Veterinary Parasitology 107 (2002) 235250

Canine spirocercosis: clinical, diagnostic, pathologic, and epidemiologic characteristics

Michal Mazaki-Tovi a , Gad Baneth a, , Itamar Aroch a , Shimon Harrus a , Philip H. Kass b , Tomer Ben-Ari a , Gila Zur a , Izhak Aizenberg a , Hylton Bark a , Eran Lavy a
a

School of Veterinary Medicine, Hebrew University of Jerusalem, P.O. Box 12, Rehovot 76100, Israel b School of Veterinary Medicine, University of California, Davis, CA, USA Received 30 November 2001; received in revised form 4 April 2002; accepted 11 April 2002

Abstract The nematode Spirocerca lupi is a parasite of dogs with beetles of several species serving as intermediate hosts. The medical records of 50 dogs diagnosed with spirocercosis at the Hebrew University Veterinary Teaching Hospital (HUVTH) in Israel during 19911999 were retrospectively reviewed and compared to a control group (n = 100). There was a seven-fold increase in the annual number of dogs diagnosed with spirocercosis during these years while the hospital caseload increased by 80%, indicating an emerging outbreak of this infection. Dogs from the greater Tel Aviv area were at the highest risk of being diagnosed with spirocercosis with 74% of the cases originating from this region compared to only 17% of the controls. The disease appeared to have a primarily urban pattern of distribution with a signicantly higher percentage (P = 0.025) of dogs from cities versus rural areas, as compared to the control group. Sixty-two percent of the cases were diagnosed during the colder months of December through April. The median age of infected dogs was 5 years, with dogs 1 year old or younger at the lowest risk of being diagnosed with spirocercosis. Large breeds were at a higher risk of infection in comparison to small breeds and the Labrador Retriever was signicantly over represented (P = 0.027) in the study group compared to the control population. The most common signs were vomiting or regurgitation (60%), pyrexia (24%), weakness (22%), respiratory abnormalities (20%), anorexia (18%), melena (18%) and paraparesis (14%). A caudal esophageal mass was identied by radiography in 53% of the dogs and spondylitis of the thoracic vertebrae in 33%. Fecal otation was positive for S. lupi eggs in 80% of the dogs, and endoscopy was found to be the most sensitive diagnostic procedure and allowed diagnosis in 100% of the examined dogs. Fifty-three percent of the dogs were anemic and creatine kinase (CK) activities were elevated in 54%. Necropsy of 14 dogs revealed esophageal or gastric granulomas in 13 dogs, and an esophageal osteosarcoma in a single animal. Aortic aneurysms were found in six (43%) dogs. Out of 24, 15 dogs (63%) for which follow-up information was available died or
Corresponding author. Tel.: +972-3-9688557; fax: +972-3-9604079. E-mail address: baneth@agri.huji.ac.il (G. Baneth).

0304-4017/02/$ see front matter 2002 Elsevier Science B.V. All rights reserved. PII: S 0 3 0 4 - 4 0 1 7 ( 0 2 ) 0 0 1 1 8 - 8

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were euthanized within 1 month of admission. The case-fatality rate decreased toward the end of the study period when improved therapy with avermectins became available. 2002 Elsevier Science B.V. All rights reserved.
Keywords: Spirocerca lupi; Spirocercosis; Dog; Israel

