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Abstract
Zoonotic
fungi can be naturally transmitted between animals and humans, and in
some cases cause significant public health problems. A number of mycoses
associated with zoonotic transmission are among the group of the most
common fungal diseases, worldwide. It is, however, notable that some
fungal diseases with zoonotic potential have lacked adequate attention
in international public health efforts, leading to insufficient
attention on their preventive strategies. This review aims to highlight
some mycoses whose zoonotic potential received less attention, including
infections caused by Talaromyces (Penicillium) marneffei, Lacazia loboi, Emmonsia spp., Basidiobolus ranarum, Conidiobolus spp. and Paracoccidioides brasiliensis.
Keywords
- Animal;
- fungi;
- human;
- mycoses;
- neglected;
- zoonoses
Introduction
Depending
on the source of infections, zoonoses are described as infectious
diseases that can be naturally transmitted between vertebrate animals
and man [1]. The causative agent may be a bacterium, a virus, an ectoparasite, a helminth, a protozoa, or a fungus [2].
An animal can be either reservoir or mechanical vector of zoonotic
pathogens, therefore the transmission may be direct or indirect [3].
In most cases, many wild and domesticated animals (including their
faeces and soil in their burrows) play an essential role in maintaining
the infection in nature and contribute in varying degrees to the
distribution and actual transmission of infection in human and animal
populations [4]. Although zoonotic agents can be transmitted from an infected host to others, inter-human transfer is uncommon.
From
a global prospective, zoonotic infections have been recognized for many
centuries, and account for the majority of emerging and re-emerging
infectious diseases, worldwide [5] and [6].
It has been shown that zoonoses occur due to increased contact between
humans and animals as a by-product of development, industrialization and
encroachment on wildlife habitats, resulting in a dynamic upward
trajectory of these diseases [7].
Fungal infections associated with zoonotic and or sapronotic transmission are an important public health problem worldwide [8]. A number of these infections are among the group of the most common fungal diseases, such as: dermatophytosis [9], sporotrichosis [10] and [11] and histoplasmosis [12].
Within this context, it is however notable that some fungal diseases
with zoonotic potential have lacked adequate attention in international
public health efforts, leading to insufficient attention on their
preventive strategies.
In
this paper, we provide an overview of neglected fungal pathogens that
could be carried and transmitted between vertebrate animals and people.
Their aetiological agents, ecology and geographical distribution,
current epidemiology, type of diseases in humans and animals, source of
infection and mode of transmission will be discussed.
Fungal zoonoses versus sapronoses
From an evolutionary viewpoint, mycotic infectious agents can be either true pathogens or opportunists [13],
and from the same perspective pathogens can be divided into
environmental pathogens (having a saprobic but infectious phase in the
environment) and obligatory pathogens (having host-to-host
transmission). Systemic environmental pathogenic fungi may produce
invasive forms in infected tissue, such as the spherule in Coccidioides or intracellular yeast in Histoplasma [12].
Nearly all fungi are able to thrive in the environment for extended
periods, but pathogens have an evolutionary advantage of the use of a
vertebrate vector during a part of their life cycle. Often an animal
other than humans is the prime target of the fungus, with humans as
non-optimal hosts. Infections originating from an animal are termed
zoonoses [1].
The clinical course of systemic pathogens can be fatal in hosts with
severe impairment of acquired immunity, but in healthy hosts the
infection is often relatively mild.
In contrast, opportunistic fungi have a preferred habitat independent from the living hosts [13].
Factors enabling survival in human tissue are purely coincidental.
Infections may nevertheless occur repeatedly from a single source, and
we then speak of sapronoses [14].
Infection of the non-preferred human host decreases fitness of the
fungus. The fungus is poorly adapted to this unexpected habitat and
therefore may provoke a strongly inflammatory response, which in
patients with severe impairment of their innate cellular immunity may be
fatal.
