Pestalotioid fungi: A rare agent of onychomycosis among agriculture workers

Document Type: Original Articles

Authors

1 Department of Life Sciences, Dibrugarh University, Dibrugarh-786004, Assam, India

2 Department of Microbiology, Jorhat Medical College, Jorhat-785001, Assam, India

3 Regional Medical Research Center for Northeast, Indian Council of Medical Research, Dibrugarh-786001, Assam, India

Abstract

Background and Purpose: Pestalotioid fungi are ubiquitous environmental molds that have received considerable attention in recent times not only because of their role as a plant pathogen but also owing to their high frequency of retrieval from human diseases. Regarding this, the present study was conducted to investigate onychomycosis caused by pestalotioid fungi, commonly considered important phytopathogens causing grey blight disease in Camellia sinensis.
Materials and Methods: A total of 122 agriculture workers were enrolled from Assam, India. Direct microscopic examination was carried out using 40% KOH to determine the presence of any fungal element. Further processing of the specimens for the isolation of fungi was performed using the standard protocol. In addition, the keratinolytic potential of the isolates was evaluated by means of the in vitro hair perforation test.
Results: Out of 103 culture-positive samples, non-dermatophyte and dermatophyte molds constituted 82.52% (n=85) and 6.79% (n=7) of the samples, followed by yeasts (n=1, 0.9%) and sterile hyphae (n=10, 9.7%). With regard to the isolated non-dermatophyte molds (82.69%), 4 cases belonged to pestalotioid fungi, such as Neopestalotiopsis piceana (n=1), Pestalotiopsis species (n=1), and Pseudopestalotiopsis theae (n=2). The keratinolytic activity of Pestalotiopsis species showed perforation by disrupting the hair cortex; furthermore, macroconidia were found to be present inside the human hair.
Conclusion: A high rate of NDM isolation may be attributed to constant exposure to adverse environmental and occupational hazards. This study highlighted the importance of “pestalotioid fungi” as the rare etiologic agent of onychomycosis. Another remarkable finding was the keratinolytic potential of Pestalotiopsis species, which is unique in this study.
 

