immunocompromised patients and their pets: still best friends?

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Immunocompromised patients and their pets: Still best friends? Daniel Elad The Kimron Veterinary Institute, P.O. Box 12, Bet Dagan 50250, Israel article info Article history: Accepted 27 May 2013 Available online xxxx Keywords: Immunocompromised Immunosuppression Pet Zoonoses Interdisciplinary communication abstract The emergence of immunosuppressive human diseases and therapies in the last decades has raised the question of the risks and benefits for this group of patients deriving from their interaction with pets and the necessity to balance them in the best interest of the pet owner. Risks are related to the possibility of contracting zoonotic infections that are more severe and occasionally lethal in immunocompromised patients. To mitigate the risks and allow the owner to keep the pet, guidelines have been devised. The cooperation and communication between the owner, the physician and the veterinarian are fundamental for a rational approach in evaluating of the potential health risks associated with pets as sources of zoo- notic diseases. The final decision should, however, be made by the owner, who alone will enjoy the ben- efits of the relationship but also be the one to bear the consequences. Ó 2013 Elsevier Ltd. All rights reserved. Introduction The emergence of immunosuppressive human diseases and therapies in the last decades has raised the question of the risks and benefits of this group of patients from their interaction with pets and the necessity to balance them in the best interest of the pet owner. The benefits of animal companionship were noted as early as 1860 by Florence Nightingale (Braun et al., 2009). It took, however, more then a century until a scientific approach to the assessment and definition of such benefits was instigated. These studies resulted in the recognition of psychological (direct through interaction with the animal and indirect through promotion of human contact opportunities) and physical benefits (Siegel et al., 1999; Braun et al., 2009). Immunocompromised (IC) pet owners are at risk of contracting infections caused by zoonotic pathogens, the consequences of which are often much more severe than in immunocompetent persons and may be occasionally lethal. This topic has been period- ically reviewed (Altamura, 1982; Glaser et al., 1994; Plaut et al., 1996; Litwin, 2003; Hemsworth and Pizer, 2006; Rabinowitz et al., 2007; Steele, 2008; Mani and Maguire, 2009; Broughton et al., 2010; Marks et al., 2011). Among the multitude of zoonotic infectious agents, some have garnered more attention in the literature, possibly indicating a more considerable impact on IC patients. These will be briefly addressed in this review. Zoonotic infections in IC patients can be prevented by applying simple rules (Rabinowitz et al., 2007). Several authors (Steele, 2008; Glaser et al., 1994; Hemsworth and Pizer, 2006) and various organizations such as the American Veterinary Medical Association (1995) and the Centers for Diseases Control and Prevention 1 have published guidelines aimed at reducing the risk of contracting such infection from pets, in general and to IC patients in particular. An additional topic addressed in this review is the repeatedly recognized lack of communication between physicians, veterinari- ans and pet owners, often resulting in misinformation and unjusti- fied recommendation to renounce the animal (Angulo et al., 1994), adding the ensuing grief to the burden of their disease. Thus deal- ing with zoonoses in general and with the reduction of infection risk in the IC patient in particular, epitomizes the need for cooper- ation between physicians and veterinarians, as suggested by the One Health Initiative (Gates, 2009). Benefits Pet ownership has been found to increase post-myocardial infarction survival time (Friedmann et al., 2011). This observation was not limited to dog owners and is thus not an exclusive result of the additional exercise associated with walking these animals. Although the authors suggested that pets were no replacements for human contact, interaction with the former was more relaxing than the latter. This might be a result of the human–pet interaction being less complicated then the human–human one (Rynearson, 1978). A more general beneficial influence on patients’ health was reported by Serpell (1991) who found that acquiring a dog or cat reduced minor health problems. More recently Friedmann et al. 1090-0233/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tvjl.2013.05.042 Tel.: +972 3 9681688. E-mail address: [email protected] 1 See: http://www.cdc.gov/healthypets. The Veterinary Journal xxx (2013) xxx–xxx Contents lists available at SciVerse ScienceDirect The Veterinary Journal journal homepage: www.elsevier.com/locate/tvjl Please cite this article in press as: Elad, D. Immunocompromised patients and their pets: Still best friends? The Veterinary Journal (2013), http://dx.doi.org/ 10.1016/j.tvjl.2013.05.042

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The Veterinary Journal xxx (2013) xxx–xxx

Contents lists available at SciVerse ScienceDirect

The Veterinary Journal

journal homepage: www.elsevier .com/ locate/ tv j l

Immunocompromised patients and their pets: Still best friends?

