A zoonosis is a disease that can be transmitted from animals to humans. Zoonoses in companion animals are known and described extensively. A lot of research has already been done, Rijks et al (2015) for example lists the 15 diseases of prime public health relevance, economical importance or both (Rijks(1)). Sterneberg-van der Maaten et al (2015) composed a list of the 15 priority zoonotic pathogens, which includes the rabies virus, Echinococcus granulosus, Toxocara canis/cati and Bartonella henselae (Sterneberg-van der Maaten(2)).
Although the research is extensive the knowledge about zoonoses and hygiene instruction of owners, health professionals and other related professions, like pet shop employees, is low. According to Van Dam et al (2016) (3)77% of the pet shop employees does not know what a zoonosis is and just 40% of the pet shops has a protocol for hygiene and disease prevention. 27% of the pet shops and asylums give instruction to their clients about zoonoses. It may therefore be assumed that the majority of the public is unaware of the health risks involving companion animals like cats and dogs. Veterinarians give information about responsible pet ownership and the risks when the pet owner visits the clinic (Van dam(3), Overgaauw (4)). In other words, dissemination obtained from research has not occurred effectively.
However, urban areas are not only populated with domestic animals. There is also a variety of non- domesticated animals living in close vicinity of domesticated animals and the human population, the so-called the urban wildlife. Urban wildlife is defined as any animal that has not been domesticated or tamed and lives or thrives in an urban environment (freedictionary(5)). Just like companion animals, urban wildlife carries pathogen that are zoonotic, for example Echinococcus multilocularis. This is a parasite that can be transmitted from foxes to humans. Another example is the rabies virus, which is transmitted by hedgehogs and bats. Some zoonotic diseases can be transmitted to humans from different animals. Q-fever occurs in mice, foxes, rabbits and sometimes even in companion animals.
There is little knowledge about the risk factors that influence the transmission of zoonoses in urban areas (Mackenstedt(6)). This is mostly due to the lack of active surveillance of carrier animals. This surveillance requires fieldwork, which is expensive and time-consuming. Often there is no immediate result for public-health authorities. This is why surveillance often is initiated during or after an epidemic (Heyman(7)). Meredith et al (2015) mentioned that due to the unavailability of a reliable serological test, for many species it is not yet know what the contribution is to the transmission to human (Meredith(8)).
The general public living in urban areas is largely unaware of the diseases transmitted from the urban wildlife that is present in their living area (Himsworth(9)), (Heyman(7)), (Dobay(10)), (Meredith(8)). Since all these diseases can also be a risk for the public health and the public may need to be informed of these risks.
The aim of this study is to determine the occurrence and prevalence of zoonoses in urban wildlife. To do this, the ecological structure of an European city will be investigated first, to determine wildlife living in the urban areas. Secondly, an overview of the most common and important zoonoses in companion animals will be discussed. Followed by zoonoses in urban wildlife.
2. Literature review
2.1 Ecological structure of the city
Humans and animals live closely together in cities. Both companion animals and urban wildlife share the environment with humans. Companion animals are important to human society. They perform working roles (dogs for hearing of visually impaired people) and they play a role in human health and childhood development (Day(11)).
A distinction can be made between animals that live in the inner city and animals that live in the outskirts of the city. The animals that live in the majority of the European inner cities are: brown rats, house mice, bats, rabbits and different species of birds. Those living outside of the stone inner city are other species of mice, hedgehogs, foxes and moles (Auke Brouwer(12)). In order to create safe passage for this particular group of animals, ecological structures are created. The structure also includes wet passageways for amphibia and snakes and dry passageways like underground tunnels, special bridges and cattle grids (Spier M(13)).
A disadvantage of human and animals living in close vicinity of each other is the possibility of transmitting diseases (Auke Brouwer(12)). Diseases can be transmitted from animals to humans in different ways. A few examples are: through eating infected food, inhalation of aerosols, via vectors or fecal-oral contact (WUR(14)). The most relevant ways of transmission for this review are: indirect physical contact (e.g. contact with contaminated surface), direct physical contact (touching an infected person or animal), through skin lesions, fecal-oral transmission and airborne transmission (aerosols). In the following section an overview of significant zoonoses of companion animals will be described. This information will enable a comparison with urban wildlife zoonoses later in this review.
