Heartworm Removal Research Articles

Evaluation of improved transvenous heartworm extraction brush in dogs with caval syndrome.

Heartworm infection in dogs is caused by Dirofilaria immitis and common in shelter animals and outdoors dogs. Caval syndrome can develop with severe infection and physical heartworm removal is essential with heartworm burdens. In this study, we used an improved transvenous heartworm extraction brush, which was expected to cause less cardiovascular damage and allow easier manipulation. This study aims to evaluate efficacy of this improved transvenous heartworm extraction brush. The brush was designed to improve upon the limitations of the previous brush-type devices. The brush was made of a polyvinyl chloride tube and threads of polyamides or polyglyconates. Metal material was inserted at the front tip for easy visualization under fluoroscopy. The eight dogs diagnosed with caval syndrome with large numbers of heartworms and pulmonary hypertension were used in this study. The removal procedure began with the dissection of the subcutaneous tissue around the right jugular vein. The device was inserted through the jugular vein. After insertion, the tube was rotated to catch the heartworms and extracted with the heartworms hanging on the threads. The procedure was repeated several times. Lastly, jugular vein and skin sutures were made. Adulticidal therapy was administered after heartworm removal. The mean number of removed heartworms was 10.5 ± 4.24 and mean number of remaining heartworms was 0.63 ± 1.06. Total procedure time was 72.63 ± 51.36. Except for three cases, heartworms were not detected on ultrasonography after the procedure. No procedure-related side effects were observed within the 1- to 2-mon. An improved transvenous heartworm extraction brush is efficient for heartworm removal in dogs with caval syndrome.

Optimized protocol for DNA/RNA co-extraction from adults of Dirofilaria immitis

Dirofilaria immitis, the etiologic agent of canine heartworm disease, like several other filarial nematodes, harbors the bacterial endosymbiont Wolbachia. To investigate metabolic and functional pathways of D. immitis and Wolbachia individually, along with their interactions, the use of both transcriptomic and genome analysis has becoming increasingly popular. Although several commercial kits are available for the single extraction of either DNA or RNA, no specific protocol has been described for simultaneous extraction of DNA and RNA from such a large organism like an adult D. immitis, where female worms generally reach ∼25 cm in length. More importantly, adult worms of D. immitis can only be obtained either through necropsy of experimentally infected dogs or by minimally-invasive surgical heartworm removal of naturally infected dogs. This makes each individual worm sample extremely important. Thus, in the context of a project aimed at the evaluation of both gene expression analysis and Wolbachia population assessment following different treatments, an optimized protocol for co-extraction of DNA and RNA from a single sample of adult D. immitis has been developed.•An optimized method for DNA/RNA co-extraction from large size nematodes using TRIzol® reagent.•Allows maximum exploitation of unique samples as adults of D. immitis.

A Homemade Snare: An Alternative Method for Mechanical Removal of Dirofilaria immitis in Dogs.

Canine dirofilariosis is a life-threatening parasitic disease that is increasingly reported worldwide. Once diagnosed the main treatment goals are to improve the animal's clinical condition and to eliminate all life stages of the parasite with minimal posttreatment side effects. This can be achieved through mechanical, surgical, or chemotherapeutical approaches. Currently, manual extraction is the preferred method to remove adult heartworms due to its diminished invasiveness, reduced damage to the vascular endothelium, and shortened anaesthesia duration. However, it remains an expensive technique that can be highly traumatic. To address this issue, a nontraumatic homemade catheter-guided snare was developed for heartworm removal by adapting and folding a 0.014-inch coronary wire (BMW, Abbott Vascular). Transvenous heartworm extraction was performed on a dog severely infected with adult heartworms by inserting the modified snare into a 6-F Judkins right coronary guiding catheter BMW (Cordis) and advancing it into the right ventricle under fluoroscopic guidance. Fifteen adult specimens of Dirofilaria immitis were successfully extracted from the pulmonary artery and right ventricle without complications. To assure the death of both larvae and adults, postoperative treatment was successfully managed using ivermectin, doxycycline, and melarsomine, with no recurrence after surgery.