1090-0233/$ - see front matter � 2013 Elsevier Ltd. All rights reserved.http://dx.doi.org/10.1016/j.tvjl.2013.05.042

⇑ Tel.: +972 3 9681688.E-mail address: [email protected] 1 See: http://www.cdc.gov/healthypets.

Please cite this article in press as: Elad, D. Immunocompromised patients and their pets: Still best friends? The Veterinary Journal (2013), http://dx.d10.1016/j.tvjl.2013.05.042

Daniel Elad ⇑The Kimron Veterinary Institute, P.O. Box 12, Bet Dagan 50250, Israel

a r t i c l e i n f o

Article history:Accepted 27 May 2013Available online xxxx

Keywords:ImmunocompromisedImmunosuppressionPetZoonosesInterdisciplinary communication

a b s t r a c t

The emergence of immunosuppressive human diseases and therapies in the last decades has raised thequestion of the risks and benefits for this group of patients deriving from their interaction with petsand the necessity to balance them in the best interest of the pet owner. Risks are related to the possibilityof contracting zoonotic infections that are more severe and occasionally lethal in immunocompromisedpatients. To mitigate the risks and allow the owner to keep the pet, guidelines have been devised. Thecooperation and communication between the owner, the physician and the veterinarian are fundamentalfor a rational approach in evaluating of the potential health risks associated with pets as sources of zoo-notic diseases. The final decision should, however, be made by the owner, who alone will enjoy the ben-efits of the relationship but also be the one to bear the consequences.

� 2013 Elsevier Ltd. All rights reserved.

Introduction

The emergence of immunosuppressive human diseases andtherapies in the last decades has raised the question of the risksand benefits of this group of patients from their interaction withpets and the necessity to balance them in the best interest of thepet owner. The benefits of animal companionship were noted asearly as 1860 by Florence Nightingale (Braun et al., 2009). It took,however, more then a century until a scientific approach to theassessment and definition of such benefits was instigated. Thesestudies resulted in the recognition of psychological (direct throughinteraction with the animal and indirect through promotion ofhuman contact opportunities) and physical benefits (Siegel et al.,1999; Braun et al., 2009).

Immunocompromised (IC) pet owners are at risk of contractinginfections caused by zoonotic pathogens, the consequences ofwhich are often much more severe than in immunocompetentpersons and may be occasionally lethal. This topic has been period-ically reviewed (Altamura, 1982; Glaser et al., 1994; Plaut et al.,1996; Litwin, 2003; Hemsworth and Pizer, 2006; Rabinowitzet al., 2007; Steele, 2008; Mani and Maguire, 2009; Broughtonet al., 2010; Marks et al., 2011). Among the multitude of zoonoticinfectious agents, some have garnered more attention in theliterature, possibly indicating a more considerable impact on ICpatients. These will be briefly addressed in this review.

Zoonotic infections in IC patients can be prevented by applyingsimple rules (Rabinowitz et al., 2007). Several authors (Steele,2008; Glaser et al., 1994; Hemsworth and Pizer, 2006) and various

organizations such as the American Veterinary Medical Association(1995) and the Centers for Diseases Control and Prevention1 havepublished guidelines aimed at reducing the risk of contracting suchinfection from pets, in general and to IC patients in particular.

An additional topic addressed in this review is the repeatedlyrecognized lack of communication between physicians, veterinari-ans and pet owners, often resulting in misinformation and unjusti-fied recommendation to renounce the animal (Angulo et al., 1994),adding the ensuing grief to the burden of their disease. Thus deal-ing with zoonoses in general and with the reduction of infectionrisk in the IC patient in particular, epitomizes the need for cooper-ation between physicians and veterinarians, as suggested by theOne Health Initiative (Gates, 2009).

Benefits

Pet ownership has been found to increase post-myocardialinfarction survival time (Friedmann et al., 2011). This observationwas not limited to dog owners and is thus not an exclusive resultof the additional exercise associated with walking these animals.Although the authors suggested that pets were no replacementsfor human contact, interaction with the former was more relaxingthan the latter. This might be a result of the human–pet interactionbeing less complicated then the human–human one (Rynearson,1978).

A more general beneficial influence on patients’ health wasreported by Serpell (1991) who found that acquiring a dog or catreduced minor health problems. More recently Friedmann et al.

oi.org/

2 D. Elad / The Veterinary Journal xxx (2013) xxx–xxx

(2011) indicated that pet ownership reduced the effect of depres-sion on post-myocardial infarction death rates.

