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Mycotic infections in animals in India: An update
*Corresponding author: Harish Chander Gugnani Department of Microbiology, Vallabhbhai Patel Chest Institute, University of Delhi, Benito Juarez Marg, South Campus, South Moti Bagh, New Delhi, Delhi-110021, India harish.gugnani@gmail.com
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Received: ,
Accepted: ,
How to cite this article: Gugnani HC. Mycotic infections in animals in India: An update. Res Vet Sci Med 2021;1:2.
Abstract
This review traces the early records of mycotic infections in India, and presents an update of animal mycoses reported from several parts of India. The types of mycoses covered are the dermatophytosis (ringworm) in domestic animals due to well-known species of zoophilic dermatophytes, viz. Trichophyton simii, T. mentagrophytes, T. verrucosum, Microsporum canis and M. nanum, and the geophilic dermatophyte, M. gypseum, Aspergillus spp, Cryptococcus species and other yeast like fungi, histoplasma and blastomyces. The brief clinical and demographic features of infections in different animals are described. A particularly noteworthy finding in literature search is the report of clinical infections in one dog and two cows by an anthropophilic dermatophyte, T. rubrum from Belgachia, Kolkata, West Bengal in 1954. Veterinary scientists are urged to investigate the possible occurrence of infections in animals due to other pathogenic fungi including the dimorphic ones like Histoplasma and Blastomyces.
Keywords
Zoophilic dermatophytes
Mycoses in animals
India
Update
INTRODUCTION
The first record of animal mycotic infection confirmed by fungus culture in India was by Witkamp in 1924[1] when he isolated a fungus from ulcerated cutaneous lesions in horses and named it as Hyphomyces destruens. The organism was later named as Pythium insidiosum, and the disease called pythiosis by De Cock et al. in 1987.[2] No subsequent report of this disease in animals in India could be traced in the literature. The first authentic description of an animal mycosis with definite etiology in India was by Weldman in 1925[3] from a case of exfoliative dermatitis in the Indian Rhinoceros (Rhinoceros unicornis) by a yeast Mallesezia (Pityrosporum), the species involved was described to be a new species, Mallesezia patchydermatitis. Malassezia (Pityrosporum) species are lipophilic yeasts that are members of the normal mycobiota of the skin and mucosal sites of a variety of homeothermic animals. Mallesezia are yeasts in the fungal class Basidiomycetes, which also includes Cryptococcus spp, Rhodotorula spp and Trichosporon spp that can produce disease in man and animals; Cryptococcus spp are quite often involved in disseminated infections in immunosuppressed patients, and occasionally in animals. Malassezia yeasts are associated mainly with certain skin diseases and have been isolated from almost all domestic animals, wild animals, and also from wildlife.[4] M. patchydermatitis is of animal origin and zoonotic transfer of this species has been documented from dogs to neonates by healthcare workers who are owners of dogs.[5] Another yeast, Candida pseudotropicalis was found to cause abortion in mares.[6] The earliest record of animal ringworm in India was by Pinoy[7] of Trichophyton (Epidermophyton) simii in a monkey imported in France from India. The first record of epizootic lymphangitis in horses caused by Histoplasma capsulatum var. farcinimosum in India was by Kapur.[8] Later Mohan et al.[9] reported an outbreak of enzootic lymphangitis in equines. Among the animal mycoses, dermatophytosis (ringworm) of several animals, viz. cattle, buffaloes, dogs, sheep, goats and poultry can be a potential source of infections in humans, sometimes causing widespread inflammatory lesions. An earlier review by Monga and Mohapatra[10] dealt with compilation of reports of mycoses in animals published up to 1980. This review presents an update of the fungal infections in animals in India reported so far. Salient clinical feature of infections caused by different species of fungi are described.