Comparison of 2 Retrieval Devices for Heartworm Removal in 52 Dogs with Heavy Worm Burden

For treating dogs with heavy heartworm infection, mechanical removal using various retrieval devices is useful. However, the efficacy and safety of retrieval devices have rarely been studied. Catheter-based heartworm removal using 2 retrieval devices (basket and tripod grasping forceps) is efficient and safe for treating dogs with heavy worm burden. Fifty-two client-owned dogs with heavy (Class III and IV) worm burden. A retrospective study was performed on 52 dogs, using a catheter-based heartworm removal approach using 2 types of retrieval devices (ie, the basket and the tripod grasping forceps). The efficacy and complications associated with the 2 devices were assessed. The basket device was used on 22 of the study group dogs, and the tripod grasping forceps was used on 30 of the dogs. The postoperative survival rate was 95.5% for the basket device and 80% for the tripod grasping forceps, but the difference was not statistically significant. The worm number captured per attempt was 3.5 ± 1.7 using the basket device and 1.9 ± 0.85 for the tripod grasping forceps (P < .05). Various complications associated with heartworm removal were noticed with both retrieval devices. This study suggests that catheter-based heartworm removal is not only a relatively safe and efficient therapeutic method in dogs with heavy worm burden, but more efficient using the basket device. Our data do not indicate a clear safety advantage between the 2 devices evaluated, although the survival rate was numerically higher in dogs undergoing a basket intervention.

Catheter-guided percutaneous heartworm removal using a nitinol basket in dogs with caval syndrome

Carval syndrome is a severe heartworm infection where the worms have migrated to the right atrium and vena cava; this condition is associated with a myriad of clinical signs. Several non-surgical and interventional methods are currently used for mechanical worm removal. However, the success rate and complications related to these methods are heavily dependent on methodology and retrieval devices used. In this study, we developed a catheter-guided heartworm removal method using a retrieval basket that can easily access pulmonary arteries and increase the number of worms removed per procedure. With this technique, we successfully treated four dogs with caval syndrome.

経食道超音波断層像下における犬糸状虫摘出法

経食道超音波断層像下における犬糸状虫摘出法

Cardiopulmonary Function in Dogs with Serious Chronic Heartworm Disease.

Cardiopulmonary function was examined in 18 dogs with serious chronic heartworm disease showing ascites, subcutaneous edema, prostration, weakness, jaundice and so on. After surgical heartworm removal from the pulmonary arteries, 10 dogs recovered (surviving group), and 8 dogs died or were euthanatized because of poor prognosis (nonsurviving group). The number of live heartworms residing in the pulmonary arteries of the surviving group tended to be larger than that in the nonsurviving group. At necropsy, severe pulmonary arterial lesions such as thromboembolism including dead heartworms, proliferative and villous lesions and intimal hyperplasia were noticed in all dogs examined, and tended to be severer in the nonsurviving group. Heartworm-coiling around the tricuspid valve chord was found in 1 dog of the surviving group and 4 dogs of the nonsurviving group. Before heartworm removal, there was no significant difference in the mean pulmonary arterial pressure (MPAP) between the surviving and nonsurviving group. Right atrial pressure (v-wave) was higher, and the cardiac index (CI) was lower in the nonsurviving group. Arterial oxygen tension was lower in the surviving group than in the heartworm-free group, and it was lower in the nonsurviving group than in the surviving group. Carbon dioxide tension was lower in the surviving group than in the heartworm-free group. Bicarbonate concentration (HCO3-) was lower both in the surviving and nonsurviving groups than in the heartworm-free group. One week after heartworm removal, MPAP decreased (P less than 0.05), and CI and HCO3- tended to increase in the surviving group.

Relationship between pulmonary arterial pressure and lesions in the pulmonary arteries and parenchyma, and cardiac valves in canine dirofilariasis.

The relationship between pulmonary hypertension and lesions was examined in 41 dogs infested naturally with heartworms, which consisted of 28 cases with pulmonary heartworm disease and 13 cases with caval syndrome. Pulmonary arterial pressure (PAP) was measured before and 1 or 7 days after heartworm removal with a flexible alligator forceps. In these dogs, lesions were examined after the last measurement of PAP. The mean PAP was 28.2 +/- 16.0 mmHg (10.9 to 81.4 mmHg in range) at post-removal phase. Pulmonary arterial intimal lesions, pulmonary thromboemboli, pneumonic lesions, tricuspid valvular lesions and mitral valvular lesions were macroscopically recognized in 95, 59, 39, 54 and 56% of cases, respectively. These lesions were classified by severity and the relationship with PAP was examined by the multiple correlation analysis. The multiple coefficient correlation was found the highest between PAP and thromboemboli, followed by mitral valvular lesion, tricuspid valvular lesion, and pneumonic lesion. There was no significant correlation between PAP and intimal lesions. The coefficient of determination showed the highest value in thromboemboli when one variable was used, and increased only very slightly when a variable of thromboemboli was added to those of other lesions. The cases with high PAP had fresh thromboemboli in large pulmonary arteries. From these evidences, it was concluded that thromboemboli following natural death of heartworm was the most important factor causing an increase in PAP and developing clinical signs in canine heartworm disease.

