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A systematic review and meta-analysis of canine, feline and human Toxocara infections in sub-Saharan Africa

Published online by Cambridge University Press:  04 November 2019

A.O. OmonijoOpen the ORCID record for A.O. Omonijo[Opens in a new window],
C. Kalinda and
S. Mukaratirwa
A.O. Omonijo*
Affiliation:
School of Life Sciences, College of Agriculture, Engineering and Science, University of KwaZulu-Natal, Westville Campus, Durban, South AfricaDepartment of Animal and Environmental Biology, Faculty of Science, Federal University Oye, Ekiti, Ekiti State, Nigeria
C. Kalinda
Affiliation:
Faculty of Agriculture and Natural Resources, University of Namibia, Katima Mulilo Campus, PB 1096 Katima Mulilo, NamibiaSchool of Nursing and Public Health, College of Health Sciences, University of KwaZulu-Natal, Howard College Campus, Durban, South Africa
S. Mukaratirwa
Affiliation:
School of Life Sciences, College of Agriculture, Engineering and Science, University of KwaZulu-Natal, Westville Campus, Durban, South Africa
*
Author for correspondence: A.O. Omonijo, E-mail: earnesthope@yahoo.com
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Abstract

Toxocariasis is an emerging zoonotic disease caused by Toxocara canis and T. cati. Toxocariasis and its etiological agents are of global public health importance, whose burden appears underestimated, especially in sub-Saharan Africa (SSA). The diversity in the transmission routes of these parasites contributes to disease prevalence and often hinders disease control measures. This study aimed to review the epidemiological distribution of Toxocara infections in SSA region. A systematic review and meta-analysis were performed using PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analysis). We identified 94 relevant, peer-reviewed articles, out of which, 75 articles were found eligible based on Toxocara infections in dogs, cats and humans. Overall, 27,102 samples were examined for T. canis in dogs, T. cati in cats and Toxocara serology in humans, out of which 6142 were positive for Toxocara infection: 3717 (13.7%) in dogs (faecal, 3487; necropsy, 180; hair, 50); 266 (1%) in cats (faecal, 101; necropsy, 165); and 2159 (8%) in humans (serology). Overall mean prevalences of 19% (95% confidence interval (CI): 14–23%), 9% (95% CI: 0–28%) and 36% (95% CI: 24–49%) were recorded in dogs, cats and humans, respectively. Substantial heterogeneity was observed between studies and subgroups (I2 = 99%, P < 0.01). Findings from the review showed that studies on the epidemiology of Toxocara infections in the SSA region are limited. We strongly recommend focused, collaborative and coordinated studies to determine Toxocara spp. prevalence in various hosts, including food animals and the environment, through a ‘One Health’ approach across SSA countries.

Keywords

Prevalencereviewrisk factorssub-Saharan AfricaToxocara infectionsmeta-analysiszoonosis

Information

Type
Review Article
Information
Journal of Helminthology , Volume 94 , 2020, e96
Copyright
Copyright © Cambridge University Press 2019 

Introduction

Toxocariasis is a zoonosis of global public health significance caused by Toxocara canis (canid roundworm) and T. cati (felid roundworm) (Luna et al., Reference Luna, Cicero and Rateau2018). Toxocara infections have been reported globally, with prevalence ranging from 1.6–93% in humans and 3.7–87.1% in soil, to 1.2–100% in definitive canid and felid hosts (Magnaval et al., Reference Magnaval, Michault, Calon and Charlet1994; Mukaratirwa & Taruvinga, Reference Mukaratirwa and Taruvinga1999; Quattrocchi et al., Reference Quattrocchi, Nicoletti, Marin, Bruno, Druet-Cabanac and Preux2012; Okewole, Reference Okewole2016; Ma et al., Reference Ma, Holland, Wang, Hofmann, Fan, Maizels, Hotez and Gasser2018). The disease burden is high in sub-Saharan African regions where poor hygiene practices and poor veterinary care of pets are prevalent (Liao et al., Reference Liao, Sukati and D'lamini2010; Ma et al., Reference Ma, Holland, Wang, Hofmann, Fan, Maizels, Hotez and Gasser2018). Toxocariasis burden is exacerbated due to the several transmission routes of the parasite via a wide range of invertebrates and vertebrate reservoir hosts, including earthworms, insects, land snails, rodents, birds and food animals (poultry, pigs, lamb, goats and cattle), which contribute to parasite maintenance in the environment (Pahari & Sasmal, Reference Pahari and Sasmal1991; Taira et al., Reference Taira, Saeed, Permin and Kapel2004; Antolová et al., Reference Antolová, Reiterová, Stanko, Zalesny, Fričová and Dvorožňáková2013; Fialho & Corrêa, Reference Fialho and Corrêa2016).