Search criteria
This review conducted an electronic (computerized) search of existing literature using the Google search engine and PubMed electronic database to identify and download relevant publications in different types of animal mycoses in India. The key words used were dermatophytosis, ringworm, aspergillosis, in livestock, domestic animals, and poultry The Boolean operator ‘AND’ was used to combine and narrow the searches. Additional information was obtained by searching the medical libraries for journals not listed in the database. The information relevant to the review was extracted from the available publications and incorporated in this review.
Literature review
Trichophyton species
The zoophilic Trichophyton species include T.simii, T. mentagrophytes, T. verrucosum and T.interdigitale as described by de Hoog et al.[11] Trichophyton simii is primarily a zoophilic dermatophyte that very frequently causes clinical infections in man and also occurs as a saprobe in soil. The first record of animal dermatophytosis (ringworm) due to T. simii in India was by Pinoy[7] in a monkey imported in France from India. Stockdale in 1965[12] identified 31 strains of an unidentified dermatophyte recovered from monkeys, poultry, a dog and a man sent from College of Veterinary Science and Animal Husbandry, Mathura (UP). T. mentagrophytes is primarily a zoophilic dermatophyte that frequently infects humans and may also survive in soil (https://www.sciencedirect/com . > topics > trichophyton - mentagrophytes). T. mentagrophytes infects number of wild and domestic animals, including baboons, buffaloes, cattle, sheep, goats, swine, dogs, cats, tigers, foxes guinea pigs, horses, chimpanzees, monkeys, chickens, rodents, mice and other laboratory animals, e.g., rabbits, rats.[13,14,15,16,17,18] According to Hubka,[19] Trichophyton interdigitale comprises human and zoophilic strains. Currently the predominant dermatophytes recovered from human ringworm lesions in India are T. rubrum and T. interdigitale.[20] Clinical infections in animals due to T. interdigitale are not yet recorded. The dermatophyte, T. verrucosum causes clinical infections in all ruminants, brief features of such infections in cattle and buffaloes in India are described in this review. Sometimes these animals may be asymptomatic carriers. T. verrucosum is the most common cause of ringworm in calves (https://www.sciencedirect/com. > topics > trichophyton-verrucosum). The brief clinical and demographic features of infections caused by the zoophilic Trichophyton species in India are described in Table 1. Diagnosis in all the cases was made by direct microscopy and recovery of the causative Trichophyton species in culture.
| Reference | Location | No. of animals infected with clinical lesions | Lesions/Sites infected | Total (percent) positiv | |
|---|---|---|---|---|---|
| Trichophyton simii | |||||
| Stockdale et al. 1965[12] | Mathura (UP) | One monkey | Not known | Not applicable | |
| Gugnani and Randhawa 1973[15] | Delhi | 70 poultry birds infected with T. simiiout of flock of 250 examined 7 birds in one additional and 2 birds in two other poultry farms | Comb, wattle and basal portion of the flank feathers. In 8 of the birds, entire combs were heavily infected, with scaly and erythematous lesion, appearing ragged | 70/250(28) | |
| Gugnani et al. 1973[17] | Hisar (Haryana) | 3 poultry birds with T. simii | Scaly erythematous lesions on flank feathers | Could not be determine | |
| Gugnani et al. 1973[17] | Meerut (Uttar Pradesh) |
3 poultry birds with T. simii | Scaly erythematous lesions on flank feathers | Could not be determine | |
| Gupta et al. 1969[21] | Hisar (Haryana) | 1 dog with T. simii | Could not be determine | ||
| Mohapatra and Mahajan 1970[22] | Delhi | 2 dogs with T. simii | Circular lesions on the nose and upper lip | Could not be determined | |
