Hair microscopy: an easy adjunct to diagnosis of systemic diseases in children

M.S. Abd Elmaksoud, N.S. Gomaa, H.G. Azouz, C.N.V. On, C.T. Ho, T.E. Omar, J.A. McGrath, A. Onoufriadis, Genetic analysis in three Egyptian patients with Griscelli syndrome type 1 reveals new nonsense mutations in MYO5A. Clin. Exp. Dermatol. 45, 789–792 (2020). https://doi.org/10.1111/ced.14220 N. Bellon, S. Hadj-Rabia, F. Moulin, C. Lambe, G. Lezmi, F. Charbit-Henrion, C. Alby, L. Le Saché-de Peufeilhoux, S. Leclerc-Mercier, A. Hadchouel, J. Steffann, A. Hovnanian, A. Lapillonne, C. Bodemer, The challenging management of a series of 43 infants with Netherton syndrome: Unexpected complications and novel mutations. Br. J. Dermatol. 184, 532–537 (2021). https://doi.org/10.1111/bjd.19265 A. Belloni Fortina, M. Alaibac, S. Piaserico, A. Peserico, PIBI(D)S: Clinical and molecular characterization of a new case. J. Eur. Acad. Dermatol. Venereol. 15, 65–69 (2001). https://doi.org/10.1046/j.1468-3083.2001.00212.x E. Bergmann, J.-M. Egly, Trichothiodystrophy, a transcription syndrome. Trends Genet. 17, 279–286 (2001). https://doi.org/10.1016/S0168-9525(01)02280-6 J. Berk-Krauss, M.E. Laird, What’s in a name—Dermoscopy vs dermatoscopy. JAMA Dermatol. 153, 1235 (2017). https://doi.org/10.1001/jamadermatol.2017.3905 V. Boccaletti, E. Zendri, G. Giordano, L. Gnetti, G. De Panfilis, Familial uncombable hair syndrome: Ultrastructural hair study and response to biotin. Pediatr. Dermatol. 24, E14–E16 (2007). https://doi.org/10.1111/j.1525-1470.2007.00385.x S.L. Bowman, J. Bi-Karchin, L. Le, M.S. Marks, The road to lysosome-related organelles: Insights from Hermansky-Pudlak syndrome and other rare diseases. Traffic 20, 404–435 (2019). https://doi.org/10.1111/tra.12646 R.B. Bradfield, Protein-calorie malnutrition diagnosis by hair tissue: A review. J. Trop. Pediatr. Environ. Child Health 19, 370–375 (1973). https://doi.org/10.1093/tropej/19.4.370 R.B. Bradfield, in Hair Research, ed. by C. E. Orfanos, W. Montagna, G. Stüttgen. Effect of undernutrition upon hair growth (Springer, Berlin, Heidelberg, 1981), pp. 251–256 J.C. Bravman, R. Sinclair, The preparation of cross-section specimens for transmission electron microscopy. J. Electron Microsc. Tech. 1, 53–61 (1984). https://doi.org/10.1002/jemt.1060010106 B.C. Broughton, Two individuals with features of both xeroderma pigmentosum and trichothiodystrophy highlight the complexity of the clinical outcomes of mutations in the XPD gene. Hum. Mol. Genet. 10, 2539–2547 (2001). https://doi.org/10.1093/hmg/10.22.2539 C.G. Burkhart, C.N. Burkhart, Trichorrhexis nodosa revisited. SKINmed 6, 57–58 (2007). https://doi.org/10.1111/j.1540-9740.2007.06044.x D. Çağdaş, T.T. Özgür, G.T. Asal, İ. Tezcan, A. Metin, N. Lambert, G. de Saint Basile, Ö. Sanal, Griscelli syndrome types 1 and 3: Analysis of four new cases and long-term evaluation of previously diagnosed patients. Eur. J. Pediatr. 171, 1527–1531 (2012). https://doi.org/10.1007/s00431-012-1765-x P. Calderon, N. Otberg, J. Shapiro, Uncombable hair syndrome. J. Am. Acad. Dermatol. 61, 512–515 (2009). https://doi.org/10.1016/j.jaad.2009.01.006 H.H. Celik, H. Tore, S. Tunali, I. Tatar, M.M. Aldur, Light and scanning electron microscopic examination of hair in Griscelli syndrome. Saudi Med. J. 28, 1275–1277 (2007) P. Chandravathi, H. Karani, S. Siddaiahgari, L. Lingappa, Light microscopy and polarized microscopy: A dermatological tool to diagnose gray hair syndromes. Int. J. Trichology 9, 38 (2017). https://doi.org/10.4103/ijt.ijt_21_16 E. Chen, J.E. Cleaver, C.A. Weber, S. Packman, A.J. Barkovich, T.K. Koch, M.L. Williams, M. Golabi, V.H. Price, Trichothiodystrophy: Clinical spectrum, central nervous system imaging, and biochemical characterization of two siblings. J. Invest. Dermatol. 