Prevalence of Dirofilaria Immitis Infection in Cats in Saitama, Japan

Prevalence of Dirofilaria immitis Infection in Cats in Saitama, Japan

Sadao NOGAMI and Tsuneo SATO Department of Veterinary Medicine, Nihon University, 1866 Kameino, Fujisawa, Kanagawa 252, Japan

(Received 26 March 1997/Accepted 13 May 1997)

ABSTRACT. To clarify Dirofilaria immitis infection among cats in Saitama Prefecture, Japan, 1,840 cats were examined postmortem for adult worms and microfilariae in the blood from 1989 to 1995. As a reference control, 500 dogs from the same area were examined in the same way and period. D. immitis worms were found in 15 cats, one of which had microfilariae in the blood. Prevalence rate of D. immitis infection was 0.8% (15/1,840) in cats and 46.8% (234/500) in dogs examined, whereas it was 4.1% and 64.6% in cats and dogs, respectively, aged 2 years and over. Worm burden per positive cat was 1.5 ± 0.7 (mean ± SD), the maximum number of worm was 3 in 2 cats, and 10 cats had a single worm each. All the worm-positive cats were tested for antibodies to feline immunodeficiency virus (FIV) and antigens of feline leukemia virus (FeLV) in sera. Positive rates of coinfection with D. immitis were 26.7% and 13.3% for FIV and FeLV, respectively. — KEY WORDS: canine, Dirofilaria immitis, feline, heartworm. J. Vet. Med. Sci. 59(10): 869–871, 1997

The canine heartworm, Dirofilaria immitis, produces a cut open and the heart, venae cavae, aorta, pulmonary serious clinical problem in dogs in the endemic areas. It is arteries, lungs and liver were searched for D. immitis worms. also well known to infect other hosts, including domestic The worms collected were counted and measured, and their cats. The clinical importance of D. immitis infection in the sex was distinguished. cat is well recognized in the U.S.A., Europe and Australia Microfilariae were examined by centrifuging 1 ml of and so on by the fact that even light infections are capable anti-coagulated blood with acetone solution. of causing severe pulmonary disease and sudden death [1, Antibodies to FIV and antigens of FeLV in sera were 3, 5–7, 10, 12–15, 18, 22, 23, 27, 28, 30]. Although feline tested using commercially available dot-ELISA diagnostic dirofilariasis has been sporadically reported in Japan [8, 16, kit (IDEXX, U.S.A.), and reaction was judged positive 19, 20, 29], importance of the parasite in cats has not yet according to the manufacturer’s recommendations. been fully recognized. Thus, examination of the status of D. immitis infection in cats seems important to RESULTS understanding feline dirofilariasis. The present study aimed to examine the prevalence of D. Table 1 shows the prevalence of D. immitis infection in immitis in cats and to collect associated individual data. the cats and dogs at necropsy. In 1,840 cats and 500 dogs Dogs obtained from the same area in the same period were examined, 0.8% (n=15) and 46.8% (n=234) were positive also examined post mortem for D. immitis worm as an for D. immitis worms, respectively. All the positive cats endemic reference. Since some seroepidemiological articles were 2 yrs and over in age, and the age was reasonable for of feline immunodeficiency virus (FIV) revealed a low to this parasite to develop in the final host. The positive rate moderate rate of coinfections with unusual pathogens such was 4.1% in 368 cats aged 2 yrs and over. Mean positive as D. immitis [4, 32], antibodies to FIV and antigens of rates in the male and female cats aged 2 yrs and over were feline leukemia virus (FeLV) were also measured. 4.8% and 3.6%, whereas 63.2% and 65.6% for both sexes of dogs, respectively. MATERIALS AND METHODS Table 1. Prevalence of Dirofilaria immitis infection in cats and The cats and dogs examined in this study were abandoned dogs at necropsy from 1989 to1995 in Saitama Prefecture, Ja- and pound animals. A total of 1,840 cats and 500 dogs kept pan in the Saitama Prefectural Pet Raiser’s Guidance Center were examined from 1989 to 1995. The animals were Sex of No. of cat No. of dog sacrificed under euthanasia following the guidelines of the animal examined positive (%) examined positive (%) Standards Relating to the Care and Management, etc. of Experimental Animals (The Prime Minister’s Office), and All animals: weighted, and their estimated age and sex were recorded. Female 1,041 8 (0.8) 279 132 (47.3) Male 799 7 (0.9) 221 102 (46.2) Blood sample was drawn by cardiac puncture immediately Total 1,840 15 (0.8) 500 234 (46.8) after euthanasia, and serum was separated. The sera Those 2 yrs and over: collected were divided into small aliquots and stored at － Female 221 8 (3.6) 195 128 (65.6) 30°C until assayed. D. immitis infection was confirmed at Male 147 7 (4.8) 155 98 (63.2) necropsy in which the thorax and peritoneal cavities were Total 368 15 (4.1) 350 226 (64.6) 870 S. NOGAMI AND T. SATO