犬糸状虫抗原検出キットの評価と虫体摘出後の血中抗原価の変化

The sensitivity and specificity of a commercial heartworm (Dirofilaria immitis) antigen test kit were evaluated in 100 dogs with and without heartworm infections. All 25 microfilaremic heartworm-infected dogs, in which the number of heartworms ranged from 3 to 91, were identified correctly as positive (sensitivity: 100%). The test detected occult infection in 18 of 25 (72.0%) dogs. All heartworm-free dogs with (25 dogs) and without (25 dogs) roundworm (Toxocala canis) infection were indentified as negative (specificity: 100%). The accuracy in all 100 dogs tested was 93%. Changes in the circulating antigen levels after surgical heartworm removal were examined in 10 dogs using this kit. By surgical treatment, all heartworms were removed in 6 dogs, and removal efficiency ranged from 65.5 to 86.7% in the 4 other dogs. After heartworm removal, the circulating antigen levels declined in all dogs. The mean antigen level in 10 dogs was×730±1238 before removal, ×84±98 at 4 weeks after removal, ×36±39 at 8weeks after, and ×14±8 at 12 weeks after. There were no dogs in which the circulating antigen disappeared.

Changes in Cardiopulmonary Function Values after Surgical Heartworm Removal in Dogs with Dirofilariasis

Changes in Cardiopulmonary Function Values after Surgical Heartworm Removal in Dogs with Dirofilariasis

Cardiopulmonary function values before and after heartworm removal in dogs with caval syndrome

SUMMARY Cardiopulmonary function values were determined before and after surgical removal of adult heartworms in 25 dogs with spontaneous and 4 dogs with drug-induced caval syndrome (cs). Fifteen dogs with spontaneous cs (recovery group) and 4 dogs with drug-induced cs (drug-induced cs group) recovered after removal, and 10 dogs with spontaneous cs were euthanatized or died (nonsurviving group). Before heartworm removal, injected radiographic contrast medium was regurgitated from the right ventricle to the right atrium. Mean pulmonary arterial pressure and total pulmonary resistance were not statistically different between the recovery and nonsurviving groups of dogs, but the end-diastolic right ventricular pressure (mean ± sd, 6.9 ±9.1 mm of Hg) and the a (8.7 ± 9.2 mm of Hg)- and v (6.3 ± 8.5 mm of Hg)-waves of the right atrial pressure curve in the recovery group were less, respectively, than the end-diastolic right ventricular pressure (17.3 ± 6.0 mm of Hg) and the a (15.8 ± 6.1 mm of Hg)- and v (21.4 ± 6.9 mm of Hg)-waves in dogs of the nonsurviving group. After heartworm removal, contrast medium regurgitation disappeared, and cardiac output of the right ventricle increased in dogs of the recovery (from 2.08 ± 0.72 to 2.38 ± 0.68 L/min; P &lt; 0.05) and drug-induced cs (from 1.42 ± 0.19 to 1.88 ± 0.26 L/ min, P &lt; 0.05) groups. However, regurgitation remained, and cardiac output did not increase in some dogs of the nonsurviving group. Mean pulmonary arterial pressure decreased significantly (from 37.7 ± 18.3 mm of Hg to 32.0 ± 16.1 mm of Hg; P &lt; 0.01) at 1 week after heart-worm removal in dogs of the recovery group, but not in those of the nonsurviving group. Total pulmonary resistance (from 12,612 ± 7,670 dynes·sec·cm-5·kg of body weight to 9,776 ± 6,089 dynes·sec·cm-5·kg; P &lt; 0.01) and right atrial pressure (a-wave: from 8.7 ± 9.2 mm of Hg to 4.1 ± 5.6 mm of Hg; v-wave: from 6.3 ± 8.5 mm of Hg to 2.1 ± 4.6 mm of Hg) decreased after heartworm removal in dogs of the recovery group. Total pulmonary resistance (from 20,309 ± 9,682 dynes·sec·cm-5·kg to 15,970 ± 6,798 dynes·sec·cm-5·kg; P &lt; 0.05) and right atrial pressure (a-wave: from 15.8 ± 6.1 mm of Hg to 10.1 ± 6.3 mm of Hg; v-wave: from 21.4 ± 6.9 mm of Hg to 11.1 ± 3.7 mm of Hg) also decreased in dogs of the nonsurviving group. However, pressures in the right side of the heart and total pulmonary resistance after heart-worm removal were greater in dogs of the nonsurviving group than in dogs of the recovery group. At necropsy, pulmonary arterial emboli containing dead heartworms were found in almost all dogs with spontaneous cs, but not in dogs with drug-induced cs. The severity of pulmonary arterial embolism correlated significantly with mean pulmonary arterial pressure before (r = 0.710; P &lt; 0.01) and 1 week after (r = 0.728; P &lt; 0.01) heartworm removal.

