On-line version ISSN 2224-9435
J. S. Afr. Vet. Assoc. vol.86 n.1 Cape Town 2015
Bruce H. NodenI; Minty SoniII
IDepartment of Entomology and Plant Pathology, Oklahoma State University, United States
IIRhino Park Veterinary Clinic, Windhoek, Namibia
Namibia has a rich history in veterinary health but little is known about the vector-borne diseases that affect companion dogs and cats. The aim of this review is to summarise the existing published and available unpublished literature, put it into a wider geographical context, and explore some significant knowledge gaps. To date, only two filarial pathogens (Dirofilaria repens andAcanthocheilonema dracunculoides) and three tick-borne pathogens (Babesia canis vogeli,Hepatozoon canis and Ehrlichia canis) have been reported. Most studies have focused solely on dogs and cats in the urban Windhoek and surrounding areas, with almost nothing reported in rural farming areas, in either the populous northern regions or the low-income urban areas where animal owners have limited access to veterinary services. With the development of several biomedical training programmes in the country, there is now an excellent opportunity to address zoonotic vector-borne diseases through a One Health approach so as to assess the risks to small companion animals as well as diseases of public health importance.
Namibia consists of a large land area (823 290 km2) with a relatively small population (2 160 000) (CIA 2014) living in 13 regions. The northern part of the country is more humid and tropical while the central and southern regions are characterised by arid, scrubland and desert (Rohde & Hoffman 2012). Most of the human population (70%) lives in the northern one-third of the country with the rest spread into Windhoek or small urban centres scattered throughout game ranches and livestock farms in the central and southern areas (Maps, Best Country 2012). Synchronised with the climate and larger population, a higher number of Neglected Tropical Diseases (NTD) have been reported in the northern regions compared with the central and southern regions (Noden & Van der Colf2013). In contrast, there is no published record of the distribution of dogs and cats and their specific vector-borne diseases throughout the country.
The rich history of veterinary health of Namibia has focused mostly on livestock and game farms which are important to the economy (OIE 2014; Schneider 2012). To date, very little attention has been paid to the health of small companion animals in the national research agenda (Noden & Van der Colf 2013). The only published estimate of domestic canines in Namibia is from a 2011 World Health Organization (WHO) rabies report which estimated a total number of 104 645 dogs in the country (WHO 2013). The spectrum of small companion animals in Namibia varies from well cared for pets to strays in urban areas, farm dogs and cats with minimal to no contact with veterinary services, and free-roaming populations in the lower-income areas and northern regions which have limited to no contact with their owners (Haimbodi, Mavenyengwa & Noden 2014). While the involvement of dogs and cats in zoonotic disease transmission is well documented in Africa as well as globally (Dantas-Torres 2007; Kelly et al. 1998; Nicholson et al. 2010), the lack of the most basic information in Namibia indicates that they may be directly or indirectly acting as reservoirs for infectious disease to other animals as well as human populations (Noden & Van der Colf 2013).
Gaining independence in 1990, Namibia has steadily been building its health infrastructure and lines of communication as regards infectious disease notification. However, the nascent biomedical programmes, including veterinary science, have yet to lead the discussion on vector-borne diseases of dogs and cats in the country (Noden & Van der Colf2013). To date, most available information is found in unpublished 'grey' literature (theses, reports) which provides small glimpses into possible disease systems already present. These programmes could begin using this information to build an understanding of the local ecology and epidemiology of each disease. The aim of this review, then, is to summarise the existing literature (published and unpublished [theses, reports and known research]) involving vector-borne diseases of companion dogs and cats in Namibia. Discussion will include pathogens reported in small companion animals in the southern Africa region but not yet reported in Namibia. For sake of brevity, the review will not cover disease cycles, pathogenesis of diseases nor the treatment regimens which have been adequately covered elsewhere. Mention will be made of the potential risk of transmission of zoonotic pathogens between dogs and cats and human owners; however, a full review of the vector-borne pathogens that are affecting human populations in Namibia already exists (Noden & Van der Colf 2013). While an effort was made to locate relevant publications, it cannot be assumed that every study was identified. The review ends with a brief discussion of possible future directions.
The presence of Dirofilaria in Namibia has not been officially recorded in the published literature (Simon et al. 2012), but Dirofilaria repens and Acanthocheilonema dracunculoideshave both been reported (Table 1).
Dirofilaria repens is normally associated with subcutaneous infections with limited reports of complications in southern Africa (Bredal et al.1998; Schwan et al. 2000). Canines are considered to be reservoirs for infections with a mandatory transmission between vertebrate hosts by mosquito vectors (Simon et al. 2012). The frequent reports of D. repens as being involved in human cases together with the recent suggested involvement of cats as reservoirs (Simon et al. 2012) indicate a need to better understand this pathogen in its local context.
Clinical-pathological infections of D. repenswere first recorded in central Namibia in 1994 with 80% (n = 8) of cases occurring in Windhoek (Schwan 2009). Between 1990 and 2007, 50% (n = 5) of cases were found in crossbred dogs, whereas 20% (n = 2) were found in domestic shorthair cats. Stuben (2004) followed by reporting the occurrence ofDirofilaria sp. in 3.2% of 600 canine blood smears obtained in central Namibia. Finally, in 2011, five clinical cases of Dirofilaria sp. out of 10 suspected dogs were identified by physical signs and blood smear at a local veterinary clinic (Noden et al. 2011).
