Hedgehog Dermatophytosis: Comparison
Please note this is a comparison between Version 2 by Rita Xu and Version 1 by Lucia Kottferová.

Pet hedgehogs, which are increasingly favoured companions, have garnered attention due to their potential as carriers of zoonotic diseases. These small insectivorous mammals, native to Europe, Asia, and Africa, are commonly kept as pets.

  • hedgehog
  • infections
  • Trichophyton erinacei
  • zoonoses

1. Introduction

In recent years, the upsurge in exotic pet ownership has introduced a charming yet intricate dimension to the human‒animal bond. Among unconventional companions, pet hedgehogs have garnered considerable attention. However, sharing our lives with these animals has not been without challenges, particularly concerning the transmission of fungal infections. Trichophyton erinacei, a dermatophytic fungal pathogen, has garnered scientific interest in recent years. Its potential to serve as a zoonotic bridge between these unconventional pets and their human caretakers has raised significant concerns within the veterinary and public health communities. A thorough scientific investigation is necessary to fully understand the complex landscape of zoonotic potential and public health consequences surrounding T. erinacei transmission from pet hedgehogs. Hedgehogs, small nocturnal insectivorous mammals widespread across Europe, Asia, and Africa, comprise sixteen recognised species organised into five genera: Hemiechinus (two species), Atelerix (four species), Erinaceus (four species), Paraechinus (four species), and Mesechinus (two species) [1,2,3,4][1][2][3][4].
Dermatomycosis infections from T. erinacei primarily originate from imported, unprotected white-bellied or African pygmy hedgehogs (Atelerix albiventris) available for purchase in pet shops, as well as Egyptian long-eared hedgehogs (Hemiechinus auritus). Understanding and addressing the potential health implications associated with these hedgehog species in the context of exotic pet ownership are crucial [5].

2. Classification and Taxonomy of the Dermatophytes

Dermatophytes, a group of highly successful pathogenic fungi, are responsible for causing superficial mycoses, commonly referred to as dermatophytosis or ringworm, in both humans and animals. These fungi are taxonomically and ecologically related, belonging to the family Arthrodermataceae within the order Onygenales. What sets them apart is their unique capability to metabolise keratin as their exclusive nutrient source [6,7][6][7]. Traditionally, dermatophytes were classified into three genera: Trichophyton, Epidermophyton, and Microsporum, with their sexual states grouped under Arthroderma [8,9][8][9]. However, recent taxonomic revisions, the elimination of dual nomenclature, and the utilisation of multi-gene phylogenies have expanded the number of genera within the dermatophyte group. Despite these changes, many of the most clinically significant primary pathogenic species still fall within the original three genera [10]. In the newly proposed taxonomy, Trichophyton contains 16 species, namely Epidermophyton (1 species), Nannizzia (9 species), Microsporum (3 species), Lophophyton (1 species), Arthroderma (21 species), and Ctenomyces (1 species), but more detailed studies remain needed to establish species borderlines. Each species now has a single valid name. Two new genera have been introduced: Guarromyces and Paraphyton. The number of genera has increased, but species that are relevant to routine diagnostics now belong to smaller groups, which enhances their identification [8]. One notable taxonomic refinement involves the former entity known as T. mentagrophytes var. erinacei. Smith and Marples first described it in 1963, but it has since undergone a reclassification and is now officially known as Trichophyton erinacei [9]. This reclassification aligns with earlier observations by mycologists who referred to it as the “hedgehog mushroom” [11,12][11][12]. The recognition of T. erinacei as a distinct dermatophyte species dates back to 1966 when Quaife emphasised that it is not a mere variant or subspecies but indeed constitutes a separate species [13]. In the last few decades, dermatophytes have come a long way in their modern systematic classification, which is mostly based on molecular species identification from ITS sequences [13]. The molecular investigations suggest a close genetic or evolutionary relationship between T. erinacei and the Trichophyton anamorph of A. benhamiae. This relationship extends to the teleomorph A. benhamiae. The findings indicate that this close relationship is observed in strains of these fungi found in both the American‒European and African regions [14,15][14][15]. Throughout the years, the aetiological agent of ringworm in hedgehogs has been reported under different names, reflecting evolving species concepts. These names include T. erinacei var. erinacei, T. erinacei, T. mentagrophytes var. erinacei, Arthroderma benhamiae var. erinacei, and A. benhamiae. These taxonomic refinements reflect a comprehensive understanding of the fungal species and their intricate relationships [12,16][12][16].