Serum Creatine Kinase Activities in Dogs with Dirofilariasis.

Total serum creatine kinase (CK) and its isozyme activities were determined in dogs with dirofilariasis. Before heartworm removal, total CK and isozyme activities in dogs of the mild group were not different from those in dogs of the heartworm-free group. BB activity was higher in dogs of the hemoptysis group. Dogs of the ascites group displayed a mild increase in MM activity. In dogs of the caval syndrome (CS) group, total CK and MM activities were highest among the heartworm-free and heartworm-infected dogs, and MM isozyme accounted for most (75%) of total CK activity. MB and BB activities were also higher. However, there were no significant differences in CK activities between the surviving and non-surviving cases. In dogs with pulmonary heartworm disease (mild and ascites groups), MM activity correlated significantly with the number of heartworms (r = 0.45), hematocrit value (Ht, r = -0.40), serum alanine aminotransferase (ALT, r = 0.42) and lactate dehydrogenase (LDH, r = 0.46) activities, mean pulmonary arterial pressure (r = 0.64) and total pulmonary resistance (r = 0.50). In dogs with CS, MM activity did not correlate with any parameter, but BB activity correlated with the number of heartworms at the right atrium (r = 0.61), Ht (r = -0.53), ALT (r = 0.80), LDH (r = 0.73) and serum urea nitrogen (r = 0.47). At 1 week after heartworm removal, BB and MM activity decreased in dogs of the hemoptysis and ascites groups, respectively. In dogs of the CS group, total CK and MM isozyme activities decreased markedly (P less than 0.01) regardless of their prognosis.

Improvement in pulmonary arterial lesions after heartworm removal using flexible alligator forceps.

Improvement of pulmonary arterial lesions after heartworm removal using flexible alligator forceps was investigated by measuring pulmonary arterial pressure (PAP), and by angiographic and histopathological examinations in 11 dogs. PAP obtained immediately after worm removal corresponded well with angiographic abnormalities. In 2 dogs, high PAP immediately after worm removal fell gradually by 12 weeks, and obstructions on angiogram were resolved at 4 to 12 weeks. In 4 dogs, slightly high PAP fell to the normal range at 4 weeks, and angiographic abnormalities were considerably reduced at 4 to 12 weeks. In 5 dogs, PAP returned to normal range immediately after worm removal, and angiographic changes almost disappeared at 4 to 8 weeks. On biopsy immediately after worm removal, samples of the main pulmonary arteries showed severe intimal proliferations with villous or papillary protrusion into the lumen. Autopsy at 12 to 20 weeks indicated that the intimal protrusions were remarkably reduced as compared with the biopsy samples in all cases. However, villous intimal protrusions were seen in the caudal lobar arteries in cases with remaining alive worms. New vessels seemed to develop into thromboemboli with time. From these findings, it is clear that the pulmonary arterial lesions improved after heartworm removal, and the clinical signs disappeared following the improvement in hemodynamics. Aspirin therapy (5 mg/kg/day) for 4 weeks after worm removal in 5 dogs did not improve the intimal lesions as compared to 3 control dogs.

