Changing epidemiology of Leptospirosis in New Zealand, with a focus on the novel strain of Leptospira borgpetersenii : a thesis presented in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Veterinary Science at Massey University, Palmerston North, New Zealand
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2024-12-25
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Massey University
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Abstract
In New Zealand, leptospirosis has been a common disease in dairy cattle since the 1940s. Six pathogenic Leptospira serovars from two species have been identified as endemic to New Zealand: Leptospira borgpetersenii serovars (sv.) Hardjobovis (Hardjo), Tarassovi, Ballum, Balcanica, and Leptospira interrogans sv. Pomona and Copenhageni. From these, sv. Pomona and Hardjo are the most commonly reported in cattle, and sv. Ballum, Tarassovi, and Copenhageni are less common. The estimated 99% of the national dairy herd is vaccinated against leptospirosis by vaccines containing antigens to Pomona and Hardjobovis and sometimes vaccines also include Copenhageni antigen. Vaccines for protecting dairy cows against Tarassovi were unavailable in New Zealand before December 2023. Historically, leptospirosis due to Tarassovi infection in New Zealand cattle was considered accidental and clinically unimportant.
Serosurveys of apparently healthy cattle in New Zealand showed that over the past fifty years, Tarassovi seroprevalence increased from 6% (50/300) at MAT ≥ 50 to 18% (698/3878) at MAT ≥ 48. More recently, a serology and urine shedding study from 2015- 2016 evaluated the status of 4,000 dairy cows from 200 randomly selected farms, stratified by New Zealand's geographical location and herd size. The study found that on the animal level, 17% of the study animals showed evidence of past infection with Tarassovi, as defined by at least one sample reacting at MAT ≥ 48 for the study's purposes. Moreover, 96% (90/94) of PCR-positive urine samples were sequenced, and 68% (54/80) of those were found to have a novel allele in the sequenced region at the glmU loci. Thus, the use of molecular diagnostic tools, specifically molecular typing targeting a partial region of the glmU gene, allowed New Zealand researchers to identify a novel L. borgpetersenii strain, informally called strain (str.) Pacifica, in the urine of these cows. The 2015-2016 survey reported that dairy cows with Tarassovi titres were associated with urinary shedding, as determined by microscopic agglutination test (MAT) and polymerase chain reaction (PCR) testing, respectively. Because of this association, str. Pacifica is thought to belong to the serogroup Tarassovi. Additionally, the DNA of str. Pacifica has been retrospectively detected in cattle and deer samples dating back as early as 2007.
Moreover, the 19-year (1999-2007) average annual incidence of notified human cases of Tarassovi leptospirosis was estimated at 12.59/100,000 in dairy farmers, compared to an overall annual average incidence of 2.01/100,000. These coincidental findings raised public health concerns.
Therefore, at least some cases of Tarassovi seropositivity, as identified by MAT and reported before 2021, could partially be attributed to str. Pacifica. To confirm str. Pacifica's serogroup, isolation by culture and complete genetic characterisation of an isolate are required. Since str. Pacifica was only recently detected, its epidemiology, morphology, maintenance, and pathogenicity in the host population, as well as its impact on animal and human health, were not well understood.
In this study, we investigated the possibility of isolating str. Pacifica from cow's urine by running a series of laboratory experiments where laboratory-adapted strains were used as a proxy for L. borgpetersenii str. Pacifica in the absence of an isolate to better understand its growth requirements. Laboratory-adapted Leptospira borgpetersenii strains were seeded into different types of media, and Leptospira growth rates were evaluated (Chapter 3). As a result, we ruled out unsuitable media and growth conditions, and this work helped to select the best media and growth conditions for a follow-up field investigation, where freshly collected cow's urine was seeded into selected media. Str. Pacifica was isolated from the urine of a shedding cow using HAN medium at 37°C and 5% CO2. However, this medium failed to sustain str. Pacifica and the culture was lost (Chapter 4).
In addition, over the 2020-2021-2022 milking seasons, we collected and tested blood and urine samples from dairy farms, identified as str. Pacifica positive from the 2016 survey. Our results revealed that str. Pacifica was still maintained in the same dairy herds six years after initial detection. Moreover, we reported an estimated prevalence ratio (PR) of 7, indicating that the prevalence of shedders was seven times as high at the beginning than at the end of lactation in primiparous cows (Chapter 4). These findings provide evidence that str. Pacifica is adapted to dairy cows in New Zealand, and the peak shedding in primiparous heifers occurs in early lactation.
Since the highest levels of str. Pacifica shedding were detected at the start of the milking season during peak milk production, which also coincides with a relatively short 3-month mating period, the associations between str. Pacifica and milk production and reproductive performance of milking cows were also investigated using herd test data and serological and PCR test results of the 2016 survey. Statistical models, including linear, logistic, and generalised mixed models with fixed and random effects, as well as a shared frailty survival model, were used to evaluate the associations between str.
Pacifica positivity and reproduction (Chapter 5) and milk reproduction (Chapter 6) in dairy cows. Results of the statistical analysis of the association between str. Pacifica positivity and reproduction (Chapter 5) of dairy herds showed that str. Pacifica delayed the time from calving to conception (HR = 0.84; 95%: CI 0.74-0.96), although there was no effect on the pregnancy rate (Chapter 5). An analysis of milk production data did not reveal any associations with str. Pacifica at either animal or herd level (Chapter 6). The absence of clinical signs and the lack of association with milk production and reproduction at both the animal and herd levels provides further evidence towards str. Pacifica being well adapted to dairy cows. Therefore, evidence from this thesis suggests that dairy cattle are the maintenance host for str. Pacifica in New Zealand. It is also important to note that str. Pacifica shedders can infect people, especially dairy farmers, milkers, and farm workers who are in regular contact with str. Pacifica-shedding animals. Therefore, the prevention of str. Pacifica transmission via vaccination or the use of appropriate personal protective gear should be prioritised.
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Keywords
leptospira borgpetersenii, str. Pacifica, dairy cows, Leptospira, New Zealand, Leptospirosis in animals, Epidemiology, Cattle, Diseases, Epidemiology, Dairy cattle