Hair regrowth following fecal microbiota transplantation in an elderly patient with alopecia areata: A case report and review of the literature

Wen-Rui Xie, Xiao-Ya Yang, Harry Hua-Xiang Xia, Li-Hao Wu, Xing-Xiang He, Wen-Rui Xie, Xiao-Ya Yang, Harry Hua-Xiang Xia, Li-Hao Wu, Xing-Xiang He

Abstract

Background: Alopecia areata is a hair loss disease associated with genetics, autoimmunity, and other factors. There is an intriguing link between alopecia areata and gut dysbiosis. Fecal microbiota transplantation (FMT) has been recommended to treat Clostridium difficile (previously known as Clostridioides difficile) infection, and has also shown potentials in the treatment of inflammatory bowel disease, irritable bowel syndrome, and non-alcohol fatty liver disease.

Case summary: An 86-year-old man, with a history of sigmoid colon carcinoma, suffered from recurrent abdominal pain and distension, and diarrhea for six months, with inappetence. At admission, he was also diagnosed with depression. Upon physical examination, the patient presented with a 1.5 cm × 2.0 cm alopecia areata on his right occiput. Due to the negative results of laboratory testing, capsule endoscopy, and colonoscopy, the patient was diagnosed with noninfectious diarrhea, depressive disorder, and patchy alopecia areata. Considering that noninfectious diarrhea in the elderly patient was mainly caused by gut dysbiosis, he was given six rounds of FMT. His diarrhea improved remarkably one month after FMT, with improved appetite and disappearance of abdominal pain, distension, and depressive symptoms. Surprisingly, he reported new hair growth on the affected region of his scalp, with some of his white hair gradually turning to black, without taking any other therapies for alopecia areata before and after FMT.

Conclusion: FMT might act as a potential therapy for patients who suffer from alopecia areata. Large and well-designed studies are required to confirm the role of FMT in alopecia areata.

Keywords: Alopecia areata; Autoimmune disease; Case report; Fecal microbiota transplantation; Gut microbiota; Psychopathogenesis.

Conflict of interest statement

Conflict-of-interest statement: All the authors have no conflicts of interest to declare.

©The Author(s) 2019. Published by Baishideng Publishing Group Inc. All rights reserved.

Figures

Figure 1
Figure 1
Colonoscopy showing a normal colonic mucosa.
Figure 2
Figure 2
Hair regrowth on an elderly Chinese patient’s scalp after fecal microbiota transplantation. The patient’s scalp 1 mo (A), 4 mo (B), and 18 mo (C) after fecal microbiota transplantation, respectively.