Dirofilaria are transmitted by mosquitoes but few studies in Africa have identified with an certainty the mosquito species responsible for mode of transmission. Aedes aegypti has been incriminated as a vector of D. repens in Africa (Anyanwu et al. 2000; Magayuka 1973) as well as in other parts of the world (Simon et al.2012). A recent survey in six locations across Windhoek determined the presence of A. aegypti in most low-income areas where veterinary contact is not normally available to affected animals and where the possibilities could exist for higher risk of transmission to humans (Noden et al. 2014a).
Acanthocheilonema dracunculoides is a vector-borne apathogenic nematode involving domestic canines and some sylvatic carnivores such a spotted hyena and aardwolf (Schwan & Schroter 2006). Schwan and Schroter (2006) reported two clinical cases of A. dracunculoides in dogs from Windhoek. The principal intermediate hosts are the louse fly (Hippobosca longipennis) or the brown dog tick (Rhipicephalus sanguineus) which is the main tick species reported on dogs throughout central and southern Namibia (Matthee et al.2010).
While two helminth species have been reported in Namibia, no information exists about whether Dirofilaria immitis orAcanthocheilonema reconditum (formerlyDipetalonema reconditum) (Nematoda: Onchocercidae) (vectored by fleas [Ctenocephalides canis and Ctenocephalides felis] and lice [Heterodoxus spiniger andTrichodectes canis]) are present in Namibian dogs and cats. Given that most reports are from arid central Namibia, there is a critical lack of epidemiological information on infections and the identity and distribution of arthropod vectors throughout the country.
Tick-borne pathogens of companion dogs and cats
A variety of tick-borne diseases including protozoa (Babesia sp., Theileria sp.,Hepatozoon canis) and bacteria (Ehrlichia canis, Anaplasma platys, Spotted fever group rickettsiae) have been reported in domestic canines and felines throughout southern Africa (Chitanga, Gaff & Mukaratirwa 2014). To date, only Babesia sp. Hepatozoon canis andEhrlichia canis have been reported in domestic canines in Namibia (Table 1).
Babesiosis is an important protozoal vector-borne disease of small companion animals throughout the world (Solano-Gallego & Baneth 2011). Babesia canis vogeli andBabesia canis rossi are the only subspecies ofB. canis to have been reported in southern Africa (Matjila et al. 2008b). Babesia canis rossi causes the most severe disease, whereasB. c. vogeli produces a milder, subclinical infection. Babesia sp. are transmitted by a variety of tick species, includingHaemaphysalis elliptica (formerlyHaemaphysalis leachi) (vector for B. c. rossi) and R. sanguineus (vector for B. c. vogeli), which are commonly reported on dogs and cats in South Africa (Bryson et al. 2000; Horak & Matthee 2003).
The first report of B. canis in Namibia occurred in the central highlands in 2004 in a study evaluating 600 dogs in low-income communities surrounding Okahandja (Stuben2004). The seroprevalence of Babesiosis was high (69.0%) and the reported blood smear observations of sick dogs were positive for B. c. vogeli but parasitaemia was low (0.3%). Following this report, Noden et al. (2011) reported one probable case of B. c. vogeli in a Windhoek clinic, diagnosed by blood smear. The main vector for B. c. vogeli in rural, communal areas of South Africa is R. sanguineus which is also the principal tick species found on dogs in central Namibia (Matthee et al. 2010). To date, no studies have identified whether B. c. rossi, the more deadly form found in urban areas of South Africa (Matjila et al. 2008b), is also present in Namibia. Another question is whether feline Babesiosis, recently described in South Africa (Bosman, Venter & Penzhorn 2007; Bosman et al. 2013), also occurs in Namibia.
Hepatozoon canis is a protozoan parasite which has a complex life-cycle that involves ticks (Baneth, Samish & Shkap 2007). In southern Africa, H. canis has been reported in wild felines and canids (Matjila et al. 2008a; Williams et al. 2014). The main vector species in southern Africa is considered to be R. sanguineus, but, to date, H. canis has yet to be found in R. sanguineus collected in sub-Saharan Africa. In Namibia, only one case ofH. canis has been recorded in a dog diagnosed in a veterinary clinic in urban Windhoek that was based only on signs and symptoms and a blood smear (Noden et al. 2011).
Ehrlichia canis is a globally important pathogen affecting canines (Harrus & Waner 2011) that has been reported in Zimbabwe and South Africa by seroprevalence studies. The main tick vector is assumed to be R. sanguineus(Matthewman et al. 1997a).
The first published record of E. canis in Namibia was by Stuben (2004) who noted clinical symptoms in 23.5% of 600 dogs studied in a low-income area around Okahandja in central Namibia. 14.2% had evident morulae in their blood smear analysis. The incidence of ehrlichiosis was significantly higher in dogs with poor nutritional status, poor grooming and heavy tick infestation.
This work was followed by Manyarara et al. (2015) who demonstrated a canine seroprevalence against E. canis using an ELISA-based assay. Dogs presenting at a clinic with signs of E. canis infection had a significantly higher seroprevelence (86.6%) compared with other dogs (41.6%). The location of habitation was significant, with a high percentage of E. canis-exposed dogs living in the northern or northwestern part of Windhoek. As the first study to establish E. canis serologically as a significant pathogen to dogs in central Namibia, it was notable that the highest proportion of positive dogs came from the low-income areas. It is assumed that the principal tick vector in Namibia is R. sanguineus as this is the primary tick recovered from dogs in veterinary clinics in central and southern Namibia (Matthee et al.2010), but this has yet to be confirmed.
To date, there is limited to no information in Namibia concerning the following tick-borne pathogens which have been reported elsewhere in southern Africa.