1. Introduction The nematode Spirocerca lupi is primarily a parasite of dogs, although other animals, particularly carnivores may be affected. It has a worldwide distribution, but is most prevalent in warm climate (Bailey, 1972). The adult S. lupi is found in a nodular mass in the wall of the hosts thoracic esophagus. The female lays embryonated eggs that are transferred through a tract in the nodule and excreted in the hosts feces. Eggs are ingested by the intermediate host, corprophagus beetles, and develop to infective (L3) stage within 2 months. Carnivores are infected by ingestion of a beetle or a variety of parathenic hosts including: birds, hedgehogs, lizards, mice, and rabbits. In the carnivore host, the infective larvae penetrate the gastric mucosa, and migrate within the walls of the gastric arteries to the thoracic aorta. About 3 months post-infection, the larvae leave the aorta and migrate to the esophagus where they provoke the development of granulomas as they mature to adults over the next 3 months (Bailey, 1972; Soulsby, 1986; Fox et al., 1988; Urquhart et al., 1996). The lesions caused by S. lupi are mainly due to the migration and persistent presence of larvae and adults in the tissues. Esophageal nodular masses and granulomas, and aortic scars and aneurysms are the most frequent lesions. Spondylitis and spondylosis of the caudal thoracic vertebrae are additional typical lesions (Soulsby, 1986; Fox et al., 1988; Urquhart et al., 1996). Neoplastic transformation of the granulomas to brosarcoma or osteosarcoma has been reported in dogs with spirocercosis sometimes with the development of hypertrophic osteopathy (Bailey, 1972; Grant et al., 1979; Johnson, 1992). Less frequently, lesions may occur due to the aberrant migration of the worms. S. lupi worms and nodules have been reported in almost every thoracic organ (Fischer and Carneiro, 1974; Garg et al., 1989; Harrus et al., 1996), the gastrointestinal tract (Babero et al., 1965; Georgi et al., 1990; Brodey et al., 1977), the urinary system (Turk, 1960, Thanikachalam et al., 1984), and the subcutaneuos tissues (Chandrasekharon et al., 1958; Turk, 1960; Harrus et al., 1996). The clinical signs reported in canine spirocercosis depend on the location and severity of the lesions. Esophageal lesions are associated with persistent vomiting and/or regurgitation followed by weakness and emaciation (Bailey, 1972; Chhabra, 1973; Fox et al., 1988). Sudden death may be caused by rupture of an aortic aneurysm induced by migration of worms in the aortic wall (Ndiritu, 1976; Ivoghli, 1977). A denite diagnosis of spirocercosis is made by detection of characteristic eggs by fecal otation (Soulsby, 1986; Markovics and Medinski, 1996). Survey thoracic radiographs of affected dogs show esophageal granulomas as areas of increased density in the caudodorsal mediastinum and contrast esophograms may outline granulomas. Spondylitis of the caudal thoracic vertebrae occasionally may be seen on radiorgraphs (Fox et al., 1988). Esophagoscopy and gastroscopy allow direct visualization of the nodules, which appear as broad-based protuberances with a distinctly nipple-like orice.

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Several anti-helminthics have been suggested for the treatment of canine spirocercosis. These include: diethylcarbamazine, disophenol, levamizole, albedazole, ivermectin and doramectin (Seneviranta et al., 1966; Fox et al., 1988; Berry, 2000). Surgical excision of esophageal granulomas and sarcomas is often not possible due to extensive or multiple lesions (Fox et al., 1988). Canine spirocercosis had been a rare diagnosis in Israel until 1988. In the period of 19801988 only two cases of spirocercosis, a fox from the Jerusalem area and a dog from Tel Aviv, were diagnosed. However during 1989, four dogs were diagnosed with spirocercosis on necropsy (Harmelin et al., 1991), and since then, the frequency of diagnosis of this infection has increased remarkably. A limited number of case studies on spirocercosis have been published describing the clinical presentation, diagnosis and management of S. lupi infection in the dog (Berry, 2000; Lobetti, 2000; Dvir et al., 2001). The emergence of an outbreak of spirocercosis and the lack of detailed large studies on this disease warranted an in-depth clinical and epidemiological investigation on this infection in Israel. The goals of this retrospective study were to describe the clinical, hematological, and biochemical ndings in 50 dogs diagnosed with spirocercosis at the Hebrew University Veterinary Teaching Hospital (HUVTH) in Israel during 19911999, and to document the emergence and spread of this disease in Israel, as expressed by the hospital medical records.

