24 minute read
Serological survey of leptospiral antibodies in clinically unwell dogs in New Zealand
StuDy RePORt
keARA BROWNlIe BVSc,
Companion Animal Veterinary Advisor, Zoetis
Aim
to investigate the prevalence of immunoglobulin m (Igm) positive antibody response to leptospirosis in clinically unwell dogs in New Zealand
Introduction
Leptospirosis is a spirochaete bacterial disease which affects all mammals worldwide. It is also considered one of the most common zoonotic diseases to affect humans globally with potentially fatal consequences (Levett 2001). Infected and carrier animals, including dogs, will shed leptospires in their urine. In this way, infection can spread to other species including humans. Dogs are recognised as a significant reservoir for human infection in tropical countries, but, although it has a temperate climate, cases have been attributed to contact with dogs in New Zealand (NZ) (Sanhueza et al. 2012; thompson 2012). Due to relatively high rates of infection in humans (ESR 2019), considerable effort has been made to reduce the risk of human infection through staff education and livestock vaccination in high-risk agricultural industries such as dairy farming and abattoirs in NZ. Despite this, relatively little attention has been paid to the role of dogs in the infection cycle for leptospirosis in NZ. there are over 250 pathogenic serovars of Leptospira interrogans and borgpeterensii, in addition to nonpathogenic serovars of Leptospira biflexa. L. borgpeterensii serovars Balcanica, Hardjo, Ballum, taravossi and L. interrogans serovars Pomona and Copenhageni which are known to be endemic in the livestock, rodent and possum populations of NZ (Hathaway et al. 1981). of those present in NZ, Copenhageni, Hardjo, Ballum and Pomona have been recognised internationally as causing disease in dogs (miller et al. 2007). Antibodies to all of these serovars have been identified in dogs in NZ (o'Keefe et al. 2002). A 2013 survey of 655 samples submitted to veterinary laboratories established that serovar Copenhageni was found most commonly (10.3% of included dogs), with serovars Hardjo, Pomona and Ballum identified less commonly (3.5%, 1.1%, 0.8% respectively) (Harland et al. 2013b). the agricultural compounds and veterinary medicines (ACVm) register lists two leptospiral vaccines licensed for dogs in New Zealand, Leptoguard (Zoetis NZ, Auckland NZ) and Nobivac Lepto (mSD Animal Health, upper Hutt, NZ). Both these vaccines contain inactivated Icterohaemorrhagiae which stimulates active immunity to both Icterohaemorrhagiae and Copenhageni serovars (Schoone 1989). the most recent serological survey of leptospiral antibodies in dogs in New Zealand concluded that there was no significant difference in the prevalence of positive leptospiral titres between dogs in the North and South Islands. However, there was uneven geographical distribution of samples submitted (Harland et al. 2013b). A recent survey on vaccination policies for dogs across New Zealand showed that 90/96 (94% )of responding veterinarians in the upper North Island often or always recommended vaccination of dogs against leptospirosis. In comparison, 52/66 (79%) of responding veterinarians in the South Island rarely or never recommended leptospirosis vaccination (Cave et al. 2016). this is in line with the anecdotal experience of Zoetis representatives speaking to veterinarians across New Zealand.
there is a common perception that leptospirosis is diagnosed infrequently in dogs residing south of Lake taupo and even more rarely in dogs south of Nelson. Anecdotally it is for this reason that veterinarians rarely consider testing unwell dogs for leptospirosis south of Nelson. Additionally, few veterinarians recommend vaccination against leptospirosis for dogs residing south of taupo. Despite this, Zoetis representatives typically receive one to two reports of confirmed leptospirosis in dogs residing south of Nelson every year. the presenting signs of leptospirosis in dogs include pyrexia, anorexia, lethargy, vomiting, anaemia, uveitis, abortion, pulmonary haemorrhage and signs of renal and/or hepatic failure. Dogs can present with only mild, non-specific clinical signs such as fever, anorexia, depression and abdominal pain. Historically, diagnosis of leptospirosis in dogs has been considered challenging. For these reasons, dogs presenting with nonspecific clinical signs may be unlikely to be tested for leptospirosis and could be misdiagnosed, further perpetuating the perception that leptospirosis does not commonly affect dogs in Southern New Zealand. It is considered likely that leptospirosis is under-diagnosed in both working and pet dogs in NZ (Harland 2013a), particularly in regions where leptospirosis in dogs is considered rare, and where it may not feature on the differential diagnosis list for some
Contact: Keara.brownlie@zoetis.com
veterinarians. In the past, diagnosis of leptospirosis has been considered challenging by many veterinarians and it has been necessary to send samples to an external laboratory for analysis. this may also have contributed to lower rates of diagnosis. A new point-of-care lateral flow assay for diagnosis of leptospirosis (WItNESS Lepto) is now available in NZ. the WItNESS Lepto test detects the primary immune response (Igm) that develops within 1 week of exposure to any canine leptospire (Greene 2006) with 98% sensitivity, 100% specificity (Kodjo et al. 2016); (troia et al. 2018) and 100% positive predictive value (Gloor et al. 2017). Igm antibodies detected by the WItNESS Lepto test predominate in the primary immune response and do not generally persist much beyond resolution of clinical signs. the availability of a reliable in-clinic test kit for leptospirosis facilitates easy, prompt diagnosis (or rule-out) of this disease. It is anticipated that the affordability of the WItNESS Lepto test will also reduce the number of canine leptospirosis diagnoses which are successfully treated with empirical antibiotic treatment for example due to pyrexia) but remain undiagnosed due to lack of owner funds.