Table 1
shows the list of clinically significant fungi with zoonotic potential
that can cause considerable medical, veterinary and/or public health
problems. Some of these fungi and corresponding infections have been
extensively investigated in the literature [8], [9], [10], [11], [12], [15], [16] and [17]. Here we discuss the fungal pathogens whose zoonotic potential is neglected, including: Talaromyces (Penicillium) marneffei, Lacazia loboi, Emmonsia spp., Conidiobolus spp., Basidiobolus ranarum and Paracoccidioides brasiliensis.
Aetiological agent Disease Known distribution Probable means of transmission to humans Target animals Clinical signs of disease in animals Clinical signs of disease in human Microsporum spp., Trichophyton spp. Dermatophytosis Worldwide Direct contact with infected animals or material All domesticated mammals and sometimes wildlife Classical ring lesion with central healing and crusts at the peripheral area, some degree of folliculitis Tinea capitis, Tinea barbae, Tinea faciei, Tinea corporis, Tinea cruris, Tinea ungium, Tinea pedis, Tinea manum, Tinea Sporothrix schenckii
Sporothix brasiliensisSporotrichosis Worldwide Work-related trauma, scratches or bites from animals Cats; occasionally dogs, horse, cow, camel, dolphin, goat, mule, bird, pig, rat, armadillo Localized cutaneous, lymphocutaneous and disseminated infection Fixed cutaneous, lymphocutaneous, osteoarticular and disseminated infection Mallasezia spp. Malassezia infection (pityriasis) Worldwide Malassezia yeasts are commensal of human skin (part of the normal microbiota) Domestic animals such as dogs, cats, cows, sheep, pig, horse, wild animals held in captivity, and animals from wildlife Dermatitis, alopecia, stenosis, otitis externa Chronic superficial disease of the skin (pityriasis versicolor), folliculitis, seborrhoeic dermatitis and dandruff, fungaemia Cryptococcus neoformans, Cryptococcus gattii Cryptococcosis Worldwide Mainly by inhalation od fungus, occasionally through breaks in the skin Wide variety of mammals, birds, reptiles and amphibians Focal or disseminated infection, affecting a single organ system or many, central nervous system involvement Cutaneous, ocular, pulmonary and central nervous system involvement Penicillium (Talaromyces) marneffei Penicilliosis Southern China and South-East Asia Unknown Bamboo rats, domestic animals such as dogs, cats Skin dermatitidis, rhinitis, otitis externa and disseminated infection Non-specific clinical signs (generalized lymphadenopathy, molluscum contagiosum-like lesions of the skin and mucosa) and disseminated infection Lacazia loboi Lobomycosis South and Central America, United States, Canada, Europe, South Africa Trauma Dolphins Granulomatous dermatitis Granulomatous dermatitis Emmonsia spp. Adiaspiromycosis Case reports from Asia, Australia, Europe, North America Inhalation of the fungus Wild rodents Deep mycoses Lung and disseminated disease Conidiobolus coronatus, Conidiobolus incongruus, Basidiobolus ranarum Entomophthoromycosis Tropical countries of Africa, Asia, United States and Europe Traumatic implantation or inhalation of the fungus Horses, dogs, sheep Cutaneous and disseminated infection Chronic subcutaneous and invasive infection Histoplasma capsulatum Histoplasmosis Worldwide (endemic in Mississippi and Ohio River valleys in USA) Inhalation of the fungus Cattle, sheep, horses Non-specific signs (chronic gastrointestinal infection) and disseminated infection Chronic progressive lung disease, chronic cutaneous or systemic disease or an acute fulminating fatal systemic disease Coccidioides immitis, Coccidioides posadasii Coccidioidomycosis Southwestern USA, northern Mexico, Central and South America Inhalation of arthroconidia and skin trauma Dogs, llamas, non-human primates, cats, horses, domesticated or wild mammals, snakes Asymptomatic to severe and fatal infection Cutaneous, pulmonary, disseminated infection Paracoccidioides brasiliensis, Paracoccidioides lutzii Paracoccidioidomycosis South America Inhalation of the fungus, injuries of the skin and mucosal membranes Dogs, domesticated and wild animals (armadillos and monkeys) Non-specific clinical signs depending on the organ involved (lymphadenomegaly, apathy, and hepatosplenomegaly) Mucocutaneous, pulmonary or disseminated infection Blastomyces dermatitidis Blastomycosis Worldwide (endemic in North American continent, autochthonous in Africa, South America and Asia Inhalation of airborne conidia Dogs, cats, horses, marine mammals Cutaneous, pulmonary, systemic infection Cutaneous, pulmonary, disseminated infection (granulomatous and suppurative lesions in lung, skin and bones) Pneumocystis carinii (mammals), Pneumocystis jirovecii (Human) Pneumocystosis Worldwide Inhalation of airborne conidia Rodents, dogs, cats, cattle Lethal pneumonia in immune debilitated animals Asymptomatic, interstitial pneumonia, progressive pneumonia (in immunocompromised hosts)
