Article

Dirofilariasis in wild canids from the Gulf coastal prairies of Texas and Louisiana, U.S.A

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Abstract

Heartworms, Dirofilaria immitis, were recovered from 17 out of 24 (71%) coyotes, Canis latrans, 38 out of 46 (83%) coyote × red wolf hybrids and all of 8 (100%) red wolves, Canis rufus gregoryi, collected from the Gulf coastal prairies of southeast Texas and southwest Louisiana. Intensities of infection ranged from 1 to 176 () worms per host. There was a significantly (P<0.05) higher intensity of infection in red wolves. Prevalence of heartworms increased significantly with increasing age. There were no significant differences between coyotes, hybrids and red wolves or between different host sexes in terms of prevalence. The female to male ratio of heartworms was close to unity (1.2:1) and was not correlated with worm burdens. Nematodes were primarily localized in the right heart, frequently extending into the pulmonary artery and the pulmonary arterial tree in the lungs. In 13 instances, 1–4 adult heartworms were recovered from the venae cavae. Pathological responses in the right heart were variable, depending on the intensity of infection. In severe infections, there were small areas of infarctive necrosis with mild to severe interstitial edema in the myocardium. Lesions in the pulmonary artery and pulmonary arterial trunk varied from mild focal hyperplastic intimal changes to extensive exudative villous endarteritis. The latter was characterized by a hyperplastic collagenous stroma with numerous histiocytes, plasma cells and eosinophils. Lung pathology varied from patchy to extensive areas of congestion, edema, hemorrhage, interstitial pneumonitis and infarction. In cases with heartworms in the venae cavae, hepatic changes were minimal and associated with liver changes such as passive congestion and centrolobular necrosis seen in cases without adult worms in the venae cavae. In heavily infected animals, hemosiderosis of the liver, spleen and kidneys was pronounced. A microfilaremia was noted in 46% of the infected wild canids. Microfilariae were observed in tissue sections of the myocardium, lungs, liver, kidney, spleen, lymph nodes, pancreas and appendix. Wild canids from this area are regarded as natural definitive hosts and primary reservoirs for heartworms and it appears that this infection is an important factor in the morbidity and mortality of these hosts.

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... Until the 1970s, heartworm was thought to be a relatively rare and unimportant pathogen in wild canids (Otto 1972; Graham 1975). More recent studies, however, have found prevalence of heartworm comparable to that in sympatric domestic dogs, suggesting that heartworm also may be an important disease agent in wild canid populations (Custer and Pence 1981; Acevedo and Theis 1982; Theis et al. 1996; Sacks 1998). However, little is known about the pathogenicity of heartworm in wild canids or its relationship to host nutritional status or activity (Gier et al. 1978; Custer and Pence 1981). ...
... More recent studies, however, have found prevalence of heartworm comparable to that in sympatric domestic dogs, suggesting that heartworm also may be an important disease agent in wild canid populations (Custer and Pence 1981; Acevedo and Theis 1982; Theis et al. 1996; Sacks 1998). However, little is known about the pathogenicity of heartworm in wild canids or its relationship to host nutritional status or activity (Gier et al. 1978; Custer and Pence 1981). Heartworm has long been recognized as a serious agent of disease in domestic dogs (Henningar and Ferguson 1957) and much is known about its pathogenicity in this host (Rawlings 1986; Sutton 1988; Rawlings and Calvert 1995). ...
... On the other hand, natural selection might result in wild canids being more resistant than domestic dogs to parasitic disease, generally. For example, necropsies of heartworminfected coyotes have revealed relatively low inflammatory responses to microfilariae in several organs (Custer and Pence 1981 ), which suggests either that hypersensitivity was relatively less pronounced in these wild hosts generally or that the sample in that study was biased toward individuals with reduced hypersensitivity due to their higher survival rate (which would also suggest selection). Coyotes also might be expected to exhibit a greater protective immune response. ...
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We used radiotelemetry to study relationships among canine heartworm (Dirofilaria immitis) infection, body condition, and activity of free-ranging coyotes (Canis latrans). Average body mass at death was lower for 17 coyotes in a high-intensity infected group (x = 33.6 heartworms) than for 18 coyotes in a control group (x = 3.6 heartworms; p < 0.01). Coyotes in the infected group lost body mass at an average rate of 20% per year relative to the control group (p < 0.01). Bone marrow fat was negatively correlated with heartworm burden (R2 = 0.27; p < 0.01). Average body mass of coyotes at initial capture (i.e., potentially before infection) did not differ between infected and control groups (p = 0.90; 1 -β = 0.70). Activity was negatively correlated with heartworm burden during the last 2 months of life (R2 = 0.30; p < 0.01), but no correlation was found 2-4 months before death. Activity of the infected group (n = 13) declined over time (p = 0.01), whereas no difference in activity was observed in the control group (n = 13; p = 0.50). Our findings indicate that heartworm infection reduced body condition and activity of coyotes but that nutritional status did not significantly affect susceptibility to infection.