Keywords


1. Maharachchikumbura SS, Hyde KD, Groenewald JZ, Xu J, Crous PW. Pestalotiopsis revisited. Stud Mycol. 2014; 79:121-86. 
2. Sane S, Sharma S, Konduri R, Fernandes M. Emerging corneal pathogens: first report of Pseudopestalotiopsis theae keratitis. Indian J Ophthalmol. 2019; 67(1):150-2. 
3. Silverio ML, Calvacanti MA, Silva GA, Oliveira RJ, Bezerra JL. A new epifoliar species of Neopestalotiopsis from Brazil. Agrotropica. 2016; 28(2):151-8.
4. Lateef AA, Sepiah M, Bolhassan MH. Molecular identification and diversity of Pestalotiopsis, Neopestalotiopsis and Pseudopestalotiopsis species from four host plants in Sarawak, Borneo island (Malaysia). J Sci Technol. 2018; 10(1):33-43. 
5. Maharachchikumbura SS, Guo LD, Chukeatirote E, Bahkali AH, Hyde KD. Pestalotiopsis-morphology, phylogeny, biochemistry and diversity. Fungal Divers. 2011; 50(1):167-87. 
6. Chen Y, Zeng L, Shu N, Jiang M, Wang H, Huang Y, et al. Pestalotiopsis-like species causing gray blight disease on Camellia sinensis in China. Plant Dis. 2018; 102(1):98-106.
7. Liu AR, Wu XP, Xu T, Guo LD, Wei JG. Notes on endophytic Pestalotiopsis from Hainan, China. Mycosystema. 2006; 25(3):389-97.
8. Wei JG, Xu T, Guo LD, Liu AR, Zhang Y, Pan XH. Endophytic Pestalotiopsis species associated with plants of Podocarpaceae, Theaceae and Taxaceae in southern China. Fungal Divers. 2007; 24(1):55-74.
9. Sutton DA. Coelomycetous fungi in human disease. A review: clinical entities, pathogenesis, identification and therapy. Rev Iberoam Micol. 1999; 16(4):171-9.
10. Seebacher C, Brasch J, Abeck D, Cornely O, Effendy I, Ginter-Hanselmayer G, et al. Onychomycosis. Mycoses. 2007; 50(4):321-7. 
11. Fernandez MS, Rojas FD, Cattana ME, Sosa Mde L, Mangiaterra ML, Giusiano GE. Aspergillus terreus complex: an emergent opportunistic agent of Onychomycosis. Mycoses. 2013; 56(4):477-81. 
12. Negroni R. Onychomycosis due to Aspergillus species. Aspergillosis: from diagnosis to prevention. Dordrecht: Springer; 2009. P. 961-71. 
13. Kim DM, Suh MK, Ha GY, Sohng SH. Fingernail onychomycosis due to Aspergillus niger. Ann Dermatol. 2012; 24(4):459-63.
14. Bonifaz A, Cruz-Aguilar P, Ponce RM. Onychomycosis by molds. Report of 78 cases. Eur J Dermatol. 2007; 17(1):70-2. 
15. Barua P, Barua S, Borkakoty B, Mahanta J. Onychomycosis by Scytalidium dimidiatum in green tea leaf pluckers: report of two case. Mycopathologia. 2007; 164(4):193-5.
16. Bontems O, Hauser PM, Monod M. Evaluation of a polymerase chain reaction-restriction fragment length polymorphism assay for dermatophyte and nondermatophyte identification in onychomycosis. Brit J Dermatol. 2009; 161(4):791-6.
17. Zaini F, Mahmoudi M, Mehbod AS, Kordbacheh P, Safara M. Fungal nail infections in Tehran, Iran. Iran J Public Health. 2009; 38(3):46-53.
18. Hashemi S, Gerami M, Zibafar E, Daei M, Moazeni M, Nasrollahi A. Onychomycosis in Tehran: mycological study of 504 patients. Mycoses. 2010; 53(3):251-5. 
19. Moreno G, Arenas R. Other fungi causing onychomycosis. Clin Dermatol. 2010; 28(2):160-3.
20. Falahati M, Ghasemi Z, Farideh Z, Assadi M, Ahmadi F. Identification of the etiological agents of onychomycosis in Tehran (2011-2012). Life Sci J. 2012; 9(4):5469-72.
21. Gupta AK, Drummond-Main C, Cooper EA, Brintnell W, Piraccini BM, Tosti A. Systematic review of nondermatophyte mold onychomycosis: diagnosis, clinical types, epidemiology, and treatment. J Am Acad Dermatol. 2012; 66(3):494-502. 
22. Nouripour-Sisakht S, Mirhendi H, Shidfar MR, Ahmadi B, Rezaei-Matehkolaei A, Geramishoar M, et al. Aspergillus species as emerging causative agents of onychomycosis. J Mycol Med. 2015; 25(2):101-7. 
23. Hubka V, Dobiasova S, Lyskova P, Mallatova N, Chlebkova J, Skorepova M, et al. Auxarthron ostraviense sp. nov., and A. umbrinum associated with non-dermatophytic onychomycosis. Med Mycol. 2013; 51(6):614-24. 
24. Barua P, Mahanta J, Barua N. Onychomycosis in green tea leaf pluckers: a clinicomycological study. Int J Infect Dis. 2012; 16:e319.
25. English MP. Nails and fungi. Br J Dermatol. 1976; 94(6):697-701. 
