Guinea worm in domestic dogs in Chad: A description and analysis of surveillance data

Guagliardo, Sarah Anne J.; Roy, Sharon L.; Ruiz‐Tiben, Ernesto; Zirimwabagabo, Hubert; Romero, Mario; Chop, Elisabeth; Ouakou, Philippe Tchindebet; Hopkins, Donald R.; Weiss, Adam

doi:10.1371/journal.pntd.0008207

Cited by 20 publications

(38 citation statements)

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“…There is not a clear temporal trend between host species and suggests fluid transmission of D. medinensis between humans and dogs. Previous genetic analyses using spatial principal components analysis had identified a geographic trend of genetic relatedness down the Chari River in Chad [47, 20, 25]. The research in this article has expanded the scope of that analysis by revealing that genetically identical and near-identical samples cluster geographically for multiple areas across Chad.…”

Section: Discussionmentioning

confidence: 82%

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Linked surveillance and genetic data uncovers programmatically relevant geographic scale of Guinea worm transmission in Chad

Ribado

Thiele

et al. 2020

Preprint

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Background Guinea worm (Dracunculus medinensis) was detected in Chad in 2010 after a supposed ten year absence, posing a challenge to the global eradication effort. Initiation of a village-based surveillance system in 2012 revealed a substantial number of dogs infected with Guinea worm, raising questions about paratenic hosts and cross-species transmission. Methodology/Principal Findings We coupled genomic and surveillance data from 2012-2018 cases to investigate the modes of transmission between hosts and the geographic connectivity for genetically similar worm populations. Eighty-six variants across three loci on the mitochondrial genome identified 41 genetically distinct worm genotypes. Spatiotemporal modeling reveals genetically identical worms are within a median range of 18.6 kilometers of each other, but largely within approximately 50 kilometers. Genetically identical worms vary in their degree of spatial clustering, suggesting there may be different factors that favor or constrain transmission. Each worm is surrounded by five to ten genetically distinct worms within a 50 kilometer radius. In an independent population, we show that more variants revealed in whole mitochondrial genome data improved the discrimination between worm pairs. Conclusions/Significance In the largest study linking genetic and surveillance data to date of Guinea worm cases in Chad, we show genetic similarity and modeling can contribute to understanding local transmission. The overlap of genetically distinct worms in quantitatively identified transmission ranges highlights the necessity for genomic tools to link cases. The improved discrimination between worm pairs from variants identified across the complete mitochondrial genome indicates expanding genomic markers could link cases at a finer scale. These results suggest that scaling up genomic surveillance for Guinea worm may provide additional value for programmatic decision-making critical for monitoring cases and intervention efficacy to achieve elimination.

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Section: Discussionmentioning

confidence: 82%

“…We linked the sequenced samples with corresponding surveillance data using national case reports and standardized surveys, described in detail in [25]. Case data was collected from an active and passive village-based surveillance system by the Chad Guinea Worm Eradication Program (CGWEP) and the Ministry of Public Health (MOHP) [21].…”

Section: Methodsmentioning

confidence: 99%

Linked surveillance and genetic data uncovers programmatically relevant geographic scale of Guinea worm transmission in Chad

Ribado

Thiele

et al. 2020

Preprint

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Section: Introductionmentioning

confidence: 99%

“…Infected dogs in Chad occur in two main areas, Moyen Chari and Chari Baguirmi Regions, 16 and peak in the month of June. 4 , 16 Infection reoccurs in about 13% of dogs, and most infected dogs are owned by people of the Sara Kaba ethnicity. 16 Previous works have reported an average of about two worms per dog, 16 with a highly aggregated distribution, but correlates of elevated worm burden in dogs remain poorly understood.…”