Penicilliosis
Penicilliosis is caused by the emerging pathogenic fungus Penicillium marneffei
that usually causes a fatal disseminated disease in immunocompromised
individuals, especially those with human immunodeficiency virus (HIV)
infection [18]. Penicillium marneffei is a dimorphic fungus exhibiting a mycelial form at 25°C and a yeast form at 37°C. Upon tissue invasion, P. marneffei undergoes a morphological phase transition from saprobic mould to yeast form that capably evades the host immune system [19]. For phylogenetic reasons the fungus was renamed as Talaromyces marneffei, underlining its remote distance to saprobic Penicillium species [20] and [21].
Ecology and source of infection
The fungus may have a natural habitat in soil in areas of southern China and South-East Asia where it is endemic [18] and [22]. Talaromyces marneffei was originally isolated from the bamboo rat, Rhizomys sinensis, in 1956 [19]. Since then, additional studies demonstrated that three other bamboo rat species may act as reservoirs: Rhizomys pruinosus, Rhizomys sumatrensis and the reddish-brown subspecies of Cannomys badius. Within these rodent species, the prevalence of infection varies widely across South-East Asia [23] and [24]. In addition, more recently, dogs have been suggested as a possible reservoir for T. marneffei [25].
Epidemiology in humans
The infection is recognized as an AIDS-defining opportunistic infection [26] and [27]
in regions where the fungus is endemic. In Thailand Chiang Mai
province, it is the third most common HIV-related opportunistic
infection (after tuberculosis and cryptococcosis) [18], [27] and [28]. Penicilliosis affects all ages and both sexes, although 90% of the cases reported in the literature are male [29].
Notably, the risk of infection is not restricted to those living in
areas where it is endemic. HIV-infected individuals who travelled to
areas of endemicity have also become infected by T. marneffei [30]. Of note, the mortality rate of untreated T. marneffei infections in HIV-infected patients is 100% [31].
Disease in humans
In
patients who are not immunocompromised, most cases of penicilliosis
show generalized lymphadenopathy, fever, weight loss, anaemia and a
non-productive cough, which may strongly resemble histoplasmosis,
cryptococcosis and tuberculosis [32].
In HIV-infected patients, the disease is usually disseminated,
affecting skin, reticuloendothelial system, lung and gut. Other tissues
can be involved in the disease such as liver, spleen, skin and mucosa,
which are the most commonly affected tissues. In contrast to
histoplasmosis and tuberculosis, adrenal involvement and central nervous
system infections are uncommon. The molluscum contagiosum-like lesions
of skin and mucosa indicate disseminated disease [29].
Most patients acquire skin lesions on the face and neck. Chest
radiographs show patchy infiltration and sometimes abscess formation.
Disease in animals
Penicilliosis is a rare infection in domestic animals such as dogs and cats [25]. Clinical signs of infection include skin dermatitis, rhinitis and otitis externa [33].
Symptomatic animals have nasal discharge and ulceration of external
nares and epistaxis. However, up to 40% of seemingly normal dogs will
have a nasal swab positive for T. marneffei on culture [25]. In addition, disseminated infections have been reported in dogs, with peripheral lymphadenopathy [34] and bronchopneumonia [35]. No clinical signs have been reported in naturally infected bamboo rats [20].
The prevalence of infection varies widely across South-East Asia,
suggesting that there are regional variations in the endemicity of
infection or there are geographical variations in the predisposition to
infection within different species of bamboo rats [18].