2. Materials and methods The medical records of all dogs diagnosed with spirocercosis at the HUVTH in Israel during 19911999 were retrospectively reviewed. The HUVTH is the only veterinary teaching hospital in Israel and it accepts referrals and emergency cases from the whole state. Criteria for inclusion in the study were the detection of S. lupi eggs by fecal examination, visualization of a typical granuloma by esophagoscopy, or ndings of typical lesions of spirocercosis at necropsy. Age, sex, breed, geographic location, month, and year of presentation, and clinical signs were recorded for all dogs. Findings of fecal examination, thoracic radiographs, complete blood count, biochemistry panel, endoscopy, and necropsy were additionally recorded. Fecal examination was performed by the sugar otation technique (Markovics and Medinski, 1996). Endoscopy was carried out under general anesthesia using an Olympus exible four-way directional tip (7.9 mm) endoscope. The dog admitted before and the dog admitted directly following a spirocercosis case were randomly selected as controls for comparison of the signalment (age, breed, sex) and the geographic distribution of the disease. In order to analyze the geographic distribution of the spirocercosis cases and the control dogs, the state of Israel was divided to seven regions representing different demographic areas. These regions included: the greater Tel Aviv area comprised of ve adjacent cities in central Israel, the city of Rishon Lezion where the HUVTH is located, Jerusalem, the eastern Sharon in the central coastal plain, the northern Sharon in the northern coastal plain, northern Israel and southern Israel. Differences in age groups, gender, breed (large versus small), and geographic location (urban versus rural) between the study and control groups were tested for signicance (P < 0.05) by the chi square ( 2 )-test. In addition, the seasonality and the differences in

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the disease incidence among the years during which the study was conducted were evaluated for signicance by the 2 -test. The effects of age and geographic region of residence on disease incidence were evaluated using exact conditional logistic regression analysis. 3. Results 3.1. Diagnosis Fifty dogs met the criteria of diagnosis with spirocercosis. The initial diagnosis was made by fecal otation in 32 dogs, at necropsy in 9, by endoscopy in 8 and by identication of an adult S. lupi worm in the vomitus in 1 dog. Five dogs had the following concurrent diseases: ehrlichiosis in two dogs, lymphosarcoma, lymphocytic thyroiditis, and intervertebral disc disease each in one dog. 3.2. Annual diagnosis of new cases The number of dogs diagnosed with spirocercosis at the HUVTH increased signicantly (P = 0.00093) from 2 in 1991 to 13 in 1999. While the number of canine spirocercosis cases increased by a seven-fold during the study period, the hospital annual case load grew only by 80% (Fig. 1). 3.3. Geographic distribution Dogs originating from the region of greater Tel Aviv were at the highest risk to be diagnosed with spirocercosis. Odds ratios for dogs originating from other geographic regions

Fig. 1. The annual incidence of spirocercosis compared to the annual case-load at the HUVTH during 19911999.

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Table 1 Odds ratios for the diagnosis of spirocercosis in dogs admitted to the HUVTH from different geographic regions in Israel Geographic region Number of dogs (%) Study Greater Tel Aviv Northern Sharon Eastern Sharon Northern Israel Southern Israel Rishon Lezion Greater Jerusalem
a b

ORa

CIb (95%)

P-value

Control 17 (17) 18 (18) 9 (9) 4 (4) 4 (4) 39 (39) 9 (9) 1.00 0.080 0.054 0.12 0.10 0.087 0.040 0.0130.32 0.00110.44 0.00231.32 0.00190.95 0.0270.25 to 0.27 <0.0001 0.0016 0.099 0.043 <0.0001 0.0003

37 (74) 3 (6) 1 (2) 1 (2) 1 (2) 7 (14) 0 (0)

Odds ratio. Condence interval.

compared to greater Tel Aviv are shown in Table 1. The geographic distribution of the dogs with spirocercosis and of the controls is shown in Fig. 2. The number of dogs with spirocercosis originating from an urban region (46 dogs, 92%) was signicantly (P = 0.025) higher than the number of dogs originating from rural regions

Fig. 2. The geographic distribution in Israel of the dogs diagnosed with spirocercosis (A) and the control group (B).

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Fig. 3. Monthly incidence of dogs diagnosed with spirocercosis during 19911999.