3. Clinical Signs

3.1. Clinical Signs in Hedgehogs

T. erinacei infections in hedgehogs are characterised by several clinical signs. These signs are essential for recognising and understanding the disease in these animals. Hedgehogs infected with T. erinacei often exhibit crusty lesions on their skin [17]. These lesions can appear as scaly patches or areas of skin with an abnormal texture. Additionally, infected hedgehogs may experience alopecia, which is the loss of fur or spines, as you can see in Figure 1 and Figure 2. These clinical signs are particularly prominent on the head area of the hedgehog or on their back [8,18][8][18].
Figure 1. Crusty lesions, alopecia, and loss of spines in pet hedgehog caused by mycotic infection.
Figure 2. Lesion on the back of an African pygmy hedgehog due to infection by T. erinaceus.
It is important to note that the course of T. erinacei infection in hedgehogs can vary. While some individuals may display noticeable clinical signs, others may experience only mild or even asymptomatic infections. This variability underscores the complexity of the disease in hedgehogs [2,8,19,20][2][8][19][20].

3.2. Clinical Signs in Humans

Trichophyton infections in humans often present with distinctive clinical signs, primarily affecting the skin. One of the most common initial signs is the emergence of itchy and inflamed skin eruptions, often displaying a reddish base at the point where the skin comes into contact with an infected animal. While these symptoms can start off as mild, they tend to intensify over time. Unfortunately, there are instances where the initial rash resembles other inflammatory skin conditions, such as eczema, leading to the improper use of topical or oral corticosteroids. Regrettably, this misdiagnosis can expedite the progression of the infection, making it more severe [21]. Usually, there are single lesions in humans, but several cases have had two or three separate body areas affected. When evaluating skin lesions, particularly on the hands, obtaining a thorough and accurate medical history is crucial. This history should include any recent contact with animals, particularly hedgehogs. In cases where recent animal contact is reported, especially with hedgehogs, maintaining a high level of suspicion is vital for initiating prompt and appropriate treatment. Early recognition of Trichophyton infection and the commencement of antifungal therapy can lead to the timely relief of symptoms and clearance of the infection [22,23,24][22][23][24]. Furthermore, T. erinacei infections in humans can manifest in various ways (Table 1), primarily affecting the skin. Recognising these clinical signs is pivotal for accurate diagnosis and tailored treatment [2]. In human cases, T. erinacei infections frequently result in inflammatory dermatological conditions, with two common presentations being tinea manus and tinea corporis. These infections can cause discomfort and skin abnormalities, including redness, itching, and, in some instances, blister formation [18]. However, T. erinacei does not stop there; it has been identified as the causative agent in a range of other dermatophyte infections, including Tinea faciei, Tinea capitis, and Tinea barbae [21,22][21][22]. These diverse clinical manifestations highlight the critical need for precise species identification and treatments tailored to the specific infection [24,25,26][24][25][26].
Table 1. Clinical presentation in humans after contact with hedgehog infected by T. erinaceus.
Clinical Signs in Humans Region Authors
Tinea corporis Asia [22,[27,2228]][27][28]
Europe [29,30][29][30]
Tinea faciei America [31]
Asia [27,32][27][32]
Europe [28,33,34][28][33][34]
Tinea barbae Europe [25]
Tinea manus America [21]
Asia [26,28,35,36,37][26][28][35][36][37]
Europe [30,38,39,30][38]40,[39]41][[40][41]
Onychomycosis Asia [42]