In addition to the physical benefits, contact with animalsreduces stress (the ‘Biophilia’ effect), which may project on theowners’ health. In fact, even viewing filmed animals had a soothingeffect. Moreover, animals reduce loneliness by being constantlyavailable and by facilitating contact between people (O’Haire,2010). Various methods aimed at the quantification of the hu-man–animal bond (reviewed by Zasloff (1996)) and commitmentto pets (Staats et al., 1996) were devised.

Research projects attempting to define the benefits of animalcompanionship suffer from an inherent and practically unavoid-able flaw in the experimental design: the random assignment tothe pet owner or pet non-owner group is not possible. However,even if the results of single studies may not be beyond critique,considering the entire body of published information on the topicclearly indicates that pet ownership has positive physical andpsychological effects on the owner (Endenburg and van Lith,2011).

Children are a special group benefiting from interaction withpets. Beck and Meyers (1996) reviewed the then available litera-ture emphasizing the positive psychological influence of pet own-ership on children. These effects have led to the establishment ofAnimal Assisted Therapy (Lefebvre et al., 2008), especially for chil-dren (Braun et al., 2009; Endenburg and van Lith, 2011).

With the advent of the acquired immunodeficiency syndrome(AIDS) epidemic, research projects dealing with human–pet rela-tions benefits were focused on patients afflicted by the disease. Sie-gel et al. (1999) found that AIDS patients without pets were almosttwice as likely to suffer from depression as those who owned one.This effect was not observed for human immunodeficiency virus(HIV) seropositive patients. More recently, Friedmann et al.(2011) published an extensive review of the bibliography on thehuman benefits from their interaction with companion animals,emphasizing effects such as stress reduction and animal assistedtherapy.

Not all animals have the same impact on their owners. Siegelet al. (1999) indicated that dog owners have a stronger attachmentto their pet then owners of other animals. Cats, on the other hand,provide more social support to HIV+ patients then dogs. The otherside of the coin is the negative influence of losing a pet, often con-sidered a family member (Beck and Meyers, 1996; O’Haire, 2010),which may reach pathological levels (Rynearson, 1978).

Risk

General

The nature of benefits provided to IC patients by interactingwith pets does not differ from those offered to non-IC persons,although their significance may vary individually. The danger ofexposure to zoonotic diseases (diseases transmitted to humansby animals), however, poses a significantly higher risk for ICpatient then the one for non-IC persons.

Infectious diseases transmitted to humans by animals, espe-cially their prevention, are important topics of human and veteri-nary medicine. In addition to the classical companion animals(dogs, cats, birds), rabbits (King et al., 2007), exotic animals(rodents, reptiles, partially domesticated carnivores, etc.) havebecome more and more popular as pets. The exotic animals maycarry zoonotic pathogens, contracted at their origin or by contactwith other animals during transport or in pet stores, more oftenor in higher loads. Moreover, their sometimes unpredictablebehavior increases the risk of infecting their owner through bites(Steele, 2008).

Please cite this article in press as: Elad, D. Immunocompromised patients and th10.1016/j.tvjl.2013.05.042

Zoonotic infections may be contracted by traumatic implanta-tion (bites, scratches), from aerosol, direct contact, animal secre-tions and excretions, vectors or fomites and contaminated animalfeed (Plaut et al., 1996; Mani and Maguire, 2009). Populations atrisk include patients whose immune system has been compro-mised by disease or therapy, but also those with other underlyingconditions such as chronic liver disease (Risi and Tomascak, 1998;Robinson and Pugh, 2002).

The risk of contracting opportunistic infections by AIDS patientshas been significantly reduced in some geographical areas by theintroduction of Highly Active Antiretroviral Therapy (HAART) in1992. Unfortunately restoring the immune system’s functionalityhas led to complications associated with the Immune Reconstitu-tion Inflammatory Syndrome, including exacerbations of infectionssuch as cryptococcosis, sporotrichosis and tuberculosis (Lucas,2012; Freitas et al., 2012).

The extent to which animals pose a risk to their IC owners is notclear. Conti et al. (1995) found no difference in the prevalence ofAIDS defining diseases in pet owners and pet non-owners affectedby the disease. Grant and Olsen (1999) note that often IC personsare more likely to contract infections from the environment thanfrom their pet. Nevertheless, a number of precautionary principleshave to be implemented to reduce the risk (see Guidelines).