(4 dogs, 8%). In comparison, 76% of the dogs from control population were from an urban region and 24% from a rural one. 3.4. Seasonality The number of dogs diagnosed with spirocercosis at the HUVTH during the colder months of December through April (31 dogs, 62%) was signicantly (P = 0.045) higher compared to the number of dogs diagnosed during the warmer months of May through November (19 dogs, 38%). Fig. 3 shows the number of dogs diagnosed with spirocercosis during each month of the year. 3.5. Signalment The ages of the dogs with spirocercosis ranged from 8 months to 11 years with an average of 4.8 years and a median of 5 years. Dogs 1 year old or younger were at the lowest risk of being diagnosed with spirocercosis. Odds ratios and 95% condence interval (CI) for dogs in other age groups compared to dogs younger than 1 year are shown in Table 2. The percentage of dogs of mixed breeds was similar in the study (30%) and control (31%) groups. The number of large purebred dogs in the case group (30 dogs, 60%) was signicantly higher (P = 0.045) than in the control group (43 dogs, 43%). Conversely, the number of small purebred dogs was lower (5 dogs, 10%) in the case group than in the control group (26 dogs, 26%). No signicant differences were found between the actual breeds distribution among the study and control groups. However, when comparing the Labrador Retriever to all other breeds together, it was signicantly over represented (P = 0.027) in the study group (10

M. Mazaki-Tovi et al. / Veterinary Parasitology 107 (2002) 235250 Table 2 Odds ratios for the diagnosis of spirocercosis in dogs from different age groups Age group (year) Number of dogs (%) Study 1 15 510 >10
a b

241

ORa Control 33 (33) 28 (28) 27 (27) 12 (12) 1.00 6.8 4.4 3.9

CIb (95%)

P-value

4 (8) 25 (50) 15 (30) 6 (12) Odds ratio. Condence interval.

2.029.9 1.220.2 0.7722.3

0.0007 0.021 0.11

dogs, 20%), compared to the control population (7%). There was no signicant difference between the distribution of male (21 dogs, 42%) and female (29 dogs, 58%) dogs diagnosed with spirocercosis, compared to the control population in which the genders were divided equally. 3.6. Clinical signs The clinical signs recorded for the infected dogs are listed in Table 3. The ve most common signs were vomiting and/or regurgitation (60%), pyrexia (24%), weakness (22%), anorexia (18%), and melena (18%). Twenty dogs presented only one clinical sign. These consisted of vomiting and/or regurgitation in eight dogs, paraparesis and weakness each in four, dyspnea in one, and anorexia and diarrhea each in one dog. Two dogs (4%) had no
Table 3 Clinical signs in 50 dogs with spirocercosis Clinical signs Gastrointestinal Vomiting/regurgitation Melena Hypersalivation Diarrhea Respiratory Dyspnea Cough Neurologic and musculoskeletal Paraparesis Back pain Other Pyrexia Weakness Anorexia Weight loss None Number of dogs (n = 50) 33 30 9 4 4 10 6 5 9 7 2 26 12 11 9 5 2

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Fig. 4. A thoracic radiograph of a dog with spirocercosis showing a caudal esophageal mass (thick arrow) and spondylitis of the thoracic vertebrae (thin arrows).

obvious abnormalities on history and physical examination, and were diagnosed by positive fecal otations. 3.7. Thoracic radiography Thoracic radiography was performed for 45 infected dogs. The most common radiographic nding was a caudal esophageal mass (Fig. 4), which was observed in 24 dogs (53%). Nine dogs (20%) had a thoracic mass, which did not present in the typical position of the caudal esophagus. Fifteen dogs (33%) had evidence of spondylitis in the thoracic vertebrae (Fig. 4). Spondylitis was found together with a caudal esophageal mass only in eight dogs (18%). Esophageal dilatation was observed in ve dogs (11%) and pneumonia was observed in four dogs (9%). Other radiographic ndings included: pleural effusion in two dogs of which one had a pyothorax and the other a hemothorax, and aortic mineralization in one dog. No abnormalities were present in the thoracic radiographs of three dogs (7%), one of which was diagnosed by detection of S. lupi eggs on fecal otation, one by endoscopy, and one on necropsy. 3.8. Fecal examination Fecal otation was performed in 40 cases. Out of 40, 32 dogs (80%) had a positive fecal otation. S. lupi eggs (Figs. 5 and 6) were identied in 23 of the positive dogs (72%) upon the rst examination, and in 9 additional dogs (28%) in a second examination performed several days after a negative one. Of eight dogs with negative fecal otations, one had an esophageal osteosarcoma and in another one no esophageal or gastric granulomas were identied by endoscopy at the time of fecal analysis, but were later found in the esophagus on necropsy.

