Open Access

Acute haemoabdomen associated with Angiostrongylus vasoruminfection in a dog: a case report

Irish Veterinary JournalThe official journal of Veterinary Ireland, the representative body for the veterinary profession in Ireland200861:591

DOI: 10.1186/2046-0481-61-9-591

Published: 1 September 2008

Abstract

A one-year-old intact female, Danish shorthaired pointer was referred to the emergency service with a history of acute collapse and pale mucous membranes after a month of reduced activity but with no other clinical signs. An ultrasound examination of the abdomen indicated the presence of a large amount of free fluid with no obvious cause such as neoplasia or splenic rupture. Fluid analysis had the macroscopic appearance of blood with no signs of infection or neoplasia. Multiple Angiostrongylus vasorum L1 larvae were revealed on a direct rectal faecal smear. The dog was treated with fenbendazole 25 mg/kg orally once daily for 20 days and given supportive treatment. The dog was stabilised on this treatment. Haemoabdomen is a clinical sign where surgical intervention is often considered an integral part of the diagnostic investigation (i.e., laparotomy) or treatment. Failing to make the diagnosis of canine angiostrongylosis before performing surgery may have a serious adverse affect on the outcome. Consequently, in areas where A. vasorum is enzootic, a Baermann test and a direct faecal smear should be included in the initial diagnostic investigation of all dogs presenting with bleeding disorders of unknown origin.

Keywords

Angiostrongylus vasorum coagulopathy haemoabdomen treatment
Angiostrongylus vasorum (French heartworm) is a nematode causing verminous pneumonia in dogs. Dogs and other Canidae such as foxes serve as definitive hosts, while snails and slugs act as intermediate hosts. It has a worldwide distribution and in Europe it is considered enzootic in certain areas in France, Denmark, Ireland and the UK [24, 9]. The adult metastrongyle (13-21 mm) resides in the pulmonary arteries and the right side of the heart [13]. First-stage (L1) larvae migrate through the respiratory system via the trachea to the gastrointestinal-tract and are excreted in faeces [1]. The migration of the L1 larvae through the blood-air barrier and the subsequent verminous pneumonia and pulmonary thrombosis causes the clinical signs (i.e., cough, exercise intolerance, dyspnoea) that are commonly associated with the pulmonary system [10, 3, 4]. Haematological changes such as neutrophilia, thrombocytopaenia and anaemia have been reported [4] whereas the most frequent changes in biochemistry are increased globulin levels and decreased fructosamine [4, 18]. A fatal outcome of infection is often associated with coagulation disorders. Suggested echanisms behind the coagulopathy are induced immune-mediated thrombocytopaenia, disseminated intravascular coagulation (DIC) or secretion of anticoagulants by the adult worms [14, 12, 8, 6, 16]. Clinical presentation of associated bleeding disorders may vary between petechial or ecchymotic bleeding on mucosal surfaces, dermis or sclera to intracranial or CNS bleeding [5, 3, 4, 7, 15]. To the authors' knowledge, this is the first reported case of haemoabdomen associated with an A. vasorum infection. A one-year-old intact female Danish shorthaired pointer (body weight 25 kg) was referred to the emergency service at the Department of Small Animal Clinical Sciences at the University of Coprnhagen with a history of acute collapse and pale mucous membranes. The owner had noted the dog to be less active over the past month, but with no other clinical signs more commonly related to canine angiostrongylosis such as cough, dyspnoea or exercise intolerance. The dog presented with a temperature of 37.1°C, pulse 120/min, respiration rate of 28/min and pale pink, dry mucous membranes with a prolonged capillary refill time greater than two seconds. A single petechia was present on the gingival mucosa. The most predominant changes in haematological and biochemical profiles were neutrophilia, packed cell volume (PCV) of 24%, elevated urea and creatinine and reduced fructosamine (Table 1).
Table 1

Haematological, biochemical and coagulation parameters at time of diagnosis

Haematological parameters

(Reference range)

Measurement

Changes

Packed cell volume (PCV)

0.39-0.55 L/L

0.24

Total red blood cells (RBC)