Theileria sp. and Anaplasma platys
Whereas both have been reported in South African dogs (Inokuma et al. 2005; Matjila et al. 2008c), these pathogens have yet to be reported in Namibia.
Spotted fever group rickettsiae
Tick-transmitted spotted fever group (SFG) rickettsiae in southern Africa mainly involvesRickettsia conorii and Rickettsia africae(Pretorius, Jensenius & Birtles 2004). The role of dogs and cats as reservoirs for these pathogenic bacteria was hypothesised in southern Africa studies in the 1990s (Kelly & Mason 1991; Matthewman et al. 1997a). Recently, domestic canines been implicated as reservoirs of SFG rickettsiae in many areas of the world, except in Africa (Izzard et al. 2010; Ortuno et al. 2009). The presence of SFG rickettsiae species has not yet been reported in Namibian dogs and cats; however, serological evidence has been reported in human populations (Noden & Van der Colf2013; Noden et al. 2014b). While the main tick reservoir or vector species in Africa for R. conorii and R. africae is probably R. sanguineus (Walker et al. 2007), the potential involvement of seven other known Namibian tick vector species remains unknown (Noden & Van der Colf 2013).
Coxiella burnetii (Q fever)
Coxiella burnetii, the causative agent for Q fever, is underreported in southern Africa. Normally associated with cattle, sheep and goats (Kelly et al. 1993; Magwedere et al.2012), seroprevalence has been reported for cats and dogs from Zimbabwe and South Africa (Kelly et al. 1993; Matthewman et al.1997b). Normally, exposure to C. burnetiioccurs by aerosol or milk products, but ticks also act as reservoirs (Kelly et al. 1993). Five species of Namibian tick could be reservoirs or carriers of Coxiella (Noden & Van der Colf2013), but the involvement of companion dogs and cats remains unknown (Magwedere et al.2012).
Flea-borne pathogens of companion animals
Rickettsia typhi (typhus group) and Rickettsia felis (spotted fever group) are rickettsiae of public health importance transmitted by fleas (Azad et al. 1997). Normally not associated with companion animals, recently dogs and cats were implicated as reservoirs for infection in Europe, thus posing a risk for zoonotic transmission to human populations (Nogueraset al. 2013a, b). Serological evidence for bothRickettsia species has been recorded in cats and dogs from Zimbabwe and South Africa (Matthewman et al. 1997a). The main vector species of these bacteria in Africa is the rat flea, Xenopsylla cheopis, and the cat flea, C. felis (Azad et al. 1997; Laudisoit et al. 2014).
Cat scratch fever
Bartonella henselae is another flea-borne bacteria of public health importance with zoonotic transmission potential reported in dogs, cats and humans in South Africa (Maggiet al. 2013; Pretorius et al. 1999), Zimbabwe (Kelly et al. 1998) and Namibia (Noden et al.2014b). Vectored by the cat flea, C. felis, or the rat flea, X. cheopis (Laudisoit et al. 2014), infected cats and their fleas have been identified as a significant risk factor for patients infected with HIV in South Africa (Frean, Arndt & Spencer 2002).
Similarly to tick-borne diseases, there is a dearth of information in Namibia and the southern Africa region concerning the ecology of fleas on small companion animals, the pathogens they carry and their possible zoonotic impact in veterinary and public health. The relatively high seropositivity rates in healthy human blood donors (Noden et al.2014b) suggest that infected fleas exist in close proximity to pet owners, but few veterinarians in Namibia even mention fleas on dogs and cats. Further study is needed to identify areas of Namibia most prone to domestic flea infestations and the possibility of flea-borne rickettsiae among canine and feline populations and local flea populations.
Important pathogen of public health importance with possible canine involvement
Leishmania is an NTD which annually affects millions of domestic dogs and cats and humans around the world (Pennisi 2015). It has been reported in the arid areas of southern Africa (South Africa [Rutherfoord & Uys 1978], Namibia [Grove 1989], and Botswana [Schwartz et al. 2012]). Both the cutaneous and visceral forms are transmitted by sandflies and the natural reservoirs are jackals, dogs and hyrax, with humans serving as accidental hosts. In recent years, the influence of dogs or cats, particularly rural or shelter canines, as reservoirs of L. infantum and other Leishmaniaspecies has been increasingly recognised in South America and Europe (Dantas-Torres2007; Pennisi 2015; Rougeron et al. 2011), with a few reported cases in north and west Africa (Berdjane-Brouk et al. 2012; Guessous-Idrissi et al. 1997). Nothing, besides historical reports and one recent tourist case study, is known about the ecology and distribution of this important pathogen in southern Africa.
Autochthonous cutaneous Leishmania (CL), aligned with the Leishmania tropica group, has been reported in Namibia since the 1970s (Grove 1989). Most of the CL cases between 1970 and 1989 were geographically located in the southern and central regions and linked to a history of picnicking, camping or living near hyrax (Procavia capensis) colonies. Although no human clinical data has been published since 1989, clinical cases involving both canines (OIE 2014) and humans (Noden, unpublished data 2012) continue to be reported in Namibia.