Table 2. Detailed data of individual cats naturally infected with many researchers in the areas where D. immitis infection is Dirofilaria immitis prevalent among dogs [2, 18, 21]. For accurate diagnosis of D. immitis infection in cats, detection of microfilariae in Cat D. immitis Antibody Antigen No. to of FeLV the peripheral blood is unsatisfactory because circulating Age Sex Mf in No. and sex FIV in serum microfilariae are rarely found [1, 5, 7, 8, 11, 14, 24, 29]. (Yrs) blood (Worm length in cm) There are other indications that aberrant migration of the fourth stage larvae occurs more frequently in cats than dogs 12 F–1; M (10.5) – – [6, 10, 12, 20, 22, 29]. Therefore, the prevalence data 24 M– 3; F (22.5) + – obtained at necropsy are more reliable as in the present F (25.0) study. F (27.5) 32 F–1; F (21.0) – – A few reports of feline dirofilariasis suggested that it is 42 F–1; M (13.4) – – relatively rare in Japan [8, 17, 24, 26, 31]. The low 52 M– 1; M (17.8) + – prevalence of D. immitis infection in cats may be due to 63 F–2; F (26.5) – – spontaneous elimination of the parasite or to death of cats M (14.2) caused by the infection. An earlier survey in Japan showed 75 M– 1; M (14.0) – + that the prevalence was 6.4% in 62 cats by postmortem 82 M– 2; F (24.5) + – M (14.5) examination in 1973 [24], but few reports are available in 92 M+2; F (19.5) – + Japan concerning the recent status of D. immitis infection in M (15.5) cats examined postmortem. Although the highest prevalence 10 5 M – 1; M (11.6) + – was reported 16% by Abbot [1] in a feline population in 11 2 F – 1; F (19.7) – – Papua New Guinea in 1966, that in Japan was 7% of 100 12 3 F – 1; F (26.0) – – cats examined in Osaka in 1974 [17]. Feline D. immitis 13 7 M – 1; M (12.0) – – infections may be endemic in all areas of Japan except for 14 2 F – 3; F (22.5) – – F (19.5) certain parts of Hokkaido with infection rates from 0.4 to F (22.0)a) 7.0% [8, 17, 24, 26, 31]. 15 2 F – 1; M (13.5) – – The prevalence is generally believed to be in parallel with that in the dog, and the positive rate in cats was almost a) A worm obtained from the peritoneal cavity of a cat. Abbrevia- one-tenth of that in dogs [21]. In Saitama Prefecture, tions: F, female; M, male; +, positive; –, negative. Okamoto et al. reported that 59% of dogs harbored the worm Table 2 shows detailed data in individual cats infected at necropsy from 1988 to 1994 [25]. The prevalence in the with D. immitis. Age of the cats was 3.0 ± 1.6 (mean ± present study was 4.1% in cats aged 2 yrs and over, whereas SD), with a range of 2 to 7 yrs. A total of 22 worms that of dogs was 64.6%. consisting of 12 females and 10 males were obtained from Most feline dirofilariasis is produced by infection with 7 15 infected cats. Most of the worms were detected in the or less worms [1, 3, 5–7]. In a control experiment, Donahoe heart and pulmonary arterial system. One female worm [9] reported that the ratio of full-grown of inoculated was detected in the peritoneal cavity of a female cat, No. infective larvae to mature adults varied between 0% and 14. Worm burden in positive cats was 1.5 ± 0.7 (mean ± 19% in cats. Although the maximum number of worms in a SD); the maximum number of worm per animal was 3 in 2 host was recorded to be 19 in an experimentally infected cat cats, and 10 cats were infected with a single worm each. [9], usually only 1 or 2 worms are present in naturally All the monosexual infections with male worms harbored a infected cats. These studies indicate that cats are not so single worm each, on the other hand, 2 of 5 cats were susceptible to D. immitis infection as dogs. The prevalence infected with 3 female