4.6-8.4 × 10 9/L

3.4

Platelets

200-500 × 10 9/L

90*

 

Total white blood cells (WBC)

6.5-18.1 × 10 9/L

26.8

Segmented neutrophils

3.2-12.1 × 10 9/L

22.0

Lymphocytes

1.0-4.8 × 10 9/L

3.1

 

Monocytes

0.0-1.2 × 10 9/L

1.6

Eosinophils

0.0-1.2 × 10 9/L

0.02

 

Biochemical parameters

   

Alanine aminotransferase (ALAT)

6-120 U/L

124

Alkaline phosphatiase (BASP)

19.8-174 U/L

109

 

Glucose

3.9-6.55 mmol/L

9.24

Urea

3.3-9.4 mmol/L

17.3

Creatinine

44-130 mmol/L

179.2

Amylase

186-798 U/L

1706

Lipase

6-498 U/L

217.4

 

Cholesterol

3.5-6.99 mmol/L

2.5

Bilirubin

1.0-5.0 μμmol/L

4.0

 

Albumin

26.0-44-0 g/L

26.8

 

Protein

57.0-82.0 g/L

53.1

Fructosamine

235-344 μμmol/L

212

Bile acid

1-6.4 μμmol/L

1

 

Calcium

2.2-3.3 mmol/L

3.2

 

Magnesium

0.63-1.05 mmol/L

0.94

 

Phosphate

0.91-1.96 mmol/L

2.47

Potassium

3.81-5.07 mmol/L

3.8

Sodium

142.2-153.6 mmol/L

141.9

Coagulation parameters

   

Fibrinogen

(1.0-4.0 g/L) pool 0.64

0.05

 

Prothrombin time (PT)

(pool 8.2 sec)

19.2

Activated prothrombin time (APPt)

(pool 18.5 sec)

15.0

 

D-dimer

(0.0-0.5 mg/L) pool 0.1

3.2

* aggregates seen on blood smear at 40× magnification.

An ultrasound examination of the abdomen (Figure 1) suggested a large amount of free fluid with no obvious cause such as neoplasia or splenic rupture. Abdominocentesis was performed and the aspirate had the macroscopic appearance of blood, a PCV of 35% and no signs of infection or neoplasia on a cytological examination. The coagulation profile showed prolonged Prothrombin time (PT) and increased D-dimer (Table 1). Phytomenadion (Konakion, Roche A/S, Hvidovre, Denmark) treatment was initiated due to potential coumarin poisoning and for initial stabilisation, the dog received two transfusions; one unit of full blood (18 ml/kg) and one unit of fresh frozen plasma (9 ml/kg). A PCV of 24% is not usually a clear indication for a blood transfusion. However, in the present case, the authors chose to carry out the procedure as a continuing loss of blood could not be ruled out at this stage. Urinalysis of a voided sample was unremarkable except that a single A. vasorum L1 larva was detected on microscopy. Subsequently, multiple L1 larvae were revealed using a direct faecal smear technique [17]. Due to the rapid establishment of the diagnosis, a buccal mucosal bleeding test was not performed. The dog was treated with fenbendazole 25 mg/kg orally once daily for 20 days following a protocol known to be efficient in the treatment of A. vasorum infections [19]. To avoid possible anaphylactic reactions, prednisolone acetate at 1 mg/kg (Prednisolon DAK, Nycomed, Roskilde, Denmark) was administered once daily for 12 days. The dog stabilised on this treatment and was discharged after two days of hospitalisation and monitoring. Four weeks later, a complete resolution of clinical signs and normalisation of haematological and coagulation blood parameters were found. Haemoabdomen associated with canine angiostrongylosis has not been reported before, although spontaneous bleeding at other sites has been reported. In the present case, no history of either surgical or accidental trauma existed. Neoplasia could not be demonstrated and treatment with phytomenadion was initially started in case of a rodenticide poisoning, although the owner reported it unlikely that the dog had been in contact with such compounds. Coumarin poisoning is not usually associated with neutrophilia and decreased fructosamine, as in this case, but could account for the prolonged PT. Prolonged PT is also often reported in dogs infected with A. vasorum [12, 6]. Increased D-dimer indicates formation of thrombi, but is non-specific regarding the underlying cause. Prolonged PT and elevated D-dimer could be indicative of disseminated intravascular coagulation (DIC) as is often reported in cases of canine angiostrongylosis [12, 7]. Immune-mediated thrombocytopaenia has been reported in association with A. vasorum infection [8]. However, with a platelet count of 90 × 109/L and aggregates present on the blood smear, it was considered unlikely to have caused the bleeding, since bleeding caused by low platelet number usually occurs only with platelet count below 40 × 109/L. The acute onset of clinical signs might also have been caused by a ruptured small vessel. Aberrant migration of adult worms probably occurs frequently [11] and rupture of the femoral artery has been reported previously in a case report of an experimentally infected dog [5]. Finally, the possible role of the parasites secreting an anticoagulant may contribute to the development of bleeding problems [6] This mechanism, however, needs to be further investigated. The finding of L1 larvae in the urinalysis may be explained by ectopic L1 larvae [11] or faecal contamination of the voided urine sample. However, due to the presumed hypocoagulable state of the dog, sampling by cystocentesis was not performed.
Figure 1