2.2 Zoonoses of cats and dogs
There are many animals living in European cities. Both companion animals and urban wildlife. 55- 59% of the Dutch households has one or more companion animals (van Dam(3)). This includes approximately 2 million dogs and 3 million cats (RIVM(15)). In all of Europe live approximately 61 million dogs and 66 million cats. Owning a pet has many advantages, but companion animals are also able to transmit diseases to humans (Day(11)). In the following section significant zoonoses for companion animals will be described.
A. Bartonellosis (cat scratch disease)
Bartonellosis is an infection by Bartonella henselae or B. clarridgeiae. Most infections in cats are thought to be subclinical. If disease does occur, the symptoms are mild and self-limiting, characterized by lethargy, fever, gingivitis, uveitis and nonspecific neurological signs (Weese JS(16)). The seroprevalence in cats is 81% (barmettler(17)).
Humans get infected by scratches or bites and sometimes by infected fleas and ticks. In the vast majority of cases, the infection is also mild and self-limiting. The clinical signs in humans include development of a papule at the site of inoculation, followed by regional lymphadenopathy and mild fever, generalized myalgia and malaise. This usually resolves spontaneously over a period of weeks to months (Weese JS(16)).
Few cases of human bartonella occur in The Netherlands. Based on laboratory diagnosis done by the RIVM, the bacteria causes 2 cases per 100.000 humans each year. However, this could be ten times higher, since the disease is mild and self-limiting most of the time, so most people do not visit a health care professional (RIVM(18)).
B. Leptospirosis
This disease is caused by the bacteria Leptospira interrogans. According to Weese et al (2002) leptospirosis is the most widespread zoonotic disease in the world. The bacteria can infect a wide range of animals (Weese(16)).
Leptospirosis is in dogs and cats a relatively small zoonosis. It is not know exactly how many dogs are infected annually subclinically or asymptomatically, but according to Houwers et al (2009), each year around 10 cases occur in The Netherlands (Houwers(19)). RIVM states that each year 0,2 cases per 100.000 humans occur (RIVM(20)).
Infection in dogs is called Weill’s disease. Clinical signs can be peracute, acute, subacute and chronic. A peracute infection usually results in in sudden death with few clinical signs. Dogs with an acute infection are icteric, have diarrhea, vomit and may experience peripheral vascular collapse. The subacute form is generally manifested as fever, vomiting, anorexia, polydipsia, dehydration and in some cases severe renal disease can develop. Symptoms of a chronical infections are: fever of unknown origin, unexplained renal failure, or hepatic disease and anterior uveitis. The majority of infections in dogs are subclinical or chronic. In cats clinical disease is infrequent (Weese(16)).
According to Barmettler et al (2011), the risk of transmission of Leptospira from dogs to humans is just theoretical. All tested humans were exposed to infected dogs, but all were seronegative to the bacteria (Barmettler(17)).
The same bacteria that causes leptospirosis in dogs is responsible for the disease in rats, namely Leptospira interrogans. This bacteria is considered the most widespread zoonotic pathogen in the world and rats are the most common source of human infection, especially in urban areas (Himsworth(21)). According to the author, the bacteria asymptomatically colonizes the rat kidney and the rats shed the bacteria via the urine (Himsworth(9)). Bacteria can survive outside the rats for some time, especially in a warm and humid environment (RIVM(20)).
People become infected through contact with urine, or through contact with contaminated soil or water (Himsworth (21)). The Leptospira-bacteria can enter the body via the mucous or open wounds (Oomen(22)). The symptoms and severity of disease can be highly variable, ranging from asymptomatic to sepsis and death. Common complaints are: headache, nausea, myalgia and vomiting. Moreover, neurologic, cardiac, respiratory, ocular and gastrointestinal manifestations can occur (Weese JS(16)).
The prevalence in rats differs between cities and even between locations in the same city. Himsworth (2013) states that in Vancouver 11% of the tested rats was positive for Leptospira (Himsworth(9)). Another study by Easterbrook (2007) found 65,3% of all tested rats in Baltimore to be positive for the bacteria (Easterbrook(23)). Krojgaard (2009) found a prevalence between 48% and 89% in different location in Copenhagen (Krojgaard(24)).