103, 154S–158S (1994). https://doi.org/10.1111/1523-1747.ep12399493 S. Cheng, J. Stone, D. de Berker, Trichothiodystrophy and fragile hair: The distinction between diagnostic signs and diagnostic labels in childhood hair disease. Br. J. Dermatol. 161, 1379–1383 (2009). https://doi.org/10.1111/j.1365-2133.2009.09403.x S. Choudhary, R. Gadegone, S. Koley, Menkes kinky hair disease. Indian J. Dermatol. 57, 407 (2012). https://doi.org/10.4103/0019-5154.100503 D.L. Coulter, T.F. Beals, R.J. Allen, Neurotrichosis: Hair-shaft abnormalities associated with neurological diseases. Dev. Med. Child Neurol. 24, 634–644 (2008). https://doi.org/10.1111/j.1469-8749.1982.tb13674.x A.B. Das-Chaudhuri, Genetic basis of hair medulla by twin study. Am. J. Phys. Anthropol. 44, 51–53 (1976). https://doi.org/10.1002/ajpa.1330440107 R. Dawber, Scanning electron microscopy of normal and abnormal hair shafts. Arch. Dermatol. 101, 316 (1970). https://doi.org/10.1001/archderm.1970.04000030060009 H.L. de Almeida, A.E. Kiszewski, T. Vicentini Xavier, F. Pirolli, L.A. Antônio Suita de Castro, Ultrastructural aspects of hairs of Chediak-Higashi syndrome. J. Eur. Acad. Dermatol. Venereol. 32, e227–e229 (2018). https://doi.org/10.1111/jdv.14750 R. De Cássia Comis Wagner, P.K. Kiyohara, M. Silveira, I. Joekes, Electron microscopic observations of human hair medulla. J. Microsc. 226, 54–63 (2007). https://doi.org/10.1111/j.1365-2818.2007.01747.x S. Faghri, D. Tamura, K.H. Kraemer, J.J. DiGiovanna, Trichothiodystrophy: A systematic review of 112 published cases characterises a wide spectrum of clinical manifestations. J. Med. Genet. 45, 609–621 (2008). https://doi.org/10.1136/jmg.2008.058743 A.M. Finner, Nutrition and hair. Dermatol. Clin. 31, 167–172 (2013). https://doi.org/10.1016/j.det.2012.08.015 F. Formanek, Y. De Wilde, G.S. Luengo, B. Querleux, Investigation of dyed human hair fibres using apertureless near-field scanning optical microscopy. J. Microsc. 224, 197–202 (2006). https://doi.org/10.1111/j.1365-2818.2006.01685.x M. Goodier, M. Hordinsky, Normal and aging hair biology and structure 'aging and hair'. Curr. Probl. Dermatol. 47, 1–9 (2015). https://doi.org/10.1159/000369594 J.A. Guevara-Patiño, L. Plaza-Rojas, It takes two to tango. J. Invest. Dermatol. 140, 1131–1133 (2020). https://doi.org/10.1016/j.jid.2020.01.017 E.L. Guo, R. Katta, Diet and hair loss: Effects of nutrient deficiency and supplement use. Dermatol. Pract. Concept. 7, 1–10 (2017). https://doi.org/10.5826/dpc.0701a01 C. Hadjur, G. Daty, G. Madry, P. Corcuff, Cosmetic assessment of the human hair by confocal microscopy. Scanning 24, 59–64 (2006). https://doi.org/10.1002/sca.4950240202 T.H. Han, J. Lee, Y.J. Kim, Hair zinc level analysis and correlative micronutrients in children presenting with malnutrition and poor growth. Pediatr. Gastroenterol. Hepatol. Nutr. 19, 259 (2016). https://doi.org/10.5223/pghn.2016.19.4.259 K. Hashimoto, The structure of human hair. Clin. Dermatol. 