| Ranganathan et al.[23] | Chennai/India | Two of 89 dogs with T. simii | ? | 211–2(0.95) | |
| Mitra 1998[24] | Several locations in Uttar Pradesh | One of 22 cattle T. simi- | ? | 22–1(4.5) | |
| Trichophyton mentagrophytes | |||||
| Mohapatra et al. 1964[25] | An animal house in AIIMS, New Delhi |
Four guinea pigs and one rabbit | Scaly erythematous lesions on flanks | Could not be determined | |
| Gupta et al. 1970[21] | Agriculture University campus, Hisar | Pigs 8 | Not known | Could not be determined | |
| Mitra 1998[23] | Uttar Pradesh | Cattle 1 of 22 | Not known | Could not be determined | |
| Debnath et al. 2016[26] | Companion animals in a private farm, Kolkata (W.B) | Dogs 49 out of 248 and cats 14 out of 103 | Animals sampled were without lesions | 49/248(19.76) 14/103(13.59) |
|
| Parmar et al. 2018[27] | Anand, Gujrat | Cattle 5 out of 52, Buffaloes 2 out of 52 | Small raised, circumscribed. grayish-white crusted alopecic lesions on body | 5/52(9.62) 2/52(3.85) |
|
| Trichophyton verrucosum | |||||
| Parmar et al. 2018[27] | Anand, Gujrat | Cattle 12 out of 52, Buffaloes 5 out of 22 |
Small raised, circumscribed. grayish-white crusted alopecic lesions on body | 12/52(23.08) 5/22(22.73) |
|
| Trichophyton rubrum | |||||
| Chakraborty et al. 1954[28] | Bengal Veterinary College & Hospital, Belgachia, Kolkata (West Bengal) |
Dog 1 Cows 2 |
Scaly, moist, partially alopecic, itching lesions on the buttocks and the trunk dorsal to the front legs. The first one had small raised plaques covered with scabs, on the head, on the muzzle and on the side of nostril. The second cow was covered with ringworm-like lesions all over the body. |
? ? |
|
| Mitra 1998[23] | Uttar Pradesh | One out of 22 cattle | Not known | Could not be determined | |
| Reference | Location | No. of animals infected with clinical lesions | Lesions/Sites infected | Total (percent) positive |
|---|---|---|---|---|
| Microsporum canis | ||||
| Pal 2001[32] | Anand, Gujarat | Goat-1, seven-year-old female | Dermatophytosis Irregular, diffuse, scaly , alopecic, yellowish-gray, crusted lesions on the face and pinna | NA |
| Debnath et al. 2015[33] | Companion animals in a private farm, Kolkata (W.B) | Dogs 108 out of 248, Cats 57 out of 103 |
Animals sampled were without lesions | 108/248(43.55) 57/103(55.34) |
| Parmar et al. 2018[34] | Anand, Gujarat | Dogs 6 | Lesions similar to that in cattle and buffalo |
6/18(33.3) |
| Microsporum gypseum | ||||
| Debnath et al. 2015[33] | Companion animals in a private farm, Kolkata (W.B) | Dogs 91 out of 248, Cats 32 out of 103 | Animals sampled were without lesions | 91/248(36.9) 32/103(34.35) |
Abbreviation: NA-Not applicable
| Reference | Location | Bird species and no. of infected | Types of lesions | Diagnosis | Total (%) positive | |
|---|---|---|---|---|---|---|
| Khan et al. 1977[37] | Zoological Park, Delhi | Imported Penguins - 7 out of 10 | Persistent dullness, anorexia, and abnormal movements of the neck. Gross pathology showed enlarged liver with calcified nodules, greyish white nodules of varying size in the lungs; with thickening of serous membrane. | Histopathology and recovery of Aspergillus fumigatusfrom fibrino-caseous deposits | 7/8(87.5) | |
| Pal 1983[38] | A buffalo (Bubalus bubalis) calf | Keratomycosis | A. fumigatus | Could not be determined | ||
| Pal 1988[39] | Anand, Gujrat, College of Vet. Science | A 9-year-old buffalo (Bubalus bubalis) aborted at 7 months of gestation | Culture of A. nigerfrom the liver, lung, lung and aborted fetus. The fungus and by demonstration of the fungus in KOH mounts of the placental tissues, skin, lung and liver | Could not be determined | ||
| Pal M 1992[40] | Anand Gujrat | A young pigeon (Columbia livia) kept by a bird fancier | Disseminated Aspergillosis | Demonstration of branched septate hyphae, characteristic of Aspergillus in tissue sections and Aspergillus terreusconidiophores in squeeze preparation of air sacs | Could not be determined | |
