Zoonotic Ancylostomiasis: An Update of a Continually Neglected Zoonosis.

Hookworm infections are classified as the most impactful of the human soil-transmitted helminth (STH) infections, causing a disease burden of ∼4 million disability-adjusted life years, with a global prevalence of 406-480 million infections. Until a decade ago, epidemiological surveys largely assumed Necator americanus and Ancylostoma duodenale as the relevant human hookworm species implicated as contributing to iron-deficiency anemia. This assumption was based on the indistinguishable morphology of the Ancylostoma spp. eggs in stool and the absence of awareness of a third zoonotic hookworm species, Ancylostoma ceylanicum. The expanded use of molecular diagnostic assays for differentiating hookworm species infections during STH surveys has now implicated A. ceylanicum, a predominant hookworm of dogs in Asia, as the second most common hookworm species infecting humans in Southeast Asia and the Pacific. Despite this, with the exception of sporadic case reports, there is a paucity of data available on the impact of this emerging zoonosis on human health at a population level. This situation also challenges the current paradigm, necessitating a One Health approach to hookworm control in populations in which this zoonosis is endemic. Here, we have summarized the available research studies and case reports on human A. ceylanicum infections in Southeast Asia and the Pacific after 2013 using a systematic review approach. We summarized eight research articles and five clinical case studies, highlighting the importance of future in-depth investigation of zoonotic A. ceylanicum infections using sensitive and cost-effective diagnostic tools.

Canine gastrointestinal nematode transmission potential in municipal dog parks in the southeast United States.

Monthly canine parasite prophylactic products prevent not only adult heartworm infection, but also patent infections with specific gastrointestinal parasites. While most monthly products control and treat certain hookworm and roundworm infections, fewer are labeled for whipworm (Trichuris vulpis). Therefore, we hypothesized that fecal samples collected from municipal dog parks will have a greater prevalence of whipworm eggs compared to hookworm and roundworm eggs. In this study, canine fecal samples were collected from municipal dog parks in three southeastern states, with up to 20 fecal samples were collected from each park. A total of 200 fecal samples were obtained from dog parks in Georgia, North Carolina, and South Carolina. All fecal samples were examined for the presence of gastrointestinal helminths by a simple centrifugal flotation using sheather's sugar flotation solution. Of the 200 samples collected, 27% were positive for gastrointestinal helminths by fecal flotation. Of these infected fecal samples, 8.5%, 17%, and 1.5% contained whipworm, hookworm, and roundworm, respectively. However, the majority of hookworm-positive samples were collected from one park, whereas whipworm and roundworm samples were collected from multiple parks. These results could indicate that dogs are at risk of infection by all three parasites at dog parks, and that preventive strategies may need to be tailored not only to the specific region, but to specific infected dog parks.

A Case of Cutaneous Larva Migrans in a Child from Vinces, Ecuador.

BACKGROUND Cutaneous larva migrans (CLM) is caused by nematode parasites of the hookworm family of Ancylostomatidae. Ancylostomiasis is a zoonosis found in cats and dogs, and humans are an accidental host. This report presents a case of CLM in an 8-year-old boy, which was due to the zoonotic transmission of Ancylostoma caninum from domestic dogs in an urban area of Vinces, Ecuador, and demonstrates how awareness and early diagnosis contributed to the timely treatment of CLM. CASE REPORT An 8-year-old boy from the urban area of Vinces city in the Los Ríos province of Ecuador presented with a serpiginous palpable lesion on the sole of the right foot, consistent with a diagnosis of cutaneous larva migrans (CLM). He was infected through contact with the soil where canine Ancylostoma larvae were found. Twenty samples of feces were analyzed from the soil, and Ancylostoma larvae were found in 100% of these samples. Also, 120 dog stool samples were examined, and 75 (62.5%) contained Ancylostoma larvae, which were identified using the modified Willis and Baermann method. CONCLUSIONS CLM is a zoonotic disease that can affect the population in endemic areas. In this case, CLM was identified in the sole of the foot of a child. The presence of Ancylostoma larvae were identified in the soil and in the feces of dogs, indicating that the community was exposed to a significant environmental risk from this zoonotic disease.