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Fig. 5. A S. lupi egg as it appears on fecal examination (400).

3.9. Endoscopy Endoscopy was performed in 17 dogs. Typical broad-based granulomas with a nipple-like orice (Fig. 7) were visualized in the distal esophagus of 14 (82%) dogs, and an adult worm was seen protruding from a granuloma in one case. Seven of these dogs had a single granuloma, and seven had multiple granulomas. An unusual esophageal mass diagnosed as osteosarcoma on necropsy was found in one dog, and a gastric mass diagnosed as a

Fig. 6. A S. lupi larva emerging from an egg on a direct fecal smear. This is an unusual event that normally takes place in the beetle vector.

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Fig. 7. An endoscopic image of an esophageal granuloma caused by S. lupi. Note the granuloma protruding into the esophageal lumen with a nipple-like orice.

granuloma by histopathology of an excisional biopsy was detected in another dog. Streaking in the distal esophageal mucosa with no esophageal or gastric granulomas or masses was observed in one case, in which multiple esophageal granulomas were found on necropsy 5 weeks later. 3.10. Hematology Complete blood counts were available for 47 dogs (Table 4). Red blood cells (RBC) counts were decreased in 25 dogs (53%). The anemia was normocytic in 22 dogs (88%) and microcytic in 3 dogs (12%). Only three dogs had severe anemia (RBC <3106 l1 ), two of which had concurrent ehrlichiosis. Fifteen dogs (32%) had leukocytosis. Differential counts were available for 22 dogs. Ten of these dogs (46%) had absolute monocytosis, and eight (36%) had absolute neutrophilia. Only four dogs (18%) had absolute eosinophilia. Platelet counts were available for 44 dogs of which 5 (11%) were throbocytopenic, 2 of which had concurrent ehrlichiosis. 3.11. Biochemistry Biochemistry panel results were available for 26 dogs (Table 4). While most biochemical parameters were within the reference ranges, serum creatine kinase (CK) activities were elevated in 14 dogs (54%). Eight of these dogs had CK activities above 250 U/l (reference range 13100). 3.12. Treatment Data concerning the treatment was available for 30 dogs in the last 3 years of the study. Nineteen dogs were treated by multiple subcutaneous injections of doramectin (Dectomax,

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Table 4 Median and range values of hematological and biochemical parameters and percent of dogs outside the reference range from 50 dogs with spirocercosis Parameter WBC (103 l1 ) Neutrophils (103 l1 ) Monocytes (103 l1 ) Lymphocytes (103 l1 ) Eosinophils (103 l1 ) RBC (106 l1 ) Hemoglobin (g/dl) Hematocrit (%) MCV () MCHC (g/dl) Platelets (103 l1 ) Total solids (g/l) Total protein (g/l) Albumin (g/l) ALP (U/l) ALT (U/l) AST (U/l) CK (U/l) Total calcium (mmol/l) Glucose (mmol/l) Bilirubin (mol/l) Median 13.0 9.3 1.2 1.5 0.3 5.9 14.1 41.7 67.0 33.5 252 72 70 32 88.5 26 30 125.5 2.39 5.4 5.3 Range 3.748.6 2.239.4 0.42.3 0.33.5 0.03.4 2.48.3 4.920.4 16.256.6 56.075.0 31.536.0 0758 40100 4092 643 21350 11308 12224 57600 1.832.96 4.16.7 0.518.2 Below range (%) 9 6 0 23 41 53 30 32 6 8 11 12 11 15 0 0 0 0 6 0 10 Above range (%) 32 36 46 0 18 0 13 0 0 0 9 33 32 11 27 19 8 54 22 0 5 Reference range 6.017.0 3.011.5 0.151.3 14.8 0.11.25 6.09.0 12.018.0 37.055.0 60.077.0 32.036.0 160500 6080 5575 2640 10140 850 950 13100 2.182.96 3.96.2 1.810.5 Number of dogs 47 22 22 22 22 47 47 47 47 12 44 42 28 27 26 32 26 26 27 12 22

WBC: white blood cells; RBC: red blood cells; MCV: mean corpuscular volume; MCHC: mean corpuscular hemoglobin concentration; ALP: alkaline phosphatase; ALT: alanine aminotransferase; AST: aspartate aminotrasferase; CK: creatine kinase.