C. Dermatophytosis (ringworm)
Dermatophytosis is a fungal dermatologic disease, caused by Microsporum spp. or Trichophyton spp. It causes disease in a variety of animals (Weese(16)). According to Kraemer (2012), the dermatophytes that occur in rabbits are Trichophyton mentagrophytes and Microsporum canis. Although the former is more common(Kraemer(25)).
Dermatophytes live in keratin layers of the skin and cause ringworm. They depend on human or animal infection for survival. Infection occurs through direct contact between dermatophyte arthrospores and keratinocytes/hairs. Transmission through indirect contact also occurs, for example through toiletries, furniture or clothes (Donnelly(26), RIVM(18)). Animals (especially cats) can transmit M. canis infection while remaining asymptomatic (Weese JS(16)).
The symptoms in both animals and humans can vary from mild or subclinical to severe lesions similar to pemphigus foliaceus (itching, alopecia and blistering). The skin lesions develop 1-3 weeks after infection(Weese JS). Healthy, intact skin cannot be infected, but only mild damage is required to make the skin susceptible to infection. No living tissue is invaded, only the keratinized stratum corneum is colonized. However, the fungus does induce an allergic and inflammatory eczematous response in the host (Donelly(26), RIVM(18)).
Dermatophytosis is not commonly occurring in humans. RIVM states that each year, 3000 per 100.000 humans get infected. Children between the age of 4 and 7 are the most susceptible to the fungal infection. In cats and dogs, the prevalence of M. canis is much higher: 23,3% according to Seebacher(27). The prevalence in rabbits is 3.3% (d’Ovidio(28)).
D. Echinococcosis
Echinococcus granulosus can be transmitted from dogs to humans. Dogs are the definitive hosts, while herbivores or humans are the intermediate hosts. Dogs can become infected by eating infected organs, for example from sheep, pigs and cattle (RIVM(29)) . The intermediate hosts develop a hydatid cyst with protoscoleces after ingesting eggs produced and excreted by definitive hosts. The protoscoleces evaginate in the small intestine and attach there(MacPherson(30)).
In most parts of Europe, Echinococcus granulosus occurs occasionally. However, in Spain, Italy, Greece, Romania and Bulgaria the bacteria is highly endemic.
Animals, either as definitive or as intermediate hosts, rarely show symptoms.
Humans, on the other hand, can show symptoms, depending on the size and site of the cyst and the growth rate. The disease can become life-threatening if a cyst in lungs or liver bursts. In that case a possible complication is an anaphylactic shock (RIVM(29)).
In the Netherlands, echinoccosis rarely occurs in humans. Between 1978 and 1991, 191 new patients were diagnosed, but it is not known how many of these were new cases. The risk of infection is higher in the case of bad hygiene and living closely together with dogs (RIVM(29)). In a study done by Fotiou et al (2012) the prevalence of Echinococcus granulosus is 1,1% (Fotiou(31)). The prevalence in dogs is much higher: 10,6% according to Barmettler et al (17).
E. Toxocariasis
Toxocariasis is caused by Toxocara canis or Toxocara cati. Toxocara is present in the intestine of 32% of all tested dogs, 39% of tested cats and 16%-26% of tested red foxes (Luty(32), LETKOVÁ(33)). In dogs younger than 6 weeks the prevalence can be up to 80% (Kantere) and in kittens of 4-6 months old it can be 64% (Luty(32)). The host becomes infected by swallowing the parasites embryonated eggs (Kantere(34)).
Dogs and red foxes are the definitive host of T. canis, cats of T. cati (Luty(32)). Humans are paratenic hosts. After ingestion, the larvae hatch in the intestine and migrate all over the body via blood vessels (visceral larva migrans). In young animals the migrations occurs via the lungs and trachea. After swallowing, the larvae mature in the intestinal tract.
In paratenic hosts and adult dogs that have some degree of acquired immunity, the larvae undergo somatic migration. There they remain as somatic larvae in the tissues. If dogs eat a Toxocara-infected paratenic host, larvae will be released and develop to adult worms in the intestinal tract (MacPherson(30)).
Humans can be infected by oral ingestion of infective eggs from contaminated soil, from unwashed hands or consumption of raw vegetables (MacPherson(30)).