6, 7–21 (1988). https://doi.org/10.1016/0738-081X(88)90060-0 A. Inamadar, A. Palit, R. Shivanna, N. Deshmukh, K. Adya, Light microscopy of the hair: A simple tool to “untangle” hair disorders. Int. J. Trichology 3, 46 (2011). https://doi.org/10.4103/0974-7753.82124 A.A. Johnson, M.C. Latham, D.A. Roe, An evaluation of the use of changes in hair root morphology in the assessment of protein-calorie malnutrition. Am. J. Clin. Nutr. 29, 502–511 (1976). https://doi.org/10.1093/ajcn/29.5.502 M.L.W. Juhász, N. Atanaskova Mesinkovska, The use of phosphodiesterase inhibitors for the treatment of alopecia. J. Dermatol. Treat. 31, 245–253 (2020). https://doi.org/10.1080/09546634.2019.1592097 F. Kaliyadan, B. Gosai, W. Al Melhim, K. Feroze, H. Qureshi, S. Ibrahim, J. Kuruvilla, Scanning electron microscopy study of hair shaft damage secondary to cosmetic treatments of the hair. Int. J. Trichology 8, 94 (2016). https://doi.org/10.4103/0974-7753.188035 J. Kaplan, I. De Domenico, D.M. Ward, Chediak-Higashi syndrome. Curr. Opin. Hematol. 15, 22–29 (2008). https://doi.org/10.1097/MOH.0b013e3282f2bcce D. Keefe, L. Liu, W. Wang, C. Silva, Imaging meiotic spindles by polarization light microscopy: Principles and applications to IVF. Reprod. BioMed. Online 7, 24–29 (2003). https://doi.org/10.1016/S1472-6483(10)61724-5 M. Koike-Tani, T. Tani, S.B. Mehta, A. Verma, R. Oldenbourg, Polarized light microscopy in reproductive and developmental biology. Mol. Reprod. Dev. 82, 548–562 (2015). https://doi.org/10.1002/mrd.22221 K. Krzewski, A.R. Cullinane, Evidence for defective Rab GTPase-dependent cargo traffic in immune disorders. Exp. Cell Res. 319, 2360–2367 (2013). https://doi.org/10.1016/j.yexcr.2013.06.012 F. Lacarrubba, G. Micali, A. Tosti, Scalp dermoscopy or trichoscopy. Curr. Probl. Dermatol. 47, 21–32 (2015). https://doi.org/10.1159/000369402 J.M. Lagarde, P. Peyre, D. Redoules, D. Black, M. Briot, Y. Gall, Confocal microscopy of hair. Cell Biol. Toxicol. 10, 301–304 (1994). https://doi.org/10.1007/BF00755774 C.A. McKenzie, K. Wakamatsu, N.A. Hanchard, T. Forrester, S. Ito, Childhood malnutrition is associated with a reduction in the total melanin content of scalp hair. Br. J. Nutr. 98, 159–164 (2007). https://doi.org/10.1017/S0007114507694458 M. Meeths, Y.T. Bryceson, E. Rudd, C. Zheng, S.M. Wood, K. Ramme, K. Beutel, H. Hasle, C. Heilmann, K. Hultenby, H.-G. Ljunggren, B. Fadeel, M. Nordenskjöld, J.-I. Henter, Clinical presentation of Griscelli syndrome type 2 and spectrum of RAB27A mutations: Spectrum of RAB27A mutations. Pediatr. Blood Cancer 54, 563–572 (2010). https://doi.org/10.1002/pbc.22357 B. Nirmal, Dermatoscopy: Physics and principles. Indian J. Dermatopathol. Diagn. Dermatol. 4, 27 (2017). https://doi.org/10.4103/ijdpdd.ijdpdd_13_17 A. Nurden, P. Nurden, Advances in our understanding of the molecular basis of disorders of platelet function: Inherited platelet disorders. J. Thromb. Haemost. 9, 76–91 (2011). https://doi.org/10.1111/j.1538-7836.2011.04274.x J. Ocampo-Garza, J. Griggs, A. Tosti, New drugs under investigation for the treatment of alopecias. Expert Opin. Investig. Drugs 28, 275–284 (2019). https://doi.org/10.1080/13543784.2019.1568989 R. Oldenbourg, Polarized light microscopy: principles and practice. Cold Spring Harb. Protoc., pdb.top078600-pdb.top078600 (2013, 2013). https://doi.org/10.1101/pdb.top078600 E.F.D. Oliveira, A.L.C.D.A. Araripe, Monilethrix: A typical case report with microscopic and dermatoscopic findings. An. Bras. Dermatol. 90, 126–127 (2015). https://doi.org/10.1590/abd1806-4841.20153357 G. Poletti, F. Orsini, C. Lenardi, E. Barborini, A comparative study between AFM and SEM imaging on human scalp hair. J. Microsc. 