Canine olfactory detection of a vectored phytobacterial pathogen, Liberibacter asiaticus, and integration with disease control

Significance Exotic infectious pathogens, like citrus huanglongbing (HLB), are increasingly introduced into agrosystems. Early detection is the key to mitigating their destructive effects. Human visual assessment is insufficiently sensitive to detect new plant infections in a responsive timeframe, and molecular assays are expensive and not easily deployable over large crop landscapes. We turned to detector dogs, an ancient technology, which can rapidly survey large plantings without laborious sample collection or laboratory processing. Dogs detected infections (>99% accuracy) weeks to years prior to visual survey and molecular methods and were highly specific, accurately discriminating target pathogens from other pathogens. Epidemiological models indicated that dogs were more effective and economical than current early detection methods for sustainable disease control.
Early detection and rapid response are crucial to avoid severe epidemics of exotic pathogens. However, most detection methods (molecular, serological, chemical) are logistically limited for large-scale survey of outbreaks due to intrinsic sampling issues and laboratory throughput. Evaluation of 10 canines trained for detection of a severe exotic phytobacterial arboreal pathogen, Candidatus Liberibacter asiaticus (CLas), demonstrated 0.9905 accuracy, 0.8579 sensitivity, and 0.9961 specificity. In a longitudinal study, cryptic CLas infections that remained subclinical visually were detected within 2 wk postinfection compared with 1 to 32 mo for qPCR. When allowed to interrogate a diverse range of in vivo pathogens infecting an international citrus pathogen collection, canines only reacted to Liberibacter pathogens of citrus and not to other bacterial, viral, or spiroplasma pathogens. Canines trained to detect CLas-infected citrus also alerted on CLas-infected tobacco and periwinkle, CLas-bearing psyllid insect vectors, and CLas cocultured with other bacteria but at CLas titers below the level of molecular detection. All of these observations suggest that canines can detect CLas directly rather than only host volatiles produced by the infection. Detection in orchards and residential properties was real time, ∼2 s per tree. Spatiotemporal epidemic simulations demonstrated that control of pathogen prevalence was possible and economically sustainable when canine detection was followed by intervention (i.e., culling infected individuals), whereas current methods of molecular (qPCR) and visual detection failed to contribute to the suppression of an exponential trajectory of infection.