Bacterial infections

Pasteurella spp.Judging by the number of publications, Pasteurella multocida,

part of the normal microflora of domestic carnivores’ oral cavity,is one of the most frequent infections contracted by IC patientsfrom their pets. Transmission is mostly through bites or scratchesbut also by aerosol, saliva and animal secretions (Casey et al.,1995). Pasteurella spp. infections in healthy and IC patient havebeen periodically reviewed (Casey et al., 1995; Kimura et al.,2004; Adler et al., 2011). Occasionally, other Pasteurella spp., suchas P. dagmatis, have caused infections in this group of patients(Ashley et al., 2004). Chronic hepatic diseases such as cirrhosisare the most frequent predisposing condition to P. multocidainfections (Casey et al., 1995; Ashley et al., 2004; Adler et al.,2011). Other factors facilitating infections with P. multocida areimmunosuppressive chemotherapy (Casey et al., 1995) and AIDS(Drabick et al., 1993).

Clinically, while P. multocida infections in immunocompetentpatients remain localized around the inoculation site, they may be-come lethal in IC patients, following bacteremia (Casey et al., 1995;Adler et al., 2011), septicemia, peritonitis (Ashley et al., 2004; Adleret al., 2011), septic shock (Kimura et al., 2004), or pneumonia(Drabick et al., 1993).

Capnocytophaga canimorsusC. canimorsus is another component of the oral microflora of

domestic carnivores (Gaastra and Lipman, 2010). Infection sourcemay be traumatic, but exposure to aerosol of carrier animal maysuffice to infect humans (Abarca et al., 2011). In immunocompe-tent persons lesions caused by C. canimorsus develop at the siteof inoculation and may spread to the draining lymph nodes, occa-sionally evolving into potentially lethal cases of septicemia. In ICpatients, septicemia is the rule rather than the exception, withmortality rates of up to 33%.

Mycobacterium marinumThis microorganism is associated with fresh and saltwater

aquaria or swimming pools (Danko et al., 2009), but infectionsmay be transmitted by fomites associated with their maintenance.Infections in immunocompetent patients may present as cutane-ous lesions, spreading in some cases to the lymphatic tissue

eir pets: Still best friends? The Veterinary Journal (2013), http://dx.doi.org/

D. Elad / The Veterinary Journal xxx (2013) xxx–xxx 3

draining the affected region (Nenoff et al., 2011). Anti tumor necro-sis factor (TNF)-a therapy (e.g. infliximab) is considered a risk fac-tor for localized (Ben Said et al., 2010; Ramos et al., 2010) or, morerarely, disseminated, M. marinum infections (Streit et al., 2006;Danko et al., 2009).

Rhodococcus equiR. equi is an environmental pathogen affecting primarily the

respiratory system and digestive tract in horses. It infects deeplyimmunosuppressed humans, most frequently causing cavitarypneumonia (Perez-Silvestre et al., 2010). The microorganism maydisseminate to the brain and other organs (Corti et al., 2009;Ferretti et al., 2011). The risk of zoonotic transmission of the micro-organism is unclear since it has been documented only in a fractionof reported cases (Harvey and Sunstrum, 1991).

Salmonella entericaS. enterica serotypes are enteric microorganisms that infect a

variety of hosts. Serotypes involved in human infections may beclassified as host-adapted (S. Typhi and S. Paratyphi) or non-typhoi-dal. Clinical symptoms may vary from asymptomatic carriage tolife-threatening systemic infections. IC patients are especially sus-ceptible to the latter, often relapsing after apparently successfultherapy (Gordon, 2008).

Infection is fecal–oral, directly or through contaminated food,environment or fomites. Pet rodents (Swanson et al., 2007) andreptiles (Marks et al., 2011) are considered to pose a high risk ofbeing a source of contagion with non-typhoidal salmonella sero-types. As a consequence, small turtles have been banned in theUSA since 1975.2 Nevertheless, an outbreak of salmonellosis associ-ated with turtles occurred in 2012.3 Other pets may become carriersby eating raw meat, ingesting garbage/excrement, drinking from toi-lets, or direct contact with other animals. An additional source ofinfection may be animal feed such as the recent outbreak linked todry dog food contaminated with S. Infantis.4 Consequently, IC per-sons are discouraged from keeping rodents or reptiles and applythe precautionary measures outlined in the Guidelines section.

Campylobacter spp.Among the Campylobacter species, three, namely C. jejuni, C. coli

and C. fetus are the ones most commonly involved in human infec-tions. The former two cause mostly gastrointestinal infectionswhereas the latter is the one most frequently associated with sys-temic dissemination, especially in patients afflicted by chronic liverdisease or immune deficiencies (Fernández-Cruz et al., 2010). Somesurveys, however, found no correlation between Campylobacterbacteremia and underlying conditions (Feodoroff et al., 2011).

Although Campylobacter spp. infections are much more likely tobe acquired from food, pets, especially the diarrheic and/or young,have been reported to shed the microorganism and thus pose a riskto the owners (Marks et al., 2011).