The clinical symptoms in animals depend on the age of the animal and number, location and stage of development of worms. After birth, puppies can suffer from pneumonia because of tracheal migration and die in 2-3 days. 2-3 weeks after birth, puppies can show emaciation and digestive disturbance because of mature worms in the intestine and stomach. Clinical signs are: diarrhea, constipation, coughing, nasal discharge and vomiting.
Clinical symptoms in adult dogs are rare(MacPherson(30)).
In most human cases following infection by small numbers of larvae, the disease occurs without symptoms. Mostly children do get infected. VLM is mainly diagnosed in children of 1-7 years old. The symptoms can be general malaise, fever, abdominal complaints, wheezing or coughing. Severe clinical symptoms are mainly found in children of 1-3 years old.
Most of the larvae seem to be distributed to the brain and can cause neurological disease. Larvae do not migrate continuously. They rest periodically, and during such periods they induce an immunologically mediated inflammatory response (MacPherson(30)).
The prevalence in children is much lower than in adults, respectively 7% and 20%. The risk of infection with Toxocara spp. increases with bad hygiene (Overgaauw(36)). In the external environment, the eggs survive for months and consequently toxocariasis represents a significant public health risk (Kantere(34)) . High rates of soil contamination with toxocara eggs are demonstrated in parks, playgrounds, sandpits and other public places. Direct contact with infected dogs is not considered as a potential risk for human infection, because embryonation to the stage of infectivity requires a minimum of 3 weeks (MacPherson(30)).
F. Toxoplasmosis
Toxoplasmosis is caused by the protozoa Toxoplasma gondii. Cats are the definitive hosts and other animals and humans act as intermediate hosts. Infected cats excrete oocysts in the feces. These oocysts end up in the environment, where they are ingested by intermediate hosts (direct or indirect via food or water). In the intermediate hosts the protozoa migrates until it gets stuck. It is then encapsulated and stays at that place. If cats eat infected intermediate hosts they become infected.
Animals rarely show symptoms, although some young cats get diarrhea, encephalitis, hepatitis and pneumonia.
In most humans, infection is asymptomatic. Pregnant women can transmit the protozoa through the placenta and infect the unborn child. The symptoms in the child depend on the stage of pregnancy. An infection in early stages leads to severe deviations and in many cases to abortion. If the infection occurs in a later stage, premature birth is seen and symptoms of an infectious disease (fever, rash, icterus, anemia and an enlarged spleen or liver). Although, in most cases the symptoms start after birth. Most damage is done in the eyes (RIVM(37)).
Based on data of the RIVM and Overgaauw (1996) the disease that is most commonly transmitted to humans is toxoplasmosis. The prevalence was 40,5% in 1996. This number is reduced in the last few decades and Jones (2009) states that in 2009 the prevalence was 24,6% (Jones(38)). The prevalence rises with age, being 17,5% in humans younger than 20 years, and 70% in humans of 65 years and older. There is no increased risk of getting an infection if humans have a cat as a pet (RIVM(37)). Birgisdottir et al (2006) studied the prevalence in cats in Sweden, Estonia and Iceland. They found a prevalence of 54,9% , 23% and 9,8%, respectively in Estonia, Sweden and Iceland (Birgisdottir(39)).
G. Q-fever
The aetiological agent of Q-fever is the bacteria Coxiella burnetti. The bacteria has a very wide host range, including ruminants, birds and mammals such as small rodents, dogs, cats and horses. Accordingly, there is a complex reservoir system (Meredith(8)).
The extracellular form of the bacteria is very resistant, therefore it can be persistent in the environment for several weeks. It can also be spread by the wind, so direct contact with animals is not required for infection. Coxiella burnetti is found in both humans and animals in the blood, lungs, spleen, liver and during pregnancy in large quantities in the placenta and mammary glands. It is shed in urine and feces and during pregnancy in the milk (Meredith(8)).
Humans that live close to animals (like in the city) have a higher risk to get infected, since the mode of transmission is aerogenic or direct contact. The bacteria is excreted through the urine feces, placenta or amnionic fluid. After drying, it is aerogenically spread (RIVM(40)). Acute infection is characterized by atypical pneumonia and hepatitis and in some cases transient bacteraemia. The bacteria then haematogenously spreads, which results in an infection in the liver, spleen, bone marrow, reproductive tract and other organs. This is followed by the formation of granulomatous lesions in the liver and bone marrow and development of an endocarditis involving the aortic and mitral valve (Woldehiwet(41)).