Section: Introductionmentioning

confidence: 99%

Correlates of Variation in Guinea Worm Burden among Infected Domestic Dogs

Guagliardo

Wiegand

Roy

et al. 2021

The American Journal of Tropical Medicine and Hygiene

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The Guinea Worm Eradication Program has been extraordinarily successful—in 2019, there were 53 human cases reported, down from the estimated 3.5 million in 1986. Yet the occurrence of guinea worm in dogs is a challenge to eradication efforts, and underlying questions about transmission dynamics remain. We used routine surveillance data to run negative binomial regressions predicting worm burden among infected dogs in Chad. Of 3,371 infected dogs reported during 2015–2018, 38.5% had multiple worms. A multivariable model showed that the number of dogs in the household was negatively associated with worm burden (adjusted incidence rate ratio [AIRR] = 0.95, 95% CI: 0.93–0.97, P < 0.0001) after adjusting for dog age (AIRR = 0.99, 95% CI: 0.96–1.01, P > 0.1). This could relate to the amount of infective inocula (e.g., contaminated food or water) shared by multiple dogs in a household. Other significant univariable associations with worm burden included dog history of guinea worm infection (IRR = 1.30, 95% CI: 1.18–1.45) and dog owners who were hunters (IRR = 0.78, 95% CI: 0.62–0.99, P < 0.05) or farmers (IRR = 0.83, 95% CI: 0.77–0.90, P < 0.0001). Further analysis showed that the number of dogs in the household was significantly and positively correlated with nearly all other independent variables (e.g., owner occupation: farmer, fisherman, or hunter; dog age, gender, and history of guinea worm). The associations we identified between worm burden and dogs per household, and dogs per household and owner characteristics should be further investigated with more targeted studies.

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“…Small numbers of dog infections have also been identified in the other recently endemic countries (in 2019, 2 from Ethiopia, 8 from Mali and none from South Sudan, although this country did report a single dog infection in 2015). There is an urgent interest in understanding the epidemiology of worm infections in dogs and wildlife, and their relationship with human infections in the same areas [ 18 , 19 ]. Greater scrutiny of animals for potential Guinea worm infection has also revealed occasional infections in wildlife, such as cats and baboons (see [ 20 ] for a full description of the situation in 2016–2017).…”

Section: Introductionmentioning

confidence: 99%

Population genomic evidence that human and animal infections in Africa come from the same populations of Dracunculus medinensis

et al. 2020

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Background Guinea worm–Dracunculus medinensis–was historically one of the major parasites of humans and has been known since antiquity. Now, Guinea worm is on the brink of eradication, as efforts to interrupt transmission have reduced the annual burden of disease from millions of infections per year in the 1980s to only 54 human cases reported globally in 2019. Despite the enormous success of eradication efforts to date, one complication has arisen. Over the last few years, hundreds of dogs have been found infected with this previously apparently anthroponotic parasite, almost all in Chad. Moreover, the relative numbers of infections in humans and dogs suggests that dogs are currently the principal reservoir on infection and key to maintaining transmission in that country. Principal findings In an effort to shed light on this peculiar epidemiology of Guinea worm in Chad, we have sequenced and compared the genomes of worms from dog, human and other animal infections. Confirming previous work with other molecular markers, we show that all of these worms are D. medinensis, and that the same population of worms are causing both infections, can confirm the suspected transmission between host species and detect signs of a population bottleneck due to the eradication efforts. The diversity of worms in Chad appears to exclude the possibility that there were no, or very few, worms present in the country during a 10-year absence of reported cases. Conclusions This work reinforces the importance of adequate surveillance of both human and dog populations in the Guinea worm eradication campaign and suggests that control programs aiming to interrupt disease transmission should stay aware of the possible emergence of unusual epidemiology as pathogens approach elimination.

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Guinea worm in domestic dogs in Chad: A description and analysis of surveillance data

Cited by 20 publications

References 21 publications

Linked surveillance and genetic data uncovers programmatically relevant geographic scale of Guinea worm transmission in Chad

Linked surveillance and genetic data uncovers programmatically relevant geographic scale of Guinea worm transmission in Chad

Correlates of Variation in Guinea Worm Burden among Infected Domestic Dogs

Population genomic evidence that human and animal infections in Africa come from the same populations of Dracunculus medinensis

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