211, 249–255 (2003). https://doi.org/10.1046/j.1365-2818.2003.01220.x M. Pomeranz, J. Campbell, D. Siegal-Gaskins, J. Engelmeier, T. Wilson, V. Fernandez, J. Brkljacic, E. Grotewold, High-resolution computational imaging of leaf hair patterning using polarized light microscopy. Plant J. 73, 701–708 (2013). https://doi.org/10.1111/tpj.12075 J. Powell, R.P. Dawber, D.J. Ferguson, W.A. Griffiths, Netherton’s syndrome: Increased likelihood of diagnosis by examining eyebrow hairs. Br. J. Dermatol. 141, 544–546 (1999). https://doi.org/10.1046/j.1365-2133.1999.03056.x A.N. Prasad, R. Ojha, Menkes disease: What a multidisciplinary approach can do. J. Multidiscip. Healthc. 9, 371–385 (2016). https://doi.org/10.2147/JMDH.S93454 V.H. Price, Trichothiodystrophy: Sulfur-deficient brittle hair as a marker for a neuroectodermal symptom complex. Arch. Dermatol. 116, 1375–1384 (1980). https://doi.org/10.1001/archderm.116.12.1375 E.D. Renner, D. Hartl, S. Rylaarsdam, M.L. Young, L. Monaco-Shawver, G. Kleiner, M.L. Markert, E.R. Stiehm, B.H. Belohradsky, M.P. Upton, T.R. Torgerson, J.S. Orange, H.D. Ochs, Comèl-Netherton syndrome defined as primary immunodeficiency. J. Allergy Clin. Immunol. 124, 536–543 (2009). https://doi.org/10.1016/j.jaci.2009.06.009 L. Rudnicka, M. Olszewska, A. Rakowska, E. Kowalska-Oledzka, M. Slowinska, Trichoscopy: A new method for diagnosing hair loss. J. Drugs Dermatol. 7, 651–654 (2008) L. Rudnicka, M. Olszewska, A. Waśkiel, A. Rakowska, Trichoscopy in hair shaft disorders. Dermatol. Clin. 36, 421–430 (2018). https://doi.org/10.1016/j.det.2018.05.009 L. Rudnicka, A. Rakowska, M. Kurzeja, M. Olszewska, Hair shafts in trichoscopy. Dermatol. Clin. 31, 695–708 (2013). https://doi.org/10.1016/j.det.2013.06.007 D. Rugar, P. Hansma, Atomic force microscopy. Phys. Today 43, 23–30 (1990). https://doi.org/10.1063/1.881238 K. Sandrock, B. Zieger, Current strategies in diagnosis of inherited storage pool defects. Transfus. Med. Hemother. 37, 4–4 (2010). https://doi.org/10.1159/000320279 C.A. Sarri, A. Roussaki-Schulze, Y. Vasilopoulos, E. Zafiriou, A. Patsatsi, C. Stamatis, P. Gidarokosta, D. Sotiriadis, T. Sarafidou, Z. Mamuris, Netherton syndrome: A genotype-phenotype review. Mol. Diagn. Ther. 21, 137–152 (2017). https://doi.org/10.1007/s40291-016-0243-y L. Shao, B. Newell, Light microscopic hair abnormalities in children: Retrospective review of 119 cases in a 10-year period. Pediatr. Dev. Pathol. 17, 36–43 (2014). https://doi.org/10.2350/13-09-1375-OA.1 Y. Shimomura, M. Ito, Human hair keratin-associated proteins. J. Investig. Dermatol. Symp. Proc. 10, 230–233 (2005). https://doi.org/10.1111/j.1087-0024.2005.10112.x R. Sinclair, Treatment of monilethrix with oral minoxidil. JAAD Case Rep. 2, 212–215 (2016). https://doi.org/10.1016/j.jdcr.2016.02.011 V.V. Smith, Light microscopic examination of scalp hair samples as an aid in the diagnosis of paediatric disorders: Retrospective review of more than 300 cases from a single centre. J. Clin. Pathol. 58, 1294–1298 (2005). https://doi.org/10.1136/jcp.2005.027581 C. Solovan, F. Doroftei, M. Pinteala, A. Chiriac, C. Cristea, Scanning electron microscopic examination of the hair shaft abnormalities in Netherton’s syndrome. Int. J. Dermatol. 