On the other hand, there is little information about the clinical signs of Q fever in animals, but variable degrees of granulomatous hepatitis, pneumonia, or bronchopneumonia have been reported in mice (Woldehiwet(41)). In pregnant animals, abortion or low foetal birth weight can occur (Meredith(8), Woldehiwet(41)).
The prevalence in the overall human population in Europe is not high (2,7 %), but in risk groups like veterinarians, the prevalence can be as high as 83% (RIVM(40)).
Meredith et al, have developed a modified indirect ELISA kit adapted for use in multiple species. They tested the prevalence of C. burnetii in wild rodents (band vole, field vole and wood mouse), red foxes and domestic cats in the United Kingdom. The prevalence in the rodents was overall 17,3%. In cats it was 61.5% and in foxes 41,2% (Meredith(8)). In rabbits, the prevalence was 32,3% (González-Barrio(42)).
H. Pasteurellosis
Pasteurellosis is caused by Pasteurella multocida. This is a coccobacillus found in the oral, nasal and respiratory cavities of many species of animals (dog, cats, rabbits, etc). It is one of the most prevalent commensal and opportunistic pathogens in domestic and wild animals (Wilson(43), Giordano(44)). Human infections are associated with animal exposure, usually after animal bites or scratches (Giordano(44)). Kissing or licking of skin abrasions or mucosal surfaces of animals can also lead to infection. Transmission between animals is through direct contact with nasal secretions. (Wilson(43)).
In both animals and humans Pasteurella multocida causes chronic or acute infections that can lead to significant morbidity with symptoms of pneumonia, atrophic rhinitis, cellulitis, abscesses, dermonecrosis, meningitis and/or hemorrhagic septicaemia. In animals the mortality is significant, but not in human. This is probably due to the immediate prophylactic treatment of animal bite wounds with antibiotics. (Wilson(43))
Disease in animals appears as a chronic infection in nasal cavity, paranasal sinuses, middle ears, lacrimal and thoracic ducts of the lymph system and lungs. Primary infections with respiratory viruses or Mycoplasma species predisposes to a Pasteurella infection (Wilson(43)).
The incidence in humans is 0,19 cases per 100.000 humans (Nseir(45)). The prevalence in dogs and cats is 25-42% (Mohan(46)). The only known prevalence in rabbits is a 29,8% in laboratory animal facilities (Kawamoto(47)).
The majority of the human population lives in cities. As a result of this, in some countries the urban landscape encompasses more than half of the land surface. This leaves little space for the wildlife species living in the country. Some species are nowadays found more in urban areas than in their native environment. They have adapted to the urban ecosystems. This is a positive aspect for biodiversity in the cities. On the other hand, just like companion animals, this urban wildlife can transmit disease to humans (Dearborn(49)). In the following section, significant zoonoses of urban wildlife will be described.
A. Zoonoses of rats
The following zoonoses occur urban rats: Leptospirosis (see 2.2B) and rat bite fever.
Rat bite fever
The rat bite fever is caused by Streptobacillus moniliformis or S. minis(Chafe(50)). These bacteria are part of the normal oropharyncheal flora of the rat and it is thought to be present in rat populations worldwide.
Since the bacteria are part of the normal flora, the rats are not susceptible to the bacteria. In people, on the other hand, the bacteria can cause rat bite fever. The transmission occurs through the bite of an infected rat and through ingestion of contaminated food. The latter causes Haverhill fever.
The clinical symptoms are fever, chills, headache, vomiting, polyarthritis and skin rash. In Haverhill fever pharyngitis and vomiting may be more pronounced. If not treated, S. moniliformis infection can progress to septicemia with a mortality rate of 7-13% (Himsworth(21)).
The prevalence of Streptobacillus spp. in rats is 25% (Gaastra(51)). According to Trucksis et al (2016), rat bite fever is very rare in humans. Only a few cases each year occur (Trucksis(52)).
B. Zoonoses of mice
The zoonotical diseases that occur in mice are: hanta viruses, lymphocytic choriomeningitis, tularemia and Q-fever (see 2.2 G).