Mode of transmission
A lot is still unknown about the natural reservoir and route of transmission of T. marneffei.
While bamboo rats are a natural reservoir, they are generally not in
close contact with humans and there is no evidence of direct
transmission from rats to humans [25]. However, bamboo rats and HIV-positive patients have been found to share genetically similar strains of T. marneffei, suggesting that rat-to-human transmission might be possible or co-infection from a common but still unidentified source [36]. Infected rats appear healthy [24]. In addition, recent studies suggested that domestic animals such as dogs might be another possible reservoir for T. marneffei in the regions where it is endemic [25]. To date T. marneffei has never been recovered from environments other than those that are intimately associated with bamboo rats.
Lobomycosis
Lobomycosis is a rare chronic, granulomatous, fungal infection of the skin and subcutaneous tissues [37] and [38].
Despite important advances having been made through the use of updated
molecular biology techniques, the aetiological agent of lobomycosis has
never been cultured and grown in vitro. In 1999, Taborda et al. proposed the agent in a new genus, Lacazia, calling it Lacazia loboi [39].
Ecology and source of infection
Soil
and vegetation are believed to be the chief habitat of the fungus.
However, increasing reports of the disease in aquatic mammals such as
the dolphin has shifted attention to water and the aquatic environment [38] and [40].
Epidemiology in humans
The
disease has been diagnosed generally in tropical areas with an average
temperature of 24°C and relative humidity higher than 75% [41]. The calculated prevalence of lobomycosis is 3.05/10 000 inhabitants in the Amazon region of Brazil [42] and [43]. Most patients diagnosed have been in the Amazon basin and countries of South and Central America [44]. There have also been imported cases in the USA, Canada, Europe and South Africa [38].
Disease in humans
Lobomycosis does not affect the general health of the patient [43].
Patients often report a bite or sting from an arthropod, snake or
stingray, or trauma from a cutting instrument. The clinical
manifestations of lobomycosis are pleomorphic lesions, dermal nodules,
either lenticular or in plaques, which can be either hyperpigmented or
hypopigmented (Fig. 1).
The lesions are generally painless, although pruritus and dysaesthesia
have been occasionally described. The cheloid-like lesions can resemble
nodular leprosy or leishmaniasis, or other subcutaneous mycoses
(sporotrichosis, chromomycosis, paracoccidioidomycosis), cheloids and
malignant tumours [37].
Disease in animals
Lobomycoses have been described in two species of dolphins (Delphinidae): the common bottlenose dolphin (Tursiops truncatus) from the Atlantic coast of the USA and Europe, and the Guyana dolphin (Sotalia guianensis) from the Surinam River estuary [45]. The lesions are characterized by greyish, white to pink verrucous lesions that may ulcerate and form large plaques (Fig. 2) [46]. The disease progresses over years and may disfigure large areas of the body [38]. The prevalence of lobomycosis in bottlenose dolphins of Florida is reported to be 6.8% [47].
Mode of transmission
The
possibility of zoonotic transmission of this disease is still under
investigation. However, it is highly probable that the transmission
occurs by direct contact with infected animals following abrasion or
trauma of the skin [40]. Lobomycosis can be transmitted directly from human-to-human under accidental circumstances [48].
Dolphin-to-human transmission of lobomycosis has also been reported in
an aquarium attendant who had had close physical contact with an
affected dolphin [49].
Adiaspiromycosis
Adiaspiromycosis is a rare chronic pulmonary infection caused by dimorphic fungi from the genus Emmonsia within the family Ajellomycetaceae [50], [51] and [52]. The infection is characterized by the presence of very large adiaspores in the lungs [53]. Inhaled conidia of Emmonsia
produced from the mycelial phase growing at ambient temperatures fail
to germinate in the lung, and instead simply increase in volume to form
thick-walled, non-replicating adiaspores [54].
Currently, two species of Emmonsia are known as main agents of pulmonary diseases in human and animals: Emmonsia crescens and Emmonsia parva [51]. However, a new species, ‘Emmonsia pasteuriana’, has been recently described causing disseminated cutaneous infection in HIV-infected patients [55].
