Babesia canis infection in a splenectomized dog.
Transcription
Babesia canis infection in a splenectomized dog.
Babesia canis infection in a splenectomized dog. A.T. Camacho (1), E. Pallas (2), J. J. Gestal (3), F. J. Guitián (1) & A. S. Olmeda (4) (1) Laboratorio Lema & Bandín.Calle Lepanto, 5,bajo. 36201. Vigo. Spain. Tel:00 34 986 43 74 00; Fax:00 34-986 43 11 45.E-mail: [email protected] (2) Servicio de Otorrinolaringología.Hospital Xeral-Cíes. C./ Pizarro. 36203. Vigo. Spain. (3) Departamento de Medicina Preventiva y Salud Pública.Hospital Clínico Universitario. A Choupana.15706.Santiago de Compostela.Spain. (4) Departamento de Patología Animal I. Facultad de Veterinaria.Universidad Complutense. Avda.Puerta de Hierro s/n.28040.Madrid.Spain. Manuscrit n°2306. “Parasitologie”. Reçu le 9 avril 2001. Accepté le 12 décembre 2001. Résumé : Infection à Babesia canis chez un chien splénectomisé. La babésiose canine est une protozoose infectieuse due à la prolifération dans les hématies du chien d´un Babesidé spécifique (Babesia canis) transmis par les morsures de tiques. Ce travail décrit le cas d´un fox-terrier de trois ans qui a vécu un cas de “babésiose non-expérimentale”. Neuf mois après avoir subi une ablation de la rate (splénectomie), le chien arrivait chez le vétérinaire avec des symptômes comme: hyperthermie, frissons et urine foncée (hémoglobinurie). Les consta tions les plus importantes furent une intense parasitémie qui incluait des groupes de près de 16 Babesiae et une activité érythrophagique. On observait également une leucocytose marquée, une trombocytopénie et une anémie régénérative. Malgré la rapidité avec laquelle lui a été administré le traitement spécifique avec imidocard dipropionate, les symptômes se sont aggravés, faisant appa raître un disfonctionnement rénal qui entraîna la mort de l´animal. La parasitémie et l’évolution aiguë de la maladie étaient associées au fait d´avoir subi l´ablation de la rate, étant donné que la splénectomie a été reconnue comme le facteur qui entraîne plus de risques pour le développement d´une grave maladie due à une infection par Babesia. maladie parasitologique du chien infection naturelle Babesia canis splénectomie parasitémie hôpital Vigo Espagne Europe méridionale Summary: The present report describes a fatal case of non-experimental babesiosis in a splenectomized 3-yearold fox terrier. A very intense parasitaemia including clusters of up to 16 Babesiae and a prominent haemophagocytic activity were the most relevant findings. A marked leukocytosis, thrombocytope nia and regenerative anaemia were observed. Despite prompt treatment with babesiacidal com pounds the condition progressed to acute renal failure and resulted in the death of the animal 48 hours after the onset of symptoms. Introduction B abesiosis is a zoonosis caused by tick-borne hematozoan parasites of the genus Babesia, which is found worldwide. Two out of the 73 identified Babesia species are known to cause natural infection in dogs: Babesia canis and Babesia gibsoni. Of the two, Babesia canis is considered to be the most important specie affecting dogs. It has a relatively large size (2.4 µm x 5.0 µm), piriform shape and can appear in red blood cells singly or in groups of 2, 4 or even more (10). The pathogenicity of the parasite is highly determined by the species involved and the immunological response of the host. Among other immunological mechanisms, infected erythrocytes incorporate Babesia antigens into their membranes inducing antibodies that opsonize the red cells leading to their removal by the mononuclear-phagocytic system (12). The spleen is the largest lymphoid organ in the body. In the adult animal it stores red blood cells that can be squeezed back into circulation, it produces lymphocytes, and removes antigenic particles and aged erythrocytes. In human patients, splenectomy has been identified as a major risk factor for the Bull Soc Pathol Exot, 2001, 94, 1, 17-19 dog-parasitical disease natural infection Babesia canis splenectomy parasitaemia Vigo Spain Southern Europe development of serious illness due to natural Babesia infection (8, 12). The objective of the present study is to report a fatal case of non-experimental babesiosis in a splenectomized 3 year old fox-terrier, with prominent haemophagocytic activity and intense parasitaemia. Materials and methods I n October 1997, a 3 year old male fox-terrier dog was admitted to a veterinary hospital presenting hyperthermia (40ºC), trembling and dark urine. The dog had been splenectomized in January 1997 due to traumatic rupture of the spleen and had lived since then in a rural area of Galicia, NW Spain. Physical examination revealed pale mucous membranes, tachycardia, tachypnoea, splenomegaly, lymphadenopathy and the presence of ticks. Blood samples were obtained by puncture in the cephalic