worms each. The length of worm and worm burden shown in our study were within the range was 23.0 ± 2.8 cm (mean ± SD) ranging from 19.5 to 27.5 previously reported. cm, for 12 female worms and 13.7 ± 2.1 cm, ranging from In terms of the sex of host, male cats are more frequently 10.5 to 17.8 cm, for 10 male worms. Of 3 cats infected infected with the worm and generally more seriously with both sexes of worm, only one male cat (No. 9) affected [3, 6, 7, 10, 13, 23, 31]. In the present study, 4.8% developed microfilaremia. and 3.6% in 147 male and 221 female cats respectively Of 15 D. immitis-positive cats, 4 (26.7%) and 2 cats were infected, showing no significant difference between (13.3%) were positive for anti-FIV antibody and for FeLV both sex of infected host. antigen, respectively. All cats positive for FIV and FeLV Most natural feline D. immitis infections compromised were males. None of the FIV-positive cats were coinfected amicrofilaremia as observed in the present study. with FeLV. Worm burden was not different between the Amicrofilaremia in cats may be due to infection with either FIV-positive and FIV-negative cats. sex of the worm or removal of microfilariae in the lung by immune mechanisms as described in the case of dogs [5]. DISCUSSION The ratio of female to male D. immitis worms collected was 1.2 in the present study. Although a tendency that D. immitis infection is widespread in the cat, and field female D. immitis develops more readily than males in the surveys have been undertaken on the prevalence in cats by cat cannot be well explained, Ash [2] and Fowler et al. [11] PREVALENCE OF D. IMMITIS INFECTION IN CATS 871 found 1.23 and 1.25 times as many female as male worms J. Am. Anim. Hosp. Assoc. 8: 79–80. in feline dirofilariasis. 12. Fukushima, K., Hutsell, D., Patton, S., and Patton, C. S. 1984. Considering the role of acquired immunodeficiency and Aberrant dirofilariasis in a cat. J. Am. Vet. Med. Assoc. 184: immunosuppression in pathogenesis of various diseases, the 199–201. influence of FIV and FeLV to D. immitis infection in cats is 13. Glaus, T. M., Jacobs, G. J., Rawlings, C. A., Watson, E. D., and Calvert, C. A. 1995. Surgical removal of heart worms of parasitological and clinical interests. Although no from a cat with caval syndrome. J. Am. Vet. Med. Assoc. 206: previous report demonstrated that immunosuppression plays 663–666. a role in increasing the pathogenicity of D. immitis in the 14. Griffiths, H. J., Schlottauer, J. C., and Gehrman, F. W. 1962. cat, Bunge and Malone [4] suggested that in the case of Feline dirofilariasis. J. Am. Vet. Med. Assoc. 140: 61. aberrant parasitic diseases in cats such as feline dirofilariasis 15. Hawe, R. S. 1979. The diagnosis and treatment of occult concomitant infection with FIV should be routinely dirofilariasis in a cat. J. Am. Anim. Hosp. Assoc. 15: 577– examined. The positive rate of 26.7% for FIV infection 582. shown in this study was not so high compared with that of 16. Horioka, E., Tagawa, M., Nakanishi, A., Ejima, H., Mitani, 31.6% in 57 male cats studied in 1992 in the same area S., Umeda, M., and Kurokawa, K. 1984. A feline case of (unpublished data). Our results showed that coinfection Dirofilaria immitis infection. J. Jpn. Vet. Med. Assoc. 37: 451–455. with FIV does not influence in increasing the susceptibility 17. Iseki, M., Tanabe, K., Uni, S., Sano, R., and Takada, S. 1974. of D. immitis in cats, so cats may be infected with D. immitis A survey on Toxoplasma and other protozoal and helminthic irrespective of immunosuppression. parasites of adult stray cats in Osaka area. Jpn. J. Parasitol. 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