54, 693–694 (2015). https://doi.org/10.1111/ijd.12848 M. Stefanini, E. Botta, M. Lanzafame, D. Orioli, Trichothiodystrophy: From basic mechanisms to clinical implications. DNA Repair 9, 2–10 (2010). https://doi.org/10.1016/j.dnarep.2009.10.005 K. Stuvel, J.J. Heeringa, V.A.S.H. Dalm, R.W.J. Meijers, E. Hoffen, S.A.M. Gerritsen, M.C. Zelm, S.G.M.A. Pasmans, Comel-Netherton syndrome: A local skin barrier defect in the absence of an underlying systemic immunodeficiency. Allergy 75, 1710–1720 (2020). https://doi.org/10.1111/all.14197 J.A. Swift, J.R. Smith, Atomic force microscopy of human hair. Scanning 22, 310–318 (2006). https://doi.org/10.1002/sca.4950220506 S.G. Tangye, W. Al-Herz, A. Bousfiha, T. Chatila, C. Cunningham-Rundles, A. Etzioni, J.L. Franco, S.M. Holland, C. Klein, T. Morio, H.D. Ochs, E. Oksenhendler, C. Picard, J. Puck, T.R. Torgerson, J.-L. Casanova, K.E. Sullivan, Human inborn errors of immunity: 2019 update on the classification from the International Union of Immunological Societies Expert Committee. J. Clin. Immunol. 40, 24–64 (2020). https://doi.org/10.1007/s10875-019-00737-x A. Trache, G.A. Meininger, Atomic force microscopy (AFM). Curr. Protoc. Microbiol. 8 (2008). https://doi.org/10.1002/9780471729259.mc02c02s8 Z. Tümer, L.B. Møller, Menkes disease. Eur. J. Hum. Genet. 18, 511–518 (2010). https://doi.org/10.1038/ejhg.2009.187 D. Utsumi, M. Yasuda, H. Amano, Y. Suga, M. Seishima, K. Takahashi, Hair abnormality in Netherton syndrome observed under polarized light microscopy. J. Am. Acad. Dermatol. 83, 847–853 (2020). https://doi.org/10.1016/j.jaad.2019.08.024 N.Y.S. Valente, M.C.M.R. Machado, P. Boggio, A.C.F. Alves, F.N. Bergonse, E. Casella, D.M. Vasconcelos, A.S. Grumach, Z.N.P.D. Oliveira, Polarized light microscopy of hair shafts aids in the differential diagnosis of Chédiak-Higashi and Griscelli-Prunieras syndromes. Clinics 61(4), 327–332 (2006). https://doi.org/10.1590/S1807-59322006000400009 V. Venkataraman, D. Panigrahi, P. Balaji, R. Jamal, Biotinidase deficiency in childhood. Neurol. India 61, 411 (2013). https://doi.org/10.4103/0028-3886.117614 A. Westphal, W. Cheng, J. Yu, G. Grassl, M. Krautkrämer, O. Holst, N. Föger, K.-H. Lee, Lysosomal trafficking regulator Lyst links membrane trafficking to toll-like receptor–mediated inflammatory responses. J. Exp. Med. 214, 227–244 (2017). https://doi.org/10.1084/jem.20141461 M. Winey, J.B. Meehl, E.T. O’Toole, T.H. Giddings, Conventional transmission electron microscopy. Mol. Biol. Cell 25, 319–323 (2014). https://doi.org/10.1091/mbc.e12-12-0863 B. Wolf, R.E. Grier, R.J. Allen, S.I. Goodman, C.L. Kien, Biotinidase deficiency: The enzymatic defect in late-onset multiple carboxylase deficiency. Clin. Chim. Acta 131, 273–281 (1983). https://doi.org/10.1016/0009-8981(83)90096-7 M.A. Yamazaki-Nakashimada, R. Roldán-Marín, S. Toussaint-Caire, A. Olaya-Vargas, N. Ramírez-Uribe, F. Rivas-Larrauri, C. Durán-McKinster, M.A. Alcántara-Ortigoza, A. González-del Angel, L. Orozco-Covarrubias, S. Scheffler-Mendoza, M. Saez-de-Ocariz, Hair pigment distribution changes after haematopoietic stem cell transplantation in Griscelli syndrome type 2. J. Eur. Acad. Dermatol. Venereol. 35(1), e53–e56 (2021). https://doi.org/10.1111/jdv.16795 H. You, L. Yu, Atomic force microscopy as a tool for study of human hair. Scanning 19, 431–437 (2006). https://doi.org/10.1002/sca.4950190606 A. Zlotogorski, D. Marek, L. Horev, A. Abu, D. Ben-Amitai, L. Gerad, A. Ingber, M. Frydman, H. Reznik-Wolf, D.A. Vardy, E. Pras, An autosomal recessive form of monilethrix is caused by mutations in DSG4: Clinical overlap with localized autosomal recessive hypotrichosis. J. Invest. Dermatol. 126, 1292–1296 (2006). https://doi.org/10.1038/sj.jid.5700251