Abdominal ultrasound of a dog diagnosed with A. vasorum. A large amount of free intraabdominal fluid was observed. PCV was 35% in a sample obtained by abdominocentesis. No signs of neoplasia or infection were observed.

Haemoabdomen is a clinical sign where surgical intervention is often considered an integral part of the diagnostic investigation (i.e., laparotomy) or treatment. Failing to make the diagnosis of canine angiostrongylosis before performing surgery may have an adverse affect on the outcome for the patient. In conclusion, in areas where A. vasorum is enzootic, a Baermann test and a direct faecal smear should be included in the initial diagnostic investigation of all dogs presenting with bleeding disorders of unknown origin.

Declarations

Acknowledgements

Dr. James Miles is thanked for the English review of this paper.

Authors’ Affiliations

(1)
Department of Small Animal Clinical Sciences, Faculty of Life Sciences, University of Copenhagen

References

  1. Bolt G, Monrad J, Koch J, Jensen AL: Canine Angiostrongylosis - A Review. Veterinary Record. 1994, 135: 447-452. 10.1136/vr.135.19.447.View ArticlePubMedGoogle Scholar
  2. Bourdeau P: Canine Angiostrongylus-Vasorum Infestation. Recueil de Medecine Veterinaire. 1993, 169: 401-407.Google Scholar
  3. Brennan SF, McCarthy G, McAllister H, Bassett H, Jones BR: Clinical signs, diagnosis and treatment of three dogs with angiostrongylosis in Ireland. Irish Veterinary Journal. 2004, 57: 103-109. 10.1186/2046-0481-57-2-103.PubMed CentralView ArticlePubMedGoogle Scholar
  4. Chapman PS, Boag AK, Guitian J, Boswood A: Angiostrongylus vasorum infection in 23 dogs (1999-2002). Journal of Small Animal Pracice. 2004, 45: 435-440. 10.1111/j.1748-5827.2004.tb00261.x.View ArticleGoogle Scholar
  5. Cury MC, Lima WS: Rupture of femoral artery in a dog infected with Angiostrongylus vasorum. Veterinary Parasitology. 1996, 65: 313-315. 10.1016/S0304-4017(96)00991-0.View ArticlePubMedGoogle Scholar
  6. Cury MC, Lima WS, Guimaraes MP, Carvalho MG: Hematological and coagulation profiles in dogs experimentally infected with Angiostrongylus vasorum (Baillet, 1866). Veterinary Parasitology. 2002, 104: 139-149. 10.1016/S0304-4017(01)00616-1.View ArticlePubMedGoogle Scholar
  7. Garosi LS, Platt SR, McConnell JF, Wrayt JD, Smith KC: Intracranial haemorrhage associated with Angiostrongylus vasorum infection in three dogs. Journal of Small Animal Practice. 2005, 46: 93-99. 10.1111/j.1748-5827.2005.tb00300.x.View ArticlePubMedGoogle Scholar
  8. Gould SM, McInnes EL: Immune-mediated thrombocytopaenia associated with Angiostrongylus vasorum infection in a dog. Journal of Small Animal Practice. 1999, 40: 227-232. 10.1111/j.1748-5827.1999.tb03068.x.View ArticlePubMedGoogle Scholar
  9. Koch J, Willesen JL: Canine pulmonary angiostrongylosis - an update. The Veterinary Journal "In previous". 2008Google Scholar