References

    1. Trüeb RM, Dias MFRG. Alopecia Areata: a Comprehensive Review of Pathogenesis and Management. Clin Rev Allergy Immunol. 2018;54:68–87.
    1. Hayashi A, Mikami Y, Miyamoto K, Kamada N, Sato T, Mizuno S, Naganuma M, Teratani T, Aoki R, Fukuda S, Suda W, Hattori M, Amagai M, Ohyama M, Kanai T. Intestinal Dysbiosis and Biotin Deprivation Induce Alopecia through Overgrowth of Lactobacillus murinus in Mice. Cell Rep. 2017;20:1513–1524.
    1. Borde A, Åstrand A. Alopecia areata and the gut-the link opens up for novel therapeutic interventions. Expert Opin Ther Targets. 2018;22:503–511.
    1. Cammarota G, Ianiro G, Tilg H, Rajilić-Stojanović M, Kump P, Satokari R, Sokol H, Arkkila P, Pintus C, Hart A, Segal J, Aloi M, Masucci L, Molinaro A, Scaldaferri F, Gasbarrini G, Lopez-Sanroman A, Link A, de Groot P, de Vos WM, Högenauer C, Malfertheiner P, Mattila E, Milosavljević T, Nieuwdorp M, Sanguinetti M, Simren M, Gasbarrini A European FMT Working Group. European consensus conference on faecal microbiota transplantation in clinical practice. Gut. 2017;66:569–580.
    1. Millan B, Laffin M, Madsen K. Fecal Microbiota Transplantation: Beyond Clostridium difficile. Curr Infect Dis Rep. 2017;19:31.
    1. Halkjær SI, Christensen AH, Lo BZS, Browne PD, Günther S, Hansen LH, Petersen AM. Faecal microbiota transplantation alters gut microbiota in patients with irritable bowel syndrome: results from a randomised, double-blind placebo-controlled study. Gut. 2018;67:2107–2115.
    1. Johnsen PH, Hilpüsch F, Cavanagh JP, Leikanger IS, Kolstad C, Valle PC, Goll R. Faecal microbiota transplantation versus placebo for moderate-to-severe irritable bowel syndrome: a double-blind, randomised, placebo-controlled, parallel-group, single-centre trial. Lancet Gastroenterol Hepatol. 2018;3:17–24.
    1. Bajaj JS, Kassam Z, Fagan A, Gavis EA, Liu E, Cox IJ, Kheradman R, Heuman D, Wang J, Gurry T, Williams R, Sikaroodi M, Fuchs M, Alm E, John B, Thacker LR, Riva A, Smith M, Taylor-Robinson SD, Gillevet PM. Fecal microbiota transplant from a rational stool donor improves hepatic encephalopathy: A randomized clinical trial. Hepatology. 2017;66:1727–1738.
    1. Tian H, Ding C, Gong J, Ge X, McFarland LV, Gu L, Wei Y, Chen Q, Zhu W, Li J, Li N. Treatment of Slow Transit Constipation With Fecal Microbiota Transplantation: A Pilot Study. J Clin Gastroenterol. 2016;50:865–870.
    1. Lee JR, Magruder M, Zhang L, Westblade LF, Satlin MJ, Robertson A, Edusei E, Crawford C, Ling L, Taur Y, Schluter J, Lubetzky M, Dadhania D, Pamer E, Suthanthiran M. Gut microbiota dysbiosis and diarrhea in kidney transplant recipients. Am J Transplant. 2019;19:488–500.
    1. Logan C, Beadsworth MB, Beeching NJ. HIV and diarrhoea: what is new? Curr Opin Infect Dis. 2016;29:486–494.
    1. Gerassy-Vainberg S, Blatt A, Danin-Poleg Y, Gershovich K, Sabo E, Nevelsky A, Daniel S, Dahan A, Ziv O, Dheer R, Abreu MT, Koren O, Kashi Y, Chowers Y. Radiation induces proinflammatory dysbiosis: transmission of inflammatory susceptibility by host cytokine induction. Gut. 2018;67:97–107.
    1. Cui B, Li P, Xu L, Zhao Y, Wang H, Peng Z, Xu H, Xiang J, He Z, Zhang T, Nie Y, Wu K, Fan D, Ji G, Zhang F. Step-up fecal microbiota transplantation strategy: a pilot study for steroid-dependent ulcerative colitis. J Transl Med. 2015;13:298.
    1. Cui B, Feng Q, Wang H, Wang M, Peng Z, Li P, Huang G, Liu Z, Wu P, Fan Z, Ji G, Wang X, Wu K, Fan D, Zhang F. Fecal microbiota transplantation through mid-gut for refractory Crohn's disease: safety, feasibility, and efficacy trial results. J Gastroenterol Hepatol. 2015;30:51–58.
    1. Bech P, Kastrup M, Rafaelsen OJ. Mini-compendium of rating scales for states of anxiety depression mania schizophrenia with corresponding DSM-III syndromes. Acta Psychiatr Scand Suppl. 1986;326:1–37.
    1. Sarker SA, Ahmed T, Brüssow H. Persistent diarrhea: a persistent infection with enteropathogens or a gut commensal dysbiosis? Environ Microbiol. 2017;19:3789–3801.