Parasitos zoonóticos em solos de praças públicas no município de Sousa, Paraíba / Zoonotic parasites in soils of public squares in the municipality of Sousa, Paraíba

Os espaços coletivos com grande circulação de pessoas e animais tutelados ou errantes, como as praças públicas, podem gerar um problema para a saúde pública, uma vez que os animais podem eliminar fezes contaminadas por parasitos nesses locais, desempenhando um importante papel epidemiológico na transmissão de zoonoses parasitárias. Portanto, este trabalho teve como objetivo avaliar a contaminação por parasitos zoonóticos em dez praças públicas da cidade de Sousa, Paraíba, bem como avaliar o melhor método de diagnóstico de infestação ambiental por estes parasitas. Foram feitas coletas de solo em cinco pontos diferentes de cada praça, por raspagem superficial em quadrantes delimitados por 15 cm, sendo coletados 200g da parte central de cada ponto. Os métodos de diagnósticos utilizados foram Flutuação Simples, Sedimentação Simples, Faust e Centrífugo-Flutuação em Solução de Sacarose. Das praças avaliadas, 90% (9/10) obtiveram pelo menos uma amostra positiva. O gênero de parasito mais frequente foi Ancylostoma spp., presente em 70% (7/ 10) das praças analisadas; seguido por Strongyloides spp., coccídeos e Taenia spp., em 40% (4/10); Toxocara spp.,em 30% (3/10); eCystoisospora spp. e Trichuris spp., em 10% (1/10). O método de Sedimentação Simples foi o mais eficaz, resultando em 44% (22/50) de amostras positivas. Os demais métodos não atingiram 15% de positividade. Concluiu-se que as praças públicas analisadas encontram-se altamente infestadas por parasitos zoonóticos, representando um risco a saúde pública no município de Sousa-PB.

Collective spaces with large circulation of people and animals domiciled or wandering, such as public squares, can generate a public health problem, since the animals can eliminate feces contaminated by parasites in these places, playing an important epidemiological role for zoonose transmission. Therefore, the objective of this work was to evaluate the contamination by zoonotic parasites in ten public squares of the city of Sousa, Paraíba, as well as to evaluate the best method for the diagnosis of environmental infestation by these parasites. Soil samples were collected at five different points of each square, by surface scraping in quadrants delimited by 15 cm, with 200g of the central part of each point being collected. The diagnostic methods used were Simple Flotation, Simple Sedimentation, Faust and Centrifugal-Fluctuation in Sucrose Solution. At least one positive sample in 90% (9/10) of the evaluated squares. The most frequent parasite genus was Ancylostoma spp., present in 70% (7/10) of the analyzed squares; followed by Strongyloides spp., coccidia and Taenia spp., in 40% (4/10); Toxocara spp., in 30% (3/10); and Cystoisospora spp. and Trichurisspp., in 10% (1/10). The Simple Sedimentation method was the most effective, resulting in 44% (22/50) of positive samples. The other methods did not reach 15% positivity. It was concluded that the analyzed public squares are highly infested by zoonotic parasites, representing a public health risk in the municipality of Sousa-PB.

Terror in the dirt: Sensory determinants of host seeking in soil-transmitted mammalian-parasitic nematodes.

Infection with gastrointestinal parasitic nematodes is a major cause of chronic morbidity and economic burden around the world, particularly in low-resource settings. Some parasitic nematode species, including the human-parasitic threadworm Strongyloides stercoralis and human-parasitic hookworms in the genera Ancylostoma and Necator, feature a soil-dwelling infective larval stage that seeks out hosts for infection using a variety of host-emitted sensory cues. Here, we review our current understanding of the behavioral responses of soil-dwelling infective larvae to host-emitted sensory cues, and the molecular and cellular mechanisms that mediate these responses. We also discuss the development of methods for transgenesis and CRISPR/Cas9-mediated targeted mutagenesis in Strongyloides stercoralis and the closely related rat parasite Strongyloides ratti. These methods have established S. stercoralis and S. ratti as genetic model systems for gastrointestinal parasitic nematodes and are enabling more detailed investigations into the neural mechanisms that underlie the sensory-driven behaviors of this medically and economically important class of parasites.