Bordetella bronchisepticaB. bronchiseptica is the etiological agent of an upper respiratory

tract infection primarily of dogs, commonly known as ‘kennelcough’. It may cause respiratory infections in IC humans, mostlyfollowing direct exposure to infected animals (Redelman-Sidiet al., 2011).

Bartonella henselaeB. henselae causes ‘cat scratch fever’ in immunocompetent peo-

ple, usually following the traumatic implantation by carrier cats or

2 See: http://www.cdc.gov/healthypets/spotlight_an_turtles.htm.3 See: http://www.cdc.gov/salmonella/small-turtles-03-12/index.html.4 See: http://www.cdc.gov/salmonella/dog-food-05-12/index.html.

Please cite this article in press as: Elad, D. Immunocompromised patients and th10.1016/j.tvjl.2013.05.042

their fleas (Glaser et al., 1994; Caniza et al., 1995). In IC people,however, infection may evolve into a life-threatening condition:bacillary angiomatosis or hepatic peliosis. The condition is charac-terized by augmented proliferation of blood vessels induced by themicroorganisms disruptive effect on the balance between anti-apoptotic and pro-apoptotic mechanisms of the endothelial cells(Mosepele et al., 2012).

Viruses

Lymphocytic choriomeningitis virusAmong the zoonotic viruses, lymphocytic choriomeningitis

virus has been the one most frequently associated with pet relatedinfections. Sources of human infection are rodent bites, excretionsor secretions (Charrel and de Lamballerie, 2010). In immunocom-petent humans, the lymphocytic choriomeningitis virus causesmostly an asymptomatic to flu-like infection but theratogeniceffects have been reported (Centers for Disease Control andPrevention, 2005). Infection in IC patients may lead to potentiallyfatal infections (Charrel and de Lamballerie, 2010).

Protozoa

Toxoplasma gondiiT. gondii is a genetically variable obligate intracellular parasite.

Its life cycle comprises two asexual stages that infect a great vari-ety of animals and a sexual stage that develops exclusively in cats(Cenci-Goga et al., 2011). The prepatent period varies according tothe stage (Dubey, 2006). Cats usually shed oocysts once, for alimited period of time, starting about 3 weeks after infection andending with the development of immunity, several weeks later.Shedding may, however, be resumed following immunosuppres-sive events (Elmore et al., 2010). Oocysts become infective1–5 days after excretion (Lappin, 2010) and survive for long peri-ods in the environment (Cenci-Goga et al., 2011).

The most frequent source of human infection is undercookedmeat of intermediate hosts with cysts (Dubey, 2006). In immuno-competent persons the infection may be asymptomatic or mild,flu-like symptoms may develop (Altamura, 1982). However, ahighly virulent strain in South America may cause pneumonia inpeople with no underlying conditions (Leal et al., 2007). In ICpatients, especially those afflicted by HIV, T. gondii may involvethe central nervous system (Luft and Chua, 2000). Many of thesecases are, however, reactivations of latent infections (Glaseret al., 1994). Cat ownership was found not to be a risk factor of T.gondii seroconversion in HIV patients (Luft and Chua, 2000).

Cryptosporidiosis and GiardiasisThese two infections and their etiological agent share many

common traits. Both comprise a variety of species that colonizethe gastrointestinal tract of diverse animals (Tangtrongsup andScorza, 2010). The most common source of human infections isthe environment through the ingestion of contaminated food orwater, by direct contact with shedding animals or humans or in-sects that act as mechanical vectors (Bajer, 2008). The organisms’long persistence in the environment and the low infective dose in-crease the risk of human contagion, especially from immunosup-pressed animals that may be persistent shedders of a significantnumber of microorganisms (Glaser et al., 1994).

Cryptosporidium spp. and Giardia spp. may be carried asymp-tomatically or cause gastroenteritis of variable severity in immu-nocompetent persons. The enteric infection in IC patients mayevolve into a chronic diarrhea leading to malabsorption and weightloss (Mani and Maguire, 2009) and occasionally, for Cryptosporidi-um spp., to organ dissemination (Bajer, 2008).

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4 D. Elad / The Veterinary Journal xxx (2013) xxx–xxx

Mycoses

GeneralMycoses of IC patients are among the most dangerous, often

life-threatening infections. The risk level is influenced by the fac-tors such as the degree of neutropenia and leukopenia as well asthe type of transplant (allogeneic or autologous) (Pagano et al.,2011). Moreover, the immune response may be influenced nega-tively the acidosis linked with certain types of diabetes.