Ecology and source of infection
Emmonsia
species are commonly found in soil but also occur in mammalian species
living in close association with soils such as rodents, insectivores,
otters, stoats, weasels, moles and ground squirrels [56]. Among species in this genus, E. crescens is widespread in continental Europe and UK, whereas E. parva is found mainly in some xerothermic regions, including parts of the Americas, Central Asia and Africa [56].
Epidemiology in humans
In
humans, adiaspiromycosis is a rare pulmonary infection. Disseminated
pulmonary adiaspiromycosis can progress to respiratory failure and
death; however, mortality rates are low [53]. There are nearly 200 reports of Emmonsia infections in human lungs and less than 20 (sub)cutaneous infections in the literature [53].
Disease in humans
Cases
of human infection are rare and primarily pulmonary conditions similar
to that observed in animals, with only a few cases of infection at other
sites [53]. The disease is usually localized, asymptomatic and self-limited; however, disseminated fatal cases have been reported [54].
The severity of the adiaspiromycosis in humans depends on the amount of
the airborne conidial burden inhaled and host immunocompetence, and
range from asymptomatic infection through necrogranulomatous pneumonia
and even death [54].
Disease in animals
Emmonsia species have an extremely broad host range and infections have been reported in many species of small mammals, worldwide [56] and [57].
Histopathological examination of the infected animals generally reveals
a multifocal extensive granulomatous reaction containing oval
adiaspores scattered irregularly throughout the lungs [57].
The frequency of infected animals varies according to geographic area,
altitude, habitat, and season. Several studies clearly indicated that
almost 30% of all small wild mammals examined in the UK and parts of
central and eastern Europe where it is endemic, had evidence of
infection [57], raising the possibility that sporadic infections might also occur in domestic animals and humans [56].
Mode of transmission
Similar to other dimorphic onygenalean fungi, Emmonsia species are environmental pathogens, having a life cycle involving soil and vectoring by the animals [50].
Entomophthoromycosis
Entomophthoromycosis is a chronic subcutaneous infection caused by zygomycetes of the order Entomophthorales: Conidiobolus coronatus, Conidiobolus incongruus and Basidiobolus ranarum [58].
Ecology and source of infection
Both Conidiobolus spp. and B. ranarum are generally considered as saprobe distributed in plant debris and soil of tropical areas [59].
In addition, these fungi are present as a commensals in the
gastrointestinal tract of amphibians, fish, reptiles and insectivorous
bats [60].
Epidemiology in humans
The
disease occurs sporadically as a result of traumatic implantation or
inhalation of the fungus that is present in plant debris in tropical
environments. Both types of entomophthoromycosis are reported in
tropical countries of Africa, Asia, USA and Europe [58]. Gastrointestinal basidiobolomycosis has a 20% mortality rate despite all of the therapeutic measures [61] and [62].
Disease in humans
Typically, B. ranarum causes subcutaneous infection in immunocompetent young adults and rarely involves the gastrointestinal tract [61]. Human infection with Conidiobolus species occurs predominately as chronic rhinofacial mycosis in otherwise healthy hosts [59].
In addition, invasive conidiobolomycosis has been reported in
immunocompromised patients that can cause endocarditis and widespread
fatal dissemination [63].
Disease in animals
Conidiobolomycosis is reported mainly in horses [64], sheep [65] and [66] and dogs [67].
Ulcerative pyogranulomatous lesions of the mucosa of the nasopharyngeal
tissue, mouth or nodular growths of the nasal mucosa and the lips may
be seen with conidiobolomycosis, similar to those caused by pythiosis
and lagenidiosis. Disseminated basidiobolomycosis is rare but has been
described in dogs and mandrills [68].
Mode of transmission
The transmission dynamics of these fungi is still under investigation. However, the isolation of Conidiobolus spp. and B. ranarum from reptiles, amphibians and fish, and infection in various animals, strongly suggest interspecific transmission [8]. Infection due to B. ranarum is thought to occur following traumatic implantation of the fungus into the subcutaneous tissues. Infections with Conidiobolus
spp. occur following inhalation of the fungal spores, which then
germinate and induce the invasion of nasal cavity, paranasal sinuses and
facial soft tissues.