other in-clinic tests are available in NZ such as the Idexx SNAP test which detects IgG. In one challenge study, seroconversion was detected using the WItNESS Lepto test by day 10 in all 32 affected dogs included in the study (Lizer et al. 2018). In contrast the Idexx SNAP test detected seroconversion in 3/32 dogs during the 2 weeks postchallenge. WItNESS Lepto has greater detection rates of canine leptospirosis on day 7 (87.5%) than traditional microscopic agglutination testing (mAt; 65.6%) (Lizer et al. 2017). Earlier detection of canine leptospirosis is particularly important to confirm the need for barrier nursing of these high-needs patients due to the potential zoonotic risk. the Idexx SNAP test has been reported to return positive results up to 12 months after vaccination against leptospirosis (Curtis et al. 2015). Vaccinal antibodies are also known to interfere with laboratory mAt testing. Vaccine interference is less likely with Igm-based WItNESS Lepto tests, as Igm does not persist for as long as IgG after vaccination. on evaluation of WItNESS Lepto in recently vaccinated, healthy animals 110/110 samples tested negative when tested 21 or more days after vaccination (Data on file). the availability of a new, reliable in-clinic test for rapid diagnosis of leptospirosis in dogs, combined with the ongoing disparity between vaccination practices and leptospirosis reports across New Zealand precipitated this study. We aimed to estimate the prevalence of leptospirosis among sick dogs presenting to veterinary clinics across New Zealand using the WItNESS Lepto test, with its superior sensitivity and specificity and lack of interference by IgG. our objective was to determine the proportion of sick dogs presenting to veterinary clinics that yield a positive result to the WItNESS Lepto test.
methods
the study was approved by the Kaiawhina Animal Ethics Committee of the Estendart Research Centre, approval number AEC 010/19.
A cross-sectional survey of unwell dogs presenting to veterinary clinics across New Zealand was conducted between July 2019 and January 2021. Zoetis representatives across New Zealand were provided with brief training on the study design, WItNESS Lepto test kits and study protocol summaries to be distributed free of charge to interested clinics. to be included in the study, participating veterinary clinics confirmed they were willing to follow study protocol, particularly around inclusion criteria and the completion of a brief, online questionnaire on the included animal’s clinical history and test results. only unwell dogs showing clinical signs compatible with leptospirosis infection were eligible for inclusion in this study. to be eligible, dogs were required to have displayed at least one of the following clinical signs in the 14 days prior to sampling: anorexia, lethargy, pyrexia, vomiting, signs of renal and/or hepatic failure, anaemia, uveitis, abortion and pulmonary haemorrhage. Dogs that received a leptospirosis vaccination within 3 weeks of blood sampling were excluded. Dogs could be retested 7–10 days after the initial test if there were ongoing clinical signs. this was only appropriate if the results of the initial WItNESS Lepto test was negative and clinical signs had been present for <14 days at initial testing. Concurrent treatments were allowed, and animals were managed as deemed appropriate by the attending veterinarian in conjunction with the dog’s owner. Veterinarians were requested to complete the online questionnaire at the provided link for all tests completed. testing procedure was to follow the instructions provided for WItNESS Lepto test. the sample collected could be whole blood (with EDtA), serum or plasma and samples should always have been collected with a sterile needle and syringe. Blood samples could be taken from unwell dogs as part of a diagnostic work up and specifically for this study, or from blood drawn for other clinical reasons such as for a serum biochemistry panel. Clinics were requested to contact Zoetis to report positive test results so that follow-up testing of acute and convalescent phase plasma by mAt testing at an external laboratory could be performed for dogs testing positive for serovars Copenhageni, Hardjo, Pomona, Ballum and tarassovi (funded by Zoetis). Data were collected into microsoft Excel spreadsheet and descriptive statistics presented. Continuous variables were categorised so that all variables could be described as proportions. Confidence intervals were calculated for the outcome variable.