... Red wolf literature.-The last free ranging red wolves in the historic Louisiana and Texas populations had high infection rates of hookworm (Riley and McBride 1972;Carley 1975;Custer and Pence 1981a), heartworm (D. immitis- Riley and McBride 1972;Carley 1975;Custer and Pence 1981b), and sarcoptic mange (S. scabiei- Riley and McBride 1972;Carley 1975;Pence et al. 1981). All 3 parasites were considered limiting factors to red wolf survival and may have affected morbidity and mortality significantly (Riley and McBride 1972;Carley 1975;Custer and Pence 1981b). ...
... last free ranging red wolves in the historic Louisiana and Texas populations had high infection rates of hookworm (Riley and McBride 1972;Carley 1975;Custer and Pence 1981a), heartworm (D. immitis- Riley and McBride 1972;Carley 1975;Custer and Pence 1981b), and sarcoptic mange (S. scabiei- Riley and McBride 1972;Carley 1975;Pence et al. 1981). All 3 parasites were considered limiting factors to red wolf survival and may have affected morbidity and mortality significantly (Riley and McBride 1972;Carley 1975;Custer and Pence 1981b). Hookworm infections were especially high in pups and juveniles and may have been a leading cause of juvenile mortality (Custer and Pence 1981a). ...
... Hookworm infections were especially high in pups and juveniles and may have been a leading cause of juvenile mortality (Custer and Pence 1981a). The severity of heartworm infections increased with age (Custer and Pence 1981b), resulting in pathological responses such as enlarged and deformed hearts, and increasing stressinduced mortality that healthy wolves would likely have survived (Riley and McBride 1972;Carley 1975). Sarcoptic mange was the most serious ectoparasite; infections were so numerous that by the 1970s, 90% of observed red wolves were at least partially devoid of hair (Riley and McBride 1972). ...
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Infectious diseases pose a significant threat to global biodiversity and may contribute to extinction. As such, establishing baseline disease prevalence in vulnerable species where disease could affect persistence is important to conservation. We assessed potential disease threats to endangered red wolves (Canis rufus) by evaluating regional (southeastern United States) disease occurrences in mammals and parasite prevalence in red wolves and sympatric coyotes (Canis latrans) in North Carolina. Common viral pathogens in the southeast region, such as canine distemper and canine parvovirus, and numerous widespread endoparasites could pose a threat to the red wolf population. The most prevalent parasites in red wolves and sympatric coyotes were heartworm (Dirofilaria immitis), hookworm (Ancylostoma caninum), and Ehrlichia spp.; several red wolves and coyotes were also positive for bacteria causing Lyme disease (Borrelia burgdorferi). Coyotes had a more species-rich parasite community than red wolves, suggesting they could harbor more parasites and act as a disease reservoir. Species identity and sex did not significantly affect parasite loads, but young canids were less likely to have heartworm and more likely to have high levels of endoparasites. Continued disease monitoring is important for red wolf recovery because low levels of genetic variability may compromise the wolves’ abilities to combat novel pathogens from closely related species, such as domestic dogs and coyotes.
... Molecular approaches have been used as alternative or complement tests in different stages of canine dirofilariosis, especially in cases with inconclusive microfilariae and/or antigen test results (Simón et al., 2012). Among wild animals, the detection of heartworm infection is usually based on the identification of D. immitis adults at necropsy (Agostine and Jones, 1982;Aher et al., 2016;Custer and Pence, 1981;Franson, 1976;Gates et al., 2014;Graham, 1975;King and Bohning, 1984;Monson et al., 1973;Nelson et al., 2003;Pappas and Lunzman, 1985;Sacks and Caswell-Chen, 2003;Thornton et al., 1974). Recently, other studies have demonstrated that commercial immunochromatographic tests used in the diagnosis of canine heartworm disease could be an alternative screening test for D. immitis infections in coyote populations (Kotwa et al., 2019;Paras et al., 2012). ...
... Our findings are consistent with recent prevalence rates of D. immitis in coyotes in North America (Kotwa et al., 2019(Kotwa et al., , 2020Paras et al., 2012). However, the prevalence of heartworm in wild canids population in the US has varied widely over the past 40 years ranging from 0.6 to 70.8% (Agostine and Jones, 1982;Aher et al., 2016;Custer and Pence, 1981;Franson, 1976;Gates et al., 2014;Graham, 1975;King and Bohning, 1984;Monson et al., 1973;Nelson et al., 2003;Pappas and Lunzman, 1985;Paras et al., 2012;Sacks and Caswell-Chen, 2003;Thornton et al., 1974;Worsley-Tonks et al., 2021). Several factors have been associated with this wide range of D. immitis prevalences in the US, including differences in geographic location, climate, population sampled, and animal age (Brown et al., 2012). ...