Normally, there is not much focus on autochthonous CL cases involving rural dogs or humans as the risk is considered low. However, as events in southern Namibia in the early 1970s demonstrated, if autochthonous CL is not investigated, it can suddenly become an epidemic should ecological and environmental conditions change (Noden & Van der Colf2013). In the mid-1970s, a small CL outbreak occurred among humans in southern Namibia during a period when hyrax populations (the reservoir hosts) were exploding because of good rains and the lack of a predator. The Verreaux's (Black) eagle populations had significantly diminished because sheep farmers believed they were targeting their lambs, when in actual fact the eagles almost exclusively prefer the hyrax. This concurrent event coincided with humans camping and fishing near hyrax burrows which contained infected sandflies looking for blood meals. The fact thatLeishmania continues to be reported vaguely in the OIE biannual reports in Namibia and occasional human encounters involving stories of a non-healing insect bite suggest that CL is probably still present and is being locally transmitted by sandflies. However, nothing is known about its epidemiology or the risks of acquiring infection. The use of domestic dogs on area farms as sentinels throughout the central and southern regions of Namibia would provide an excellent means of determining potential 'hot spots' where a zoonotic infection could spill over into human populations. While Leishmania is prone to outbreaks that could affect the tourism industry, often infections in dogs are often not curable, which results in significant morbidity and a drawn-out period until death.
Points to consider
Go beyond the urban areas of central Namibia
Most of the Namibia-based studies summarised in this review focused solely on dogs and cats in urban areas with relatively affluent owners working with established veterinary practices from Windhoek and the immediate surrounding central regions (Table 1). This is convenience sampling at best. As in the case of Leishmania, little to nothing is known about what dogs and cats are exposed to in rural farming areas, in the populous northern regions or in the low-income urban areas where animal owners have limited access to veterinary services or no money to pay for them. There is a need for the developing veterinary health programme to focus on the whole country when evaluating the epidemiology of each pathogen in order to gain a holistic understanding of its unique ecology and distribution within Namibia.
One Health assessment of vector-borne disease epidemiology in Namibia
Use of sentinel animals to focus on diseases of public health importance
The One Health paradigm is a way to consider zoonotic diseases in a holistic way, focusing on the environment, animals, and humans, by addressing specific aspects of disease epidemiology at a reduced cost (Okello et al.2014; Yancey et al. 2014). One globally accepted idea is the use of dogs and cats as sentinel animals in public health surveillance efforts (Schmidt 2009; Schurer et al. 2012). By strategically focusing on particular areas in the country to reduce costs, blood samples could be obtained from companion dogs and cats instead of people. These could then be tested for exposure to various vector-borne pathogens of importance to both veterinary and public health (Yancey et al. 2014) (Table 2). This method has been used in other countries to monitor exposure rates in local areas for many vector-borne diseases (De Paiva Diniz et al. 2007; Izzard et al. 2010; Ortuno et al. 2009; Resnick et al. 2008; Schurer et al. 2012; Smith et al. 2012).
For example, a One Health approach focusing on farm dogs and cats could be used to provide critical information regarding the Crimean Congo Hemorrhagic Fever virus (CCHFV), an extremely dangerous tick-borne virus that occasionally occurs in Namibia. Even through infrequent cases indicate the virus is autochthonous in the country (Noden & Van der Colf 2013), it is a BSL-4 level virus and an outbreak could have a critical impact on the agricultural and tourism sectors. To date, almost nothing is known about the ecology and epidemiology of this lethal zoonotic pathogen in Namibia (Noden & Van der Colf 2013). The use of serological tests from companion dogs or cats on farms could provide useful epidemiological data as to potential 'hot-spots' in the central and southern regions to which more effort could be directed to study the ecology, vectors and risk potential. Such an approach was taken in the mid-1970s to describe the epidemiology of CCHFV in South Africa using a variety of serum samples from various mammals, including domestic dogs (Shepherd et al. 1987). An exposure prevalence of 6% was reported in 1978 canine samples tested from around South Africa.
In conclusion, to date, only five vector-borne pathogens affecting domestic dogs and cats have been reported in Namibia. However, many others are known to occur within the southern Africa region, some of which are zoonotic and can spread to human populations. As highlighted, there is much work to be done by nascent training programmes throughout the region. In addition to monitoring the impact of other pathogens on small companion animals in rural and urban areas, there is a need to verify the arthropod vectors of these diseases. The useful development of a One Health paradigm between the veterinary and public health services could assist in effectively tracking the epidemiology of these important pathogens in small companion animals as well as in the public health domain.
The authors would like to thank the Permanent Secretary of the Namibian Ministry of Agriculture, Water and Forestry and the Directorate of Veterinary Services for their permission to publish this article. B.H.N. was partially supported by the Oklahoma Agricultural Experiment Station (OKL-02909).
The authors declare that they have no financial or personal relationships which may have inappropriately influenced them in writing this article.
B.H.N. (Oklahoma State University) was the project leader. B.H.N. and M.S. (Rhino Park Veterinary Clinic) procured the published and grey literature studies cited and contributed equally to the writing of the manuscript.