DermatophytesThe most frequent zoonotic mycotic infections affecting IC pa-

tients are; based on number of publications; the dermatophytoses.This is to be expected considering that they are the most prevalentfungal infections in animals (Rabinowitz et al., 2007). The etiolog-ical agent was almost exclusively Microsporum canis.

Infections caused by dermatophytes in IC patients may presentas disseminated infections (Lowther et al., 2007) or subcutaneousmycoses (dermatophytic mycetoma) (Nir-Paz et al., 2003), similarto those observed in veterinary practices in long-haired cats. Thismay be the result of the immune system’s failure to limit the fun-gus to the upper layers of the skin (Akiba et al., 2001). Such caseshave also (but rarely) been reported in immunocompetent patients(Colwell et al., 2004). The severity and outcome of the infectionsdepend, at least partially, on the characteristics of the patient’simmunosuppression. Animal contact was documented in 7/14cases, but the presence of dermatophytes was confirmed in onlyone case (Bournerias et al., 1996). Various antimycotic regimenswere applied, mostly successfully (Table 1).

Cryptococcus spp.Two species of the genus Cryptococcus, namely C. neoformans

(formerly C. neoformans var. neoformans) and C. gattii (formerlyC. neoformans var. gattii) are involved in human and animalinfections (Harris et al., 2012). The environmental ecology of thesespecies is different: while C. neoformans was isolated primarilyfrom bird droppings, C. gattii was associated with trees, especiallyvarious species of eucalyptus, initially in Australia but subse-

Table 1Infections caused by zoophilic dermatophytes in immunocompromised patients. The etiolowith Trichophyton granulosum (Lowinger-Seoane et al., 1992) or T. mentagrophytes and T. r

Underlying condition Clinical aspect Thera

Systemic lupuserythematosus

Tinea and dermatophyticmycetoma

Griseofulvin and micinto the nodules

AIDS Tinea capitis Griseofulvin, econazoAIDS Tinea capitis and corporis GriseofulvinAIDS Tinea corporis and unguium

Solid organ transplant Dermatophytic mycetoma FluconazoleAIDS Fungal invasion of bacillary

angiomatosisFluconazole

AIDS Tinea capitis Itraconazole (ketoconterbinafine ineffectiv

AIDS Tinea capitis and unguium Itraconazole (ketoconterbinafine ineffectiv

Solid organ transplant Tinea capitis Terbinafine, (griseofu

Solid organ transplant Dermatophitic mycetoma FluconazoleGlucocorticoid treated

polyarthritisTinea capitis and corporis Terbinafine and ciclo

Solid organ transplant Dermatophytic mycetoma FluconazoleAlogenic bone marrow

transplantTinea capitis Itraconazole and cicl

Epidermal growth factorinhibitor therapy

Tinea capitis Terbinafine and ciclo

Please cite this article in press as: Elad, D. Immunocompromised patients and th10.1016/j.tvjl.2013.05.042

quently in other areas as well. Of special interest is the recentspreading of this fungus from Vancouver, Canada to theNorth-West of the United States.

Sources of infection of humans and animals vary accordingly.Contamination with bird droppings have only rarely beenassociated with human infections, including in HIV+ patients(Hajjeh et al., 1999). Environmental and clinical isolates were,however, been matched in some cases by molecular analysis(Garcia-Hermoso et al., 1997). Moreover, while C. gattii may infectimmunocompetent hosts, C. neoformans is primarily a pathogen ofthe IC patient and has been, in fact, qualified as an AIDS defininginfection (Centers for Disease Control and Prevention, 2008).

A single case of meningitis in an immunocompetent person,caused by an isolate identical to one found in his magpie (Picapica), was reported (Lagrou et al., 2005). Similarly, very few casesof IC humans contracting cryptococcosis from bird droppings havebeen published (Table 2). Two of these cases had AIDS and threereceived immunosuppressive medication. An attempt to provethe zoonotic source of the infection was done in one case (Nosan-chuk et al., 2000). The human and avian isolates were matchedphenotypically and genetically. The mode of transmission in thatcase was not clear, since the patient did not live on the same flooras the bird, had only brief contact with it while passing the cage,and did not clean its cage.

In addition to birds, other pets such as dogs and cats (Maliket al., 1997) and ferrets (Eshar et al., 2010) may be infected byCryptococcus spp., but to the best of our knowledge, they havenot been implicated in transmission of the yeast to IC patients.