Article
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Wild canids serve as reservoir for various vector-borne pathogens of veterinary and medical importance, including the canine heartworm, Dirofilaria immitis. In North and Central America, coyotes (Canis latrans) may be a relevant reservoir host for heartworm transmission. The objective of this study was to determine the occurrence of D. immitis in coyotes across Texas using integrated antigen detection test and molecular assays. Matching whole blood and serum samples were collected from 122 coyotes from different locations across the state of Texas, United States, encompassing nine counties. Collections occurred from February to April, 2016, and December, 2016. Samples were assessed serologically using a commercial microtiter plate ELISA (DiroCHEK®), and molecularly by conventional PCR targeting the cytochrome oxidase c subunit 1 (cox1) and NADH dehydrogenase subunit 5 (nad5) of the mitochondrial DNA, and via a TaqMan© probe-based real-time PCR protocol, also targeting a fragment of the cox1 gene. Overall, 12 (9.83%) samples tested positive when serological and molecular results were combined. Seven of 122 samples (5.73%) were antigen-positive, 8 (6.55%) were qPCR-positive, and 4 (3.27%) were positive using conventional PCR. Of 12 positive samples, 4 tested antigen-positive by DiroCHEK® but were negative in all molecular tests, another 4 tested positive by at least one of the molecular assays but tested negative by DiroCHEK®, and 3 samples tested positive by both antigen test and at least one of the molecular assays. Two samples (16.67%) tested positive on both the antigen test and both conventional PCR and qPCR. Our study confirmed the presence of D. immitis infection in coyotes from southern and northern Texas. The combination of serologic and molecular diagnostic tests was proven synergistic for the identification of D. immitis infections, including occult dirofilariosis, and revealed a more accurate picture of heartworm occurrence in the sampled coyotes.
... Canine heartworm disease was not an important cause of mortality for coyotes in Tucson during our study. By contrast, animals in Georgia (Holzman et al., 1992 ) and other southeastern states (Custer and Pence, 1981) tested positive for canine heartworm. Weinmann and Garcia (1980) demonstrated that 45% of coyotes from central California had heartworms and postulated that coyotes were a good potential reservoir for disease transmission to domestic canids. ...
... Drewek et al. (1981 , however, reported that 44% of coyotes in another Arizona study tested positive for leptospirosis. Some researchers have suggested that CDV, ICH, CPV, and other viral and bacterial diseases have the capacity to exist in an enzootic state within coyote populations (Thomas et al., 1984; Pence, 1995) and may only cause significant mortality during stressful conditions such as high density, food scarcity, or parasitism (Trainer and Knowlton, 1968; Pence and Custer, 1981). The annual survival rate of coyotes in Tucson (0.72) is similar to that reported by other studies in North America, which range from 0.68 to 0.90 (Andelt, 1985; Harrison, 1992). ...
Article
The health of coyotes (Canis latrans) in urban areas has not been studied. Our objectives were to assess the health of coyotes in Tucson (Arizona, USA) by determining the prevalence of antibodies to selected pathogens, estimating survival rates, and identifying sources of mortality. We drew blood from 22 coyotes to evaluate the prevalence of heartworm (Dirofilaria immitis) antigens, and antibodies to canine distemper virus (CDV), infectious canine hepatitis (ICH), canine parvovirus (CPV), and seven serovars of Leptospira interrogans. We trapped and radiocollared 19 coyotes to determine survival rates. We performed necropsies on 19 coyotes to quantify their general health, the presence of internal and external parasites, and causes of mortality. No coyotes tested positive for heartworm antigens. The prevalence of antibody to CDV, ICH, and CPV was 27, 50, and 100%, respectively. Twenty-seven percent of coyotes tested positive for one of five serovars of L. interrogans. The diseases for which coyotes in Tucson possessed antibodies appear to be enzootic in the population. The annual survival rate of coyotes was 0.72. Eleven necropsied coyotes were killed by cars, five coyotes were hit by cars, two were killed by a trapper, and the cause of death for one coyote was unknown. Coyotes in Tucson appear to be exposed to the viral, bacterial, and parasitic infections common in many coyote populations, but humans are the major source of mortality.
... C oyotes, Canis latrans, can be infected with Dirofilaria immitis, the causative agent of canine heartworm, through the bite of an infected mosquito. Studies of coyotes suggest a strong geographical influence determining its occurrence, with surveys in the eastern and midwestern United States demonstrating a high prevalence of D. immitis infection (Custer and Pence 1981;Nelson et al. 2003). Conversely, surveys from the West Coast of the United States have generally shown a low prevalence of infection (Sacks et al. 2004;Foryet 2008). ...
... Sacks and associates (2004) collected coyotes at the county level in California, and found prevalence estimates from 0-25% per county. On the other hand, studies in eastern states have reported high prevalences of D. immitis in coyotes, ranging from 16% to as high as 71% (Custer and Pence 1981;Nelson et al. 2003). Bowman and colleagues (2009) found D. immitis antigens to be prevalent in domestic dogs in Craig and Creek Counties at a rate of 2.1-4%; there were not enough data to report on dogs from Okmulgee and Collingsworth Counties. ...