Anyanwu, I.N., Agbede, R.I., Ajanusi, O.J., Umoh, J.U. & Ibrahim, N.D., 2000, 'The incrimination of Aedes (Stegomyia) aegypti as the vector of Dirofilaria repens in Nigeria',Veterinary Parasitology 92, 319-327. PMID: 10996744, http://dx.doi.org/10.1016/S0304-4017(00)00311-3 [ Links ]
Azad, A.F., Radulovic, S., Higgins, J.A., Noden, B.H. & Troyer, J.M., 1997, 'Flea-borne rickettsioses: Ecologic considerations',Emerging Infectious Diseases 3(3), 319-327. PMID: 9284376, http://dx.doi.org/10.3201/eid0303.970308 [ Links ]
Baneth, G., Samish, M. & Shkap, V., 2007, 'Life cycle of Hepatozoon canis (Apicomplexa: Adeleorina: Hepatozoidae) in the tickRhipicephalus sanguineus and domestic dog (Canis familiaris)', Journal of Parasitology 93, 283-299. PMID: 17539411, http://dx.doi.org/10.1645/GE-494R.1 [ Links ]
Berdjane-Brouk, Z., Kone, A.K., Djimde, A.A., Charrel, R.N., Ravel, C., Delaunay, P. et al., 2012, 'First detection of Leishmania major DNA in Sergentomyia (Spelaeomyia) darlingi from cutaneous leishmaniasis foci in Mali', PLoS One7(1), e28266. PMID: 22276095, http://dx.doi.org/10.1371/journal.pone.0028266 [ Links ]
Bosman, A.-M., Oosthuizen, M.C., Venter, E.H., Steyl, J.C.A., Gous, T.A. & Penzhorn, B.L., 2013, 'Babesia lengau associated with cerebral and haemolytic babesiosis in two domestic cats', Parasite and Vectors 6, 128. PMID: 23634743, http://dx.doi.org/10.1186/1756-3305-6-128 [ Links ]
Bosman, A.-M., Venter, E.H. & Penzhorn, B.L., 2007, 'Occurrence of Babesia felis and Babesia leo in various wild felid species and domestic cats in southern Africa, based on reverse line blot analysis', Veterinary Parasitology 144, 33-38. PMID: 17084029, http://dx.doi.org/10.1016/j.vetpar.2006.09.025 [ Links ]
Bredal, W.P., Gjerde, B., Eberhard, M.L., Aleksandersen, M., Wilhelmsen, D.K. & Mansfield, L.S., 1998, 'Adult Dirofilaria repensin a subcutaneous granuloma on the chest of a dog', Journal of Small Animal Practice 39, 595-604. PMID: 9888115, http://dx.doi.org/10.1111/j.1748-5827.1998.tb03715.x [ Links ]
Bryson, N.R., Horak, I.G., Hohn, E.W. & Louw, J.P., 2000, 'Ectoparasites of dogs belonging to people in resource-poor communities in North West Province, South Africa', Journal of the South African Veterinary Association 71, 175-179. PMID: 11205167, http://dx.doi.org/10.4102/jsava.v71i3.709 [ Links ]
Chitanga, S., Gaff, H. & Mukaratirwa, S., 2014, 'Tick-borne pathogens of potential zoonotic importance in the southern African Region',Journal of the South African Veterinary Association 85, 1-3. PMID: 25685942, http://dx.doi.org/10.4102/jsava.v85i1.1084 [ Links ]
CIA, 2014, World fact book: Africa: Namibia. [Online], viewed from https://www.cia.gov/library/publications/the-world-factbook/geos/wa.html. [ Links ]
Dantas-Torres, F., 2007, 'The role of dogs as reservoirs of Leishmania parasites, with emphasis on Leishmania (Leishmania)infantum and Leishmania (Viannia)braziliensis', Veterinary Parasitology 149, 139-146. PMID: 17703890, http://dx.doi.org/10.1016/j.vetpar.2007.07.007 [ Links ]
de Paiva Diniz, P.P.V., Schwartz, D.S., De Morais, H.S.A. & Breitschwerdt, E.B., 2007, 'Surveillance for zoonotic vector-borne infections using sick dogs from southeastern Brazil', Vector-borne and Zoonotic Diseases 7, 689-698. PMID: 18021025, http://dx.doi.org/10.1089/vbz.2007.0129 [ Links ]
Frean, J., Arndt, S. & Spencer, D., 2002, 'High rate of Bartonella henselae infection in HIV-positive outpatients in Johannesburg, South Africa', Transactions of the Royal Society of Tropical Medicine and Hygiene 96, 549-550. PMID: 12474487, http://dx.doi.org/10.1016/S0035-9203(02)90437-2 [ Links ]
Grove, S.S., 1989, 'Leishmaniasis in South West Africa/Namibia to date', South African Medical Journal 75, 290-292. PMID: 2648612. [ Links ]
Guessous-Idrissi, N., Chiheb, S., Hamdani, A., Riyad, M., Bichichi, M., Hamdani, S. et al., 1997, 'Cutaneous leishmaniasis: An emerging epidemic focus of Leishmania tropica in north Morocco', Transactions of the Royal Society of Tropical Medicine and Hygiene 91, 660-663. PMID: 9509172, http://dx.doi.org/10.1016/S0035-9203(97)90511-3 [ Links ]
Haimbodi, F., Mavenyengwa, R.T. & Noden, B.H., 2014, 'Knowledge and practices about rabies and companion animal care among residents of two towns in northern Namibia',Southern African Journal of Infectious Diseases29, 141-146. [ Links ]
Harrus, S. & Waner, T., 2011, 'Diagnosis of canine monocytotropic ehrlichiosis (Ehrlichia canis): An overview', Veterinary Journal 187, 292-296. PMID: 20226700, http://dx.doi.org/10.1016/j.tvjl.2010.02.001 [ Links ]