Hanta viruses
There are different types of hanta viruses, each carried by a specific rodent host species. In Europe, three types occur: Puumala virus(PUUV), carried by bank vole; Dobrava virus(DOBV), carried by yellow-necked mouse; Saaremaa virus(SAAV), carried by the striped field mouse (Heyman(7)). SAAV has been found in Estonia, Russia, South-Eastern Finland, Germany, Denmark, Slovenia and Slovakia. PUUV is very common in Finland, Northern Sweden, Estonia, the Ardennes Forest Region, parts of Germany, Slovenia and in parts of European Russia. DOBV has been found in The Balkans, Russia, Germany, Estonia and Slovakia (Heyman(7)).
Hantaviruses are transmitted via direct and indirect contact. Infective particles fare secreted in feces, urine and saliva (Kallio(53)).
The disease is asymptomatic in mice (Himsworth(21)). Humans on the other hand do get symptoms. All types of the Hanta virus cause hemorrhagic fever with renal syndrome (HFRS), but they differ in severity. HFRS is characterized by acute onset, fever, headache, abdominal pains, backache, temporary renal insufficiency and thrombocytopenia. In DOBV the extent of hemorrhages, requirement for dialysis treatment, hypotension and case-fatality rates are much higher than in PUUV or SAAV. Mortality is very low (approximately 0.1%)(Heyman(7)).
Hanta viruses are an endemic zoonosis in Europe. Tens of thousands of people get infected each year (Heyman(7)). The prevalence in mice is 9,5% (Sadkowska(54)).
Lymphocytic choriomeningitis
Lymphocytic choriomeningitis is a viral disease, caused by an arena virus (Cahfe(50)). The natural reservoirs of arenaviruses are rodent species. They are asymptomatically infected (Oldstone(55)).
In humans the disease is characterized by varying signs, from inapparent infection to the acute, fatal meningoencephalitis. The transmission of the disease is through mice bites and material contaminated with excretions and secretions of infected mice (Cahfe(50)).
The virus causes little or no toxicity to the infected cells. The disease- and associated cell and tissue injury- are caused mostly by activity of the hosts immune system. The antiviral response produces factors that act against the infected cells and damage them. Another factor is the displacement of cellular molecules that are normally attached to cellular receptors by viral proteins. This could result in conformational changes, which causes the cell membrane to become fragile and interfere with normal signalling events (Oldstone(55)).
The prevalence of lymphocytic choriomeningitis in human is 1,1 %(Lledó(56). In mice, the prevalence is 2,4% (Forbes(57)).
Tularemia
Tularemia is caused by the bacterium Franscisella tularensis. Only few animal outbreaks have been reported and so far only one outbreak in wildlife has been closely monitored(Dobay(10)). The bacteria can infect a large number of animal species. Outbreaks among mammals and human are rare. However, outbreaks can occur when the source of infection is widely spread and/or many people or animals are exposed. Outbreaks are difficult to monitor and trace, because mostly wild rodents and lagomorphs are affected (Dobay(10)).
People get infected in five ways: ingestion, direct contact with a contaminated source, inhalation, arthropod intermediates and animal bites. In animals the route of transmission is not yet known. The research of Dobay et al(2015) suggests that tularemia can cause sever outbreaks in small rodents such as house mice. The outbreak is self-exhausting in approximately three months, so no treatment is needed (Dobay(10)).
Tularemia is a potentially lethal disease. There are different clinical manifestations, depending on the route of infection. The ulceroglandular form is the most common and occurs after handling contaminated sources. The oropharyngeal form can be caused by ingestion of contaminated food or water. The pulmonary, typhoidal, glandular and ocular forms occur less frequently (Dobay(10)), Anda(58)).
In humans the symptoms of the glandular and ulceroglandular form are cervical, occipital, axillary or inguinal lymphadenopathy. The symptoms of pneumonic tularemia are fever, cough and shortness of breath (Weber(59)). Clinical manifestation of the oropharyngeal form include adenopathies on the elbow/ armpit/both, cutaneous lesions, fever, malaise, chills and shivering, painful sore throat with swollen tonsils and enlarged cervical lymph nodes (Sahn(60), Anda(58)).
