al: Successful treatment of alopecia areata-like hair loss with the contact sensitizer squalic acid dibutylester (SADBE) in C3H/HeJ mice, J Invest Dermatol, 113: 61-68, 1999.
157. McElwee KJ, Boggess D, King LE, et al: Alopecia areata versus juvenile alopecia in C3H/HeJ mice: Tools to dissect the role of inflammation in focal alopecia, Exp Dermatol, 8: 354-355, 1999.
158. Shapiro J, Sundber JP, Bissonnette R, et al: Alopecia areata-like hair loss in C3H/Hel mice and DFBR rats can be reversed using topical diphencyprone, J Investig Dermatol Symp Proc, 4: 239, 1999.
159. McElwee KJ, Spers EM, Oliver RF, et al: Partial restoration of hair growth in the DEBR model for Alopecia areata after in vivo depletion of CD4+ T cells, Br J Dermatol, 140: 432-437, 1999.
160. Freyschmidt-Paul P, Ziegler A, McElwee KJ, et al: Treatment of alopecia areata in C3H/HeJ mice with the topical immuno-suppressant FK506 (Tacrolimus), Eur J Dermatol, 11: 405-409, 2001.
161. Gilhar A, Shalaginov R, Assy B, et al: Alopecia areata is a T-lymphocyte mediated autoimmune disease: Lesional human T-lymphocytes transfer alopecia areata to human skin grafts on SCID mice, J Invest Dermatol Symp Proc, 4: 207-210, 1999.
162. Sundberg JP, Cordy WR, King LE Jr: Alopecia areata in aging C3H/HeJ mice, J Invest Dermatol, 102: 847-856, 1994.
163. Sundberg JP, Bogess D, Montagutelli X, et al: C3H/HeJ mouse model for alopecia areata, J Invest Dermatol, 104: 16S-17S, 1995.
164. McElwee KJ, Boggess D, King LG, et al: Experimental induction of alopecia areata-like hair loss in C3H/HeJ mice using full thickness skin graft, J Invest Dermatol, 111: 797-803, 1998.
165. McElwee KJ, Pickett P, Oliver RF: Hair follicle auto-antibodies in DEBR rat sera, J Invest Dermatol, 104: 335-345, 1995.
166. Zhang J-G, Oliver RF: Immuno-histological study of the development of the cellular infiltrate in the pelage follicles of the DEBR model for alopecia areata, Br J Dermatol, 130: 405-414, 1994.
167. Sundberg JP, Oliver RF, McElwee KJ, et al: Alopecia areata in humans and other mammalian species, J Invest Dermatol, 104: 325-335, 1995.
168. Price VH, Khoury EL: Alopecia areata, Prog Dermatol, 25: 1-7, 1991.
169. Michie HJ, Jahoda CAB, Oliver RF, et al: The DEBR rat: An animal model of human alopecia areata, Br J Dermatol, 125: 94-100, 1991.
170. Hamm H, Traupe H: Loose anagen hair of childhood: The phenomenon of easy pluckable hair, J Am Acad Dermatol, 20: 242-248, 1989.