Clinical studies on canine dirofilarial hemoglobinuria: Measured and calculated serum osmolalities and osmolar gap.

Serum osmolalities and osmolar gap were determined in 43 normal healthy beagles (control group) and 40 dogs with dirofilarial hemoglobinuria (hemoglobinuria group). In the control group, the measured and calculated serum osmolality levels were in the means of 296 +/- 5 (SD) mOsm/kg and 293 +/- 6 mOsm/kg respectively, showing an osmolar gap less than 10 mOsm/kg. In the hemoglobinuria group, the measured serum osmolality ranged from 272 to 370 mOsm/kg. A considerable number of dogs had normal serum osmolalities in spite of severe intravascular hemolysis, suggesting that the changes in serum osmolality would not be the direct cause of intravascular hemolysis. The measured serum osmolality (331 +/- 28 mOsm/kg) was significantly higher in 11 dogs which died after a surgical removal heartworms than in 29 dogs which recovered after the removal (302 +/- 17 mOsm/kg). The calculated serum osmolality level was 296 +/- 16 mOsm/kg in 24 recovered cases, and 304 +/- 22 mOsm/kg in 10 fatal cases. The osmolar gap stayed in the normal ranges of 5.4 +/- 5.9 mOsm/kg in recovered cases, but it attained a higher level of 22.7 +/- 8.9 mOsm/kg in fatal cases, suggesting poor prognosis in cases with large osmolar gaps. There were significant positive correlations between the measured serum osmolality and osmolar gap, serum sodium, potassium, BUN, GOT, GPT, creatinine, bilirubin and plasma hemoglobin values, as well as between the osmolar gap and serum potassium, BUN, GOT, GPT, creatinine and bilirubin values. The plasma hemoglobin concentration fell markedly without significant change in serum osmolality 20 hr after the heartworm removal.

Efficacy of heartworm removal in dogs with dirofilarial hemoglobinuria using flexible alligator forceps.

Heartworms were removed from the right atrium and the pulmonary arteries through the jugular vein using a flexible alligator forceps in dogs with dirofilarial hemoglobinuria (caval syndrome). In 23 outpatient dogs (without autopsy), the heartworms in the right atrium and the tricuspid valve orifice were removed completely. Moreover, 1 to 36 worms were removed from the pulmonary artefy in 16 of 23 dogs (69.9%). In 9 experimental dogs with autopsy, 8 to 34 worms were removed from the right atrium, and 1 to 21 worms were removed from the pulmonary artery in all dogs. Zero to 11 worms remained in the pulmonary arteries, and mean removal efficacy was 89.3% in 9 dogs. Cardiopulmonary values were measured before and 24 hr after heartworm removal in 9 experimental dogs. Right cardiac output, cardiac index and stroke volume tended to increase in 5 dogs which recovered after heartworm removal. These parameters tended to decrease in 3 of 4 dogs with poor prognosis. Pressures in the pulmonary artery and the right ventricle ranged variously from normal value to extremely higher level (>100 mmHg) before heartworm removal. The pressures showed varying changes after heartworm removal without correlation to the prognosis. The heartworm removal with a flexible alligator forceps was safer and more available than that with a hard forceps as therapy for canine dirofilarial hemoglobinuria, because the worms in the right atrium and the tricuspid valve orifice could be removed completely, and the worms in the pulmonary artery were also removed with high efficacy and no harm.

Clinical effects after heartworm removal from pulmonary arteries using flexible alligator forceps in dogs with common dirofilariasis.

Changes in clinical features after heatworm removal flom the pulmonary arteries using flexible alligator forceps were examined in 36 dogs with common dirofilariasis. No dogs died owing to the removal manipulations. The removal efficiency was 90% in 18 dogs autopsied. In the mild cases (23 dogs), the signs such as coughing, anemia and so on were relieved or disappeared rapidly after removal. Serious cases were divided into ascites (9 dogs) and hemoptysis (4 dogs) cases. Their prominent signs before removal were less activity, anorexia, dyspnea and anemia in almost all cases, and subcutaneous edema, hydrothorax, icterus and hypothermia were seen in some ascites cases. The general condition improved considerably and the main symptoms were relieved or disappeared within 4 weeks after removal in most cases. The post-removal progress was good in all cases with hemoptysis and in 7 of 9 cases with ascites. However, 2 cases with ascites died of severe heart valvular disease or renal failure 3.5 or 4 months after removal. Anemia, leukocytosis and hypoalbuminemia were alleviated after removal in some mild and serious cases on laboratory tests. LDH and CK activities, which showed high levels before removal, decreased within 1 or 4 weeks after. These findings might suggest that injuries of the heart, lung and liver healed after the heartworm removal. However, the cases with insufficient compensation for severe lesions could not recover completely. These results showed that the heartworm removal using flexible alligator forceps was safe and excellent as a radical therapy for heartworm disease and could be recommended to apply for even serious cases.