References

  1. Solari, S.; Baker, R.J. Mammal species of the world: A taxonomic and geographic reference. J. Mammal. 2007, 88, 824–830.
  2. Čmoková, A.; Kolařík, M.; Guillot, J.; Risco-Castillo, V.; Cabañes, F.J.; Nenoff, P.; Hubka, V. Host-driven subspeciation in the hedgehog fungus, Trichophyton erinacei, an emerging cause of human dermatophytosis. Persoonia-Mol. Phylogeny Evol. Fungi 2022, 48, 203–218.
  3. Gräser, Y.; Kuijpers, A.F.A.; Presber, W.; De Hoog, G.S. Molecular taxonomy of Trichophyton mentagrophytes and T. tonsurans. Med. Mycol. 1999, 37, 315–330.
  4. Havlickova, B.; Czaika, V.A.; Friedrich, M. Epidemiological trends in skin mycoses worldwide. Mycoses 2008, 51, 2–15.
  5. Bond, R. Superficial veterinary mycoses. Clin. Dermatol. 2010, 28, 226–236.
  6. Weitzman, I.; Summerbell, R.C. The dermatophytes. Clin. Microbiol. Rev. 1995, 8, 240–259.
  7. Summerbell, R.C. Form and function in the evolution of dermatophytes. Biol. Dermatophytes Other Keratinophilic Fungi 2000, 30–43. Available online: https://www.researchgate.net/publication/228543150_Form_and_function_in_the_evolution_of_dermatophytes (accessed on 19 November 2023).
  8. Donnelly, T.M.; Rush, E.M.; Lackner, P.A. Ringworm in small exotic pets. Semin. Avian Exot. Pet Med. 2000, 9, 82–93.
  9. Marples, M.J.; Smith, J.M.B. The hedgehog as a source of human ringworm. Nature 1960, 188, 867–868.
  10. Heatley, J.J.; Mitchell, M.A.; Tully, T.N. Manual of Exotic Pet Practice; Saunders Elsevier: St. Louis, MO, USA, 2009; pp. 433–455.
  11. de Hoog, G.S.; Dukik, K.; Monod, M.; Packeu, A.; Stubbe, D.; Hendrick, M.; Kupsch, C.; Stielow, J.B.; Freeke, J.; Göker, M.; et al. Toward a Novel Multilocus Phylogenetic Taxonomy for the Dermatophytes. Mycopathologia 2017, 182, 5–31.
  12. Abarca, M.L.; Castellá, G.; Martorell, J.; Cabañes, F.J. Trichophyton erinacei in pet hedgehogs in Spain: Occurrence and revision of its taxonomic status. Med. Mycol. 2017, 55, 164–172.
  13. Quaife, R.A. Human infection due to the hedgehog fungus, Trichophyton mentagrophytes var erinacei. J. Clin. Pathol. 1966, 19, 177–178.
  14. Gräser, Y.; El Fari, M.; Vilgalys, R.; Kuijpers, A.F.A.; De Hoog, G.S.; Presber, W.; Tietz, H.J. Phylogeny and taxonomy of the family Arthrodermataceae (dermatophytes) using sequence analysis of the ribosomal ITS region. Med. Mycol. 1999, 37, 105–114.
  15. Gräser, Y.; Scott, J.; Summerbell, R. The new species concept in dermatophytes-a polyphasic approach. Mycopathologia 2008, 166, 239–256.
  16. Cafarchia, C.; Iatta, R.; Latrofa, M.S.; Gräser, Y.; Otranto, D. Molecular epidemiology, phylogeny, and evolution of dermatophytes. Infect. Genet. Evol. 2013, 20, 336–351.
  17. Jury, C.S.; Lucke, T.W.; Bilsland, D. Trichophyton erinacei: An unusual cause of kerion. Br. J. Dermatol. 1999, 141, 606–607.
  18. Bonifaz, A.; Araiza, J.; de la Cruz, H.V.; Morales-Peña, N.; Treviño-Rangel, R.; González, G.S. 2d Dermatophytosis due to Trichophyton erinacei caused by contact with African hedgehogs as family pets. Med. Mycol. 2022, 60 (Suppl. S1), myac072S62d.
  19. Hui, L.; Choo, K.J.L.; Tan, J.B.X.; Yeo, Y.W. Inflammatory tinea manuum due to Trichophyton erinacei from a hedgehog: A case report and review of the literature. J. Bacteriol. Mycol. 2017, 4, 1057.
  20. Morris, P.; English, M. Transmission and course of Trichophyton erinacei infections in British hedgehogs. Sabouraudia 1973, 11, 42–47.
  21. Walsh, A.L.; Merchan, N.; Harper, C.M. Hedgehog-transmitted Trichophyton erinaceid causing painful bullous tinea manuum. J. Hand Surg. 2021, 46, 430-e1.
  22. Kim, J.; Tsuchihashi, H.; Hiruma, M.; Kano, R.; Ikeda, S. Tinea corporis due to Trichophyton erinacei probably transmitted from a hedgehog the second case report from Japan. Med. Mycol. J. 2018, 59, E77–E79.
  23. Uhrlaß, S.; Verma, S.B.; Gräser, Y.; Rezaei-Matehkolaei, A.; Hatami, M.; Schaller, M.; Nenoff, P. Trichophyton indotineae—An emerging pathogen causing recalcitrant dermatophytoses in India and worldwide—A multidimensional perspective. J. Fungi 2022, 8, 757.
