Can heartworm prevalence in dogs be used as provisional data for assessing the prevalence of the infection in cats?

Can heartworm prevalence in dogs be used as provisional data for assessing the prevalence of the infection in cats?

Veterinary Parasitology 176 (2011) 300–303 Contents lists available at ScienceDirect Veterinary Parasitology journal homepage: www.elsevier.com/loca...

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Veterinary Parasitology 176 (2011) 300–303

Contents lists available at ScienceDirect

Veterinary Parasitology journal homepage: www.elsevier.com/locate/vetpar

Can heartworm prevalence in dogs be used as provisional data for assessing the prevalence of the infection in cats? L. Venco a,∗ , M. Genchi b , C. Genchi b , D. Gatti c , L. Kramer d a b c d

Veterinary Hospital Città di Pavia, 27100 Pavia, Italy Università degli Studi di Milano, Facoltà di Medicina Veterinaria, Milano, Italy Bayer Animal Health, Italy Università degli studi di Parma, Facoltà di Medicina Veterinaria, Parma, Italy

a r t i c l e

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Keywords: Cats Feline heartworm disease Epidemiology Dirofilaria immitis

a b s t r a c t Cats are considered a susceptible host for Dirofilaria immitis; however, increased host resistance is reflected by relatively low adult worm burdens in natural and experimental infections; the prolonged prepatent period (8 months); the low level and short duration of microfilaremia; and the short life span of adult worms (2–3 years). From April to September 2006, 212 cats and 608 dogs, all exposed for at least one transmission season, were screened for D. immitis infection in a multi-center study in the Po River Valley in northern Italy. Cats were initially evaluated by antibody testing; positive subjects were followed up by antigen testing and echocardiography (and necropsy if death occurred). The prevalence in dogs was 29% by a modified Knott test and antigen testing compared with a prevalence of 4.7% in cats by an antibody test; six of these infections (2.8%) were confirmed by the follow-up evaluations. This field study demonstrated that the prevalence of heartworm infection in cats in this area is within the expected limits of 9–18% of the prevalence in dogs. Antibody testing likely underestimates the real prevalence of D. immitis infection in cats. These results also emphasize the importance of preventive treatment in cats. © 2011 Elsevier B.V. All rights reserved.

1. Introduction Cats are considered a susceptible host for Dirofilaria immitis, but enhanced host resistance is reflected by relatively low adult worm burdens in natural (2–4 worms being the usual burden) and experimental infections; the prolonged prepatent period (8 months); the low level and short duration of microfilaremia; and the short life span of adult worms (2–3 years). Most cats seem to tolerate D. immitis infection for extended periods. Some spontaneously self-cure as a result of natural death of parasites without demonstrating clinical signs, or they may suddenly show dramatic acute res-

∗ Corresponding author. Tel.: +39 0382 571510. E-mail address: [email protected] (L. Venco). 0304-4017/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.vetpar.2011.01.013

piratory signs. Furthermore, sudden death in apparently healthy cats is a not rare event. Chronic symptoms include coughing, vomiting, diarrhea, and weight loss (Calvert et al., 1994, Dillon, 1984; McCall et al., 1994). In a recent study of 34 infected, asymptomatic cats, 82% self-cured, 62% never showed clinical signs, and 18% died (Venco et al., 2007). In the majority of cats (62%) enrolled in that study, the infection lasted more than 3 years. It is now generally accepted that heartworm disease may occur in cats in any area where dogs are infected (Dillon, 1984; Genchi et al., 1998a, 1992; Guerrero et al., 1992; Kramer and Genchi, 2002), but the frequency and level of infection are less predictable in cats than in dogs. If one takes into account that cats do not attract mosquitoes to the same extent as dogs, have a natural resistance to infection (only 75% of cats develop infections following experimental inoculation with infective D. immitis larvae)

L. Venco et al. / Veterinary Parasitology 176 (2011) 300–303 Table 1 Heartworm prevalence in dogs by Knott and antigen testing. Parameter

No. of dogs (%)

Total tested Total infected Knott and Ag positive Knott negative and Ag positive Knott positive and Ag negative

608 221 (29) 176 (80)a 40 (18)a 5 (2)a

a

Table 2 Heartworm prevalence in cats by antibody, antigen, echocardiography, and necropsy.

Number and percentage of total infected dogs.