The clinical features in animals are unspecific and the pathological effects vary substantially between different animal species and geographical locations. The disease can be very acute (for example in highly susceptible species like mice), with development of sepsis, liver and spleen enlargement and pinpoint white foci in the affected organs. The subacute form can be found in moderately susceptible species like hares. The symptoms are granulomatous lesions in lungs, pericardium and kidneys.
Infected animals are usually easy to catch, moribund or even dead (Maurin(61)).
Rossow et al (2015) states that the prevalence in humans is 2% (Rossow(62)). Highest prevalence found in small mammals during outbreak in Central Europe is 3,9% (Gurycová(63)).
C. Zoonoses of foxes
The zoonosis that can be transmitted from foxes to human are Q-fever (see 2.2G), toxocariasis (see 2.2E) and echinococcus multilocularis.
Echinococcus multilocularis
This is considered one of the most serious parasitic zoonosis in Europe. The red foxes are the main definitive hosts. The natural intermediate host are voles, but a lot of animals can act as accidental hosts, for example monkeys, human, pigs and dogs. The larval stage of Echinococcus multilocularis causes Alveolar echinococcosis (AE). The infection is widely distributed in foxes, with a prevalence of 70% in some areas. RIVM states that the prevalence in The Netherlands is 10-13%. The prevalence in humans differs throughout Europe, and has to do with the prevalence in foxes. If the prevalence in foxes is high, the prevalence in human increases. However, there has not been reported a prevalence higher than 0,81 per 100.000 inhabitants (RIVM(29)). Foxes living in urban areas pose a threat to the public health and there is concern that that risk may rise due to the suspected geographical spread of the parasite (Conraths(64)).
In foxes the helminth colonizes the intestines, but it does not cause disease. In intermediate hosts and accidental hosts cysts are formed after oral intake of eggs excreted by foxes, which causes AE. The size, site and growth rate of the larval stage determine the symptoms. Most of the time, infection starts in the liver, causing local deviations. The larvae grow invasively to other organs and blood vessels. It can take five to fifteen years before clear symptoms show (RIVM(29)). In human AE is a very rare disease, but incidences have increased in recent years.
D. Zoonoses of rabbits
The zoonoses that can be transmitted from rabbits to human are: Pasteurellosis (see 2.2H), tularemia (see 2.3B), Q fever (see 2.2G), dermatophytosis (see 2.2C) and cryptosporidiosis.
Cryptosporidiosis
Cryptosporidium is a protozoa. It is considered the most important zoonotic pathogen causing diarrhea in humans and animals. In rabbits, Cryptosporidium cuniculus (rabbit genotype) is the most common genotype (Zhang(65)). Two large studies have been done in rabbits, they showed a prevalence between 0,0% and 0,9% in rabbits (Robinson(66)).
The risks of cryptosporidiosis for the public health from wildlife are poorly understood. No studies of the host range and biological features of the Cryptosporidium rabbit genotype were identified. However human-infectious Cryptosporidium (including Cryptosporidium parvum) have caused experimental infections in rabbits and there is some evidence that his occurs naturally (Robinson(66)).
In human and neonatal animals, the pathogen causes gastroenteritis, chronic diarrhea or even severe diarrhea (Zhang(65), Robinson(66)). In >98% of these cases, the disease is caused by C. hominis or C. parvum, but recently, the rabbit genotype has emerged as a human pathogen. Little is known yet about this genotype, because only a few cases in humans were reported (Robinson(66)). Since little isolates have been found in humans and little is known about human infection with Cryptosporidium rabbit genotype, Robinson et al (2008) assumed this genotype is insignificant to public health and further investigation is needed (Robinson(67)).
E. Zoonoses of hedgehogs
Hedgehogs pose a risk for a number of potential zoonotic disease, for example microbial infections like Salmonella spp, Yersinia pseudotuberculosis, Mycobacterium marinum and dermatophytosis.
Salmonellosis
Salmonellosis is the most important zoonotic disease in hedgehogs. The prevalence of Salmonella in hedgehogs is 18,9%. The infection can either be asymptomatic or symptomatic. The hedgehogs that do show symptoms can display anorexia, diarrhea and weight loss. Humans get infected through ingestion of the bacteria, after handling the hedgehog or contact with feces (Riley(68)).