Pzer), given every 24 weeks at 200400 g/kg. Eight dogs received multiple subcutaneous injections of ivermectin (Iveomc, Merial) every 2 weeks at the same doses as doramectin. 3.13. Necropsy ndings Necropsy was performed in 14 cases. One dog had a granuloma that was excised by surgery. Out of 13 remaining dogs, 11 (85%) had esophageal granulomas, 1 had an esophageal osteosarcoma, and 1 had a gastric granuloma. Aortic aneurysms were found in six (43%) dogs, and spondylitis of thoracic vertebra in four (29%). Three dogs had additional pathologies directly related to spirocercosis: one had meningitis of the thoracic spine, one had thoracic hematoma, and one had pancreatitis with S. lupi larvae identied in the pancreas. 3.14. Outcome and prognosis of infected dogs Follow-up data was available for 24 dogs. Fifteen dogs (63%) died or were euthanized within 1 month of admission. One of the dogs that were euthanized had an osteosarcoma associated with spirocercosis, and another dog died of surgical complications after the

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excision of a gastric granuloma. The case-fatality rate during the rst month after diagnosis was higher (12/13; 92%) for the rst half of the dogs included in the study, and lower (3/11; 27%) for the dogs diagnosed during the later years of the study.

4. Discussion The increase in the number of dogs diagnosed with spirocercosis at the HUVTH during the course of this study suggests that an outbreak of this disease has occurred in Israel. Spirocercosis was rst reported in Israel in 1934 (Witenberg, 1934), but it had been a rare clinical and pathologic diagnosis until 1988. The esophageal lesions caused by adult S. lupi are prominent and it is unlikely that a large number of infected dogs would have been overlooked at necropsies performed prior to 1988. In addition, although the veterinarians awareness of spirocercosis might have increased in the recent years of the study, this alone could probably not account for the signicant increase of the rate of diagnosis of the disease during these years. Dogs from Tel Aviv and four adjacent cities in central Israel were found to be at a higher risk for spirocercosis than all other regions. This indicates a higher prevalence of the disease in this area compared to other municipalities. Therefore, it appears that spirocercosis was mainly conned to a limited region in the period during which the study was conducted. Similarly, the prevalence of Spirocerca infection varies appreciably within endemic areas in the south of the United States (Bailey, 1972). Spirocercosis appears to be mainly an urban disease in Israel, in contrast to observations from South Africa and Kenya, where the prevalence of the disease was higher in rural areas and among stray dogs (Fitzsimmons, 1960; Brodey et al., 1977; Evans, 1983). It appears that the most important factors inuencing the prevalence of spirocercosis is the proximity of the dogs to the intermediate and transport hosts (Lobetti, 2000), and the density of such infected hosts which are preyed upon in the environment. The rate of detection of spirocercosis in Israel was signicantly higher in the colder months, December through April. This might be explained by the seasonality of the beetle Onthophagus sellatus, which is the main intermediate host of S. lupi in Israel. The numbers and infection rates of O. sellatus with S. lupi in Israel were found to be highest during the months of September and October (Markovics, unpublished data). Therefore, most of the dogs are probably infected during the warmer months when the vector beetles are abundant and carry large numbers of larvae. The clinical signs of the disease are manifested during the colder months approximately 6 months later, when the adult worms reach the esophagus. Fewer dogs are presented with clinical signs in the warmer months, and these are probably chronic cases, that have carried the infection for several months before presentation. A questionnaire survey conducted in South Africa indicated a tendency towards a summer seasonal incidence (Lobetti, 2000). Different climate conditions might affect the seasonality of the intermediate hosts, and therefore, the seasonality of the disease. The incidence of spirocercosis was signicantly higher among large purebred dogs compared to smaller breeds. This is in agreement with ndings from South Africa, where in one study, 85% of 39 dogs were of large breeds (Dvir et al., 2001). Most likely, dogs of large breeds are more prone to be infected by S. lupi because they spend more time outdoors