Sporothrichium spp.Human and animal infections are caused almost exclusively by

Sporothrix shenckii, although at least one case in an IC patient wasattributed to S. cyanescens, a species subsequently considered asnot pathogenic. Although the source of the infection is mostlyenvironmental, animals, especially cats, through the high load ofyeast cells they carry, have been associated with human infections(Barros et al., 2011). Cats may be asymptomatic carriers of thefungus and bites or scratches are the common mode of contagion.

gical agent in all cases was Microsporum canis, except for two cases of mixed infectionubrum (Oriba et al., 1990).

py Outcome Animalcontact

Reference

onazole injected Recovered (1 month) Yes Barson (1985)

le, ketoconazole No response No Oriba et al. (1990)Lost Yes Hevia et al. (1991)Died of unrelatedcomplications

No Lowinger-Seoaneet al. (1992)

Recovered (2 weeks) No King et al. (1996)Relapse No King et al. (1996)

azole,e)

Recovered (after14 months)

Yes,cultured

Bournerias et al.(1996)

azole,e)

Relapse, lost No Bournerias et al.(1996)

lvin – relapses) Recovered (12 weeks) Yes Virgili and Zampino(1998)

Recovered (1 month) Yes Voisard et al. (1999)piroxolamine Recovered (6 weeks) No Möhrenschlager

et al. (2003)Recovered (1 year) No Berg et al. (2007)

opiroxolamine Recovered (3 months) Yes Anemüller et al.(2008)

piroxolamine Recovered Yes Mansur et al. (2010)

eir pets: Still best friends? The Veterinary Journal (2013), http://dx.doi.org/

Table 2Cases of suspected zoonotic infections with Cryptococcus spp.

Underlying condition Clinical aspect Exposure (time) Remarks Reference

AIDS Meningitis Dismantling aviary Not cultured Fessel (1993)AIDS Meningitis Pigeon droppings Not cultured Fessel (1993)Immunosuppressive therapy Subcutaneous nodules Cockatoo (6 weeks) Biopsy, serology. Bird not cultured. Harper and Schwartz (1993)Immunosuppressive therapy Meningitis Cockatoo (7 years) Human and bird isolates identical Nosanchuk et al. (2000)

The patient did not clean the cageThe bird rarely left the cage

Immunosuppressive therapy Pneumonia Cockatiel (1 week) Cryptococcus not isolated from bird excrement Shrestha et al. (2004)Cleaned cage 1 week prior to symptoms

D. Elad / The Veterinary Journal xxx (2013) xxx–xxx 5

Contact with an infected cat may, however, be sufficient. Thezoonotic transmission of S. shenckii from cats to IC humans wasreported during a massive outbreak of sporotrichosis in Rio deJaneiro, but the cats assumed to be the source of the infectionswere not cultured (Freitas et al., 2012). Dogs may be infected,but there is no indication that they pose a zoonotic threat. Theinfection involves the skin, subcutis and draining lymph nodes,but may spread, especially in IC patients, to internal organs (Barroset al., 2011).

Other fungi

Several other etiological agents of human mycoses have beenoccasionally associated with animal sources. Malassezia pachyder-matis, isolated from the hands of health care workers and theirdogs, were found to be genetically identical. Subsequently,however, dogs carrying the fungus were found to pose no risk toIC persons (Morris et al., 2005). Blastomyces dermatitidis is not con-sidered zoonotic, as humans and animals contract the infectionfrom the environment and not one from another. However, humaninfection following traumatic inoculation (bite of an infected dog)of the fungus has been reported (Gnann et al., 1983).

Although not reported, other potential sources of fungal infec-tion of IC patients may be the urine of dogs afflicted with dissem-inated aspergillosis (Elad et al., 2008) and moldy animal feed.

Vaccines

Several vaccines used in veterinary medicine, such as thoseagainst Brucella spp., Bacillus anthracis and B. bronchiseptica,contain live attenuated microorganisms. These vaccines maycause human infections following exposure to the preparationsor their persistence in and shedding by immunized animals(Berkelman, 2003). To the best of the author’s knowledge, onlyone case of an IC person being infected from her pet immunizedwith a live B. bronchiseptica vaccine has been reported (Giselet al., 2009).

5 See: http://eurogroupforanimals.org/publications/report-on-health-risks-from-new-companion-animals.

Guidelines

Many microorganisms discussed in the current review arecommensally carried by animals with no clinical signs. Even if atthe time of acquisition they are tested and found free from thesemicroorganisms, they may be contaminated later on and conse-quently they must be tested frequently. Moreover, since thecarriage of such microorganisms cannot be unequivocally ex-cluded, general rules of hygiene should be strictly kept up.