Results
Five hundred WItNESS Lepto test kits were distributed to >50 veterinary clinics throughout New Zealand. In total, completed questionnaires for 105 dogs were received during the study period. there was a relatively even distribution of ages from 8 weeks to 18 years of age and 56% of dogs tested were female. A variety of breeds were represented and 24% of dogs had worked with livestock or wildlife in their lifetime. unfortunately no responses were received from the Gisborne, Wellington, tasman, Nelson and marlborough regions (Figure 1). Dogs residing in both urban (51%) and Rural (49%) environments were represented. of the dogs included, 58% had never received a vaccination against
leptospirosis: 30/61 dogs in the North Island had been vaccinated but only 1/44 dogs in the South Island had received a vaccine. of the respondents, 91% (99/105) described the WItNESS Lepto test as being easy or very easy to use. In total, five positive cases (4.8% of samples) were identified and 3/5 of the dogs who tested positive for Igm antibodies using the WItNESS Lepto test had worked with livestock or wildlife and 4/5 would be considered as a working breed. one positive case was identified in each of the Hawke’s Bay, Bay of Plenty, taranaki, Auckland and the Waikato. three of the positive cases had never received a vaccination against leptospirosis. three of these cases were identified during the summer months (November and December) and interestingly pyrexia was not listed as a clinical sign in any positive case. All positive cases presented with clinical signs of lethargy and renal and/ or hepatic failure. 4/5 positive cases presented with anorexia, and 3/5 with vomiting. Interestingly, pyrexia was not reported as a clinical sign for any positive dog. the clinical signs reported overall give an indication of clinical signs which prompt vets to test for leptospirosis in dogs. Lethargy and anorexia were identified as clinical signs in 91% and 83% of reports received, respectively, regardless of test outcome. Vomiting (54%) and pyrexia (38%) were also commonly reported alongside 36% of dogs showing signs of renal failure and 48% showing signs of hepatic failure, this is also regardless of test outcome. Follow-up mAt testing was conducted on 2/5 positive cases. the three remaining positive cases were lost to follow-up due to incompleteness. In one case, a two-fold increase in titre in acute and convalescent phase samples for Pomona and Copenhageni was supportive, though not confirmatory, that one of these serovars was the infecting serovar. For the other case, a four-fold increase in titre against Copenhageni, and two-fold increase in titre against Hardjo was supportive, though not confirmatory that Copenhageni was the infecting serovar. overall, 5/105 (4.8%, 95% CI=1.6–10.8%) dogs were positive using the WItNESS Lepto test. For dogs in the study from the South Island, based on 0/44 positive cases identified, the upper one-sided 95% exact confidence limit for the prevalence is 6.6%. For the North Island, based on 5/61 (8.2%) positive cases identified, the upper one-sided 95% exact confidence limit for the prevalence is 16.5%.
Figure 1. Region of New Zealand where dog selected for testing using WItNeSS lepto test kit resides
Discussion
the results of this study align with previously published work and anecdotal evidence on the prevalence of leptospirosis in dogs in NZ. o’Keefe et al. (2002) detected antibodies to leptospiral antigen in 14.2% of 466 samples from a serum bank of apparently healthy dogs in the lower North Island. Harland et al. (2013) detected antibodies to leptospiral antigen in 10.3% of 655 samples submitted to external veterinary laboratories from the lower North Island and South Island of NZ. Although the overall proportion of sick dogs testing positive (4.8%) for leptospirosis in this study is lower than that reported in previous studies (o'Keefe et al. 2002; Harland et al. 2013b), if the proportion of unwell dogs that were positive for leptospirosis is representative of NZ dogs as a whole, then this would suggest that there may be a large number of canine leptospirosis cases occurring annually. When comparing the prevalence of a positive test result between the North and South Islands, the precision, and hence confidence intervals, of our estimates were likely limited by sample size. However, the estimated prevalence among unwell dogs presented to veterinary clinics with signs consistent with leptospirosis was <16.5% (95% upper one sided CI) in the North Island and less than 6.6% (95% upper one sided CI) for dogs residing in the South Island in this study. It is unclear why the prevalence was lower in our study than previous studies, but the sampled population likely contributes to this difference. We enrolled dogs that presented with any one of the applicable clinical signs and provided in house test kits to use free of charge. this lower prevalence is not likely to be due to reduced rates of disease, but more likely due to the broader sample set achieved in this study where vets were encouraged to test any dog that presented with any one of the applicable clinical signs and provided with in house test kits to use free of charge. this included mild and non-specific clinical signs such as anorexia and lethargy. Harland et al. 2013 relied on mAt testing of conveniencebased samples submitted to massey university teaching Hospital and NZVP for other diagnostic purposes. the increased cost and time involved in the process of submitting to an external veterinary laboratory means it is likely samples are only submitted where there is suspicion of serious illness. Igm