In humans, infection is acquired via waterborne or foodborne route via consumption of contaminated water, foods and vegetables, and/or geophagia (Salem & Schantz, Reference Salem and Schantz1992; Yoshikawa et al., Reference Yoshikawa, Nishiofuku and Moriya2008; Macpherson, Reference Macpherson2013; Fialho & Corrêa, Reference Fialho and Corrêa2016; Zibaei et al., Reference Zibaei, Sadjjadi and Maraghi2017; McManus et al., Reference McManus, Hamilton and Holland2018). There is substantial evidence of a strong association between human toxocariasis and the consumption of undercooked/raw meat viscera of food animals among people with such dietary habits in countries like Japan and Korea (Choi et al., Reference Choi, Lim, Choi, Lee, Paik, Kim, Choi and Huh2012; Yoshida et al., Reference Yoshida, Hombu, Wang and Maruyama2016). In definitive hosts, Toxocara infections occur via several routes, including the accidental ingestion of infective eggs from a contaminated environment, the consumption of infective larvae via predator–prey interactions, mainly in felids, and transmission via lactogenic (canids and felids) and/or transplacental (in canids) transfer (Macpherson, Reference Macpherson2013; Overgaauw & van Knapen, Reference Overgaauw and van Knapen2013).

In the definitive hosts, the larvae hatch in the small intestine and migrate via the liver, heart and lungs through the circulatory system, during which the larvae enter the trachea from the lungs through the bronchus and reach the pharynx where they are re-ingested and reach the small intestine where maturity is attained (Selek et al., Reference Selek, Karagoz and Baylan2016). Un-embryonated eggs are voided with faeces in 4–5 weeks post-infection in dogs (Schnieder et al., Reference Schnieder, Laabs and Welz2011) and in eight weeks post-infection in cats (Sprent, Reference Sprent1956). If larvae are ingested from infected paratenic hosts where lifecycle migration has been satisfied, migration no longer holds in definitive hosts; rather, the larvae are released and develop to maturity in the small intestine (Overgaauw & van Knapen, Reference Overgaauw and van Knapen2013).

Both adults and migrating larvae of Toxocara spp. are pathogenic, causing a variety of pathological conditions in the definitive hosts (Fisher, Reference Fisher2014). Toxocara cati infections in cats are associated with increased eosinophils in blood and bronchoalveolar fluid and peribronchiolar opacity (Dillon et al., Reference Dillon, Tillson and Hathcock2013), while T. canis causes eosinophilic gastroenteritis and focal lesions in a variety of tissues, including the liver and lungs (Fisher, Reference Fisher2014), as well as retinitis by migrating larvae (Schnieder et al., Reference Schnieder, Laabs and Welz2011; Cooper et al., Reference Cooper, Ahonen, Rowlan, Duncan, Seppälä, Vanhapelto, Lohi and Komáromy2014). In humans, only the migrating larvae are pathogenic, causing a varying degree of morbidities depending on the affected organs, infection intensity and duration, host age and immunity status of the infected host (Holland & Hamilton, Reference Holland and Hamilton2013; Lee et al., Reference Lee, Moore, Bottazzi and Hotez2014; Fan et al., Reference Fan, Holland, Loxton and Barghouth2015). Clinical manifestations include ocular larva migrans, visceral larva migrans, covert or common toxocariasis and neurotoxocariasis (González-García et al., Reference González-García, Muñoz-Guzmán, Sánchez-Arroyo, Prado-Ochoa, Cuéllar-Ordaz and Alba-Hurtado2017; Ma et al., Reference Ma, Holland, Wang, Hofmann, Fan, Maizels, Hotez and Gasser2018). Other toxocariasis-associated manifestations are reduced cognitive function in children, poor academic performance, perpetuation of poverty in affected communities and health disparities in endemic areas (Walsh & Haseeb, Reference Walsh and Haseeb2012; Lee et al., Reference Lee, Moore, Bottazzi and Hotez2014).

