Epidemiology of Mycobacterium avium subspecies paratuberculosis infection on sheep, beef cattle and deer farms in New Zealand : a thesis presented in partial fulfilment of the requirements for the degree of Doctor of Philosophy at Massey University, Institute of Veterinary, Animal and Biomedical Sciences, Massey University, Palmerston North, New Zealand

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Paratuberculosis (Ptb) is a chronic enteric infection caused by Mycobacterium avium subspecies paratuberculosis (MAP), affecting wild and domestic ruminants. In domestic ruminants MAP infection is largely sub-clinical, but can result in chronic diarrhoea leading to emaciation and death. Clinical disease is commonly observed in adult cattle and sheep but in deer the disease incidence is higher in young animals (8-12 months). In the New Zealand pastoral farming system, it is common practice to co-graze Ptb susceptible livestock species (sheep, cattle, and deer) together, either concurrently or successively, on the same pasture. Thus several susceptible species have contact at farm level, being at risk of transmitting MAP between species through contaminated pasture. Johne’s Disease Research Consortium (JDRC), a partnership between livestock industries, government and research providers was created to study Ptb in an overarching approach, involving all susceptible species, aiming to generate scientific knowledge to support Ptb control policies. The present research was implemented under the financial support of JDRC, aiming to generate epidemiological information about Ptb infection and clinical disease on mixedspecies pastoral farms, grazing sheep, beef cattle, and/or deer. A total of 350 mixedspecies farms (11,089 animals) were faecal and blood sampled and related epidemiological information was collected. Data was used to estimate: i) the national herd level true prevalence (HTP) of MAP infection on sheep, beef cattle and deer, ii) the risk of MAP infection and clinical disease incidence associated with species co-grazing,iii) the association between infected and affected herds/flocks and production outputs, and iv) relationships between molecular strain types of MAP isolates and their distribution across livestock sectors and geographical areas. Finally, data and results from previous studies allowed v) the development and calibration of a two host-species (sheep & beef cattle) mathematical model, simulating MAP transmission between species and the effect of several control measures under mixed species farming. MAP infection is widely spread in New Zealand. A Bayesian analysis to account for lack of sensitivity (Se) and specificity (Sp) of testing protocols, indicated that the highest HTP estimate for sheep flocks (75%, posterior probability interval (PPI) 68- 82%), followed by deer (46%, PPI 39-54%) and beef herds (43%, PPI 359-51%). Sheep and beef cattle flocks/herds presented a higher prevalence in the North Island (NI), whereas deer infection was mainly located in the South Island (SI). Logistic and Poisson regression models using Bayesian inference to adjust for lack of Se and Sp of diagnostic tests and of farmer’s recall of clinical Ptb indicated that the shared use of pasture was associated with Ptb prevalence and incidence. When beef cattle and sheep were co-grazed, the infection risk increased 3-4 times in each species. Similarly, co-grazing of beef cattle and deer increased 3 times the risk of infection on deer. Co-grazing beef cattle with sheep, or beef cattle with deer, also was associated with increased clinical incidence in these species. Conversely, the co-grazing of sheep and deer was associated with a lower clinical disease incidence in both species. Classical logistic and Poisson regression models indicated that MAP ‘infection’ status was significantly (p =0.03) associated with reduced calving rates in beef cattle herds and lower culling rates in deer herds and sheep flocks. Moreover, in sheep flocks and deer herds, a significant and a marginally significant (p = 0.05 and 0.09, respectively)Molecular analysis of MAP isolates obtained from sheep, cattle (beef and dairy) and deer, using a combination of the variable number of tandem repeats (VNTR) method and the short sequence repeat (SSR) method, rendered 17 MAP subtypes. Analysis indicated significantly higher subtype richness in dairy cattle and livestock sector as the main source of subtype variation. Moreover, similar subtypes were sourced from sheep and beef cattle, which tended to be different to the ones obtained from other livestock sectors. However, when beef cattle and deer were both present on the same farm, they harboured similar subtypes. These results provided strong evidence for transmission of MAP between species through the joint use of pasture. Simulation results of a mathematical infectious disease model for Ptb indicated that the length of the co-grazing period was positively associated with the infection prevalence of sheep and beef cattle. Long pasture spelling periods from 9 to 15 months reduced MAP contamination up to 99%. However, the infection of naïve animals was still possible, but the prevalence remained <1% for at least 25 years. The simultaneous application of control measures on both species was the most efficient approach to reduce the prevalence and incidence. The separation of co-grazed species in tandem with an increased farmer surveillance, to reduce the time that clinical animals remained on the farm, was most effective in sheep, whereas T&C was in beef cattle. The present research provides evidence that MAP infection is highly endemic in New Zealand farming livestock, and that the clinical disease incidence is generally low (<0.5%) in most infected farms. Moreover, inference from molecular pathogen typing of strategically collected isolates from farms across New Zealand strongly suggested that MAP is transmitted between species, mainly from sheep to beef cattle and between beef cattle and deer, all of which are commonly grazed together in the New Zealand pastoral farming system.
Paratuberculosis, Mycobacterium avium paratuberculosis, Epidemiology, New Zealand, Research Subject Categories::VETERINARY MEDICINE::Veterinary epidemiology