| Singh 1994[41] | Ludhiana, Punjab Agricultural University | Japanese Quail. (Coturnix japonica). The bird died | Mycotic salpingitis. Necropsy revealed white to grayish 2–5 mm nodules on the setosal surface of the oviduct and the muscular wall of the oviduct. | Histopathology and culture of Aspergillusflavus | Could not be determined Could not be determined |
|
| Singh et al. 2009[42] | Jaipur, Rajasthan | Turkey poults. 85 of 120 brooding poults aged 3 days had ruffled feathers, gasping, nasal discharge and trembling. Mortality 65 (76.47) | Ruffled feathers, gasping, nasal discharge and trembling. Mortality 65(76.47) | Histopathology and culture of A. fumigatus | 85/120(70.8) | |
| Shukla 2012[43] | Mhow, Indore (M.P.) Local Emu farm | Emu (Dromaius novahollandiae) 11 out of 146 Emu chicks infected in an outbreak died | History of respiratory symptoms and mild nervous signs | Histopathology and recovery of A. fumigatusin culture | 1/146(0.68) | |
| Brathisdasan et al. 2013[44] |
Izatnagar (U.P.) | Angioinvasive pulmonary aspergillosis in a Himalayan Griffin vulture (Gyps Himalyensis) | Weakness, emaciation, dyspnea, incoordination, and inability to fly, the bird, succumbing to the illness. | Gross pathological examination revealed several yellowish circumscribed, raised, miliary nodules on the surface of the lungs, air sac membranes, trachea, pericardium, aorta, pulmonary artery and kidneys. Diagnosis was based on histopathology and culture of A. fumigatuslungs and air sacs of the bird. | Could not be determined | |
| Singh and Mahajan 2016[45] | Hisar, Bhivani, Jind, Sirsa and Fatehabad, Haryana | Four outbreaks in poultry of different age groups: 0–7 days old – 20 with 4.42% morbidity and 2–89% mortality, 8–14 days with 9.49% morbidity and 6–36% mortality 15–21-day old–13 with 7.4% morbidity and 5.29% mortality, > 21 days – 7 with 3.7% morbidity and 2.23% mortality |
On gross pathology examination, pin-head sized yellowish nodules were observed on the lungs and air sac | Demonstration of characteristic septate hyphae in PAS- stained tissue sections of lungs, and recovery of A. fumigatus in culture. |
||
| Ahmad DB et al. 2018[46] | Thanjavur, Tamil Nadu | Of the 200 desi chickens 40(20%) had systemic aspergillosis with symptoms of anorexia, whitish droppings, dullness, difficulty in respiration. 5(12.5%) died. | 40/200(20%) | |||
Abbreviation: NA-Not applicable
| Reference | Location | Animal species and no infected | Types of infection/lesions | Diagnosis | Total (%) positive |
|---|---|---|---|---|---|
| Cryyptococcus neoformans | |||||
| Singh et al. 2007[54] | Bamboo thicket, Jabalpur (M.P.) | Bandicoot rat (Bandicota indica)-2 healthy male rats | Discrete, soft, confluent, elevated lesions in the lung, (some caseated) observed on dissection of the euthanized rats | Demonstration of encapsulated yeast cells in direct microscopy of lungs, liver, kidney and spleen and isolation of C. neoformansvar, grubiifrom these organs | Not known |
| Singh et al 2020[55] | Kolkata, West Bengal | An 8-month-old adopted stray bitch | Anorexia, depression, urinary incontinence, dysuria for 10 days, emaciated; was dehydrated and had sunken eyes, ocular and nasal discharge and had fever (103°F). Physical examination showed distended urinary bladder and abdominal pain. Blood profile revealed low hemoglobin, leucocytosis, neutrophilia, and lymphopenia. |
Demonstration of budding yeast cells in urine and isolation of C. neoformansconfirmed by sequencing the ITS region of rRNA | Not known |
| Candida species | |||||
| Sikdar et al. 1972[6] | Kolkata, West Bengal | Mares (13) in outbreak of abortion | Not described | Demonstration of yeast cells in placenta and fetal organs by histopathology and culture of Candida pseudotropicalis |