Paracoccidioidomycosis
Paracoccidioidomycosis is an acute to chronic systemic infection caused by a thermally dimorphic fungus, Paracoccidioides brasiliensis [12] and [69] and its relative Paracoccidioides lutzii.
Ecology and source of infection
The natural habitat of P. brasiliensis,
its environmental niche and life cycle in nature remain unknown, but it
is presumed that the fungus is able to survive and proliferate in the
soil [69]. The fungus generally enters via the respiratory tract or injuries of the skin and mucosal membranes [70].
Epidemiology in humans
Paracoccidioidomycosis
is considered to be the third leading cause of death from chronic
infectious disease in South America, and the mortality rate for
paracoccidioidomycosis is 1.65 cases/1 000 000 population [71].
It is endemic in the American continent, and the highest incidence of
the disease was registered in South American countries including Brazil,
Argentina, Colombia and Venezuela [72].
However, cases outside of the areas of endemicity continue to be
described, in general with long periods of latency, representing
endogenous reactivations of the infectious focus previously acquired in
endemic regions [73].
The annual prevalence of the disease in areas where it is endemic
ranges from three or four new cases/1 000 000 population to one to three
new cases/100 000 population. Most patients are males (>90%),
agricultural workers, often malnourished, and usually 30–60 years of age
[12] and [72].
Disease in humans
Following inhalation, P. brasiliensis
typically causes asymptomatic chronic pulmonary infection that
disseminates as ulcerative granulomata in the mucosal surfaces of the
nose, mouth and gastrointestinal tract [69]. In addition to the skin and lymph nodes, the infection may spread to internal organs [12] and [72]. Symptomatic cases may develop an acute and or sub-acute or chronic pneumonia with clinical features resembling tuberculosis (Fig. 3) [12].
This form of infection is almost always observed in children,
adolescents, and adults <30 years of age, and represents <10% of
the cases [69], [72] and [74].
Disease in animals
The disease has been demonstrated in domestic [75] and wild (armadillos and monkeys) [76] and [77] animals. Experimental infection can be obtained in dogs [78] and [79]. Naturally acquired infection is also reported in dogs with emaciation, lymphadenomegaly and hepatosplenomegaly (Fig. 4) [75] and [80].
Mode of transmission
The epidemiology of the disease indicates a rural predilection, consistent with most zoonotic infections [34].
The infection, in both humans and other animals, is transmitted in an
airborne manner by inhalation of conidia present in the environment [75].
Given that armadillos can harbour the fungus at high frequencies, this
suggests their role as a wild host in the epidemiological cycle of the
disease [76].
In addition, in areas of endemicity, it has been shown that infected
armadillos and humans share genetically similar strains of P. brasiliensis [81], which also suggests a zoonotic role for this infection.
Conclusions
The
importance of fungal zoonotic or sapronotic infections has been
demonstrated. There is no doubt that these types of fungi need to be
controlled. Control of human exposure to animal reservoirs can protect
susceptible populations and is a critical component of prevention. From a
global public health prospective, clearly more efforts are needed to
raise awareness of the scale of the problem for neglected zoonotic or
sapronotic fungi in order to better define the burden, distribution,
mortality and socio-economic consequences, and also provide an
integrated platform of prevention and control strategies.
Transparency declaration
SS has received travel grants from Astellas Pharma B.V. and Gilead Sciences. JG
has served as consultant to Lilly Elanco, Merial, MSD, Novartis, and
Bayer. AT and GSdH have no conflict of interests. PEV has served as
consultant and has received research grants from Astellas, Basilea, Gilead Sciences, Merck, and Pfizer.
Acknowledgements
This
publication was prepared as a collaborative study between the
Department of Medical Microbiology, Radboud University Medical Centre,
Nijmegen, the Netherlands, the Dynamyc Research Group, Maisons-Alfort,
Créteil, France, and the Veterinary Mycology and Black Yeast Working
groups of the International Society for Human and Animal Mycology
(ISHAM-VMWG).
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