Ecology of domestic dogs Canis familiaris as an emerging reservoir of Guinea worm Dracunculus medinensis infection

Abstract

<jats:title>Abstract</jats:title><jats:p>Global eradication of human Guinea worm disease (dracunculiasis) has been set back by the emergence of infections in animals, particularly domestic dogs <jats:italic>Canis familiaris</jats:italic>. The ecology and epidemiology of this reservoir is unknown. We tracked dogs using GPS, inferred diets using stable isotope analysis and analysed correlates of infection in Chad, where numbers of Guinea worm infections are greatest. Dogs had small ranges that varied markedly among villages. Diets consisted largely of human staples and human faeces. A minority of ponds, mostly &lt;200 m from dog-owning households, accounted for most dog exposure to potentially unsafe water. The risk of a dog having had Guinea worm was reduced in dogs living in households providing water for animals but increased with increasing fish consumption by dogs. Provision of safe water might reduce dog exposure to unsafe water, while prioritisation of proactive temephos (Abate) application to the small number of ponds to which dogs have most access is recommended. Fish might have an additional role as transport hosts for Guinea worm, by concentrating copepods infected with worm larvae.</jats:p><jats:sec><jats:title>Author summary</jats:title><jats:p>Guinea worm is a parasite that causes profoundly debilitating disease in humans. An eradication program has been successful in nearly eliminating the disease from people. However, the same worm has now been found in domestic dogs and the frequency of detecting Guinea worm in dogs has been increasing. This means that to eradicate Guinea worm, the infection must be eliminated in dogs as well as in people. However, not much is known about the disease in dogs. This study is the first to investigate dog ecology in relation to Guinea worm infection. We worked in the worst-affected country, Chad. We attached GPS collars to dogs to track their ranging and use of water bodies and analysed their diets using a forensic technique, based on analysing stable isotope compostion of their whiskers and potential food items. We showed that dogs living in households that provided water to their animals had a lower risk of having had Guinea worm and that dogs that ate more fish had an increased risk. These findings suggest there is a classical route for worm transmission in dogs, via drinking contaminated water, as well as a novel route, potentially by eating fish carrying a source of infection.</jats:p></jats:sec>

A pond-side test for Guinea worm: Development of a loop-mediated isothermal amplification (LAMP) assay for detection of Dracunculus medinensis

“…Using copepods of unknown genera collected from ponds in villages alongside the River Chari in Chad, where Guinea worm infections in dogs were commonplace ( McDonald et al, 2020 ), DNA was extracted using several methods, to identify the one most suited to pond-side use. As a standard, DNA was extracted from single copepods using a DNeasy extraction kit following the manufacturers protocols (Qiagen).…”

“…The worm looked likely to be only the second human pathogen, after smallpox virus, to be eradicated. The eradication campaign, however, has experienced a major setback with the apparent emergence of non-human animal reservoirs, principally in domestic dogs Canis familiaris ( Eberhard et al, 2014 ; McDonald et al, 2020 ) . There were 1040 infections in dogs in Chad in 2018 and dog infections have also been recorded in Ethiopia and Mali.…”

Copepod consumption by amphibians and fish with implications for transmission of Dracunculus species

“…to animals, including of D. medinensis to dogs in Chad . In Chad, it was noted that many villages experiencing high Guinea worm transmission are fishing villages where small fish and fish viscera are fed to or scavenged by dogs and cats, and that increased fish consumption is positively correlated with the likelihood of dog infection ( Eberhard et al, 2014 ; McDonald et al, 2020 ; Richards et al, 2020 ). Because fish consumed high numbers of copepods during our 24-h trials, it is likely that they would concentrate high numbers of copepods in their gastrointestinal tract after feeding (also concentrating Dracunculus larvae inside the fish if those copepods were infected).…”

Spillback in the Anthropocene: the risk of human-to-wildlife pathogen transmission for conservation and public health

“…Perhaps the best example of this phenomenon is of feral dogs (Canis familiaris) and dracunculiasis ("Guinea worm"), caused by the nematode Dracunculus medinensis in sub-saharan Africa. Although the disease is nearing elimination, recent re-emergence events have been traced to feral dog populations (Eberhard et al 2014;McDonald et al 2020), severely complicating efforts to eliminate the disease using public health measures (Hopkins et al 2019). Note that we do not count this example as a documented secondary spillover because, while Guinea worm provides an excellent example of the difficulties created by animal reservoirs in elimination settings, the spillback story is complicated by the fact that it is unclear whether dogs' infections were sourced by humans recently (making them a novel host), or whether they are a long-standing maintenance reservoir that have played a role in D. medinensis ecology for a considerable time (McDonald et al 2020).…”