    1. Battaglioli EJ, Hale VL, Chen J, Jeraldo P, Ruiz-Mojica C, Schmidt BA, Rekdal VM, Till LM, Huq L, Smits SA, Moor WJ, Jones-Hall Y, Smyrk T, Khanna S, Pardi DS, Grover M, Patel R, Chia N, Nelson H, Sonnenburg JL, Farrugia G, Kashyap PC. Clostridioides difficile uses amino acids associated with gut microbial dysbiosis in a subset of patients with diarrhea. Sci Transl Med. 2018;10:eaam7019.
    1. Moayyedi P, Yuan Y, Baharith H, Ford AC. Faecal microbiota transplantation for Clostridium difficile-associated diarrhoea: a systematic review of randomised controlled trials. Med J Aust. 2017;207:166–172.
    1. Pratt CH, King LE, Jr, Messenger AG, Christiano AM, Sundberg JP. Alopecia areata. Nat Rev Dis Primers. 2017;3:17011.
    1. Simakou T, Butcher JP, Reid S, Henriquez FL. Alopecia areata: A multifactorial autoimmune condition. J Autoimmun. 2019;98:74–85.
    1. Manolache L, Petrescu-Seceleanu D, Benea V. Alopecia areata and relationship with stressful events in children. J Eur Acad Dermatol Venereol. 2009;23:107–109.
    1. Manolache L, Benea V. Stress in patients with alopecia areata and vitiligo. J Eur Acad Dermatol Venereol. 2007;21:921–928.
    1. Picardi A, Pasquini P, Cattaruzza MS, Gaetano P, Baliva G, Melchi CF, Papi M, Camaioni D, Tiago A, Gobello T, Biondi M. Psychosomatic factors in first-onset alopecia areata. Psychosomatics. 2003;44:374–381.
    1. Nakajima T, Inui S, Itami S. Pulse corticosteroid therapy for alopecia areata: study of 139 patients. Dermatology. 2007;215:320–324.
    1. Yang CC, Lee CT, Hsu CK, Lee YP, Wong TW, Chao SC, Lee JY, Sheu HM, Chen W. Early intervention with high-dose steroid pulse therapy prolongs disease-free interval of severe alopecia areata: a retrospective study. Ann Dermatol. 2013;25:471–474.
    1. Penders J, Stobberingh EE, van den Brandt PA, Thijs C. The role of the intestinal microbiota in the development of atopic disorders. Allergy. 2007;62:1223–1236.
    1. Scher JU, Ubeda C, Artacho A, Attur M, Isaac S, Reddy SM, Marmon S, Neimann A, Brusca S, Patel T, Manasson J, Pamer EG, Littman DR, Abramson SB. Decreased bacterial diversity characterizes the altered gut microbiota in patients with psoriatic arthritis, resembling dysbiosis in inflammatory bowel disease. Arthritis Rheumatol. 2015;67:128–139.
    1. Song H, Yoo Y, Hwang J, Na YC, Kim HS. Faecalibacterium prausnitzii subspecies-level dysbiosis in the human gut microbiome underlying atopic dermatitis. J Allergy Clin Immunol. 2016;137:852–860.
    1. Visser MJE, Kell DB, Pretorius E. Bacterial Dysbiosis and Translocation in Psoriasis Vulgaris. Front Cell Infect Microbiol. 2019;9:7.
    1. Skogberg G, Jackson S, Åstrand A. Mechanisms of tolerance and potential therapeutic interventions in Alopecia Areata. Pharmacol Ther. 2017;179:102–110.
    1. Safina DD, Abdulkhakov RA, Abdulkhakov SR, Odintsova AKh, Cheremina NA. [Clinical case of a combination of ulcerative colitis and alopecia areata] Eksp Klin Gastroenterol. 2013:92–96.
    1. Treem WR, Veligati LN, Rotter JI, Targan SR, Hyams JS. Ulcerative colitis and total alopecia in a mother and her son. Gastroenterology. 1993;104:1187–1191.
    1. Patel KV, Farrant P, Sanderson JD, Irving PM. Hair loss in patients with inflammatory bowel disease. Inflamm Bowel Dis. 2013;19:1753–1763.
    1. Sobolewska-Włodarczyk A, Włodarczyk M, Fichna J, Wiśniewska-Jarosińska M. Alopecia areata in patients with inflammatory bowel disease: an overview. Folia Med Cracov. 2016;56:5–12.
    1. Ramos GP, Papadakis KA. Mechanisms of Disease: Inflammatory Bowel Diseases. Mayo Clin Proc. 2019;94:155–165.
    1. Sartor RB, Wu GD. Roles for Intestinal Bacteria, Viruses, and Fungi in Pathogenesis of Inflammatory Bowel Diseases and Therapeutic Approaches. Gastroenterology. 2017;152:327–339.e4.
    1. Rapozo DC, Bernardazzi C, de Souza HS. Diet and microbiota in inflammatory bowel disease: The gut in disharmony. World J Gastroenterol. 2017;23:2124–2140.
    1. Zempleni J, Hassan YI, Wijeratne SS. Biotin and biotinidase deficiency. Expert Rev Endocrinol Metab. 2008;3:715–724.
    1. Fernandez-Banares F, Abad-Lacruz A, Xiol X, Gine JJ, Dolz C, Cabre E, Esteve M, Gonzalez-Huix F, Gassull MA. Vitamin status in patients with inflammatory bowel disease. Am J Gastroenterol. 1989;84:744–748.
