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Hindlimb Lameness Secondary to Bilateral Femoral Artery Occlusion in a Dog with Systemic Arterial Dirofilariasis
Woo-shin Choi, Jin-young Song, Young-jae Lee, Dong-hoon Lee, Ju-hyung Kim, Jin-hwa Chang, Ji-Houn Kang and Dong-woo Chang1
College of Veterinary Medicine, Chungbuk National University, Cheongju, Chungbuk 361-763, Korea (Accepted: August 16, 2012)
Abstract : A 3-year-old, intact male Pungsan dog was presented for a 2-week history of a non-weight-bearing lameness of left hindlimb with anorexia. The dog had no history of trauma, and never been routinely vaccinated or treated with heartworm preventatives. The complete blood count showed severe leukocytosis and neutrophilia with left shift.
Serum biochemistry showed hypoalbuminemia, azotemia, and increased hepatobilliary enzyme activity. A canine heartworm antigen test was positive. Thoracic radiographs were consistent with heartworm disease as evidences by main pulmonary artery enlargement, right-sided cardiomegaly, and interstitial lung pattern. Echocardiography revealed pulmonary valvular regurgitation and pulmonary hypertension. Selective femoral arterial angiogram was performed, and bilateral femoral arterial occlusion was identified. The dog died after angiogram, and necropsy was performed.
At necropsy, adult heartworm and a large blood clot were found within the lumen of left and right femoral artery.
This case report describes an unusual migration of heartworm to femoral artery that caused hindlimb lameness.
Key words : Dog, femoral artery, systemic arterial dirofilariasis.
Introduction
The heartworm is an infectious disease widespread through- out the world. In general, heartworm usually located caudal lobar arteries, main pulmonary artery, and right ventricle.
Adult heartworms also have been documented in the cranial and caudal vena cava and right atrium in the case of caval syndrome (9). Systemic arterial dirofilariasis is an unusual manifestation that occurs as a result of an aberrant migration or development of adult heartworms within the systemic arte- rial circulation (7). Several reports suggested aberrant migra- tion of heartworm such as brain, spinal cord, epidural space, anterior chamber, vitreous, peritoneal cavity, subcutis, and femoral artery (6-8,13,15). This report describes a case pre- sented for acute hindlimb lameness resulting from bilateral femoral arterial occlusion by Dirofilaria immitis.
Case
A 3-year-old, intact male Pungsan dog weighing 18 kg was presented to the Veterinary Medical Center, Chungbuk National University for a 2-week history of a non-weight-bearing lameness of left hindlimb, and progressive anorexia. The dog was housed outside, and never been routinely vaccinated or treated with heartworm prevention. The dog had no history
of trauma. At the time of admission, the dog exhibited a non- weight bearing lameness and moderately decreased muscle tone of the left hindlimb, and had necrotic wound on the left tarsal joint region (Fig 1). Pain was evident during palpation and hyperflexion of the left tarsal joint.
Abnormalities on physical examination included pyrexia (40.5oC), severe dehydration (8~10%), lethargy, and cool ex- tremities on the left tarsal joint region. On neurologic exami- nation, cranial nerves, conscious proprioception, and spinal
1Corresponding author.
E-mail: [email protected] Fig 1. Ischemic necrosis of left tarsal region.
reflexes (e.g., withdrawl, patella, perineal, cutanenous trunci) were normal. The complete blood count (CBC) abnormali- ties included severe leukocytosis, neutrophilia with left shift, mild monocytosis, decreased hematocrit, and hemoglobin.
Serum biochemistry abnormalities included decreased albu- min, and marked increased alanine aminotransferase (ALT), aspartate aminotransferase (AST), alkaline phosphatase (ALP), gamma(γ)-glutamyl transferase (GGT), blood urea nitrogen (BUN), and creatinine (Table 1). Urinalysis, which included dipstick and sediment analyses, revealed hematuria (3+), pro- teinuria (100 mg/dL), a pH of 6.5, struvite, and a urine spe- cific gravity of 1.025. A canine heartworm antigen test was positive. Radiographic examination was performed of thorax, abdomen, and both pelvic limbs. Abdominal radiographs showed decreased serosal detail due to emaciation, and radio- graphs of pelvic limb showed decreased muscle mass of left thigh muscle (Fig 2). Thoracic radiographs showed right-sided cardiomegaly, severe dilation of main pulmonary artery, tor-
tuous and markedly dilated of the cranial and caudal pulmo- nary arteries, and diffuse interstitial lung pattern (Fig 3). On echocardiographic examination, right atrial enlargement and main pulmonary arterial dilation were confirmed, but no heart- worm was visualized in the pulmonary artery and right ventri- cle (Fig 4). In addition, Doppler echocardiography revealed that pulmonary regurgitation (2.7 m/s) and pulmonary hyper- tension (49.2 mmHg). At that time, the presumptive diagno- Table 1. Blood profiles in this patient
Parameter Result Reference range Unit
WBC 56.4 6-17 103/µL
Segmented
neutrophils 52.5 3-11.8 103/µL
Monocytes 2.26 0.2-2 103/µL
PCV 29.9 37-55 %
Hemoglobin 10.1 12-18 g/dL
Albumin 1.9 2.6-3.3 g/dL
ALT 722 21-102 U/L
AST 310 23-66 U/L
ALP 1462 29-97 U/L
GGT 12 1.2-6.4 U/L
BUN 41.4 7-25 mg/dL
Creatinine 2.6 0.5-1.5 mg/dL
Abbreviations: WBC, white blood cell; PCV, packed cell volume;
ALT, alanine aminotransferase; AST, aspartate aminotransferase;
ALP, alkaline phosphatase; GGT, gamma(γ)-glutamyl transferase;
BUN, blood urea nitrogen.