Ancylostoma ceylanicum Hookworm in the Solomon Islands.

Although hookworm is highly prevalent in the Solomon Islands, the species involved are unknown. We initiated this study in response to finding Ancylostoma ceylanicum hookworm in a peacekeeper in Australia who had returned from the Solomon Islands. Kato-Katz fecal surveys performed in 2013 and 2014 in 2 village groups in East Malaita, Solomon Islands, identified hookworm-positive samples. These specimens were tested by cytochrome oxidase 1 (cox-1) gene multiplex PCR and sequenced. Of 66 positive specimens, 54 (81.8%) contained only Necator americanus, 11 (16.7%) contained only A. ceylanicum, and 1 (1.5%) contained both species. A. duodenale was not found. Haplotype analysis of cox-1 sequences placed all human isolates (99% bootstrap support) of A. ceylanicum within the zoonotic clade rather than the human-specific clade. This study confirms that A. ceylanicum is endemic in the East Malaita region of this Pacific Island nation. The strain of the A. ceylanicum in this region can be shared among humans, dogs, and cats.

Understanding Heterogeneity in the Impact of National Neglected Tropical Disease Control Programmes: Evidence from School-Based Deworming in Kenya.

BACKGROUND: The implementation of soil-transmitted helminth (STH) treatment programmes occurs in varied environmental, social and economic contexts. Programme impact will be influenced by factors that affect the reduction in the prevalence and intensity of infections following treatment, as well as the subsequent rate of reinfection. To better understand the heterogeneity of programme impact and its underlying reasons, we investigated the influence of contextual factors on reduction in STH infection as part of the national school based deworming (SBD) programme in Kenya. MATERIALS AND METHODS: Data on the prevalence and intensity of infection were collected within the monitoring and evaluation component of the SBD programme at baseline and after delivery of two annual treatment rounds in 153 schools in western Kenya. Using a framework that considers STH epidemiology and transmission dynamics, capacity to deliver treatment, operational feasibility and financial capacity, data were assembled at both school and district (county) levels. Geographic heterogeneity of programme impact was assessed by descriptive and spatial analyses. Factors associated with absolute reductions of Ascaris lumbricoides and hookworm infection prevalence and intensity were identified using mixed effects linear regression modelling adjusting for baseline infection levels. PRINCIPAL FINDINGS: The reduction in prevalence and intensity of A. lumbricoides and hookworms varied significantly by county and within counties by school. Multivariable analysis of factors associated with programme impact showed that absolute A. lumbricoides reductions varied by environmental conditions and access to improved sanitation at schools or within the community. Larger reduction in prevalence and intensity of hookworms were found in schools located within areas with higher community level access to improved sanitation and within counties with higher economic and health service delivery indicator scores. CONCLUSIONS: The study identifies factors associated with the impact of school-based deworming and in particular highlights how access to water, sanitation and hygiene and environmental conditions influence the impact of deworming programmes.

The zoonotic risk of Ancylostoma ceylanicum isolated from stray dogs and cats in Guangzhou, South China.

Canine and feline hookworm infection is endemic in many countries with zoonotic transmission representing a potentially significant public health concern. However, there is limited data available on the zoonotic transmission of canine and feline hookworms in China. This study was conducted to evaluate the zoonotic risk of Ancylostoma ceylanicum isolated from stray dogs and cats in Guangzhou, south China. Primer pairs CAF/CAR were designed to amplify complete ITS sequences of obtained A. ceylanicum. The results were compared with fourteen ITS reference sequences of human-derived A. ceylanicum registered in GenBank, and phylogenetic trees were established by using NJ and ML methods. The sequence similarity of three dog-derived and five cat-derived A. ceylanicum with fourteen human-derived A. ceylanicum were 96.8%~100% and 97.8%~100%, respectively. Phylogenetic analysis placed A. ceylanicum isolated from dogs and cats in the same group with A. ceylanicum human isolates. Due to the ability of A. ceylanicum to cause a patent infection in humans, the zoonotic risk arising from dog and cat reservoirs to communities in this region should be determined.

