Dirofilaria immitis parasite infection in cats: first case reported in the Legal Amazon region, Brazil - case report

ABSTRACT A case of infection with Dirofilaria immitis in a cat is reported here with clinical signs of apathy, anorexia, dyspnea, polypnea, slight dehydration and pale mucus membranes. The radiographic examination showed cardiomegaly, lobar arteries dilation of the cranial lobes and tortuosity, enlargement of the caudal lobar arteries. In the right lobe of the lung parenchyma, interstitial pulmonary opacification tending to alveolar opacification was seen. The clinical signs, the movements, and the morphology of the microfilariae in the direct examination of fresh blood, peripheral blood smear and Knott’s modified test supported the diagnosis. We alert to the need for clinicians to consider feline heartworm diseases as a differential diagnosis in endemic areas when cats show respiratory signs.


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Filariae are a group of parasitic nematodes that belong to the family Onchocercidae and inhabit the circulatory and lymphatic systems of its hosts (Biasato et al., 2017).Dirofilaria immitis is the causative agent of dirofilariasis.The typical hosts for D. immitis are domestic dogs, and transmission of this parasite takes place via species of mosquitoes.Unlike dogs, in cats, few larvae develop into adults (Lee and Atkins, 2010), because most of the immature worms that reach the caudal pulmonary arteries die, leading Arq.Bras.Med.Vet.Zootec., v.75, n.2, p.237-241, 2023 with the cardiovascular and respiratory systems.The aim of this work was to report on a case of microfilaremia in a cat in São Luis, Maranhão (northeastern region of Brazil) where canine heartworm disease is endemic.

CASE REPORT
A female mixed-breed short-haired cat of indeterminate age was found on a street and was taken for veterinary medical care at the University of Maranhão State in the city of São Luis (44°18′10″ W; 2°31′46″ S).
A clinical examination was conducted, and the following signs were observed: apathy, anorexia, dyspnea, polypnea, slight dehydration and pale mucus membranes.The other physiological parameters were within normal limits.From the radiographic examination of the animal, heartworm infection was suspected.
Therefore, direct examination of fresh blood and Knott's modified test (Newton and Wright, 1956) were done.Afterwards, the sample was examined under an optical microscope at different magnifications (40 and 100X).
The radiographic examination showed notable cardiomegaly with hemosedimentation rate-VHS = 9.7 V, dilation of the cranial lobar arteries and tortuosity.Enlargement of the caudal lobar arteries and loss of its definition were observed.In the right lobe of the lung parenchyma, interstitial pulmonary opacification tending to alveolar opacification was seen.Pulmonary hyperinflation was also observed, with pulmonary area going beyond the last costal arch and flat diaphragm.In the abdomen, loss of abdominal conspicuity could be seen, suggestive of peritoneal effusion (Figure 1 a,b).In the direct examination of fresh blood, microfilariae with serpent-like movements in the blood-cell layer were observed consistent with D. immitis, while Acantocheinolema reconditum (Syn: Dipetalonema reconditum) microfilaria have erratic fast movements.To identify the microfilariae, peripheral blood smear and Knott's modified test, were done and small numbers of   Branco et al., 2009;Moraes et al., 2021;Pereira et al., 2018;).Our study provides the first report in the state of Maranhão, Legal Amazon region, thus increasing the known geographical area of feline heartworm disease in Brazil.
The case reported here consisted of feline heartworm infection that was suspected through radiography and clinical signs lead to suspicion of heartworm diseases and confirmed through parasitological tests.According to AHS (Current…, 2020), radiography may provide pieces of evidence of this infection, as seen in the case reported here.The animal died one day after the appointment with the veterinarian and its rescuer did not authorize a necropsy.
Concerning clinical manifestations, the most evident of these were: apathy, anorexia, dyspnea, polypnea, slight dehydration and pale mucus membranes.
However, the following manifestations have also been reported in the literature: salivation, intermittent vomiting, lethargy, anorexia, weight loss, respiratory signs (such as coughing, intermittent dyspnea, tachypnea or hemoptysis), tachycardia, collapse, shock, syncope and death due to thromboembolism (Ettinger and Feldman, 2005).
In this study, the thoracic radiograph (lateral and ventrodorsal) revealed alterations suggestive of dirofilariasis.Heart enlargement and right lobar pulmonary arteries dilation are suggestive of dirofilariasis (Biasato et al., 2017), and enlargement of the main lobar and peripheral pulmonary arteries is the most consistent lesion in infected cats (Current…, 2020).The ration of the width of the right pulmonary artery and the width of the rib 9 was higher than the reference Arq.Bras.Med.Vet.Zootec., v.75, n.2, p.237-241, 2023 values is a sign that strongly suggests the presence of heartworm infection (Lister et al., 2005).Hyperinflation is less common (Lister et al., 2008), but it was observed in the case reported here.
The diagnosis of feline heartworm disease could be done by the detection of microfilariae in peripheral blood through examination of stained blood smears under a microscope, but this approach has several limitations (Phuakrod et al., 2019).Given that microfilaremia is unusual and may be transient or may present with low parasite loads, false-negative results can occur (Current…, 2020).However, when present, microfilaremia provides a definitive diagnosis (Current…, 2020).Thus, the finding of microfilariae in our study, even in small quantities, allowed us to make a definitive diagnosis.
Sudden death may occur in up to 47% of cats with heartworm (Evans et al., 2000), as occurred in our study.According to Lister et al. (2008), this has been attributed to circulatory collapse and respiratory failure due to acute pulmonary artery infarction.This acute infarction occurs due to sudden pulmonary thromboembolism, caused by spontaneous death of the adult worm, which can results in an intense intravascular inflammatory reaction (Lister et al., 2008).
On São Luís Island, state of Maranhão, a survey on the prevalence of canine heartworm disease was carried out among dogs from 64 locations, from 1991 to 1994 (Ahid et al., 1999).However, since then, the disease has not been reported in the literature.Our finding of a cat with microfilariae raises the hypothesis of lake of clinician acuity in diagnose the disease.However, a large study on dogs would be needed to determine the real prevalence among these animals.

CONCLUSION
In conclusion, we reported here the first diagnosis of feline heartworm disease in the state of Maranhão, Legal Amazon region, Brazil.The presence of microfilaremia in the present case confirms the diagnosis of feline heartworm.

Figure 1 .
Figure 1.(a) Ventral dorsal view radiography showing cardiomegaly, (b) Lateral view radiography showing pulmonary artery dilatation and pulmonary alveolar pattern.
microfilariae were detected.Morphological examination showed long and narrow microfilaria with absence of hyaline sheath, a pointed cephalic end and a straight tail with a pointed end (Figure2 a,b,c).The microfilariae examined in this study had the morphology and movement of D. immitis(Ciocan et al., 2010).

Figure 2 .
Figure 2. (a) Microfilaria of Dirofilaria immitis, observed in examination of fresh blood, (b) Peripheral blood smear and (c) The modified Knott technique -40x DISCUSSION In Brazil, there have been reports of feline heartworm disease in the states of Rio de Janeiro and Rio Grande do Norte (Alberigi et al. 2020;Branco et al., 2009;Moraes et al., 2021;Pereira et al., 2018;).Our study provides the first report in the state of Maranhão, Legal Amazon region, thus increasing the known geographical area of feline heartworm disease in Brazil.