  10. Martin MWS, Ashton G, Simpson VR, Neal C: Angiostrongylosis in Cornwall - Clinical Presentations of Eight Cases. Journal of Small Animal Practice. 1993, 34: 20-25. 10.1111/j.1748-5827.1993.tb02570.x.View ArticleGoogle Scholar
  11. Oliveira-Junior SD, Barcante JMP, Barcante TA, Ribeiro VM, Lima WS: Ectopic location of adult worms and first-stage larvae of Angiostrongylus vasorum in an infected dog. Veterinary Parasitology. 2004, 121: 293-296. 10.1016/j.vetpar.2004.02.018.View ArticlePubMedGoogle Scholar
  12. Ramsey IK, Littlewood JD, Dunn JK, Herrtage ME: Role of chronic disseminated intravascular coagulation in a case of canine angiostrongylosis. Veterinary Record. 1996, 138: 360-363. 10.1136/vr.138.15.360.View ArticlePubMedGoogle Scholar
  13. Rosen L, Ash LR, Wallace GD: Life history of canine lungworm Angiostrongylus vasorum (Baillet). American Journal of Veterinary Research. 1970, 31: 131-141.PubMedGoogle Scholar
  14. Schelling CG, Greene CE, Prestwood AK, Tsang VCW: Coagulation abnormalities associated with acute Angiostrongylus vasorum infection in dogs. American Journal of Veterinary Research. 1986, 47: 2669-2673.PubMedGoogle Scholar
  15. Wessmann A, Lu D, Lamb CR, Smyth B, Mantis P, Chandler K, Boag A, Cherubini GB, Cappello R: Brain and spinal cord haemorrhages associated with Angiostrongylus vasorum infection in four dogs. The Veterinary Record. 2006, 158: 858-863. 10.1136/vr.158.25.858.View ArticlePubMedGoogle Scholar
  16. Whitley NT, Corzo-Menendez N, Carmichael NG, McGarry JW: Cerebral and conjunctival haemorrhages associated with von Willebrand factor deficiency and canine angiostrongylosis. Journal of Small Animal Practice. 2005, 46: 75-78. 10.1111/j.1748-5827.2005.tb00296.x.View ArticlePubMedGoogle Scholar
  17. Willesen J, Møller J, Koch J, Jensen AL, Kristensen AT: Tidlig diagnostik af Angiostrongylus vasorum (Fransk hjerteorm) og Crenosoma vulpis (Rævens lungeorm) hos hunde er mulig ved hjælp af modificeret Baermann test. Dansk Veterinær Tidsskrift. 2004, 87: 6-10. (English summary: Early diagnosis of Angiostrongylus vasorum (French Heartworm) and Crenosoma vulpis (Fox lungworm) is possible by means of modified Baermann Test)Google Scholar
  18. Willesen JL, Jensen AL, Kristensen AT, Kjelgaard-Hansen M, Jessen R, Koch J: Serum fructosamine concentrations in 59 dogs naturally infected with Angiostrongylus vasorum. Journal of Veterinary Medicine Series A. 2006, 53: 266-269. 10.1111/j.1439-0442.2006.00828.x.View ArticlePubMedGoogle Scholar
  19. Willesen JL, Kristensen AT, Jensen AL, Heine J, Koch J: Efficacy and safety of imidacloprid/moxidectin spot-on solution and fenbendazole in the treatment of dogs naturally infected with Angiostrongylus vasorum (Baillet, 1866). Veterinary Parasitology. 2007, 147: 258-264. 10.1016/j.vetpar.2007.05.001.View ArticlePubMedGoogle Scholar

Copyright

© The Author(s) 2008

Advertisement