Article
There is a lack of knowledge regarding the prevalence of Dirofilaria immitis and Ehrlichia spp. in coyotes in Oklahoma and Texas. Documenting the prevalence of these vector-borne disease agents in coyotes from Oklahoma and Texas underscores the importance of wild canids as reservoir hosts that infect companion animals and humans. To learn more about the sylvatic cycle of D. immitis and Ehrlichia spp. in coyotes from Oklahoma and Texas, we tested for infection with and exposure to, respectively, these disease agents. Coyote carcasses were collected opportunistically from animal control experts and hunters in seven counties in Oklahoma and Texas from January to March, 2010. Serum samples from 77 coyotes were tested with a commercial ELISA test. Five (6.5%) coyotes had D. immitis antigens, and four (5.2%) had antibodies to Ehrlichia spp. The overall prevalence of D. immitis was low relative to studies from the eastern United States. Little is known about the prevalence of Ehrlichia spp. throughout the United States, but coyotes from rural Oklahoma in the current study had a higher exposure rate than those reported from California, and a lower rate than data from an earlier study from Oklahoma.
... (Guerra et al., 2013;Ito et al., 2013;Schurer et al., 2014) and Toxocara canis (Segovia et al., 2001;Szafranska et al., 2010). So far, studies on wolf parasite infections were performed in Nearctic (Choquette et al., 1973;Custer and Pence, 1981;Holmes and Podesta, 1968;Messier et al., 1989;Samuel et al., 1978) and Palearctic regions (Craig and Craig, 2005;Guberti et al., 1993;Ito et al., 2013;Papadopoulos et al., 1997;Schurer et al., 2014;Shimalov and Shimalov, 2000) and parahttp://dx.doi.org/10. 1016/j.vetpar.2016.11.011 0304-4017/© 2016 Elsevier B.V. All rights reserved. ...
... The prevalence of D. immitis in red foxes and gray foxes is usually lower than in coyotes from the same area (Cromwell et al. 1978, King and Bohning 1984). Other important wildlife species from which dog heartworm has been recovered include red wolves (Canis rufus) and muskrats from the wild as well as gray wolves, wolverines, black bears, and beavers from zoos (Goble 1942, Foil and Orihel 1975, Johnson 1975, Williams and Dade 1976, Custer and Pence 1981, Pratt et al. 1981). In Canada, D. immitis is becoming increasingly prevalent in dogs (Slocombe and McMillan 1984) but is seldom reported from wildlife. ...
... Background heartworm prevalence in reservoir populations could be estimated from published coyote survey results, as well data from dogs in shelters. Many reports on coyote and other wild canid species' Dirofilaria infections have been published with report rates as high as 71% [35]; however, most surveys occurred in the early 1980's [36]. More recent surveys conducted in Oklahoma/Texas, Illinois, Florida and California have reported 6.5, 16, 40 and 42-44% of coyotes being positive3637383940. ...
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An examination of the Companion Animal Parasite Council's (CAPC) canine heartworm data to clarify the spatial prevalence of heartworm in the United States. Factors thought to influence the spatial risk of disease, as identified in a recent CAPC workshop, are discussed.
... Several authors affirm the role of this carnivore in epidemiological chain of dirofilariosis (Mańas et al. , 2005;Magi et al., 2008Magi et al., , 2009Marks & Bloomfield, 1998). Dirofilarosis caused by D. immitis was also detected in other wild carnivore species -in wolves, coyotes, dingoes, raccoons, and black-footed ferrets (Pascucci et al., 2007;Custer & Pence, 1981;Starr & Mulley, 1988;Nakagaki et al., 2000;Wisely et al., 2008). A beech marten naturally infected was also found in Slovakia (Miterpáková et al., 2013). ...
Article
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Dirofilariosis belongs to zoonotic vector-borne diseases with fastest spread into new areas caused by extreme weather and seasonal changes in climate. In Slovakia, Dirofilaria spp. parasites affect more than 30 % of dogs living in endemic regions in southern parts of territory, however, data on wildlife circulation of this parasite are still scarce. In order to clarify the role of red fox (Vulpes vulpes) as the most abundant canid species in Europe in maintaining the parasite in natural foci, an initial survey of dirofilariosis in this carnivore species was conducted in Slovakia. The samples of 183 red foxes hunted in 2007 - 2009 in regions of South-Eastern and Northern Slovakia with different geographical and climate characteristics were examined by means of PCR method using specific D. repens, D. immitis and Acantocheilonema recognitum primers. The DNA was isolated from spleen samples using commercial kit and PCR approach was used for diagnostics. After amplification selected products were purified and sequenced to elucidate any homologies with previously deposited sequences in Gen Bank. The results showed 105 out of 183 examined specimens (57.4 %) being infected, with great regional differences in prevalence. Phylogenetic relationships within Dirofilaria species indicate that obtained isolates belong to D. repens. The results confirmed the role of red foxes as the reservoir of parasite. Herein, epidemiological factors that may be coherent with the Dirofilaria parasites distribution and circulation in wildlife and implications in risk assessment and prevention for domestic animals and human are discussed.