    1. Maslowski KM, Mackay CR. Diet, gut microbiota and immune responses. Nat Immunol. 2011;12:5–9.
    1. Lieben L, Carmeliet G. Vitamin D signaling in osteocytes: effects on bone and mineral homeostasis. Bone. 2013;54:237–243.
    1. Fraser DR, Kodicek E. Unique biosynthesis by kidney of a biological active vitamin D metabolite. Nature. 1970;228:764–766.
    1. Singh P, Kumar M, Al Khodor S. Vitamin D Deficiency in the Gulf Cooperation Council: Exploring the Triad of Genetic Predisposition, the Gut Microbiome and the Immune System. Front Immunol. 2019;10:1042.
    1. Thompson JM, Mirza MA, Park MK, Qureshi AA, Cho E. The Role of Micronutrients in Alopecia Areata: A Review. Am J Clin Dermatol. 2017;18:663–679.
    1. Tsai TY, Huang YC. Vitamin D deficiency in patients with alopecia areata: A systematic review and meta-analysis. J Am Acad Dermatol. 2018;78:207–209.
    1. Lee S, Kim BJ, Lee CH, Lee WS. Increased prevalence of vitamin D deficiency in patients with alopecia areata: a systematic review and meta-analysis. J Eur Acad Dermatol Venereol. 2018;32:1214–1221.
    1. Chen CH, Sakai Y, Demay MB. Targeting expression of the human vitamin D receptor to the keratinocytes of vitamin D receptor null mice prevents alopecia. Endocrinology. 2001;142:5386–5389.
    1. Xie Z, Komuves L, Yu QC, Elalieh H, Ng DC, Leary C, Chang S, Crumrine D, Yoshizawa T, Kato S, Bikle DD. Lack of the vitamin D receptor is associated with reduced epidermal differentiation and hair follicle growth. J Invest Dermatol. 2002;118:11–16.
    1. Fawzi MM, Mahmoud SB, Ahmed SF, Shaker OG. Assessment of vitamin D receptors in alopecia areata and androgenetic alopecia. J Cosmet Dermatol. 2016;15:318–323.
    1. Zhu W, Yan J, Zhi C, Zhou Q, Yuan X. 1,25(OH) 2D3 deficiency-induced gut microbial dysbiosis degrades the colonic mucus barrier in Cyp27b1 knockout mouse model. Gut Pathog. 2019;11:8.
    1. Waterhouse JC, Perez TH, Albert PJ. Reversing bacteria-induced vitamin D receptor dysfunction is key to autoimmune disease. Ann N Y Acad Sci. 2009;1173:757–765.
    1. Appleyard CB, Cruz ML, Isidro AA, Arthur JC, Jobin C, De Simone C. Pretreatment with the probiotic VSL#3 delays transition from inflammation to dysplasia in a rat model of colitis-associated cancer. Am J Physiol Gastrointest Liver Physiol. 2011;301:G1004–G1013.
    1. Mukherji A, Kobiita A, Ye T, Chambon P. Homeostasis in intestinal epithelium is orchestrated by the circadian clock and microbiota cues transduced by TLRs. Cell. 2013;153:812–827.
    1. Hvas CL, Dahl Jørgensen SM, Jørgensen SP, Storgaard M, Lemming L, Hansen MM, Erikstrup C, Dahlerup JF. Fecal Microbiota Transplantation Is Superior to Fidaxomicin for Treatment of Recurrent Clostridium difficile Infection. Gastroenterology. 2019;156:1324–1332.e3.
    1. Chen D, Wu J, Jin D, Wang B, Cao H. Fecal microbiota transplantation in cancer management: Current status and perspectives. Int J Cancer. 2019;145:2021–2031.
    1. Borody T, Fischer M, Mitchell S, Campbell J. Fecal microbiota transplantation in gastrointestinal disease: 2015 update and the road ahead. Expert Rev Gastroenterol Hepatol. 2015;9:1379–1391.
    1. Xie WR, Yang XX, Xia HHX, He XX. Fecal microbiota transplantation for treating hepatic encephalopathy: Experimental and clinical evidence and possible underlying mechanisms. J Explor Res Pharmacol. 2018;3:119–124.
    1. Ooijevaar RE, Terveer EM, Verspaget HW, Kuijper EJ, Keller JJ. Clinical Application and Potential of Fecal Microbiota Transplantation. Annu Rev Med. 2019;70:335–351.
    1. Rebello D, Wang E, Yen E, Lio PA, Kelly CR. Hair Growth in Two Alopecia Patients after Fecal Microbiota Transplant. ACG Case Rep J. 2017;4:e107.
    1. Pandhi D, Khanna D. Premature graying of hair. Indian J Dermatol Venereol Leprol. 2013;79:641–653.
    1. Kuty-Pachecka M. Psychological and psychopathological factors in alopecia areata. Psychiatr Pol. 2015;49:955–964.
    1. Groen RN, de Clercq NC, Nieuwdorp M, Hoenders HJR, Groen AK. Gut microbiota, metabolism and psychopathology: A critical review and novel perspectives. Crit Rev Clin Lab Sci. 2018;55:283–293.

Source: PubMed

스폰서 및 공동 작업자

건강 상태

약물 개입

3
구독하다