  24. Baert, F.; Lefevere, P.; D’hooge, E.; Stubbe, D.; Packeu, A. A polyphasic approach to classification and identification of species within the Trichophyton benhamiae complex. J. Fungi 2021, 7, 602.
  25. Sidwell, R.U.; Chan, I.; Francis, N.; Bunker, C.B. Trichophyton erinacei kerion barbae from a hedgehog with direct osculatory transfer to another person. Clin. Exp. Dermatol. 2014, 39, 38–40.
  26. Rhee, D.Y.; Kim, M.S.; Chang, S.E.; Lee, M.W.; Choi, J.H.; Moon, K.C.; Choi, J.S. A case of tinea manuum caused by Trichophyton mentagrophytes var. erinacei: The first isolation in Korea. Mycoses 2009, 52, 287–290.
  27. Hsieh, C.W.; Sun, P.L.; Wu, Y.H. Trichophyton erinacei infection from a hedgehog: A case report from Taiwan. Mycopathologia 2010, 170, 417–421.
  28. Masaoodi, N.; Al-Janabi, J. Occurrence, morphological, and molecular characteristics of Trichophyton erinacei in Iraq. Drug Invent. Today 2020, 14, 889–896.
  29. Lysková, P.; Dobiáš, R.; Kuklová, I.; Mallátová, N.; Čmoková, A.; Kolařík, M.; Vojtíšková, V.; Karpetová, L.; Hubka, V. Pět případů lidských dermatofytóz vyvolaných zoofilním druhem Trichophyton erinacei přeneseným z ježků. Čes-Slov. Derm. 2018, 6, 237–243.
  30. Schauder, S.; Kirsch-Nietzki, M.; Wegener, S.; Switzer, E.; Qadripur, S.A. From hedgehogs to men: Zoophilic dermatophytosis caused by Trichophyton erinacei in eight patients. Der Hautarzt 2007, 58, 62–67.
  31. Concha, M.; Nicklas, C.; Balcells, E.; Guzmán, A.M.; Poggi, H.; León, E.; Fich, F. The first case of tinea faciei caused by Trichophyton mentagrophytes var. erinacei isolated in Chile. Int. J. Dermatol 2012, 51, 283–285.
  32. Lee, D.W.; Yang, J.H.; Choi, S.J.; Won, C.H.; Chang, S.E.; Lee, M.W.; Choi, J.H.; Moon, K.C.; Kim, M.N. An unusual clinical presentation of tinea faciei caused by Trichophyton mentagrophytes var. erinacei. Pediatr. Dermatol. 2011, 28, 210–212.
  33. Rivaya, B.; Fernández-Rivas, G.; Cabañes, F.J.; Bielsa, I.; Castellá, G.; Wang, J.H.; Matas, L. Trichophyton erinacei: An emergent pathogen of pediatric dermatophytosis. Rev. Iberoam. Micol. 2020, 37, 94–96.
  34. Kromer, C.; Nenoff, P.; Uhrlaß, S.; Apel, A.; Schön, M.P.; Lippert, U. Trichophyton erinacei transmitted to a pregnant woman from her pet hedgehogs. JAMA Dermatol. 2018, 154, 967–968.
  35. Mochizuki, T.; Takeda, K.; Nakagawa, M.; Kawasaki, M.; Tanabe, H.; Ishizaki, H. The first isolation in Japan of Trichophyton mentagrophytes var. erinacei causing tinea manuum. Int. J. Dermatol. 2005, 44, 765–768.
  36. Choi, E.; Huang, J.; Chew, K.L.; Jaffar, H.; Tan, C. Pustular tinea manuum from Trichophyton erinacei infection. JAAD Case Rep. 2018, 4, 518.
  37. De Brito, M.; Halliday, C.; Dutta, B.; Fanning, E.; Kossard, S.; Curtin, L.; Murrell, D.F. A prickly souvenir from a hedgehog cafe: Tinea manuum secondary to Trichophyton erinacei via international spread. Clin. Exp. Dermatol. 2019, 45, 459–461.
  38. Philpot, C.M.; Bowen, R.G. Hazards from hedgehogs: Two case reports with a survey of the epidemiology of hedgehog ringworm. Clin. Exp. Dermatol. 1992, 17, 156–158.
  39. Kargl, A.; Kosse, B.; Uhrlaß, S.; Koch, D.; Krüger, C.; Eckert, K.; Nenoff, P. Hedgehog fungi in a dermatological office in Munich: Case reports and review. Der Hautarzt 2018, 69, 576–585.
  40. Weishaupt, J.; Kolb-Mäurer, A.; Lempert, S.; Nenoff, P.; Uhrlaß, S.; Hamm, H.; Goebeler, M. A different kind of hedgehog pathway: Tinea manus due to Trichophyton erinacei transmitted by an African pygmy hedgehog (Atelerix albiventris). Mycoses 2014, 57, 125–127.
  41. Perrier, P.; Monod, M. Tinea manuum caused by Trichophyton erinacei: First report in Switzerland. Int. J. Dermatol. 2015, 54, 959–960.
  42. Phaitoonwattanakij, S.; Leeyaphan, C.; Bunyaratavej, S.; Chinhiran, K. Trichophyton erinacei onychomycosis: The first to evidence a proximal subungual onychomycosis pattern. Case Rep. Dermatol. 2019, 11, 198–203.
More
Video Production Service