26. Baghela A, Thungapathra M, Shivaprakash MR, Chakrabarti A. Multilocus microsatellite typing for Rhizopus oryzae. J Med Microbiol. 2010; 59(Pt 12):1449-55. 
27. White TJ, Bruns T, Lee SJ, Taylor J. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. PCR Protocols. 1990; 18(1):315-22.
28. Rudramurthy SM, Shankarnarayan SA, Dogra S, Shaw D, Mushtaq K, Paul RA, et al. Mutation in the squalene epoxidase gene of Trichophyton interdigitale and Trichophyton rubrum associated with allylamine resistance. Antimicrob Agents Chemother. 2018; 62(5):e02522-17. 
29. Salkin IF, Hollick GE, Hurd NJ, Kemna ME. Evaluation of human hair sources for the in vitro hair perforation test. J Clin Microbiol. 1985; 22(6):1048-9.
30. Agarwal A, Agarwal S, Kbanal B. Onychomycosis in eastern Nepal. Nepal Med Coll J. 2006; 8(4):215-9. 
31. Neupane S, Pokhrel DB, Pokhrel BM. Onychomycosis: a clinic-epidemiological study. Nepal Med Coll J. 2009; 11(2):92-5. 
32. Harika DR, Usharani A. A study of onychomycosis in Krishna district of Andhra Pradesh, India. Our Dermatol Online. 2015; 6(4):384-91. 
33. Kaur R, Kashyap B, Bhalla P. Onychomycosis-epidemiology, diagnosis and management. Indian J Med Microbiol. 2008; 26(2):108-16.
34. Tosti A, Piraccini BM, Lorenzi S, Iorizzo M. Treatment of nondermatophyte mold and Candida onychomycosis. Dermatol Clin. 2003; 21(3):491-7. 
35. Tainwala R, Sharma YK. Current clinico-mycological trends of onychomycosis in Pune. Indian J Dermatol. 2012; 57(3):242-3. 
36. Monden Y, Yamamoto S, Yamakawa R, Sunada A, Asari S, Makimura K, et al. First case of fungal keratitis caused by Pestalotiopsis clavispora. Clin Ophthalmol. 2013; 7:2261-4.
37. Hu H, Jeewon R, Zhou D, Zhou T, Hyde KD. Phylogenetic diversity of endophytic Pestalotiopsis species in Pinus armandii and Ribes spp.: evidence from rDNA and β-tubulin gene phylogenies. Fungal Divers. 2007; 24:1-22. 
38. Lee S, Crous PW, Wingfield MJ. Pestalotioid fungi from Restionaceae in the Cape floral kingdom. Stud Mycol. 2006; 55:175-87.
39. Katiar F, Kushwaha RK. Human hair perforating ability of Chrysosporium tropicum strains. Int J Pharm Biol Arch. 2012; 3(5):1260-4. 
40. Shin GH, Park HK, Hur JS, Koh YJ. First report on gray blight of tea plant caused by Pestalotiopsis theae in Korea. Plant Pathol J. 1999; 15(5):308-10.
41. Arzanlou M, Torbati M, Khodaei S, Bakhshi M. Contribution to the knowledge of pestalotioid fungi of Iran. Mycosphere. 2012; 3(5):871-8. 
42. Maharachchikumbura SS, Chukeatirote E, Guo LD, Crous PW, Mckenzie EH, Hyde KD. Pestalotiopsis species associated with Camellia sinensis (tea). Mycotaxon. 2013; 123(1):47-61. 
43. Rabha AJ, Naglot A, Sharma GD, Gogoi HK, Veer V. In vitro evaluation of antagonism of endophytic Colletotrichum gloeosporioides against potent fungal pathogens of Camellia sinensis. Indian J Microbiol. 2014; 54(3):302-9.
44. Barman H, Roy A, Das SK. Evaluation of plant products and antagonistic microbes against grey blight (Pestalotiopsis theae), a devastating pathogen of tea. Afr J Microbiol Res. 2015; 9(18):1263-7. 
45. Kumhar KC, Babu A, Bordoloi M, Benarjee P, Rajbongshi H. Comparative bioefficacy of fungicides and Trichoderma spp. against Pestalotiopsis theae, causing grey blight in tea (Camellia sp.): an in vitro study. Int J Curr Res Biosci Plant Biol. 2016; 3(4):20-7. 
46. Maharachchikumbura SS, Guo LD, Liu ZY, Hyde KD. Pseudopestalotiopsis ignota and Ps. camelliae spp. nov. associated with grey blight disease of tea in China. Mycol Prog. 2016; 15(3):22. 
47. Liu F, Hou L, Raza M, Cai L. Pestalotiopsis and allied genera from Camellia, with description of 11 new species from China. Sci Rep. 2017; 7(1):866-85. 
48. Win PM, Matsumura E, Fukuda K. Diversity of tea endophytic fungi: cultivar-and tissue preferences. Appl Ecol Env Res. 2017; 16(1):677-95. 
49. Ertaș MN, Karakaya A. Pestalotiopsis species causing diseases on tea and kiwifruit plants. Harran J Agric Food Sci. 2018; 22(1):152-68. 
50. Joshi SD, Sanjay R, Baby UI, Mandal AK. Molecular characterization of Pestalotiopsis spp. associated with tea (Camellia sinensis) in southern India using RAPD and ISSR markers. Indian J Biotechnol. 2009; 8:377-83.