Parameter

No. of cats (%)

Total screened Total antibody positive Total antigen positive Total echo positive Total necropsy positive Total verified positive

212 10 (4.7) 2 (20)a 4 (40)a 1 (10)a 6 (2.8)

a

(McCall et al., 1992), and that the lifespan of the worms in cats is 50% shorter than in dogs, a theoretical prevalence of 9–18% of the prevalence in dogs is expected. To verify this assumption, a multi-center study was conducted in a defined area of the Po River Valley in northern Italy. 2. Material and methods From April to September 2006, 212 cats (110 males, 102 females with ages ranging from 2 to 12 years) and 608 dogs (335 males, 273 females with ages ranging from 2 to 14 years), all of which had been exposed to mosquitoes for at least one transmission season and were allowed to be outdoors during the evenings, were screened for D. immitis infection in a multi-center study involving 19 veterinary hospitals in a defined area of the Po River Valley. The area included the provinces Pavia, Lodi, Piacenza, Milan, and Alessandria Cats were first investigated with an antibody test (Solo Step FH Heartworm Test; Heska, Loveland, CO), followed, in the positive subjects, by antigen testing (SNAP Feline Triple Test; Idexx, Westbrook ME) and echocardiography. Necropsies were performed whenever possible for any animal that died during the study. Dogs were evaluated by modified Knott test and antigen testing. Concurrent feline immunodeficiency virus (FIV)) and feline leukemia virus (FeLV) infections, the presence of other parasites, and number of dogs residing in the same residence were recorded for each cat.

301

Number and percentage of cats positive by antibody testing.

(occult infections), and 2% (5/221) had circulating microfilariae but were negative by the antigen test. Testing of cats detected antibodies to D. immitis in 10 animals (4.7%) (Tables 2 and 3). Infections were confirmed for six of these cats (2.8%). One was negative by the antigen test, but was positive on necropsy for two adult male worms (Table 2). One cat was positive for antigen testing and echocardiography; three were negative by antigen testing but were positive by echocardiography; one cat was positive by antigen testing and no additional testing was required (Table 2). Four of the 10 cats positive by antibody test displayed no clinical signs at the time of testing; dyspnea was a common observation for six of these cats (Table 3). Six of the antibody-positive cats eventually tested antibody negative 1–3 years after the initial evaluation for the study (Table 3). Three of the 10 cats died; one had two male heartworms at necropsy, one was negative for adult heartworms, and one was unavailable for necropsy (Table 3). Sixty of the 212 screened cats were living in homes that had one or more dogs (all dogs were receiving a heartworm preventative), and eight cats were positive for FeLV infection, five for FIV, and three were positive for both FeLV and FIV infection (none of these cats were positive by antibody testing for heartworm disease). Of the 212 cats in the study, 58 had fleas, seven had Otodectes cynotis, and one was infested with Notoedres cati. No intestinal parasite infections were reported.

3. Results 4. Discussion The overall prevalence in dogs was 29% (Table 1). Eighty percent of the positive dogs (176/221) yielded a positive result both on Knott and antigen testing, 18% (40/221) were positive by antigen testing but negative for the Knott test

Diagnosis of feline heartworm disease is more elusive than for dogs, and multiple procedures and tests are needed to confirm the presence of infection. Moreover, the occur-

Table 3 Antigen testing, echocardiography, necropsy result in cats with positive antibody test. Ag test

Echocardiography

Clinical signs

Outcome

Negative Negative Negative Positive Negative

Negative Not done Positive Positive Negative

None Dyspnea Dyspnea Dyspnea, vomiting None

Positive Negative Negative

Not done Negative Not done

Cough, dyspnea None Dyspnea

Negative Negative

Positive Positive

None Dyspnea

Ab negative after 1 year Died; 2 male worms recovered Ab negative after 1 year Ab negative after 1 year Ab positive after 1 year Ab negative after 2 years Died; no necropsy Ab negative after 1 year Died; neg for adult D. immitis Echo negative after 2 years Ab negative after 3 years Died due to unrelated disease; no necropsy