Horak, I.G. & Matthee, S., 2003, 'Parasites of domestic and wild animals in South Africa. XLIII. Ixodid ticks of domestic dogs and cats in the Western Cape Province', Onderstepoort Journal of Veterinary Research 70, 187-195. PMID: 14621314. [ Links ]
Inokuma, H., Oyamada, M., Kelly, P.J., Jacobson, L.A., Fournier, P.-E., Itamoto, K. et al., 2005, 'Molecular detection of a newAnaplasma species closely related toAnaplasma phagocytophilum in canine blood from South Africa', Journal of Clinical Microbiology 43, 2934-2937. PMID: 15956424, http://dx.doi.org/10.1128/JCM.43.6.2934-2937.2005 [ Links ]
Izzard, L., Cox, E., Stenos, J., Waterston, M., Fenwick, S. & Graves, S., 2010, 'Serological prevalence study of exposure of cats and dogs in Launceston, Tasmania, Australia to spotted fever group rickettsiae', Australian Veterinary Journal 88, 29-31. PMID: 20148824, http://dx.doi.org/10.1111/j.1751-0813.2009.00538.x [ Links ]
Kelly, P.J. & Mason, P.R., 1991, 'Tick-bite fever in Zimbabwe - Survey of antibodies to Rickettsia conorii in man and dogs, and of rickettsia-like organisms in dog ticks', South African Medical Journal 80, 233-236. PMID: 1887350. [ Links ]
Kelly, P.J., Matthewman, L.A., Mason, P.R. & Raoult, D., 1993, 'Q fever in Zimbabwe. A review of the disease and the results of a serosurvey of humans, cattle, goats and dogs',South African Medical Journal 83, 21-25. PMID: 8424194. [ Links ]
Kelly, P.J., Rooney, J.J., Marston, E.L., Jones, D.C. & Regnery, R.L., 1998, 'Bartonella henselae isolated from cats in Zimbabwe',Lancet 351, 1706. PMID: 9734895, http://dx.doi.org/10.1016/S0140-6736(05)77744-8 [ Links ]
Laudisoit, A., Falay, D., Amundala, N., Akaibe, D., De Bellocq, J.G., Van Houtte, N. et al., 2014, 'High prevalence of Rickettsia typhi andBartonella species in rats and fleas, Kisangani, Democratic Republic of the Congo', American Journal of Tropical Medicine and Hygiene 90, 463-468. PMID: 24445202, http://dx.doi.org/10.4269/ajtmh.13-0216 [ Links ]
Magayuka, S.A., 1973, 'Development of filarial parasites in mosquitos in north-east Tanzania',Bulletin of the World Health Organization 49, 110-111. PMID: 4151063. [ Links ]
Maggi, R.G., Mascarelli, P.E., Havenga, L.N., Naidoo, V. & Breitschwerdt, E.B., 2013, 'Co-infection with Anaplasma platys, Bartonella henselae and Candidatus mycoplasma haematoparvum in a veterinarian', Parasites and Vectors 6, 103. PMID: 23587235, http://dx.doi.org/10.1186/1756-3305-6-103 [ Links ]
Magwedere, K., Hemberger, M.Y., Hoffman, L.C. & Dziva, F., 2012, 'Zoonoses: A potential obstacle to the growing wildlife industry of Namibia', Infection, Ecology and Epidemiology2, Art. 18365. PMID: 23077724, http://dx.doi.org/10.3402/iee.v2i0.18365 [ Links ]
Manyarara, R., Tubbesing, U., Soni, M. & Noden, B.H., 2015, 'Serodetection of Ehrlichia canis amongst dogs in central Namibia',Journal of the South African Veterinary Association 86(1), 3 pages. PMID: 26244587, http://dx.doi.org/10.4102/jsava.v86i1.1272 [ Links ]
Maps, Best Country, 2012, Population density map of Namibia [Online], viewed from http://www.bestcountryreports.com/Population_Map_Namibia.php. [ Links ]
Matjila, P.T., Leisewitz, A.L., Jongejan, F., Bertschinger, H.J. & Penzhorn, B.L., 2008a, 'Molecular detection of Babesia rossi andHepatozoon sp. in African wild dogs (Lycaon pictus) in South Africa', Veterinary Parasitology157, 123-127. PMID: 18752897, http://dx.doi.org/10.1016/j.vetpar.2008.07.016 [ Links ]
Matjila, P.T., Leisewitz, A.L., Jongejan, F. & Penzhorn, B.L., 2008b, 'Molecular detection of tick-borne protozoal and ehrlichial infections in domestic dogs in South Africa', Veterinary Parasitology 155, 152-157. PMID: 18502588, http://dx.doi.org/10.1016/j.vetpar.2008.04.012 [ Links ]
Matjila, P.T., Leisewitz, A.L., Oosthuizen, M.C., Jongejan, F. & Penzhorn, B.L., 2008c, 'Detection of a Theileria species in dogs in South Africa', Veterinary Parasitology 157, 34-40. PMID: 18687528, http://dx.doi.org/10.1016/j.vetpar.2008.06.025 [ Links ]
Matthee, S., Lovely, C., Gaugler, A., Beeker, R., Venter, H.R. & Horak, I.G., 2010, 'Ixodid ticks on domestic dogs in the Northern Cape Province of South Africa and in Namibia',Journal of the South African Veterinary Association 81, 126-128. PMID: 21247023, http://dx.doi.org/10.4102/jsava.v81i2.125 [ Links ]
Matthewman, L., Kelly, P., Hayter, D., Downie, S., Wray, K., Bryson, N. et al., 1997a, 'Domestic cats as indicators of the presence of spotted fever and typhus group rickettsiae',European Journal of Epidemiology 13, 109-111. PMID: 9062789, http://dx.doi.org/10.1023/A:1007375718204 [ Links ]
