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Neglected Fungal Zoonoses: Hidden Threats to Man and Animals

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Neglected Fungal Zoonoses: Hidden Threats to Man and Animals View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector REVIEW Neglected fungal zoonoses: hidden threats to man and animals S. Seyedmousavi1,2,3, J. Guillot4, A. Tolooe5, P. E. Verweij2 and G. S. de Hoog6,7,8,9,10 1) Department of Medical Microbiology and Infectious Diseases, Erasmus MC, Rotterdam, 2) Department of Medical Microbiology, Radboud University Medical Centre, Nijmegen, The Netherlands, 3) Invasive Fungi Research Center, Mazandaran University of Medical Sciences, Sari, Iran, 4) Department of Parasitology- Mycology, Dynamyic Research Group, EnvA, UPEC, UPE, École Nationale Vétérinaire d’Alfort, Maisons-Alfort, France, 5) Faculty of Veterinary Medicine, University of Tehran, Tehran, Iran, 6) CBS-KNAW Fungal Biodiversity Centre, Utrecht, 7) Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands, 8) Peking University Health Science Center, Research Center for Medical Mycology, Beijing, 9) Sun Yat-sen Memorial Hospital, Sun Yat-sen University, Guangzhou, China and 10) King Abdullaziz University, Jeddah, Saudi Arabia 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. Clinical Microbiology and Infection © 2015 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All rights reserved. Keywords: Animal, fungi, human, mycoses, neglected, zoonoses Article published online: 11 March 2015 animal populations [4]. Although zoonotic agents can be Corresponding author: Seyedmojtaba Seyedmousavi, Department transmitted from an infected host to others, inter-human of Medical Microbiology and Infectious Diseases, Erasmus MC, P.O.Box. 2040, 3000 CA, Rotterdam, The Netherlands transfer is uncommon. E-mail: [email protected] 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 [5,6]. It has been shown that zoonoses occur due to increased con- Introduction tact between humans and animals as a by-product of develop- ment, industrialization and encroachment on wildlife habitats, Depending on the source of infections, zoonoses are resulting in a dynamic upward trajectory of these diseases [7]. described as infectious diseases that can be naturally trans- Fungal infections associated with zoonotic and or sapronotic mitted between vertebrate animals and man [1]. The causative transmission are an important public health problem worldwide agent may be a bacterium, a virus, an ectoparasite, a helminth, [8]. A number of these infections are among the group of the most a protozoa, or a fungus [2].Ananimalcanbeeitherreservoir common fungal diseases, such as: dermatophytosis [9],sporotri- or mechanical vector of zoonotic pathogens, therefore the chosis [10,11] and histoplasmosis [12]. Within this context, it is transmission may be direct or indirect [3]. In most cases, many however notable that some fungal diseases with zoonotic potential wild and domesticated animals (including their faeces and soil have lacked adequate attention in international public health ef- fi in their burrows) play an essential role in maintaining the forts, leading to insuf cient attention on their preventive strategies. infection in nature and contribute in varying degrees to the In this paper, we provide an overview of neglected fungal distribution and actual transmission of infection in human and pathogens that could be carried and transmitted between Clin Microbiol Infect 2015; 21: 416–425 Clinical Microbiology and Infection © 2015 European Society of Clinical Microbiology and Infectious Diseases. Published by Elsevier Ltd. All rightsreserved http://dx.doi.org/10.1016/j.cmi.2015.02.031 CMI Seyedmousavi et al. Neglected fungal zoonoses 417 vertebrate animals and people. Their aetiological agents, ecol- marneffei is a dimorphic fungus exhibiting a mycelial form at 25° ogy and geographical distribution, current epidemiology, type of C and a yeast form at 37°C. Upon tissue invasion, P. marneffei diseases in humans and animals, source of infection and mode of undergoes a morphological phase transition from saprobic transmission will be discussed. 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 Fungal zoonoses versus sapronoses saprobic Penicillium species [20,21]. From an evolutionary viewpoint, mycotic infectious agents can Ecology and source of infection be either true pathogens or opportunists [13], and from the same The fungus may have a natural habitat in soil in areas of perspective pathogens can be divided into environmental path- southern China and South-East Asia where it is endemic ogens (having a saprobic but infectious phase in the environment) [18,22]. Talaromyces marneffei was originally isolated from the and obligatory pathogens (having host-to-host transmission). bamboo rat, Rhizomys sinensis, in 1956 [19]. Since then, addi- Systemic environmental pathogenic fungi may produce invasive tional studies demonstrated that three other bamboo rat spe- forms in infected tissue, such as the spherule in Coccidioides or cies may act as reservoirs: Rhizomys pruinosus, Rhizomys intracellular yeast in Histoplasma [12]. Nearly all fungi are able to sumatrensis and the reddish-brown subspecies of Cannomys thrive in the environment for extended periods, but pathogens badius. Within these rodent species, the prevalence of infection have an evolutionary advantage of the use of a vertebrate vector varies widely across South-East Asia [23,24]. In addition, more during a part of their life cycle. Often an animal other than recently, dogs have been suggested as a possible reservoir for humans is the prime target of the fungus, with humans as non- T. marneffei [25]. optimal hosts. Infections originating from an animal are termed zoonoses [1]. The clinical course of systemic pathogens can be Epidemiology in humans fi fatal in hosts with severe impairment of acquired immunity, but in The infection is recognized as an AIDS-de ning opportunistic healthy hosts the infection is often relatively mild. infection [26,27] in regions where the fungus is endemic. In In contrast, opportunistic fungi have a preferred habitat in- Thailand Chiang Mai province, it is the third most common dependent from the living hosts [13]. Factors enabling survival HIV-related opportunistic infection (after tuberculosis and in human tissue are purely coincidental. Infections may never- cryptococcosis) [18,27,28]. Penicilliosis affects all ages and both theless occur repeatedly from a single source, and we then sexes, although 90% of the cases reported in the literature are speak of sapronoses [14]. Infection of the non-preferred human male [29]. Notably, the risk of infection is not restricted to host decreases fitness of the fungus. The fungus is poorly those living in areas where it is endemic. HIV-infected in- adapted to this unexpected habitat and therefore may provoke dividuals who travelled to areas of endemicity have also become a strongly inflammatory response, which in patients with severe infected by T. marneffei [30]. Of note, the mortality rate of impairment of their innate cellular immunity may be fatal. untreated T. marneffei infections in HIV-infected patients is Table 1 shows the list of clinically significant fungi with 100% [31]. zoonotic potential that can cause considerable medical, veter- inary and/or public health problems. Some of these fungi and Disease in humans corresponding infections have been extensively investigated in In patients who are not immunocompromised, most cases of the literature [8–12,15–17]. Here we discuss the fungal path- penicilliosis show generalized lymphadenopathy, fever, weight ogens whose zoonotic potential is neglected, including: Talar- loss, anaemia and a non-productive cough, which may strongly omyces (Penicillium) marneffei, Lacazia loboi, Emmonsia spp., resemble histoplasmosis, cryptococcosis and tuberculosis [32]. Conidiobolus spp., Basidiobolus ranarum and Paracoccidioides In HIV-infected patients, the disease is usually disseminated, brasiliensis. 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 Penicilliosis contrast to histoplasmosis and tuberculosis, adrenal involve- ment and central nervous system infections are uncommon. The molluscum contagiosum-like lesions of skin and mucosa Penicilliosis is caused by the emerging pathogenic fungus Peni- indicate disseminated disease [29]. Most patients acquire skin cillium marneffei that usually causes a fatal disseminated disease lesions on the face and neck. Chest radiographs show patchy
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