Changes in cardiopulmonary values after heartworm removal from pulmonary artery using flexible alligator forceps.

Radiograph, arteriograph, echocardiogram, electrocardiogram and cardiopulmonary values were obtained in dogs with dirofilariasis before and after heartworm removal with a flexible alligator forceps. After heartworm removal, the following results were obtained: 1) Dilations of the pulmonary artery, the right ventricle and the right atrium reduced on radiograph and ultrasonic echocardiogram; 2) tortuousness of the pulmonary artery was reduced, and pruning of the peripheral arteries improved on arteriogram: 3) electrocardiographic findings indicated the correction of right axis deviation in mean electric axis in frontal plane and decreases of voltages; 4) pulmonary arterial and right ventricular pressures fell (improvement of pulmonary hypertension); 5) right cardiac output declreased; 6) heart rate tended to decrease; and 7) total pulmonary arterial resistance decreased. These results indicated that pulmonary arterial resistance and blood flow volume might be reduced, thus decreasing the burden on the heart. It was considered that not only lesions of the pulmonary arteries but also heartworms themselves in the pulmonary artery play an important role in affecting right heart hemodynamics.

Clinical studies on canine dirofilarial hemoglobinuria: relationship between the presence of heartworm mass at the tricuspid valve orifice and plasma hemoglobin concentration.

A heartworm mass was confirmed by echocardiography at the tricuspid valve orifice of dogs with dirofilarial hemoglobinuria (caval syndrome). It disappeared by surgical heartworm removal, and the symptoms of "caval syndrome" also improved. The plasma hemoglobin concentration, which was very high before heartworm removal, decreased 30 min after heartworm removal. It fell progressively to almost the normal level 20 hr after heartworm removal. In 5 dogs developing the caval syndrome after milbemycin D administration, the presence of heartworms at the tricuspid valve orifice and the increase of plasma hemoglobin concentration were observed to occur simultaneously. These findings suggest that the heartworm mass at the tricuspid valve orifice may be a direct cause of the onset of this disease, and these heartworms may trigger the increased intravascular hemolysis.

Clinical studies on dirofilarial hemoglobinuria: Central venous pressure before and after heartworm removal.

Central venous pressure (CVP) was measured before and immediately after surgical heartworm removal from the jugular vein in 22 dogs with dirofilarial hemoglobinuria (caval syndrome). In 19 cases which recovered by sugical removal, CVP was considerably high from 32 mmH2O to 187 mmH2O with a mean of 101.6±35.1(S.D.)mmH2O before heartworm removal. CVP fell in all cases immediately after heartworm removal. The mean CVP after heartworm removal was 61.0±42.9 mmH2O. This level was significantly lower than that before heartworm removal (p<0.001). After heartworm removal, systolic cardiac murmur and jugular pulse improved and hemoglobinemia and hemoglobinuria disappeared. Two of 3 cases, which died after heartworm removal, indicated a high CVP over 200 mmH2O and showed the signs of severe circulatory failure (right heart failure). They also displays terminal signs such as prostration and low body temperature. After heartworm removval, systolic murmur improved passably, but high CVP levels over 175 mmH2Oremained in both cases. Another case did not indicate a high CVP level (66 mmH2O) before heartworm removal. Forty-seven heartworms were removed from this case. However, there was no recovery of the systolic murmur, and CVP fell only 5 mmH2O. In this case, the knotting of a heartworm around the tricuspid chordae was confirmed by autopsy. It was considered that the existence of heartworm mass at the tricuspid valve orifice would be the cause of the high CVP level in this disease. And it was suggested that the tricuspid insufficiency by heartworm mass at the tricuspid valve orifice would be the direct cause of acute circulatory insufficiency that indicates the onset of dirofilarial hemoglobinuria together with many symptoms.