Matthewman, L., Kelly, P., Hayter, D., Downie, S., Wray, K., Bryson, N. et al., 1997b, 'Exposure of cats in southern Africa to Coxiella burnetii, the agent of Q fever', European Journal of Epidemiology 13, 477-479. PMID: 9258556, http://dx.doi.org/10.1023/A:1007317032647 [ Links ]
Nicholson, W.L., Allen, K.E., McQuiston, J.H., Breitschwerdt, E.B. & Little, S.E., 2010, 'The increasing recognition of rickettsial pathogens in dogs and people', Trends in Parasitology 26, 205-212. PMID: 20207197, http://dx.doi.org/10.1016/j.pt.2010.01.007 [ Links ]
Noden, B.H., Morkel, C., Manyarara, R., Tubbesing, U. & Soni, M., 2011, 'Emerging zoonotic diseases of companion animals in Namibia' [abstract 98]. ASTMH 31, viewed from http://www.astmh.org/AM/Template.cfm?Section=Meeting_Archives&Template=/CM/ContentDisplay. cfm&ContentID=3953. [ Links ]
Noden, B.H., Musuuo, M., Aku-Akai, L., Van der Colf, B., Chipare, I. & Wilkinson, R., 2014a, 'Risk assessment of flavivirus transmission in Namibia', Acta Tropica 137, 123-129. PMID: 24865792, http://dx.doi.org/10.1016/j.actatropica.2014.05.010 [ Links ]
Noden, B.H., Tshavuka, F., Van der Colf, B.E., Chipare, I. & Wilkinson, R., 2014b, 'Sero-prevelance of Coxiella, spotted fever and typhus group rickettsia, and Bartonella henselae antibodies among blood donors in Namibia', PLOS One 9, e108674. [ Links ]
Noden, B.H. & Van der Colf, B.E., 2013, 'Neglected tropical diseases of Namibia: Unsolved mysteries', Acta Tropica 125, 1-17. PMID: 23006744, http://dx.doi.org/10.1016/j.actatropica.2012.09.007 [ Links ]
Nogueras, M.M., Pons, I., Ortuño, A., Miret, J., Pla, J., Castella, J. et al., 2013a, 'Molecular detection of Rickettsia typhi in cats and fleas',PLoS One 8, e71386. PMID: 23940746, http://dx.doi.org/10.1371/journal.pone.0071386 [ Links ]
Nogueras, M.M., Pons, I., Pla, J., Ortuño, A., Miret, J., Sanfeliu, I. et al., 2013b, 'The role of dogs in the eco-epidemiology of Rickettsia typhi, etiological agent of murine typhus',Veterinary Microbiology 163, 97-102. PMID: 23290118, http://dx.doi.org/10.1016/j.vetmic.2012.11.043 [ Links ]
OIE, 2014, Namibia reports. [Online], viewed from http://www.oie.int/wahis_2/public/wahid.php/Countryinformation/countryhome. [ Links ]
Okello, A.L., Bardosh, K., Smith, J. & Welburn, S.C., 2014, 'One Health: Past successes and future challenges in three African contexts',PLoS Neglected Tropical Diseases 8, e2884. PMID: 24851901, http://dx.doi.org/10.1371/journal.pntd.0002884 [ Links ]
Ortuno, A., Pons, I., Nogueras, M.M., Castella, J. & Segura, F., 2009, 'The dog as an epidemiological marker of Rickettsia conoriiinfection', Clinical Microbiology and Infection 15 (Suppl. 2), 241-242. PMID: 19392897, http://dx.doi.org/10.1111/j.1469-0691.2008.02158.x [ Links ]
Pretorius, A.M., Jensenius, M. & Birtles, R.J., 2004, 'Update on spotted fever group Rickettsiae in South Africa', Vector-borne and Zoonotic Diseases 4, 249-260. PMID: 15631070, http://dx.doi.org/10.1089/1530366042162551 [ Links ]
Pretorius, A.M., Kelly, P.J., Birtles, R.J. & Raoult, D., 1999, 'Isolation of Bartonella henselae from a serologically negative cat in Bloemfontein, South Africa', Journal of the South African Veterinary Association 70, 154-155. PMID: 10855838. [ Links ]
Resnick, M.P., Grunenwald, P., Blackmar, D., Hailey, C., Bueno, R. & Murray, K.O., 2008, 'Juvenile dogs as potential sentinels for West Nile virus surveillance', Zoonoses and Public Health 55, 443-447. PMID: 18399945, http://dx.doi.org/10.1111/j.1863-2378.2008.01116.x [ Links ]
Rohde, R.F. & Hoffman, M.T., 2012, 'The historical ecology of Namibian rangelands: Vegetation change since 1876 in response to local and global drivers', Science of the Total Environment 416, 276-288. PMID: 22188617, http://dx.doi.org/10.1016/j.scitotenv.2011.10.067 [ Links ]
Rougeron, V., Catzeflis, F., Hide, M., De Meeus, T. & Banuls, A.L., 2011, 'First clinical case of cutaneous leishmaniasis due to Leishmania(Viannia) braziliensis in a domestic cat from French Guiana', Veterinary Parasitology 181, 325-328. PMID: 21570189, http://dx.doi.org/10.1016/j.vetpar.2011.04.028 [ Links ]
Rutherfoord, G.S. & Uys, C.J., 1978, 'Cutaneous leishmaniasis in southern Africa. A case report', South African Medical Journal 53, 716-718. PMID: 694606. [ Links ]