High prevalence of Ancylostoma ceylanicum hookworm infections in humans, Cambodia, 2012.

Ancylostoma ceylanicum, a hookworm of canids and felids in Asia, is becoming the second most common hookworm infecting humans. In 2012, we investigated the prevalence and infection dynamics of and risk factors for hookworm infections in humans and dogs in a rural Cambodian village. Over 57% of the population was infected with hookworms; of those, 52% harbored A. ceylanicum hookworms. The greatest intensities of A. ceylanicum eggs were in persons 21-30 years of age. Over 90% of dogs also harbored A. ceylanicum hookworms. Characterization of the cytochrome oxidase-1 gene divided isolates of A. ceylanicum hookworms into 2 groups, 1 containing isolates from humans only and the other a mix of isolates from humans and animals. We hypothesize that preventative chemotherapy in the absence of concurrent hygiene and animal health programs may be a factor leading to emergence of A. ceylanicum infections; thus, we advocate for a One Health approach to control this zoonosis.

Epidemiological and genetic data supporting the transmission of Ancylostoma ceylanicum among human and domestic animals.

BACKGROUND: Currently, information on species-specific hookworm infection is unavailable in Malaysia and is restricted worldwide due to limited application of molecular diagnostic tools. Given the importance of accurate identification of hookworms, this study was conducted as part of an ongoing molecular epidemiological investigation aimed at providing the first documented data on species-specific hookworm infection, associated risk factors and the role of domestic animals as reservoirs for hookworm infections in endemic communities of Malaysia. METHODS/FINDINGS: A total of 634 human and 105 domestic canine and feline fecal samples were randomly collected. The overall prevalence of hookworm in humans and animals determined via microscopy was 9.1% (95% CI = 7.0-11.7%) and 61.9% (95% CI = 51.2-71.2%), respectively. Multivariate analysis indicated that participants without the provision of proper latrine systems (OR = 3.5; 95% CI = 1.53-8.00; p = 0.003), walking barefooted (OR = 5.6; 95% CI = 2.91-10.73; p<0.001) and in close contact with pets or livestock (OR = 2.9; 95% CI = 1.19-7.15; p = 0.009) were more likely to be infected with hookworms. Molecular analysis revealed that while most hookworm-positive individuals were infected with Necator americanus, Ancylostoma ceylanicum constituted 12.8% of single infections and 10.6% mixed infections with N. americanus. As for cats and dogs, 52.0% were positive for A. ceylanicum, 46.0% for Ancylostoma caninum and 2.0% for Ancylostoma braziliense and all were single infections. CONCLUSION: This present study provided evidence based on the combination of epidemiological, conventional diagnostic and molecular tools that A. ceylanicum infection is common and that its transmission dynamic in endemic areas in Malaysia is heightened by the close contact of human and domestic animal (i.e., dogs and cats) populations.

Hookworms of dogs and cats as agents of cutaneous larva migrans.

Dogs and cats are hosts to hookworms that may cause zoonotic disease, most notably, cutaneous larva migrans. Ancylostoma braziliense is most often implicated in dermatological lesions, and Ancylostoma caninum has been associated with eosinophilic enteritis and suggested as a possible cause of diffuse unilateral subacute neuroretinitis in humans. Other manifestations include eosinophilic pneumonitis, localized myositis, folliculitis, erythema multiforme, or ophthalmological manifestations. Ancylostoma eggs are morphologically indistinguishable, which complicates epidemiological studies. Surveys of dermatologists, gastroenterologists, and ophthalmologists would help to define the incidence of these zoonotic infections. Improved diagnostic tests are needed to identify the causative species involved and understand the epidemiology of hookworm disease. This review describes the discovery of the disease, the biology of the agents, and how that biology may impact disease.

Investigations into the prevention of neonatal Ancylostoma caninum infections in puppies by application of imidacloprid 10% plus moxidectin 2.5% topical solution to the pregnant dog.