... Endemic as well as introduced hemoparasites may also impact health and fitness of wildlife (e.g. Custer and Pence, 1981;Atkinson et al., 2000;Garvin et al., 2003;Donahoe et al., 2015). Furthermore, babesiosis is an emerging zoonosis worldwide, with wildlife reservoirs playing a particular role in its epidemiology (Gray et al., 2010;Yabsley and Shock, 2013). ...
Article
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Hemoparasites can cause serious morbidity in humans and animals and often involve wildlife reservoirs. Understanding patterns of hemoparasite infections in natural populations can therefore inform about emerging disease risks, especially in the light of climate change and human disruption of natural ecosystems. We investigated the effects of host age, sex, host group size and season on infection patterns of Plasmodium sp., Babesia sp. and filarial nematodes in a population of wild Malagasy primates, Verreaux’s sifakas (Propithecus verreauxi), as well as the effects of these infections on hematological variables. We tested 45 blood samples from 36 individuals and identified two species of Plasmodium, one species of Babesia and two species of filarial nematodes. Plasmodium spp. and Babesia sp. infections showed opposite patterns of age-dependency, with babesiosis being prevalent among young animals, while older animals were infected with Plasmodium sp. In addition, Babesia sp. infection was a statistically significant negative predictor of Plasmodium sp. infection. These results suggest that Plasmodium and Babesia parasites may interact within the host, either through cross-immunity or via resource competition, so that Plasmodium infections can only establish after babesiosis has resolved. We found no effects of host sex, host group size and season on hemoparasite infections. Infections showed high prevalences and did not influence hematological variables. This preliminary evidence supports the impression that the hosts and parasites considered in this study appear to be well-adapted to each other, resulting in persistent infections with low pathogenic and probably low zoonotic potential. Our results illustrate the crucial role of biodiversity in host-parasite relationships, specifically how within-host pathogen diversity may regulate the abundance of parasites.
... Endemic as well as introduced hemoparasites may also impact health and fitness of wildlife (e.g. Custer and Pence, 1981;Atkinson et al., 2000;Garvin et al., 2003;Donahoe et al., 2015). Furthermore, babesiosis is an emerging zoonosis worldwide, with wildlife reservoirs playing a particular role in its epidemiology (Gray et al., 2010;Yabsley and Shock, 2013). ...
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The white-tailed deer (Odocoileus virginianus) is a common and widespread North American game species. To evaluate the incidence, clinical manifestations, demography, and pathology of bacterial and parasitic dermatologic diseases in white-tailed deer in the southeastern United States, we retrospectively evaluated white-tailed deer cases submitted to the Southeastern Cooperative Wildlife Disease Study from 1975 to 2012. Among 2569 deer examined, bacterial or parasitic dermatologic disease was diagnosed in 88 (3.4%) individuals, with Demodex spp (n = 37; 42.0%) and Dermatophilus congolensis (n = 19; 21.6%) as the most common causes. Demodicosis was significantly more common in deer older than 2 years and was most often detected in the fall; no statistically significant sex predilection was identified. Affected animals had patchy to generalized alopecia, often distributed over the head, neck, limbs, and trunk; microscopic lesions included epidermal crusts and cutaneous nodules with mild perifollicular, lymphoplasmacytic inflammation. Dermatophilosis was most common in males younger than 1 year that were often found dead. Crusting, erythema, and alopecia occurred on the face, ears, and distal extremities. Less commonly, infectious dermatologic diseases were associated with other bacteria (n = 13; 14.8%), fungi (n = 5; 5.7%), ectoparasites (chiggers, lice, mites, and ticks; n = 11; 12.5%), and larval nematodes (n = 7; 8.0%). Population-level effects of these diseases in white-tailed deer are likely minimal; however, due to their dramatic presentation, demodicosis, dermatophilosis, and other infectious skin diseases can be of concern to hunters and, in some cases, may have zoonotic potential.