Sanogo, Y.O., Davoust, B., Inokuma, H., Camicas, J.L., Parola, P. & Brouqui, P., 2003, 'First evidence of Anaplasma platys in Rhipicephalus sanguineus (Acari: Ixodida) collected from dogs in Africa', Onderstepoort Journal of Veterinary Research 70, 205-212. PMID: 14621316. [ Links ]
Schmidt, P.L., 2009, 'Companion animals as sentinels for public health', Veterinary Clinics of North America: Small Animal Practice 39, 241-250. PMID: 19185191, http://dx.doi.org/10.1016/j.cvsm.2008.10.010 [ Links ]
Schneider, H.P., 2012, 'The history of veterinary medicine in Namibia', Journal of the South African Veterinary Association 83(1), Art. #4, 9 pages. PMID: 23327121, http://dx.doi.org/10.4102/jsava.v83i1.4 [ Links ]
Schurer, J.M., Hill, J.E., Fernando, C. & Jenkins, E.J., 2012, 'Sentinel surveillance for zoonotic parasites in companion animals in indigenous communities of Saskatchewan',American Journal of Tropical Medicine and Hygiene 87, 495-498. PMID: 22826486, http://dx.doi.org/10.4269/ajtmh.2012.12-0273 [ Links ]
Schwan, E.V., 2009, Filariosis of domestic carnivores in Gauteng, KwaZulu-Natal and Mpumalanga provinces, South Africa, and Maputo province, Mozambique. PhD thesis, University of Pretoria, viewed from http://repository.up.ac.za/handle/2263/30061. [ Links ]
Schwan, E.V., Miller, D.B., De Kock, D. & Van Heerden, A., 2000, 'Dirofilaria repens in a cat with acute liver failure', Journal of the South African Veterinary Association 71, 197-200. PMID: 11205171, http://dx.doi.org/10.4102/jsava.v71i3.713 [ Links ]
Schwan, E.V. & Schroter, F.G., 2006, 'First record of Acanthocheilonema dracunculoidesfrom domestic dogs in Namibia', Journal of the South African Veterinary Association 77, 220-221. PMID: 17458349, http://dx.doi.org/10.4102/jsava.v77i4.381 [ Links ]
Schwartz, R.A., Kapila, R., Mcelligott, S.C., Atkin, S.H. & Lambert, W.C., 2012, 'Cutaneous leishmaniasis and rickettsial African tick-bite fever: A combination of exotic traveler's diseases in the same patient', International Journal of Dermatology 51, 960-963. PMID: 22788813, http://dx.doi.org/10.1111/j.1365-4632.2011.05362.x [ Links ]
Shepherd, A.J., Swanepoel, R., Shepherd, S.P., McGillivray, G.M. & Searle, L.A., 1987, 'Antibody to Crimean-Congo hemorrhagic fever virus in wild mammals from southern Africa', American Journal of Tropical Medicine and Hygiene 36, 133-142. PMID: 3101526. [ Links ]
Simon, F., Siles-Lucas, M., Morchon, R., Gonzalez-Miguel, J., Mellado, I., Carreton, E. et al., 2012, 'Human and animal dirofilariasis: The emergence of a zoonotic mosaic', Clinical Microbiology Reviews 25, 507-544. PMID: 22763636, http://dx.doi.org/10.1128/CMR.00012-12 [ Links ]
Smith, F.D., Ballantyne, R., Morgan, E.R. & Wall, R., 2012, 'Estimating Lyme disease risk using pet dogs as sentinels', Comparative Immunology, Microbiology and Infectious Diseases 35, 163-167. PMID: 22257866, http://dx.doi.org/10.1016/j.cimid.2011.12.009 [ Links ]
Solano-Gallego, L. & Baneth, G., 2011, 'Babesiosis in dogs and cats-Expanding parasitological and clinical spectra', Veterinary Parasitology 181, 48-60. PMID: 21571435, http://dx.doi.org/10.1016/j.vetpar.2011.04.023 [ Links ]
Stuben, J., 2004, 'Investigations on the prevalence of ehrlichiosis and babesiosis in dogs in Namibia with special consideration of the housing conditions.' [German]. Master's Dissertation, Free University. [ Links ]
Walker, A.R., Bouattour, A., Camicas, J.L., Estrada-Pena, A., Horak, I.G., Latif, A.A. et al., 2007, Ticks of domestic animals in Africa: A guide to identification of species, Bioscience Reports, The University of Edinburgh, Edinburgh. [ Links ]
WHO, 2013, Namibia rabies country profile. [Online], viewed from http://www.who.int/rabies/epidemiology/Rabies_CP_Namibia_09_2013.pdf. [ Links ]
Williams, B.M., Berentsen, A., Shock, B.C., Teixiera, M., Dunbar, M.R., Becker, M.S. et al., 2014, 'Prevalence and diversity of Babesia,Hepatozoon, Ehrlichia, and Bartonella in wild and domestic carnivores from Zambia, Africa',Parasitology Research 113, 911-918. PMID: 24363181, http://dx.doi.org/10.1007/s00436-013-3722-7 [ Links ]
Yancey, C.B., Hegarty, B.C., Qurollo, B.A., Levy, M.G., Birkenheuer, A.J., Weber, D.J. et al., 2014, 'Regional seroreactivity and vector-borne disease co-exposures in dogs in the United States from 2004-2010: Utility of canine surveillance', Vector-borne and Zoonotic Diseases 14, 724-732. PMID: 25325316, http://dx.doi.org/10.1089/vbz.2014.1592 [ Links ]
127 Noble Research Center
Department of Entomology and Plant Pathology
Oklahoma State University, Stillwater
OK 74078, United States
Received: 19 May 2015
Accepted: 28 Aug. 2015
Published: 06 Nov. 2015