The risk has to be assessed prior to the introduction of a pet intoa household with an IC person (Robinson and Pugh, 2002), prefer-entially by a physician (infectious diseases specialist if possible)and a veterinarian. In general the animal chosen has to fit the

Please cite this article in press as: Elad, D. Immunocompromised patients and th10.1016/j.tvjl.2013.05.042

limitations of the owner. Animals defined as ‘new companion ani-mals’,5 such as reptiles, rodents, primates and wild carnivores, arenot recommended due to their unpredictable aggressive behavioror relatively frequent carriage of pathogens (Hoff et al., 1999).

Aquaria have been shown to have a soothing effect (O’Haire,2010). Cats, dogs and birds have advantages and disadvantages.Dogs are very good and affectionate companions and trauma in-flicted to owner is exceptional. They need to be walked and thusthere is an increased risk to contract potential infective agents,especially considering that dogs are not very particular as to whatthey ingest or what they rub their coat in. On the other hand, theadditional physical activity and the opportunities of human con-tact may benefit the owner. Cats are cleaner and more hygienicthan dogs and do not need to be walked. They are known, however,to bite or scratch their owner during play, a risk that may be re-duced by using toys (Overall et al., 2005). Certain pathogens mayhave a predilection for certain animals or breeds in a region depen-dent mode. Trivedi et al. (2011) found that in California dogs aremore often infected with Cryptococcus neoformans and that Amer-ican Cocker Spaniels were overrepresented whereas cats are moreoften infected with C. gattii.

General recommendations as to the acquisition of pets includethe following precautions:

New pets:

(1) Young animals are more prone to be carriers/infected bymicroorganisms with zoonotic potential and thus older ani-mals are preferred. This may, however, cause other prob-lems: cats that have no human contact during the first3 months may be more aggressive (Overall et al., 2005).

(2) Animals should not come from crowded facilities.(3) Animal dealerships that crowd animals or mix animals from

different origins should be avoided. Transmission of atypical,sometimes exotic, microorganisms through contact withimported animals in such dealerships has been documented(Reed et al., 2004).

(4) Animals should be examined by a veterinarian before intro-ducing it into the patient’s household.

Some authors (Hemsworth and Pizer, 2006) do not recommendthe introduction of new pets into households with IC patients.

Existing pet(s):

(1) Animals should not be fed raw meat and not be allowed todrink from the toilets.

(2) Frequent veterinary visits for early detection of infections.(3) Handle animal excrements promptly and carefully.(4) Wash hands frequently.(5) Refrain from face and mouth contact with the animal.

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6 D. Elad / The Veterinary Journal xxx (2013) xxx–xxx

If the necessary steps are taken, the transmission of zoonoticinfections is significantly reduced (Wong et al., 1999).

Interdisciplinary communication

Several authors have emphasized the communication problemsthat hinder a rational approach to actual or potential health prob-lems of pets owned by IC persons (Robinson and Pugh, 2002; Maniand Maguire, 2009). Grant and Olsen (1999) reported that, in gen-eral, clients prefer discussing zoonotic disease with their physicianrather than with their veterinarian, but that the former (exceptinfectious disease specialists) may not be familiar with the moredynamic aspects of zoonotic diseases, such as changes in their geo-graphic distribution. Seemingly, physicians and veterinarians eachexpect the other to discuss zoonotic diseases with patients (Anguloet al., 1994).

Conti et al. (1995) reported that only 10% of AIDS patients wereinformed by their physicians of the risks of zoonotic infections. Ingeneral, veterinarians should inquire the eventual exposure of ICpeople to the animals they are treating, including immunizationwith live vaccines, such as the one used to prevent B. bronchisepticainfections (Berkelman, 2003). Physicians, on the other hand, shouldseek information regarding the exposure of the IC patient toanimals (Hoff et al., 1999).

Conclusions

While there is a genuine risk posed to IC patients by pets, it isoften overstated causing unnecessary removal of the animal andincreasing owners’ distress. Observing simple rules will reducethe risk significantly and thus allow retaining the pet. The finaldecision should, however, be made by owners, since they will en-joy the benefits of the relationship but also be the ones to bear theconsequences. It is imperative that the decision be based on a real-istic risk assessment that can be provided only by cooperation be-tween physicians and veterinarians. Thus, dealing with the topic ofzoonoses in general and with the reduction of infection risk of ICpatients in particular, epitomizes the need of cooperation betweenphysicians and veterinarians as proposed by the One HealthInitiative.

Conflict of interest statement

The author of this paper has no financial or personal relation-ship with other people or organizations that could inappropriatelyinfluence or bias the content of the paper.

Acknowledgments

Part of this review was presented as an invited lecture at the18th Congress of the International Society of Human and AnimalMycology, Berlin, 11–15 June 2012. Abstract in Mycoses 55 (Suppl.4), 29.

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