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This study (1) elucidates the composition, degree, and similarity and/or variance of helminth parasitism in a wild canid population consisting of red wolves (Canis rufus), coyotes (Canis latrans), and their hybrids from the Gulf Coastal Prairies of southeastern Texas and southwestern Louisiana; (2) examines the relationships between helminth species within these hosts; and (3) compares the helminth faunal similarities of the wild Canidae in North America using the above data on Gulf Coast wild canids and data on helminth parasitism of coyotes and timber wolves (Canis lupus) from previous studies in the literature. Fifteen species of helminths were collected from 78 wild canids (8 red wolves, 24 coyotes, and 46 red wolf x coyote hybrids). Helminths recovered were as follows: Nematoda.-Ancylostoma caninum (82% of hosts infected); Capillaria hepatica (3%); Dirofilaria immitis (81%); Oslerus osleri (5%); Physaloptera rara (1%); Spirocerca lupi (4%); Toxascaris leonina (6%); Trichuris vulpis (4%); Trematoda.-Heterobilharzia americana (35%); Eurytrema procyonis (1%); Cestoda.-Mesocestoides corti (1%); Taenia macrocystis (9%); T. pisiformis (94%); T. multiceps (1%); T. taeniaeformis (1%). All canids were infected with from one to seven (x̄ = 3.3)$ helminth species. New host records of helminths from Gulf Coast wild canids included Heterobilharzia americana from red wolves, coyotes, and hybrids, Eurytrema procyonis from a hybrid, and Taenia taeniaeformis from a hybrid. Of the helminths recovered, only Dirofilaria immitis and Ancyclostoma caninum are regarded as having an effect on populations of these hosts. Dirofilaria immitis and Heterobilharzia americana were significantly more prevalent in older animals, and mean densities of D. immitis were significantly higher in older hosts. This apparently resulted from increased chance of exposure with increased age. Ancylostoma caninum had significantly higher mean densities in male hosts; presumably this was caused by increased female resistance. Taenia pisiformis had a significantly greater prevalence in female than in male wild canids. Red wolves had significantly higher mean densities of D. immitis than coyotes or hybrids. Because of their tendency toward hybridization, similarity of helminth faunas, and other common traits, the helminth faunas of red wolves, coyotes, and their hybrids were considered as a single or lumped fauna referred to as the Gulf Coast wild canid helminth fauna in the following analyses. Associations between pairs of common helminth species (A. caninum, D. immitis, H. americana, and T. pisiformis) were analyzed in terms of prevalence (chi-square analysis of 2 x 2 contingency tables, Cole's coefficients, and the Fager index), numbers of individuals (coefficient of association), and mean densities (Kruskal-Wallis and Mann-Whitney U-tests). Affinities between five of the six species pairs, as determined by prevalence, were noted. The mean density of T. pisiformis was significantly higher in the presence of A. caninum. These results indicate a superdispersed (clumped) distribution of the common helminth species of Gulf Coast wild canids. This was attributed to common requirements for similar environmental factors, rather than mutualistic relationships based on physiological interactions. The female to male ratios of heartworms and hookworms were 1.2:1 and 1.7:1, respectively, and were not correlated to density of infection. There were no correlations between weight of host's spleen and/or heart to mean densities of D. immitis. Comparison of helminth faunas of Gulf Coast wild canids, timber wolves, and coyotes from several geographic regions (Simpson's index, percent similarity, and multivariate analyses using hierarchical clustering) indicated (1) lack of dominance by a particular helminth species in any of the faunas from these different hosts, (2) the uniqueness of the Gulf Coast helminth fauna in terms of species composition and prevalence, and (3) considerable diversity in the helminth faunas of wild canids, particularly coyotes, from different geographic regions. The wild canid population of the Gulf Coast prairies most closely resembled populations of coyotes from other regions in terms of the helminth fauna. Classification of helminth species of Gulf Coast wild canids according to importance values revealed five dominant, four codominant, five successful immigrant, and one unsuccessful immigrant species in this helminth community. When helminth communities from several geographic areas were compared, T. pisiformis and T. hydatigena emerged as the only ubiquitously common, dominant helminths from coyotes and timber wolves, respectively.
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Sex ratios in invertebrates commonly deviate from parity (1:1). Various genetic and epigenetic factors distort sex ratios to favor males or females. We examined sex ratios in Dirofilaria immitis (heartworms) obtained from naturally-infected dogs. Dirofilaria from 84 naturally-infected pound-source dogs were extracted at necropsy, counted and sexed. Dogs had a median worm intensity of 15 filariae. Overall, sex ratios equaled 1. However, at low worm intensities, dogs were more likely to have female than male worms. Of eight unisex infections, seven were all-female (range 1-11 worms), while only one dog had a single male worm. Similarly, in mixed-sex infection at worm intensities <20 worms, dogs were more likely to have more female worms than male worms. Our results suggest that sex disequilibrium exists in D. immitis at lower worm intensities, but disappears with higher worm intensities. Reasons for this disequilibrium are unknown, but presumably confer a species survival advantage.
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Dirofilariasis represents a zoonotic mosaic, which includes two main filarial species (Dirofilaria immitis and D. repens) that have adapted to canine, feline, and human hosts with distinct biological and clinical implications. At the same time, both D. immitis and D. repens are themselves hosts to symbiotic bacteria of the genus Wolbachia, the study of which has resulted in a profound shift in the understanding of filarial biology, the mechanisms of the pathologies that they produce in their hosts, and issues related to dirofilariasis treatment. Moreover, because dirofilariasis is a vector-borne transmitted disease, their distribution and infection rates have undergone significant modifications influenced by global climate change. Despite advances in our knowledge of D. immitis and D. repens and the pathologies that they inflict on different hosts, there are still many unknown aspects of dirofilariasis. This review is focused on human and animal dirofilariasis, including the basic morphology, biology, protein composition, and metabolism of Dirofilaria species; the climate and human behavioral factors that influence distribution dynamics; the disease pathology; the host-parasite relationship; the mechanisms involved in parasite survival; the immune response and pathogenesis; and the clinical management of human and animal infections.