antibodies detected by the WItNESS Lepto test predominate in the primary immune response and do not generally persist much beyond resolution of clinical signs. In contrast mAt titres will persist and may give false positive results after vaccination or exposure (Schuller et al. 2015). As the Harland 2013 study looked for evidence of historic exposure (IgG) rather than recent active infection (Igm) in this study, this could also help account for the higher proportion of dogs with positive mAt titres to Leptospira spp. in the Harland 2013 survey. multiple overseas studies have indicated the proportion of dogs with serological evidence of exposure to leptospirosis is higher than the proportion of dogs with confirmed cases of leptospirosis (Ellis 2010; Rojas et al. 2010; Sykes et al. 2011). this would suggest that subclinical infections are common, or that veterinarians are not diagnosing mild cases of leptospirosis. It was felt that providing in-house test kits free of charge and encouraging veterinarians to test any dog that presented with any clinical sign consistent with leptospirosis would provide a larger sample in this study. Leptospirosis in NZ dogs is typically associated with acute renal and/or hepatic failure. Less than 50% of respondent veterinarians reported clinical signs and/or diagnostic results consistent with renal failure (36%) or hepatic failure (48%). the majority of respondents reported less specific clinical signs such as anorexia (83%), lethargy (91%), vomiting (54%) or pyrexia (38%). this suggests that veterinarians may be considering leptospirosis as a differential diagnosis in dogs that present with vague clinical signs as well as those with typical clinical signs of renal and/ hepatic failure. However, it is likely that this may have been encouraged by the provision and promotion of WItNESS Lepto test kits for the purposes of this study. Previous studies of Leptospira spp. infection in NZ dogs have considered mAt titres >96 as positive for leptospirosis. Harland et al. (2013b) considered the infecting serovar to be that generating the highest titre and that co-infection had occurred if there were two serovars with equally high titres. However, the authors also noted that the interpretation of mAt testing for canine leptospirosis can be challenging. Generally, a single titre >1:800 in an unvaccinated dog with classic signs of canine leptospirosis is considered valid for a presumptive diagnosis of leptospirosis, although higher titres, ≥1:3200, are considered by some investigators to be a more reliable threshold for a positive test. It is possible that the lower cut points used to define a positive result in previous NZ surveys could contribute to the higher prevalence identified in these surveys. Because a single mAt may fail to detect antibodies in the early phase of disease or may give false positive results after vaccination or exposure in enzootic areas (Barr et al. 2005), the authors of the Consensus Statement of the American College of Veterinary Internal medicine and of the European Consensus Statement on Leptospirosis in Dogs and Cats recommend paired serologic testing. A 4-fold change in mAt convalescent titre compared with the baseline titre is consistent with active infection (Goldstein 2010; Sykes et al. 2011; Schuller et al. 2015). Interpretation of the mAt is further complicated by the high degree of cross-reaction that occurs between the different serogroups, especially in acute phase samples (Greenlee et al. 2005). Dogs often have similar titres to all serovars of an individual serogroup and at the same time, higher titres to a serogroup unrelated to the infecting serogroup (Levett 2001). this crossreactivity in the acute phase, followed by relative serogroup-specificity in the convalescent phase, results from the detection in the mAt of both Igm and IgG antibodies and the presence of several common antigens among leptospires (Schuller et al. 2015). Additionally, both the mAt and the ELISA that detects canine IgG suffer from the same limitations; namely, they may not detect antibodies early in the course of infection but do detect their presence as a result of vaccination (Schuller et al. 2015). this may also have impacted the results of previous NZ surveys. Despite widespread use of the mAt for the diagnosis of leptospirosis in dogs, investigators have noted that the test lacks the degree of sensitivity, specificity, and repeatability expected of a reference standard test (midence et al. 2012). Serovar cross reactivity has been observed even when dogs have been experimentally infected with a single known serovar (including Copenhageni and Pomona) (Lizer et al. 2018). the uS ACVIm and European Consensus Statements on leptospirosis in dogs both highlight that determination of infecting serovar by mAt testing is flawed due to the high levels of cross reactivity between serovars as well as serogroups (Sykes et al. 2011; Schuller et al. 2015). Anecdotally there has been an increase in awareness of leptospirosis in the South Island of New Zealand due to ongoing reports of sporadic leptospirosis cases in this region. Interestingly, no results were received from the upper South Island region, despite anecdotal reports of increasing vaccination against and prevalence of canine leptospirosis in this region. Despite the finding of Harland et al. in 2013 that there was no statistically significant difference in prevalence of leptospirosis between the North and South Island, anecdotal reports suggest that there has been no increase in vaccination rates against leptospirosis in the South Island. In this survey, 58% of dogs had never been vaccinated against leptospirosis; 30/61 (49%) dogs in the North Island had been vaccinated but only 1/44 (2%) dogs in the South Island were reported to have received a vaccine. this suggests a need for ongoing promotion of awareness among owners and veterinarians of the importance of maintaining vaccination against this potentially fatal disease. It is recognised that the addition of a licensed canine leptospirosis vaccine providing cross protection against a broad range of serovars (e.g. Hardjo and Pomona) would be useful in NZ, although Harland et al. (2013) and o’Keefe (2002) both identified Copenhageni as the most common serovar.