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compared to dogs of small breeds. The Labrador Retriever, in particularly, was suggested to be at higher risk for spirocercosis in this study. This might be accounted for by the relatively ravenous and non-selective appetite of this breed. In addition, dogs younger than 1 year were found to be at the lowest risk for the disease. This is explained by the long life cycle of the worm and the possibility of a long stage of subclinical infection prior to the appearance of clinical disease. The most common clinical signs of spirocercosis in the present study were vomiting and/or regurgitation. This is in agreement with previous observations (Bailey, 1972; Chhabra, 1973; Fox et al., 1988; Lobetti, 2000; Dvir et al., 2001). Nevertheless, 34% of the dogs in this study had respiratory, neuromuscular, or other disturbances with no gastrointestinal signs. Therefore, spirocercosis should not be ruled out in the absence of gastrointestinal signs. Melena was a relatively common nding in the present study, and its appearance in combination with vomiting and/or regurgitation should be suggestive of spirocercosis in endemic areas. The other common clinical ndings of pyrexia, weakness, and anorexia are non-specic and, therefore, will be less helpful in the diagnosis of spirocercosis. Although, paraparesis was a less common nding in the study, it was the only clinical sign reported in four out of seven infected dogs in which it appeared. Paraparesis is associated with the spondylitic lesions found in infected dogs (Bailey, 1972; Chhabra, 1973; Fox et al., 1988), and also with meninigeal inammation found in one of the dogs in this study. Paraplegia due to myelomalacia of the thoracic spinal cord is reportedly caused by the presence of an immature female S. lupi (Tudury et al., 1995). Weight loss and respiratory signs appeared in 10 and 20% of the dogs in this study, respectively, compared to 77 and 41% in a previous study (Dvir et al., 2001) that included more chronic cases. This might explain the higher percentage of dogs showing these complications at the time of presentation in the earlier study. Eighty percent of the dogs in the present study with clinical signs of the respiratory system did not have radiographic or pathologic evidence of pulmonary or pleural lesions. It is possible that the cough and dyspnea were a result of direct airway compression by the granuloma. Cranially located thoracic masses might be associated with an increased tendency for regurgitation resulting in aspiration pneumonia, and with an abnormal opening into the pleural cavity or the trachea, resulting in pleuritis, pyothorax, and pneumonia. This concept is supported by the nding that four of nine dogs (44%) with atypical thoracic masses in the present study had radiographic evidence of pneumonia or pleural effusion, compared to 1 out of 24 dogs (4%) with caudal esophageal masses. Thoracic radiography has been considered an important diagnostic tool for spirocercosis. In this study, thoracic masses were the most common radiographic ndings, and yet, they were not detectable in 31% of the radiographs. Masses were atypically located outside of the caudal esophagus in 29% of the cases in which they appeared. Spondylitis was observed only in one third of the dogs and it was reported together with a caudal esophageal mass only in 18% of the cases. Although thoracic radiography was found to be less sensitive and specic in the diagnosis of spirocercosis, compared to endoscopy, it allowed detection of possible complications of the disease such as pneumonia, pleural effusion, and aortic mineralization and is, therefore, recommended in the diagnostic process for spirocercosis. Endoscopy emerged as the most sensitive tool for the diagnosis of spirocercosis, as abnormalities associated with the infection were found in 100% of the endoscopies performed