vein two weeks after splenectomy in order to check the postoperatory evolution of the animal as well as 9 months later, during the acute febrile syndrome. Babesia canis was observed in 17 A.T. Camacho,E. Pallas, J. J. Gestal et al. giemsa-stained blood smears from the second sample. Haematological count and different serum biochemistry tests were carried out by a STKS-2 VCS automatic counter (Coulter) and a clinical chemistry analyser CL-7200 (Shimadzu). Serum protein electrophoresis was conducted by a DVS 480 photodensitometer (Sevia). The dog was hospitalised and treated with imidocarb d i p ro pionate (4 mg/kg [1.8 mg/lb], SC) and tetracycline (60 mg/kg/12 hours [27 mg/lb/12 hours], PO). Despite treatment with conventional babesiacidals the dog died 48 hours after the onset of symptoms. Results and discussion B ased on the visual observation of the parasite in giemsastained blood smears, a diagnosis of babesiosis by Babe sia canis was made for the acute febrile syndrome the dog presented in October 1997, 9 months after being splenectomized. The main characteristics of the syndrome were an intense parasitaemia and regenerative anaemia, thrombocytopenia, a marked leukocytosis (the white blood cell count (WBC) was so high that it was necessary to make a one-infive dilution in order to obtain a valid measure) and evolution towards renal failure. Results of the haematological count confirmed the clinical impression of a marked anaemia (Table 1). The anaemia appeared to have clear regenerative characteristics as reticulocyte count and presence of nucleated red cells demonstrated. The high values obtained for the red cell distribution width (RDW) support this finding, since anisocytosis seems to reflect the presence of two erythrocytic populations: a microcytic one represented by erythrocytes and a macrocytic one corresponding to reticulocytes. Behaviour of the levels of LDH is in agreement with the intense haemolytic anaemia. Thrombocytosis, a common finding in splenectomized patients, was also observed in this dog after splenectomy (7). However, during the acute febrile syndrome an important thrombocytopenia was observed (Table 1). The presence of giant platelets was visually detected in blood smears and is consistent with the regenerative character of the anaemia and the thrombocytopenia. The observed leukocytosis was not described in other previously published reports on canine babesiosis and in fact leukopenia had been frequently reported by other authors (1, 5). In this case, as suggested by the peripheral blood smear and by the cytogram (Figure 1), the apparent marked leukocytosis could be an artefact due to the high number of nucleated red cells, since automatic counters can erroneously count them as leukocytes (9). Figure 1. Coulter STKS-2 cytogram report from a splenectomized dog during an acute episode of babesiosis by Babesia canis. Nucleated red cells cause a spurious increase of the WBC. Rapport de cytogramme Coulter STLS-2 d’un chien après splénectomie au cours d’un épisode aigu de babésiose par Babesia canis. Les cellules rouges nucléées mènent à une apparente augmentation des globules blancs. Table I. Results of haematological and serum biochemistry analysis of a male fox-terrier two weeks after been splenectomized and 9 months later during an acute episode of babesiosis by Babesia canis (1997). Résultats de l’analyse biochimique hématologique et sérologique d’un fox-terrier male deux semaines après une splénectomie et 9 mois plus tard, au cours d’un épisode aigu de babésiose dû à Babesia canis. parameter (normal reference range and units) leukocyte count (6.0-17.0 x 103 cells/ml) neutrophils (60.0-77.0%) lymphocytes (12.0-30.0%) monocytes (3.0-10.0%) eosinophils (2.0-10.0%) basophils (0-1.0%) red blood cell count (5.5-8.5 x 10 6 cells/ml) reticulocytes (0.5-1.5%) haemoglobin (12.0-18.0 gr/dl) Hct (37.0-55.0%) red cell distribution width (< 19%) platelet count (120-500 x 10 3 cells/ml) glucose (77-120 mg/dl) urea (14-53 mg/dl) creatinine (0.5-1.4 mg/dl) aspartate aminotransferase (16-43 mUI/ml) alanine aminotransferase (15-58 mUI/ml) γ- glutamyltransferase (1-5 mUI/ml) alkaline phosphatase (10-73 mUI/ml) total bilirubin (0.1-0.3 mg/dl) creatin kinase (40-254 UI/l) lactate dehydrogenase (65-149 mUI/ml) total proteins (5.5-7.5 g/dl) albumin (2.3-3.4 g/dl) α1-globulin (0.20-0.50 g/dl) α2-globulin (0.30-1.10 g/dl) β-globulin (0.10-2.70 g/dl) γ-globulin (0.50-1.20 g/dl) * Two weeks after splenectomy. ° During acute phase of babesiosis by Babesia canis. Parasitologie 1st sample* 2nd sample° 23.3 120 69.5 74.8 20.4 18.1 8.0 6.6 1.9 0.4 0.2 0.1 4.1 1.8 1.9 4.3 9.4 5.2 29.5 16.0 15.6 18.0 647 31 55 49 32 325 1.0 4.5 25 71 35 85 4 7 125 369 0.9 1.7 150 512 149 692 5.8 4.9 2.9 1.9 0.30 0.28 0.51 0.54 1.10 0.97 0.99 1.21 WBC : leukocytes ; N : neutrophils ; L : lymphocytes ; M : monocytes ; E : eosinophils ; B : basophils Examination of giemsa-stained peripheral blood smears showed a very intense parasitaemia with clusters of up to 16 Babesia (Figure 2). Other findings were a high number of reticulocytes and nucleated red cells, an important presence of Howell-Jolly bodies in the erythrocytes, an intense haemophagocytic activity and the presence of atypical lymphocytes and vacuolated macrophages. The high number of Babesia present in circulating red blood cells is very likely a reflection of the splenectomy, on the other hand, erytrophagocytosis could be related to the activation of the macrophage-monocyte system as a consequence of the disease, a previously reported finding by other authors (11). Differential white cell count clearly showed a tendency towards neutrophilia and eosinopenia which is very likely a result of a stress-induced corticosteroid discharge provoked by babesiosis. The role of babesiosis as a risk factor for renal failure had been previously suggested (4). In the case we present, signs of an acute renal failure were observed, with urea and creatinine levels highly elevated (Table 1). Serum protein electrophoresis showed a decrease of albumin and total protein as normally associated to renal failure (Table 1). 18 Babesia canis infection in a splenectomized dog Figure 2. Giemsa-stained peripheral blood smear from a splenectomyzed dog during acute babesiosis by Babesia canis (x100). Goutte de sang périphérique colorée au Giemsa d’un chien après spénectomie au cours d’un épisode aigu de babésiose par Babesia canis (x100). such as the prophylactic administration of babesiacidal compounds or vaccination for splenectomized dogs living in endemic areas. Références bibliographiques 1. 2. 3. 4. Both hepatic and neuromuscular affectations have been reported in babesiosis (2, 6, 13). In this case, elevation of serum AST and ALT values was very discrete and could be, in our opinion, mainly associated not with direct hepatic damage but with neuromuscular affectation. This would be consistent with the high values of creatin kinase (CK) and the observed trembling of the animal during the acute phase. Caution should be taken when interpreting serum bilirubin levels. The apparent contradiction among the marked haemolytic anaemia and the very discretely elevated serum bilirubin levels could be explained by the interference among the Jendrassik method for bilirubin measurement and the presence of haemoglobin in the serum, which produces false results by defect (3). 5. 6. 7. 8. 9. 10. 11. Conclusions O ur report overlaps with others in human medicine literature by indicating the severity of naturally-occurring Babesiosis in splenectomized patients. Babesia canis infection in splenectomized dogs should be considered as a medical emergency. The often fatal nature of the condition in these animals could justify the adoption of preventive measures, Bull Soc Pathol Exot, 2001, 94, 1, 17-19 12. 13. ABDULLAHI SU, MOHAMMED AA, TRIMNELL AR et al. - Clinical and haematological findings in 70 naturally occurring cases of canine babesiosis. J Small Anim Pract, 1990, 31 , 145-147. BOURDEAU P - La Babésiose canine. Rec Méd Vét, 1993, 169 , 439-450. CARAWAY WT & KAMMEYER CW - Chemical interference by drugs and other substances with clinical laboratory test procedures. Clin Chim Acta, 1972, 41 , 395. HARAPIN I, RAMADAN P, BEDNICA L, TADIC M & ALEGRE A - Clinical picture and the blood urea nitrogen (BUN) and creatinine content in the blood serum of piroplasmosis affected dogs. Veterinarski-Archiv, 1993, 63 , 11-17. PAGES JP & TROUILLET JL - Thrombocytopénie dans la babesiose du chien. A propos de 153 observations. Prat Méd Chir Anim Comp, 1984, 19 , 222-227. PAGES JP, VIDOR E, TROUILLET JL, BISSUEL G, LECOINTRE O & MOREAU Y - Description clinique, hématologique et sérologique de 133 cas de babésiose canine. Prat Méd Chir Anim Comp, 1990, 25 , 89-97. PEARSON HA, JOHNSTON D, SMITH KA & TOULOUKIAN RJ - The born-again spleen. Return of splenic function after splenectomy for trauma. N Engl J Med, 1978, 298 , 1389-1392. ROSNER F, ZARRABI MH, BENACH JL & HABICHT GS - Babesiosis in splenectomized adults: review of 22 reported cases. Am J Med, 1984, 76 , 696-701. SCHOENTAG RA - Hematology analyzers. Clinics in Laboratory Medicine, 1988, 8, 653-673. TABOADA J - Babesiosis. In: GREENE CE (Ed), Infectious diseases of the dog and cat. W.B. Saunders, Philadelphia, 1998, pp. 473481. TABOADA J & MERCHANT SR - Babesiosis of companion animals and man. Vet Clin North Am: Small Anim Pract, 1991, 21 , 103123. TIZARD IR - Veterinary Immunology. W.B. Saunders, Philadelphia, 1996, pp. 315-329. WOZNIA EJ, BARR BC, THOMFORD JW et al.- Clinical, anatomic and immunopathologic characterisation of Babesia gibsoni infection in the domestic dog (Canis familiaris). J Parasitol, 1997, 83 , 628-629. 19