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Captive carnivores are susceptible to a wide array of infectious and parasitic diseases, which reflects the diversity of the seven families of Carnivora. Unfortunately, relatively few in-depth studies have been conducted on diseases of non-domestic carnivores, and much remains to be learned, especially regarding diseases of small carnivores (e.g. mustelids, viverrids and procyonids). The more important infectious diseases of carnivores include rabies, canine distemper, and diseases caused by parvoviruses, coronaviruses and herpesviruses. Few parasitic or bacterial pathogens are significant in captive populations, and appropriate husbandry, therapy, vaccines and quarantine minimize the risk of disease. Extrapolations from one species to another regarding disease susceptibility may be incorrect. The black-footed ferret (Mustela nigripes) serves as an example of a carnivore significantly affected by infectious diseases, some of which were expected while others could not have been predicted from generalized knowledge of diseases of mustelids. This highlights the need to understand the natural history of each species maintained in captivity.
Article
Thirty-seven subadult and adult coyotes (Canis latrans), collected August 1992 through December 1996 from a coastal foothill area in northern California (USA), were examined for adult heartworm (Dirofilaria immitis). During 1992 through 1993, at the end of a 6 yr drought, none of four coyotes examined were infected with heartworms. However, during 1994 through 1996, after the drought had ended, prevalences were 91% in 23 adult coyotes and 40% in 10 subadult coyotes. Heartworm intensity did not differ by sex of coyote, and averaged (+/- SE) 19.4 +/- 3.8 among adults; one subadult had > 238 heartworms. The prevalence and intensity of heartworm infection in coyotes reported here for 1994 through 1996 are the highest reported anywhere in the United States.
Article
In the USA, the ocelot (Leopardus pardalis) is a highly endangered felid found only in a few remaining vestiges of native thornshrub brushland in the Lower Rio Grande Valley (LRGV) of extreme southern Texas. From 1987-1998, carcasses of 15 adult ocelots that died of vehicular accidents or natural causes were examined for helminths. All cats had 1-8 (mean = 3) helminth species. All were infected with 1-101 (mean +/- SE = 32 +/- 7) Toxascaris leonina. Other helminths from these ocelots were Alaria marcianae, Brachylaima sp., Mesocestoides lineatus, Taenia rileyi, Oncicola canis, Dirofilaria immitis, Physaloptera rara, Ancylostoma tubaeformae, Cylicospirura chevreuxi, Vogeloides felis, and Metathelazia californica. Additionally, two cats had scarring of the aorta with lesions typical of those caused by Spriocerca lupi, although larval nematodes were not seen. A clinal variation in size of nearly three orders of magnitude was noted in the diplostomatid trematodes in the small intestine of one adult male ocelot. Despite the differences in size, all specimens appeared morphologically identical and were regarded as A. marcianae. Helminth prevalences and abundances, including those of potentially pathogenic species like D. immitis, were low. Although a single heartworm infection may have contributed to the death of one ocelot, helminth infections in general seemed to be of no great consequence to this endangered ocelot population. The helminth fauna of ocelots in the LRGV is reflective of that from wild felids in general; all have been reported previously from the bobcat (Lynx rufus) and mountain lion (Puma concolor) elsewhere in Texas.
Article
Canine heartworm (Dirofilaria immitis) disease affects wild canids and may be a factor impacting the health and population dynamics of coyotes (Canis latrans). Coyotes may serve also as a potential reservoir for transmission of these parasites to domestic dogs. We investigated 920 coyotes harvested by hunters and trappers throughout Illinois (USA) from 1995-1997. The objectives of the study were to: 1) survey the regional prevalence and intensity of heartworms in coyotes in Illinois, 2) determine whether heartworm intensity correlates with physical condition, particularly body weight and winter fat levels, and 3) evaluate the relationship between heartworm infections and the reproductive success of females. Prevalence of heartworms statewide was 16.0%. Prevalence was significantly higher in males (17.7%) than in females (14.1%; P = 0.04) and was higher in the older age-classes (P < 0.0001). The regional prevalence of heartworms increased from northern to southern Illinois. Intensity ranged from 1 to 111 with a mean of 8.7 (SD = 13.2) worms. Intensities did not differ significantly between sexes (P = 0.53) or among age-classes (P = 0.84). Most infected coyotes had low intensity infections, 78.2% carried < 12 heartworms, 11.6% had 12-24 worms, and 10.2% were infected with > 24 worms. Body weights were not correlated with the presence of heartworms, nor were levels of kidney fat and marrow fat. However, reproductive success was lower in infected females. The percent of yearling females that bred was lower among infected females, as was the number of offspring produced by adults > or = 3.5 yr old. Our study demonstrates that heavy infections adversely affect fur quality and reduce fecundity of some females, but these effects are small and few coyotes (4.1%) had enough worms to trigger them. Coyote populations have increased in Illinois during the past 20 yr, but prevalence and intensity of heartworm disease appears to have changed little in that period. We conclude that heartworm disease is only a minor factor influencing coyote population dynamics in Illinois.