Fig 3. Right lateral (A) and ventrodorsal (B) thoracic radiographs of this dog. Thoracic radiographs show right-sided cardiomegaly and severe dilation of main pulmonary artery. The cranial and caudal pulmonary arteries are tortuous and markedly dilated. Dif- fuse interstitial lung pattern is evident.
Fig 2. Right lateral abdominal radiograph (A) and ventrodorsal pelvic radiograph (B) of this dog. Abdominal radiograph shows decreased serosal detail due to emaciation, and pelvic radiograph presents atrophy of left thigh muscle.
Fig 4. Right parasternal long axis four chamber view (A) and right parasternal short axis five chamber echocardiographic view (B) of this dog. Echocardiography shows dilation of right ventricle, atrium, and main pulmonary artery. There are no visible heartworms in the right ventricle, atrium, and main pulmonary artery.
sis was caval syndrome with vascular thromboembolism due to severe heartworm infection. Angiography was considered necessary to confirm vascular thromboembolism, and deter- mine if the right femoral artery was patent. At angiogram, a catheter was directed into the aorta via the left carotid artery.
With an injection of contrast medium (300 mgI/ml, iohexol), caudal abdominal aorta was seen, and the entire courses of the internal and external arteries were seen. The right femoral artery could be visualized only to the level of middle aspect of right femoral artery, but the remaining course of artery was not visualized. Numerous collateral arterioles were visu- alized around the right femoral artery. In contrast, the left external iliac artery could be visualized only to the level of the deep femoral artery, and the remaining course of artery was not visualized. Linear radiolucent filling defects represent- ing adult heartworm was seen in the medial aspect of right
femoral artery, and in the end of left external iliac artery (Fig 5). Femoral arteriotomy was considered but the dog died for acute cardiac arrest after angiography, and necropsy was per- formed. At necropsy, adult heartworms and large blood clot were found within the lumen of left and right femoral artery (Fig 6). Additionally small adult heartworms were seen in right ventricle, lung parenchyma, small intestinal lumen, renal parenchyma, and peripheral arteries (Fig 7).
Fig 6. Resected right (A, B) and left (C) femoral artery during necropsy. Adult heartworms and large blood clots are found within the lumens of left and right femoral artery.
Fig 5. Right lateral (A) and left lateral (B) radiographic views of femur taken post-angiogram. The right femoral artery could be visualized only to the level of right femoral artery, and collateral arterioles are visualized around the femoral artery. The left exter- nal iliac artery could be visualized only to the level of the deep femoral artery, and the remaining course of artery is not visual- ized. Linear radiolucent filling defects representing adult heart- worm are seen in the medial aspect of right femoral artery (white arrow), and in the end of left external iliac artery (white arrow- head).
Fig 7. Resected kidney (A) and small intestine (B) during necropsy. Many adult heartworms found in sub-capsular region of kidney, and small intestinal lumen.
Discussion
Adult heartworms are found most commonly in the right ventricle, main pulmonary artery, and peripheral pulmonary arteries of affected dog. Although heartworms in the dog typ- ically inhabit the pulmonary arteries of the caudal lung lobes, and rarely they may be found in the right atrium, cranial, and caudal vena cava in case of caval syndrome (1,2,4-7). Much less frequently, immature five-stage larvae may aberrantly migrate to other sites, including the brain, spinal cord, epidu- ral space, anterior chamber of the eye, the vitreous, the sub- cutis, and the peritoneal cavity (1-10,12,16,17). In addition, the heartworms may inhabit the systemic circulation, produc- ing systemic thromboembolic disease (7). In this case, the dog first exhibited a non-weight bearing lameness of left hindlimb, and had necrotic wound on the left tarsal joint region. Thoracic radiographs suggested heartworm infection, and it confirmed with heartworm kit. Considering the result of blood panel analysis and urinalysis, presumptive diagno- sis was caval syndrome with vascular thromboembolism. At that time, we considered transvenous extraction of adult heart- worms, however there were no visible heartworms during echocardiographic examination despite severe infection of heartworms. Therefore, selective angiogram was performed to confirm femoral arterial occlusion by thrombus. At angio- gram and necropsy, adult heartworms and large thrombi were found in right and left femoral arteries. Femoral arterial occlusion secondary to systemic dirofilariasis and thrombo- sis were the cause of lameness in this case. Adult heart- worms in the peripheral arterial system are unusual, although they have been reported in the cerebral arteries, abdominal aorta, iliac, femoral, popliteal, renal, and testicular arteries (6-8,13,15). The common clinical signs were hindlimb lame- ness and pedal parasthesia (2,7). All of cases, heartworms aberrantly migrated to femoral artery, and resulted in occlu- sion of femoral artery. These were consistent with this case report. The presence of living or dead adult worms within a vessel lumen causes mechanical irritation resulting in the inflammatory and proliferative changes. Villous intimal pro- liferation, endarteritis, and granulomatous reactions often are seen histologically. These pathologic changes lead to throm- bosis and vascular obstruction, and result in pain and lame- ness (2,8,15).