The aim of the investigation was to examine whether a single topical administration of a combination of imidacloprid and moxidectin to pregnant dogs could prevent neonatal infections with reactivated Ancylostoma caninum larvae. Three pregnant beagles, infected with A. caninum, were treated topically with the combination on day 56 of pregnancy. Three further dogs served as untreated controls. Treatment appeared to prevent neonatal infections in the puppies completely. Neither intestinal stages nor somatic larvae were found in two examined puppies per litter. All puppies and dams of the treatment group remained coproscopically negative. No side-effects in dams or puppies were observed. Two of three untreated dams showed a patent infection after parturition. Necropsy of two puppies of each negative control litter revealed seven intestinal and five somatic A. caninum stages in total. One litter of the untreated dams showed a patent infection 33 days after parturition. In the other two litters, no representative sample sizes could be collected.

Seasonal contamination of public squares and lawns by parasites with zoonotic potential in southern Brazil.

The presence of helminths and protozoans in public squares and lawns of the city of Maringá, southern Brazil, during winter and summer was assessed in order to evaluate their seasonal fluctuations in relation to edaphic and climatic factors. Samples were collected from January 2003 through June 2004 in 90% (13) of all public squares covered by sand, and in 30% (4) of all lawns used as leisure areas. The samples were analysed quantitatively by modified centrifugal-flotation and sedimentation in water techniques, and qualitatively by a method based on positive larval thermo-hydrotropism. Meteorological data were recorded, and physical, chemical and structural characteristics of the soil were analysed. One hundred and thirty samples of sand from squares, 65 in summer and 65 in winter, and 40 samples of grass from lawns, 20 in each season, were collected. All samples from lawns, 62 (95.38%) from squares in winter and 45 (69.23%) in summer, contained protozoans and/or helminths. Eggs of Toxocara spp. were the most frequently observed parasites in both winter and summer in squares (P < 0.0001) and in lawns (P = 0.6142), being equally distributed among the different locations (P = 0.2038). Species diversity was lower in winter; fewer parasites were found in summer. This region, with a tropical climate and a mild winter dry season, has favourable edaphic and climatic conditions for soil contaminants to persist year-round. In addition, the high frequency of animals such as dogs and cats and the poor sanitary measures in force made it possible for zoonoses to be transmitted in the public spaces.

Seasonal fluctuations in prevalence of dog intestinal parasites in public squares of Mar del Plata city, Argentina and its risk for humans / Estacionalidad en la prevalencia de parásitos intestinales caninos en plazas públicas de Mar del Plata, Argentina, y su riesgo para la salud humana

The aim of this work is to analyze whether there is a seasonal prevalence of parasites in dog feces from public squares in Mar del Plata city, Argentina, and to evaluate the climatic conditions that promote the development of parasites and allow the transmission to people. The study was performed in 21 squares from June 2001 to May 2002. Samples were processed by the Willis technique. Differences in prevalence of parasites were examined for significance by the Chisquare test. Climatic data were obtained from the Library of the National Meteorological Service of Argentina. Total parasitic prevalence was higher in winter than in summer. The prevalence of Ancylostoma spp. was higher in the summer-autumn period. For Toxocara canis, the prevalence was higher in winter whereas for Trichuris vulpis, it was higher in winter, spring and summer. This work shows high prevalence of total parasites throughout the year. For Ancylostoma spp., summer and autumn might be the seasons with higher sanitary risk. On the other hand, T. canis could present the higher risk to people in winter and, T. vulpis, would be transmitted throughout the whole year. The seasonal variation in prevalence of dog parasites results in continuous exposure to people visiting the squares, not only Mar del Plata residents but also tourists from other regions of Argentina and the world, with at least one species of parasite with sanitary risk.