During the study period of this report, Zoetis received anecdotal reports of two cases of leptospirosis in dogs from suburban Christchurch. 4/5 WItNESS Lepto test positive dogs identified in this survey were reported as residing in a rural setting. 3/5 dogs had worked with livestock or wildlife and 4/5 were
classed as working breeds. this differs from the findings of Harland et al. (2013) which concluded that small breeds (considered less likely to be working dogs) did not have a lower prevalence of Copenhageni titres than other breeds. It is likely that this difference is due to the small sample size included in this current study, and possible selection bias of veterinarians selecting dogs considered higher risk for leptospirosis for inclusion in this survey. Although the ministry of Internal Affairs lists 574,349 dogs registered on the national dog database in 2020, according to Companion Animal NZ 2020 survey data there are a total of 851,000 dogs in NZ and 44% of these live rurally (Anonymous 2020). It has been estimated that there are 200,000 working dogs in NZ (o'Connell et al. 2019), which is equivalent to the proportion of working dogs represented in the survey (24%). Exposure to Leptospira spp. organisms is considered common in dogs in New Zealand (o'Keefe et al. 2002; Harland et al. 2013b), with zoonotic potential and possibly fatal consequences. As recommended by the WSAVA vaccination guidelines group, vaccination should be recommended on a risk/benefit basis. Risk factors for leptospirosis in dogs in New Zealand include access to livestock, wildlife and water courses. (Policy 2017) Due to the non-specific nature of presenting clinical signs, veterinarians are encouraged to keep leptospirosis on their differential list, regardless of geographic location. the zoonotic potential of canine leptospirosis and potential for rapid progression of clinical disease, combined with the poor performance of other available tests for leptospirosis early in the course of clinical disease, make the WItNESS Lepto Igm test a useful addition to diagnostic tests available for diagnosis of leptospirosis in NZ. the availability of reliable, simple, non-serovar specific, in-clinic lateral flow assays should facilitate faster diagnosis of leptospirosis in dogs and allow the disease to be ruled out cost effectively in dogs with vague clinical signs. the use of in-clinic tests combined with information from local pathologists, will also allow veterinarians to develop deeper understanding of the prevalence of leptospirosis in their specific regions on which to base vaccine recommendations.
this study provides updated information on the prevalence of leptospirosis among sick dogs presenting to veterinary clinics across New Zealand. the overall prevalence of 4.8% among sampled dogs highlights the importance of continued awareness of leptospirosis in dogs in New Zealand. Vets should consider using the WItNESS Lepto test for dogs presenting with vague clinical signs as well as more typical clinical signs associated with hepatic and renal failure. Although no cases of leptospirosis were identified in the South Island as part of this study, ongoing sporadic reports of confirmed cases in the South Island from laboratories suggest that vets should keep leptospirosis on their differential diagnosis list and consider recommending vaccination following risk/benefit analysis. Further studies on the prevalence and epidemiology of leptospirosis in New Zealand would improve our understanding of the potential zoonotic risk, successful case treatment and provision of advice on vaccination for dogs across NZ.
Oliver young of VetSouth, gore holds the iStAt handheld blood analyser they received as the randomly selected winner of the prize draw for clinics who completed the online survey.
Acknowledgements
this study could not have been undertaken without the support of all the veterinarians across New Zealand who completed this survey, thank you for your time. thanks also to the team at Zoetis who assisted extensively with test distribution, clinic education, study design and review.
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