The cause of systemic dirofilariasis is unknown and devel- opment of heartworms in the arterial circulation is still contro- versial (2,6,7). Adult heartworms lack mechanical structures for penetration of, and migration through, vessel walls and most likely arrive in aberrant locations as a result of migra- tion of third- and fourth-stage larvae (3). In previous reports with systemic arterial dirofilariasis, cardiovascular shunts are a possible cause of aberrant location of adult heartworm. How- ever, most dogs with adult heartworms in the systemic arterial system did not have any cardiovascular shunts (8,13,16). In this case, there were no cardiovascular shunts during necropsy.
In addition, some report suggested that pulmonary hyperten-
sion could have caused a pressure differential allowing the worms to migrate the systemic circulation (7). The interesting point of this case is that there were no visible heartworms in the right ventricle, atrium, and main pulmonary artery. It is assumed that presence of pulmonary hypertension, and ele- vated right ventricular, and atrial pressure result in aberrant migration of heartworms to systemic circulation. In a dog with caval syndrome, heartworms were found in the abdominal aorta, renal, iliac, femoral artery on ultrasonographic exami- nation (6).
In this case, the dog exhibited lameness of left hindlimb with ischemic necrosis despite bilateral occlusion of femoral artery. Although the exact reason was unclear, it is assumed that collateral circulation in response to occlusion of right femoral artery was more developed than left femoral artery.
So, it seemed that collateral circulation of right femoral artery prevent ischemic damage to some extent (11,14).
In this dog, hindlimb lameness with necrosis was initially suspected due to thromboembolism with caval syndrome, but were likely attributable to a combination of femoral arterial occlusion by adult heartworms and thrombus. Therefore, dogs with clinical signs of lameness, ischemic wound, poor peripheral perfusion in heartworm-endemic area, it should be considered possibility of systemic arterial dirofilariasis.
Conclusion
This case report described the rare case of hindlimb lame- ness caused by bilateral femoral artery occlusion secondary to systemic arterial dirofilariasis. Systemic arterial dirofilariasis is not common manifestation of heartworm infection, but it should be considered that the possibility of systemic arterial dirofilariasis when diagnosis of dogs with clinical signs such as lameness and thromboembolic ischemia is made in heart- worm-endemic areas.
Acknowledgment
This work was supported by a research grant of Chungbuk National University in 2011.
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전신성 동맥 사상충증에 이환된 개의 양측성 대퇴동맥의 폐쇄
최우신·송진영·이영재·이동훈·김주형·장진화·강지훈·장동우1
충북대학교 수의과대학
요 약 : 3세 수컷 풍산견이 2주동안 지속된 좌측후지 파행과 식욕저하로 내원하였다. 환자의 외상 병력은 없었으며, 백신과 심장사상충 예방은 하지 않았다. 전혈구검사에서 중증의 백혈구 증가증과 호중구 핵좌방이동이 확인되었고, 혈 액화학검사에서 저알부민혈증, 질소혈증, 간담도계 효소수치의 상승을 확인되었으며, 심장사상충 항원 키트에서 양성으 로 확인되었다. 흉부 방사선 검사에서는 주폐동맥의 확장, 우심비대, 폐의 간질패턴이 관찰되었으며, 심장사상충 감염 소견과 일치하였다. 이후 실시된 심초음파 검사에서 페동맥판역류와 폐성 고혈압이 확인되었다. 선택적 대퇴동맥 혈관 조영술에서 양측성 대퇴동맥의 폐쇄가 확인되었고, 환자는 혈관조영술후 폐사하였고 부검이 실시되었다. 부검결과 심 장사상충 성충과 혈전이 좌우측 대퇴동맥 내강을 폐쇄시키고 있는 것이 확인되었다. 본 증례보고는 심장사상충이 대 퇴동맥으로 비정상적 이주를 하여 후지의 파행을 유발한 케이스이며, 이를 보고하고자 한다.
주요어 : 개, 대퇴동맥, 전신성 동맥 사상충증
