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The epidemiology of avian mycobacteriosis: Using social network analysis to uncover patterns of disease transmission

Abstract

Background: Transmission of avian mycobacteriosis is generally considered a contagious process, but is not well understood and environmental sources may be important. The large, dynamic population of birds at San Diego Zoo Global (SDZG) with complete population ascertainment over a 22-year period offered an opportunity to use social network analysis to understand disease epidemiology and test for patterns of contagion.

Objectives: Study one evaluated the social network structure of birds for evidence of a contagious process. Study two examined patterns of genetic similarities using whole genome sequencing (WGS) along pathways of network connectivity. Study three examined whether network connectivity predicts future disease.

Methods: Study one identified cases of mycobacteriosis and constructed a social network from enclosure histories (n=16,430) in the SDZG population. Stratification of network edges by spatial and temporal characteristics tested for contagion and other drivers of disease in directly- and indirectly-connected birds. Study two characterized mycobacteria isolated from 124/275 cases. For the subset with WGS (n=97), the probability of having similar genotypes given connectivity was estimated and significance determined from random permutation tests. Study three used longitudinal, mixed-effects logistic regression to evaluate the association between network exposure and mycobacteriosis development.

Results: Study one: Disease clustered significantly among directly- and indirectly-connected birds. The RR of disease given exposure to 2° contacts never housed in the same enclosure was 1.31 (p=0.004), providing strong evidence that a contagious process is present, because the association persisted when common environmental exposure was removed. Study two: Mycobacterium avium avium (MAA) and M. genavense were the most common species. The WGS showed genotypes of MAA were significantly related along paths of network connectivity; however, no significant patterns were identified for M. genavense. Study three: Results showed significant associations between direct (OR=2.15) and indirect (OR=1.56) exposure to positive birds (compared to no exposure) and mycobacteriosis. Risk-stratified models provided estimates with further characterization of exposure; not all findings were robust to model variation.

Conclusion: Social network analysis was a powerful method for evaluating complex contact patterns and mycobacteriosis. The data strongly support a contagious process, show low transmissibility, and provide new information on disease epidemiology.

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