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rence of sudden death complicates diagnosis even further (Dillon, 1988, 1998). Tests and procedures available to facilitate the antemortem diagnosis of infection currently include antibody or antigen detection tests and echocardiography (Atkins et al., 1998a; Snyder et al., 2000; Venco et al., 1998a,b,c). Antibody testing alone as a screening for feline heartworm infections likely underestimates the actual prevalence infection in cats, as many infected cats do not maintain detectable levels of antibodies as the parasites mature (American Heartworm Society, 2010). In this study, D. immitis antibodies were detected in 10 (4.7%) of the cats tested; however, necropsy results verified only six of the 10 cats (2.8% of the total cats tested) were positive for adult D. immitis, approximately 10% of the prevalence in dogs (29%). Commercially available antibody detection tests were initially reported to be highly sensitive and specific, particularly in cats with relatively heavy experimentally induced infections (Bestul et al., 1998; Watkins et al., 1998; McCall et al., 1995, 1998, 2001). Thus, antibody tests were previously recommended for testing cats with suspected heartworm infections (Genchi et al., 1998a,b; Knight et al., 2001; McCall et al., 2001). However, results have been variable in cats with naturally acquired infections (Nelson, 1998; Snyder et al., 2000; Levy et al., 2003). According to Levy (2007), the specificity of the antibody detection tests for cats with naturally acquired infections ranges from 78% to 99% and the sensitivity from 32% to 90%. Interrupted infections are still immunogenic enough to stimulate a persistent antibody response even in the absence of adult parasites (Donoghue et al., 1998; McCall et al., 2001). Tests for detection of D. immitis circulating antigens are heavily dependent on the number of mature female parasites present in the animal (McCall et al., 1995, 1998). In earlier studies, sensitivity of antigen testing was relatively low in cats with more typical, light worm burdens (McCall et al., 1995, 1998; Genchi et al., 1998b). In general, it appears that the sensitivity of these tests has improved over the past several years (McCall et al., 2001). Levy (2007) reported a specificity of 78–99% and a sensitivity of 68–86% for cats with naturally acquired infections. A positive antigen detection test result is indicative of active adult infection; however, a negative test does not rule out that the animal may be infected with only male worms, a single adult female, young (prepatent period) adult worms, or very old adult worms—most of which are common for cats (McCall et al., 1995; Piché et al., 1998). Ecocardiography is a useful diagnostic tool with high sensitivity, but it relies strongly on the expertise of the individual performing the test. (Venco et al., 1998a,c; DeFrancesco et al., 2001). The adult parasite is echogenic, producing images of two, short parallel lines (Badertscher et al., 1988). The pulmonary arteries, right ventricle, and the right atria must be examined carefully because infections with one or only a few parasites could be overlooked. Recently Atkins et al. (2007) evaluated 80 adult cats, each inoculated with 60 D. immitis L3 on test day 1, to test the potential quantification of the parasite burden (confirmed at necropsy) by echocardiography. Worm burden by echocardiography correlated well, but not precisely,

with post mortem counts, and both false-negative and false-positive results were obtained. In any case, echocardiography is a fundamental tool for the diagnosis of feline heartworm infection. Necropsy has long been considered a gold standard for post mortem diagnosis, but dissection of the heart and lungs is insensitive for immature infections as well as for ectopic infections (McCall et al., 1992; 1995; Genchi et al., 1998b; Levy et al., 2007). The observation of neurologic signs before death indicates the need for a more complete necropsy involving the brain, spinal cord, heart, lungs, and body cavities (Atkins et al., 1995; Miller et al., 1998). Heartworm prevalence and distribution are better defined for dogs, but there is a significant lack of information on the frequency of infection in cats because of diagnostic difficulties. In highly endemic areas. essentially every unprotected dog becomes infected (McTier et al., 1992a). This study highlights the lack of awareness of both owners and local practitioners concerning feline heartworm disease. The results of this field study demonstrated that the prevalence of the heartworm infection in cats in a small hyperendemic area is within the theoretically expected limits of 9–18% of the prevalence in dogs. None of the cats included in the study were receiving a heartworm preventative, nor had they received prophylactic treatment in the past; however, all dogs living in homes that also had cats were receiving a heartworm preventative. It also seems that cats are not routinely screened for other parasitic diseases (i.e., gastrointestinal parasites), as only external parasites were reported by the participating veterinarians. Furthermore, no apparent correlation with FeLV and FIV infection was noted.

5. Conclusion Based on the results of this study, the prevalence of feline heartworm disease can be roughly estimated as 10% of the known prevalence of the infection in dogs. This information could be useful given the diagnostic problems in cats that do not allow large epidemiological studies in this species: antibody testing is not specific and antigen testing shows poor sensitivity. These results also emphasize the importance of preventive treatment for heartworm infection in cats. Even in those areas where prevalence of canine infections may be low, feline infections could still occur. It would be interesting to confirm this hypothesis in areas of low endemicity in dogs. Finally, it would appear that awareness of the disease (as for other parasitic diseases that require specific diagnostic screening) is still low, and major efforts should be directed to inform and educate veterinarians and pet owners of the need for screening cats for heartworm infection and for cats to receive prophylactic treatment.

Funding/conflicts of interest The study did not have any external funding. The authors declare no conflicts of interest.

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