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in this study. Esophagoscopy often allows differentiation between typical granulomas to tumors. However, the endoscopic ndings may be variable. In dogs with advanced granulomas, the endoscopic appearance may mimic a neoplasm and endoscopic biopsies of esophageal masses may not allow differentiation between a tumor and a granuloma (Berry, 2000; Dvir et al., 2001). Dogs without apparent granulomas may present with other ndings related to spirocercosis during esophagoscopy. In this study, streaking of the esophageal mucosa with no protruding granuloma was detected at the time of endoscopy in one dog. On necropsy, which was performed 5 weeks later, multiple esophageal granulomas were found, and most of them were not protruding into the lumen of the esophagus. The lines observed in the esophageal mucosa were probably evidence of worm migration tracts (Evans, 1983) and should not be overlooked. Repetition of an inconclusive endoscopy in several weeks may be benecial in some cases. Moreover, some dogs with spirocercosis may have gastric granulomas and no esophageal abnormalities by endoscopy. In this study, one dog had a gastric granuloma and a normal esophagus. Gastric granulomas were found in necropsies in 5% of the dogs with spirocercosis in Iraq (Babero et al., 1965), and in 3% in Kenya (Brodey et al., 1977). Therefore, gastroscopy should follow esophagoscopy, particularly in the absence of esophageal lesions. Identication of S. lupi eggs in the feces allows a denite diagnosis of spirocercosis, but fecal examination has been considered an unreliable procedure for the diagnosis of this disease (Evans, 1983; Fox et al., 1988). A study on dogs with spirocercosis conrmed by necropsy and/or endoscopy in South Africa described the identication of S. lupi eggs in only 1 out of 30 dogs which had fecal otations (Dvir et al., 2001). However, in the present study, fecal otations were positive in 80% of the infected dogs and proven to be a sensitive diagnostic tool. The results of the fecal analysis may be affected by several factors. First, the passage of eggs in the feces occurs for an unpredictable, relatively short period of the adult female worm life span (Fox et al., 1988). Second, eggs will be found in the feces only when the adult female worm has a patent passage to the gastrointestinal tract. This does not happen in the earlier stages of the infection, in cases of aberrant migration of worms, or when a neoplasia has developed. Third, the laboratory techniques used for fecal analysis in order to identify S. lupi eggs are problematic due to the small size of the eggs (Markovics and Medinski, 1996). The higher sensitivity of fecal examinations in the present study as compared to the ndings of Dvir et al. (2001) is probably due to larger number of dogs with esophageal neoplasia, the lack of repetition of the fecal examination in the former study, and the use of different fecal otation techniques in the two studies. Although a negative fecal otation should never rule out a diagnosis of spirocercosis, the authors consider this procedure an invaluable tool for conrmation of the diagnosis and recommend using the sugar otation technique (Markovics and Medinski, 1996) and repeating the analysis when a negative result is obtained in a suspected dog. The most common hematologic abnormality in this study was anemia. The anemia was mild to moderate and normocytic in most cases, and therefore, probably caused by inammation. In a few cases, the anemia was microcytic or associated with the appearance of melena, and attributed to chronic blood loss from an ulcerated granuloma, as described previously (Grant et al., 1979). Monocytosis, neutrophilia, and leukocytosis were common ndings in the study whereas eosinophilia was relatively rare. All the dogs in this study had granulomas at the time of presentation, and these hematologic ndings probably reect the

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pyogranulomatous process caused by the presence of the adult worms within the granulomas. In addition, no correlation between the white blood cells counts and the existence of other inammatory conditions such as pneumonia or spondylitis was apparent in this study. Therefore, it seems that the leukocytosis appears in response to the granuloma itself. Spirocercosis does not seem to cause overt biochemical abnormalities except for an increased CK activity, which may be a result of direct muscular damage by the migrating larvae and adult worms or indirect injury induced by inammatory mediators. In this study, of 11 dogs that were treated with avermectins on which follow-up data was available, three died or were euthanized, four lived for over 1 year and four lived at least 1 month and were then lost to follow-up. Additional clinical studies are required to evaluate the efcacy of these medications in the treatment of spirocercosis. The prognosis for dogs with spirocercosis appeared to improve during the later years of the study. The increased awareness of the disease in the later years, probably allowed earlier diagnosis and treatment. The increased usage of ivermectin and doramectin against spirocercosis by practitioners most likely contributed considerably to the increased survival of the dogs in the later years of the study. Doramectin has been found to be effective in the treatment of spirocercosis (Berry, 2000). Canine spirocercosis has emerged in central Israel during 1991 through 1999. In order to reduce the incidence of canine spirocercosis in endemic regions, it is advisable to remove dog feces from public places, control the beetles population, and prevent dogs from ingesting beetles and possible parathenic hosts. Periodic fecal examinations and anti-helminthic preventative treatment with avermectins are also recommended in endemic regions in order to detect subclinical dogs and eliminate the infection before the development of complications and neoplasia.

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