The Salmonella serotypes that are associated with hedgehogs are S. tilene and S. typhimurium (Woodward(69), Riley(68)).
Clinical manifestations in human (mainly adults) of both serotypes involve self-limiting gastroenteritis (including headache, malaise, nausea, fever, vomiting, abdominal pain and diarrhea (Woodward(69))), but bacteriamia, localized and endovascular infections may also occur (Crum Cianflone(70)). Infection with S. typhimurium and S. tilene is rare in humans, approximately 0,057 per 100.000 inhabitants (CDC(71))
Yersinia pseudotuberculosis.
No clinical symptoms for Yersinia pseudotuberculosis infection in hedgehogs are described in the literature. However, this bacteria causes a gastroenteritis in humans, characterized by a self-limiting mesenteric lymphadenitis, which mimics appendicitis. Complications can occur, which include erythema nodosum and reactive arthritis (Riley(68)). Since only Riley et al (2005) reported a case concerning Y. pseudotuberculosis, no information in available yet about the prevalence in hedgehogs or humans, or about the route of transmission. Although Riley et al (2005) claim that the zoonosis in commonly occurring (Riley(68)).
Myobacterium marinum
Mycobacterium marinum infection is not common in hedgehogs. The bacteria causes systemic myocbacteriosis. The porte d’entrée of the bacteria is through a wound or abrasion in the skin and the bacteria spreads systemically through the lymphatic system. This is also the way in which hedgehogs transmit the bacteria to human; the spines of the hedgehog can cause wounds and the bacteria can enter. Symptoms in human consist of clusters of papules or superficial nodules and can be painful. (Riley(68)). No information is reported regarding the prevalence of the bacteria in hedgehogs or humans.
Dermatophytosis
Dermatophytosis has been seen in hedgehogs. The most isolated dermatophyte is Trichophyton mentagrophytes var. erinacei. Microsporum spp. have also been reported. Lesions in the hedgehog are similar to those in other species: nonpruritic , dry, scaly skin with bald patches and spine loss. Hedgehogs can also be asymptomatic carriers, and that is a risk for potential zoonotic transmission (Riley(68)).
In human, Trichophyton mentagrophytes var. erinacei causes a local rash with pustules at the edges and an intensely irritating and thickened area in centre of the lesion. This usually resolves spontaneously after 2-3 weeks (Riley(68)).
Few cases of Trichophyton mentagrophytes var. erinacei have been reported (Pierard-Franchimont(72), Schauder(73), Keymer(74)), but no prevalence is known for humans and hedgehogs.
F. Zoonoses of bats
According to Calisher et al (2009) bat viruses that are proven to cause highly pathogenic disease in human are rabies virus and related lyssaviruses, Nipah and Hendra viruses, and SARS-CoV-like virus (Calisher(75)). Only the former is relevant for this review, since Nipah and Hendra do not occur in Europe (Munir(76)) and SARS is not directly transmitted to human (Hu(77)).
Rabies virus and related lyssaviruses
The rabies virus is present in the saliva of infected animals. Accordingly, the virus is transmitted from mammals to human through a bite (Calisher(75)).
Symptoms are equal in animals and humans. The disease starts with a prodromal stage. Symptoms are non-specific, and consist of fever, itching and pain near the site of the bite wound.
Subsequently follows the furious stage. Clinical features are hydrophobia (violent inspiratory muscle spasms, hyperextension and anxiety after attempts to drink), hallucinations, fear, aggression, cardiac tachyarrhythmias, paralysis and coma.
The final stage is the paralytic stage. It is characterized by ascending paralysis and loss of tendon reflexes, sphincter dysfunction, bulbar/respiratory paralysis, sensory symptoms, fever, sweating, gooseflesh and fasciculation.
Untreaded, the disease is fatal in approximately five days after showing the first symptoms (Warrell(78)).
Lyssaviruses from bats are related to the rabies virus. There are seven lyssavirus genotypes. Some of these cause disease in human, similar to rabies. Others, on the other hand, do not cause disease. Although it is still unclear, transmission is thought to be through bites (Calisher(75)).
Since 1977 4 cases of human rabies coming from a bat bite have been reported in The Netherlands. In bats living there, the prevalence is 7% (RIVM).
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