El objetivo de este trabajo es analizar la variación estacional de la prevalencia de los parásitos presentes en las heces caninas halladas en plazas públicas de la ciudad de Mar del Plata y evaluar aquellas condiciones climáticas que promueven su desarrollo y permiten su transmisión a la gente. El estudio se realizó en 21 plazas desde junio de 2001 hasta mayo de 2002. Las muestras fueron procesadas con la técnica de Willis. Se utilizó el test de c² para comparar la prevalencia de los diferentes parásitos. Los datos climáticos fueron obtenidos en la biblioteca del Servicio Meteorológico Nacional. La prevalencia total de parásitos fue considerablemente más alta en invierno que en verano. Ancylostoma spp. fue la especie prevalente en el período otoño-verano. La incidencia de Toxocara canis fue más alta en invierno que en el resto de las estaciones, y la de Trichuris vulpis fue alta en invierno, primavera y verano. Este trabajo muestra alta prevalencia de parásitos totales a lo largo de todo el año en las plazas públicas de Mar del Plata. Para Ancylostoma spp. verano y otoño podrían ser las estaciones con riesgo sanitario más alto para la gente. Por otra parte, T. canis podría presentar mayor riesgo para la gente en invierno y T. vulpis sería transmitido durante todo el año. La variación estacional en la prevalencia de los distintos parásitos caninos, con al menos una especie con riesgo sanitario, hace que la exposición para la gente que visita las plazas sea continua e involucre no sólo a la gente que vive en Mar del Plata sino también turistas de otras regiones de Argentina y el mundo.

Geophagia is not associated with Trichuris or hookworm transmission in Zanzibar, Tanzania.

Geophagia may be harmful as a method for the transmission of geohelminths. In this study, we pose two questions in a representative sample of 970 pregnant women from Pemba Island, Zanzibar, Tanzania. Can consumed earth be a vector for geohelminth infection? And do geophagists have differential parasitic infection? The parasitological content of 59 non-food substance samples was analysed. Cross-sectional data regarding pica behaviour were collected through interviews conducted by local researchers. Ascaris, Trichuris and hookworm status was ascertained through Kato-Katz smears. The prevalence of geophagia at baseline was 5.6% and the overall prevalence of Ascaris, Trichuris and hookworm infection was 5.6%, 33.2% and 32.9%, respectively. No consumed soil samples contained infectious parasitic stages, and only one of the consumed pica substances (charcoal) contained parasites of potential risk to human health. In bivariate analyses, neither the prevalence nor the intensity of infection with Ascaris, Trichuris or hookworm differed significantly by geophagia status. Furthermore, in multivariate models, geophagia was not a significant predictor of helminth infection status. We conclude that geophagia is not a source of Trichuris or hookworm infection among pregnant women in Pemba (insufficient power to evaluate the effect of Ascaris), which is in contrast to existing findings of helminth infection and geophagia.

Seasonal fluctuations in prevalence of dog intestinal parasites in public squares of Mar del Plata city, Argentina and its risk for humans.

The aim of this work is to analyze whether there is a seasonal prevalence of parasites in dog feces from public squares in Mar del Plata city, Argentina, and to evaluate the climatic conditions that promote the development of parasites and allow the transmission to people. The study was performed in 21 squares from June 2001 to May 2002. Samples were processed by the Willis technique. Differences in prevalence of parasites were examined for significance by the Chi-square test. Climatic data were obtained from the Library of the National Meteorological Service of Argentina. Total parasitic prevalence was higher in winter than in summer. The prevalence of Ancylostoma spp. was higher in the summer-autumn period. For Toxocara canis, the prevalence was higher in winter whereas for Trichuris vulpis, it was higher in winter, spring and summer. This work shows high prevalence of total parasites throughout the year. For Ancylostoma spp., summer and autumn might be the seasons with higher sanitary risk. On the other hand, T. canis could present the higher risk to people in winter and, T. vulpis, would be transmitted throughout the whole year. The seasonal variation in prevalence of dog parasites results in continuous exposure to people visiting the squares, not only Mar del Plata residents but also tourists from other regions of Argentina and the world, with at least one species of parasite with sanitary risk.

Canine gastrointestinal parasitic zoonoses in India.

Although well recognized and studied in developed countries, canine parasitic zoonoses pose a lowly prioritized public health problem in developing countries such as India, where conditions are conducive for transmission. A study of the most recent parasite survey determining prevalence and epidemiology of canine parasitic zoonoses among tea-growing communities of northeast India demonstrated the endemicity of the problem. This particular study serves as a model using conventional, as well as molecular parasitological, tools to provide novel insights into the role of dogs as mechanical transmitters of human parasites such as Ascaris and Trichuris, and discusses the risks dogs pose with regards to zoonotic transmission of hookworms and Giardia.