Article
During the winter of 1970-71, 39 red foxes (Vulpes fulva) were trapped from an area where heartworm (Dirofilaria immitis) is endemic in dogs. Eleven of the 39 foxes (five males and six females) had heartworms in the right ventricles, or pulmonary arteries, or both. Although a few adult filarids contained larvae in an advanced stage, no microfilariae were seen in blood smears prepared from the peripheral blood. Incidental to the finding of heartworms was the presence of the lung fluke (Paragonimus kellicotti) encysted in the lungs of four foxes. This is the first report of the heartworm in any free-living wild mammal in Michigan and a new host for the lung fluke in this state.
Article
Prevalence of Dirofilaria immitis in a sample of 133 coyotes (Canis latrans) from Kansas and Colorado was determined during winter, 1972. Adult heartworms were found in 11 of 133 coyotes examined (8%). Among coyotes from northeastern Kansas, 9 of 111 (8%) were infected with D. immitis. Neither of 2 coyotes from central Kansas was infected, but 2 of 20 eastern Colorado coyotes (10%) were infected with D. immitis. The highest percentage (30%) of D. immitis infection occurred among coyotes aged 5 to 6 years, although 3 yearling coyotes were infected. Single sex infections with D. immitis occurred in 5 of 11 coyotes, and maximum worm burden was 12. Based on local bounty records for 1949 to 1969, the average estimated number of adult coyotes in 450 sq. miles of Leavenworth County, Kansas, was 250 or 1 adult coyote for each 1.8 sq. mile. In any year approximately 20 adult coyotes in the county would contain 1 or more adult D. immitis; however, only 10 of these 20 coyotes would contain both sexes of D. immitis and would be capable of producing microfilariae. In Leaven-worth County coyotes infected with D. immitis were estimated to comprise less than 1% of infected canine hosts.
Article
Eighteen helminth species were recovered from 150 coyotes necropsied in West Texas: 2 trematodes, Alaria marcianae (12% of hosts infected) and Alaria sp. (0.6%); 3 cestodes, Taenia pisiformis (39%), T. serialis (4%) and Mesocestoides corti (58%); 2 acanthocephalans, Oncicola canis (26%) and Pachysentis canicola (23%); and 11 nematodes, Physaloptera rara (60%), Pterygondermatites cahirensis (37%), Spirocerca lupi (83%), Subulura s.p. (1.3%), Filaroides osleri (28%), Ancylostoma caninum (87%), Toxascaris leonina (89%), Dermatoxys veligera (1.3%), Syphacia sp. (0.6%), Dirofilaria immitis (0.6%), and Trichuris sp. (0.6%). All hosts were infected with from 1 to 10 helminth species (-x = 5.5 species). Simpson's index was very low (0.12) indicating a diverse helminth fauna. The helminth fauna of West Texas coyotes demonstrated only low similarity with those from other geographic regions in North America. Significant positive relationships were found between pairs of prevalent helminth species in terms of frequency of occurrence. Comparison of mean levels of infection between pairs of helminth species indicated 6 significant relationships. A clumped distribution was indicated in those helminths utilizing arthropod intermediate hosts or paratenic hosts. Analysis of prevalence of helminth species in terms of host sex by frequency of occurrence and mean levels of infection revealed only one significant relationship; T. leonina occurred more frequently in females than males. Similar analysis of age relationships ( ⩽ 1 year and ⩾ 2 years) and helminth parasitism indicated P. rara occurred more frequently in older animals while A. caninum and P. cahirensis occurred more frequently and with higher levels of infection in younger animals. The results of these findings are discussed in terms of food niche and behavioral aspects of this host from the Rolling Plains of Texas.
Article
Dirofilaria immitis was found in the right ventricle, pulmonary artery, and lungs of 2 red foxes (Vulpes fulva) in Connecticut. The most significant lesions occurred in the pulmonary artery and consisted of focal atheromatous-like intimal plaques, diffuse subintimal accumulations of inflammatory cells, and marked villose endarteritis in the elastic portion of the pulmonary artery. Medial hyperplasia of the muscular branches, along with periarteritis, was found in 1 fox. These 2 cases may be a further indication of the increased incidence of this disease in Carnivora in the State of Connecticut.
Article
(Dirofilaria immitis) were found in eight of 220 (3.6%) coyotes (Canis latrans) collected from fur buyers in Adams, Carroll, Cass, and Warren counties in southwestern Iowa. Infections ranged from one to 23 worms per coyote.
Article
Thirteen coyotes (Canis latrans) collected from Nueces County, Texas, harbored the following helminths: Filaroides osleri, Dirofilaria immitis, Physalaptera sp., Alaria americana, Ancylostoma caninum and Taenia sp. Aortic aneurysms were present in nine of ten adult coyotes (90%) while Spirocerca lupi was found on or in the wall of the thoracic esophagus of only three adult coyotes (30%). Oocysts of Isospora rivolta were found in the feces from one of two coyotes examined.
Epizootiology of canine heartworm disease
  • Otto
Dirofilaria immitis in the red fox (Vulpes fulva) in Minnesota
  • Schlotthauser