Not known |
| Kumar and James 2012[56] | Nammakal, Kerala | Cattle, out of 21 samples of milk from suspected cases of mastitis, yielded I each of Rhodotorula mucilaginosa. Torulopsissp, Saccharomyces cerevisae, Candida guillermondii, 2 of C . parapsilosis, 3 of Trichospsoron cutaneum, 4 of Geotrichum candidum, 7 of Candida tropicalis | Lesions not described | Isolation of causative agents from centrifuged deposits of mil samples | 18/21 (85.7%) |
| Jadhav and Pal, 2013[57] | Out of 69 dogs, seven had clinical infection, 1 - otitis, stomatitis - 4, dermatitis - 2. Out of 21 buffaloes, 5 - otitis, 1 - stomatitis, 1 - mastitis |
4 dogs and I buffalo with stomatitis had symptoms of salivation, halitosis and anorexia. Details of clinical features in cases of mastitis not mentioned. |
Demonstration of Candida in. skin scrapings and pus swabs and isolation of C. albicansin culture in cases of stomatitis. In cases of mastitis, demonstration of Candida in centrifuged deposits of milk samples and recovery of C. albicans. | Dogs 7/69 (12.5%) Buffaloes 8/21 (38.0) |
|
| Weldman 1925[2] | Single horned India Rhinoceros (Rhinoceros unicornis)-1 | Not known | Exfoliative dermatitis | Culture of Mallesezia patchydermatitis, (described as a new species) from skin lesions | Not known |
| Reddy and Kumari 2015[58] | Tirupati, Andhra Pradesh India | Recurrent pyoderma with Malassezia and hyperadrenocorticism in a dog. | Not known | Not known | Not known |
| Reddy and Sivajothi 215[59] | Tirupati, Andhra Pradesh India | An adult dog | Chronic discolored pruritic lesions with rancid odor on the ventral chin, neck, abdomen and inner surface of the legs | Demonstration of yeast cells of M. patchydermatitisin smears of the skin scrapings and hair from the lesions |
Not known |
| Rasamala and Kumar, 2018[60] | Kerala (India) | Dogs.- P. patchydermatitis associated with 6.6% of dogs with dermatitis, 4–4% of dogs with pyoderma, 2% of dogs with dermatophytosis. Pigs - 2% |
Skin lesions, details of clinical features not known | Isolation of P. patchydermatitis from the skin scrapings of the lesions | Not known |
| Gangna et al. 2021[61] |
Thrissur, Kerala (India) | Dogs 15 with dermatitis and 10 with otitis | Dogs with dermatitis showed primary and secondary scaly skin lesions with erythematous papules, alopecia, crusts, pruritis excoriations, and hyperkeratosis. The clinical signs in dogs with otitis were excessive discharge from ears with offensive odor. |
Recovery of M. patchydermatitisfrom the ear swabs of cases of otitis, and skin scrapings of the lesions in cases of dermatitis. | |
Histoplasma and Blastomyces species
Histoplasmosis, a non-contagious fungal disease caused by a thermally dimorphic, histoplasma capsulatum is found worldwide. Infection is acquired by inhalation of the hyphal elements and microconidia of the fungus from old avian excreta or bat guano, which reach the alveoli followed by rapid conversion to yeast form that can persist and spread in the body through the blood stream and lymphatics causing disseminated disease [Wheat et al. 2016,[62] Gugnani et al. 2018[63]]. Infection has been described in several species of small mammals including wild rats and opossum. The disease is uncommon or rarely detected in dogs and cats. Demonstration of histoplasmosis in the animals helps to establish the endemicity of the disease in a given area.[62] There is no report of Histoplasma from small mammals in India. Singh published his study of clinical cases in 1966[64] but the clinical details of the lesions are not available, nor were there in the report of equine mycotic respiratory disease by Ramachandran in 1995[65]; all attempts to locate clinical features of the cases described in the reports by an exhaustive search of the literature in different search engines were unsuccessful.
