Molecular identification of hookworm isolates from stray dogs, humans and selected wildlife from South Africa

Ngcamphalala, P I; Lamb, Jennifer; Mukaratirwa, Samson

doi:10.1017/s0022149x19000130

Cited by 32 publications

(27 citation statements)

References 38 publications

(90 reference statements)

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“…Humans infected percutaneously may develop cutaneous larva migrans (CLM) [35]. Cases of eosinophilic enteritis [36], as well as patent infections have also been described [37].…”

Section: Introductionmentioning

confidence: 99%

Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat?

et al. 2019

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BackgroundThe canine hookworm, Ancylostoma caninum is the most prevalent and important intestinal nematode parasite of dogs in the USA. Hookworms are typically well controlled by treatment with all commonly used anthelmintics that are approved for this use in dogs. However, in the past few years, cases of recurrent/persistent canine hookworm infections appear to have dramatically increased, suggesting that anthelmintic resistance (AR) may have evolved in this parasite. These cases are highly overrepresented by greyhounds, but multiple other breeds are also represented. The aim of this study was to characterize several of these suspected resistant isolates using in vitro, genetic and clinical testing to determine if these cases represent true anthelmintic resistance in A. caninum.MethodsFecal samples containing hookworm eggs from three cases of persistent hookworm infections; one from a greyhound, one from a miniature schnauzer and one from a hound-mix, were received by our laboratory. These were then used to establish infections in laboratory dogs and to perform egg hatch assays (EHA) and larval development assays (LDA) for detecting resistance to benzimidazoles and macrocyclic lactones, respectively. Additional EHA and LDA were performed on eggs recovered from the laboratory-induced infections. Fecal egg count reduction tests were performed to detect resistance to pyrantel. Deep amplicon sequencing assays were developed to measure the frequency of non-synonymous single nucleotide polymorphisms (SNP) at codons 167, 198 and 200 of the A. caninum isotype-1 β-tubulin gene.ResultsResistance ratios for the three A. caninum isolates tested ranged from 6.0 to > 100 and 5.5 to 69.8 for the EHA and LDA, respectively. Following treatment with pyrantel, reduction in faecal egg counts was negative or 0%. Deep amplicon sequencing of the isotype-1 β-tubulin gene identified a high frequency of resistance-associated SNPs at codon 167 in all three resistant isolates and in two additional clinical cases.ConclusionsThese data conclusively demonstrate multiple anthelmintic resistance in multiple independent isolates of A. caninum, strongly suggesting that this is an emerging problem in the USA. Furthermore, evidence suggest that these resistant hookworms originate from racing greyhound farms and kennels, though additional research is needed to confirm this.

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“…Humans infected percutaneously may develop cutaneous larva migrans (CLM) [35]. Cases of eosinophilic enteritis [36], as well as patent infections have also been described [37].…”

Section: Introductionmentioning

confidence: 99%

Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat?

et al. 2019

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“…Previously, cases of CLM could be treated fairly easily using topical anthelmintics (Heukelbach and Feldmeier, 2008); however, such treatments will not be effective against MDR worms. Cases of eosinophilic enteritis (Prociv and Croese, 1996), as well as patent infections have also been described (Ngcamphalala et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Multiple Drug Resistance in the canine hookwormAncylostoma caninum: an Emerging Threat

Castro

Howell

Schaefer

et al. 2019

Preprint

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In the past few years, diagnoses by veterinarians of recurrent canine hookworm infections have dramatically increased, suggesting that anthelmintic resistance (AR) may have evolved in the parasite Ancylostoma caninum. To investigate this, we established three “suspected-resistant” and two susceptible A. caninum isolates in research dogs for further study. The egg hatch assay (EHA) and the larval development assay (LDA) were used for detecting resistance to benzimidazoles, and macrocyclic lactones, respectively. Resistance ratios ranged from 6.0 to >100 and 5.5-69.8 for the EHA and LDA, respectively. Following treatments with fenbendazole, pyrantel and milbemycin oxime, reduction in faecal egg counts ranged from 64–86%, 0–72% and 58–92%, respectively. Deep amplicon sequencing of the isotype-1 β tubulin gene identified a high frequency of resistance-associated single nucleotide polymorphisms at codon 167 in the resistant isolates and clinical cases.. These data conclusively demonstrate multiple anthelmintic resistance in A. caninum, and provide pivotal evidence that this is an emerging problem in the United States. Consequently, these findings should provide some concern to the global health community, as the scale-up of mass drug administration for soil-transmitted helminths (STH) is now placing similar selection pressures for benzimidazole resistance in human hookworms.

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“…Limitations of the study included the following: (a) no clinical samples were collected to confirm whether the organisms isolated have been associated with infections caused in humans; (b) not all the samples could be sequenced due to a very limited budget for molecular studies and sequencing; and (c) many of the samples also contained hookworms and rotifers and could not be further assessed. Several studies have shown that hookworms are present in the faeces of livestock [ 185 ] and domestic animals [ 186 ], and therefore, the eggs could have entered underground aquifers, while several reports on the prevalence of rotifers in groundwater have been published [ 187 , 188 ]. Hence, more studies are needed to determine the health risk to vulnerable individuals drinking water containing these organisms and the effectiveness of point-of-use devices in eliminating them.…”

Section: Discussionmentioning

confidence: 99%

Detection of Free-Living Amoebae and Their Intracellular Bacteria in Borehole Water before and after a Ceramic Pot Filter Point-of-Use Intervention in Rural Communities in South Africa

Loo

Bartie²,

Barnard

et al. 2021

IJERPH

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Free-living amoebae (FLA) are ubiquitous in nature, whereas amoeba-resistant bacteria (ARB) have evolved virulent mechanisms that allow them to resist FLA digestion mechanisms and survive inside the amoeba during hostile environmental conditions. This study assessed the prevalence of FLA and ARB species in borehole water before and after a ceramic point-of-use intervention in rural households. A total of 529 water samples were collected over a five-month period from 82 households. All water samples were subjected to amoebal enrichment, bacterial isolation on selective media, and molecular identification using 16S PCR/sequencing to determine ARB species and 18S rRNA PCR/sequencing to determine FLA species present in the water samples before and after the ceramic pot intervention. Several FLA species including Acanthamoeba spp. and Mycobacterium spp. were isolated. The ceramic pot filter removed many of these microorganisms from the borehole water. However, design flaws could have been responsible for some FLA and ARB detected in the filtered water. FLA and their associated ARB are ubiquitous in borehole water, and some of these species might be potentially harmful and a health risk to vulnerable individuals. There is a need to do more investigations into the health risk of these organisms after point-of-use treatment.

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Molecular identification of hookworm isolates from stray dogs, humans and selected wildlife from South Africa

Cited by 32 publications

References 38 publications

Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat?

Multiple drug resistance in the canine hookworm Ancylostoma caninum: an emerging threat?

Multiple Drug Resistance in the canine hookwormAncylostoma caninum: an Emerging Threat

Detection of Free-Living Amoebae and Their Intracellular Bacteria in Borehole Water before and after a Ceramic Pot Filter Point-of-Use Intervention in Rural Communities in South Africa

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