Blastomycosis, a serious fungal disease caused by a thermally dimorphic fungus, Blatomyces dermatidis, affects dogs, humans and occasionally other mammals with a restricted geographic distribution. It is primarily a canine disease with approximately 10 dogs for every human case (Schwartz, 2018).[66] Blastomycosis is acquired primarily through inhalation of airborne conidia of Blastomyces species that are liberated from the mold phase of the fungus, which is associated with moist, acidic, sandy soils enriched with decaying organic matter and animal droppings (Restrepo et al. 2000).[67] Dogs develop the disease more rapidly than humans. Most dogs get infected by inhaling spores of B. dermatitiids from soil and organic debris. Detection of blastomycosis in dogs is a sentinel of possible occurrence of human cases of this disease.[67] There is one reported case of canine blastomycosis from India in a Mongrel dog, found dead in Indian Veterinary Research Institute Campus, Izatnagar, Bareilly (Uttar Pradesh) by Iyer, 1982.[68] Infection was diagnosed by histopathological demonstration of thick-walled, broad-based yeast cells typical of B. dermatitidis in tissue sections of necropsied lung lesions.[68] Other animals including cats are very less commonly affected. No case of blastomycosis in cats or other animals in India could be traced in the literature search.
DISCUSSION
The present review of literature updates our knowledge on the different type of mycoses in domestic animals and poultry in India caused by zoophilic dermatophytes, Aspergillus species, and yeast-like fungi. The salient clinical and demographic features of infections in several parts of India caused by different species of fungi are aptly described. An unusual observation in the literature review was the report of Trichophyton rubrum infection in one dog and two cows from Belgachia, Kolkata, West Bengal,[26] this being the first record of animal infections due to T. rubrum in the world at that time. Also noteworthy is the report of cryptococcosis due to C. neoformans var. grubii in a bandicoot rat,[52] constituting the first record of this disease in a bandicoot rat. Another notable observation in our literature search is the detection of a canine case of blastomycosis in Uttar Pradesh.[67] Surveillance for more canine cases in other parts of India may facilitate detection of endemic foci of B. dermatitidis in the country. It is worth mentioning here about a case of tinea faciens due to Microsporum canis in a goat handler reported by Pal in 2001.[31] Thus, it is suggested that dairy and veterinary scientists should investigate occurrence of fungal infections in animal handlers and their contacts in the livestock farms under their care.
CONCLUSION
This review of animal infections describes the early records of mycotic infections in India, and gives many insights updating our knowledge on this topic. Reports on the prevalence of Trichophyton simii infection in animals in different parts of India covered in this review establish the endemicity of this infection in animals in India. A noteworthy finding in literature search is the report of clinical infections in one dog and two cows by an anthropophilic dermatophyte, T. rubrum from Belgachia, Kolkata, West Bengal in 1954. By tracing many publications on dermatophytosis, aspergillosis, and infections due to yeast-like fungi in domestic animals and poultry, this review has given a true picture of the prevalence of these mycoses in different parts of India. Dairy and veterinary scientists should look for transmission of fungal infection from livestock to animal handlers and their contacts. Investigation of the possible occurrence of fungal infections due to other fungi including the dimorphic fungal pathogens e.g. Histoplasma and Blastomyces in animals in India is also suggested.
Declaration of patient consent
Patient’s consent not required as there are no patients in this study.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
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