Diagnosis of Toxocara infection in non-definitive hosts includes histopathological examination for larvae in suspected tissues, and morphometric assessment of larvae, or the specific detection of larval DNA from tissue or body fluid samples (Smith & Noordin, Reference Smith and Noordin2006; Machado et al., Reference Machado, De Araujo and De Leão E Neves Eduardo2017; Ma et al., Reference Ma, Holland, Wang, Hofmann, Fan, Maizels, Hotez and Gasser2018). In definitive hosts, infection is diagnosed by the morphological identification of eggs in faeces (Machado et al., Reference Machado, De Araujo and De Leão E Neves Eduardo2017). Recent advancements in molecular technology and applications has enhanced the specific identification of Toxocara spp., which has contributed immensely to research in clinical toxocariasis and epidemiological studies (Smith et al., Reference Smith, Holland, Taylor, Magnaval, Schantz and Maizels2009; Strube et al., Reference Strube, Heuer and Janecek2013; Poulsen et al., Reference Poulsen, Skov, Yoshida, Skallerup, Maruyama, Thamsborg and Nejsum2015; Ma et al., Reference Ma, Holland, Wang, Hofmann, Fan, Maizels, Hotez and Gasser2018).

Despite the availability of improved diagnostic tools and increasing global awareness of the public health importance of Toxocara spp., there is still limited information on the epidemiology of infections in sub-Saharan Africa (SSA). In order to recognize the public health importance and status of toxocariasis in SSA, it is important that the available information on epidemiology and incidence in animals, humans and the environment within sub-Saharan regions be assessed and analysed. Therefore, this review focused on the systematic review and analysis of existing studies on Toxocara infection in SSA, to determine the epidemiological distribution of infection in various hosts in the region and identify research gaps for future research.

Methods

Search strategy

A systematic search was conducted in the search engines Google Scholar, PubMed, AJOL and EBSCO Host database using the following terms and Boolean operators (AND, OR): Toxocara cati AND Toxocara canis, Toxocara in dogs OR humans AND sub-Saharan Africa, Toxocara in cats AND sub-Saharan Africa, Toxocara in soil, visceral larva migrans AND ocular larva migrans. The titles and abstracts of the search results were perused for the selection of relevant articles. References within the identified articles were additionally used as a guide to other literature. The literature search was concluded in May 2018. Full-text articles were retrieved and managed in Endnote reference manager, version X7 (Clarivate Analytics, Philadelphia, PA, USA).

Inclusion and exclusion criteria

An article was included in this study if it was published between 1979 and 2018 in a peer-reviewed journal and reported on (1) prevalence of T. canis in dogs and/or T. cati in cats, and/or T. canis/T. cati in soil in sub-Saharan African countries; and (2) Toxocara serology in humans. Grey literatures, dead links and duplicate results were excluded during the abstract review.

Quality assessment

A tool developed by Munn et al. (Reference Munn, Moola, Lisy, Riitano and Tufanaru2015) was used to assess the quality of the selected articles for inclusion in the meta-analysis. The tool was modified to suit the kind of information that we desired to extract from the articles. Each article was assessed based on the following: (1) if the research objective(s) were relevant to the study; (2) if the prevalence of Toxocara was the main objective of the study; (3) if the study design was appropriately defined (observation, cross-sectional); (4) if the samples were randomly selected; (5) if the study subjects were categorized by age/sex where relevant; (6) if the study used valid diagnostic methods; (7) if the method(s) of diagnosis were conducted in a reliable and replicable way; (8) if the target sample was representative of the general population; (9) if the endemic status of Toxocara infection in the study community/animals was described; and (10) if the history of prior treatment of subjects for Toxocara infection was described (supplementary file S1). The quality index score for each article was calculated by dividing the study quality score by ten.

Data extraction

From each paper that had been selected for inclusion, we extracted data on the country the study was conducted, study period, the type of study subjects or hosts (dogs, cats, humans), the sample size, number of infected subjects/hosts, Toxocara spp., the percentage prevalence and the diagnostic method(s) used.

Data analysis

All of the data extracted from the search were entered in Microsoft Excel for analysis. The MetaXL add-in for Microsoft Excel (www.epigear.com) was used to carry out a meta-analysis. Prevalence estimates with their 95% confidence intervals (CIs) and heterogeneity were computed using the quality-effect model. Heterogeneity was quantified using the inverse variance statistic (I 2 index) and we tested for its significance using Cochran's Q test. The I 2 index was interpreted as no, low, moderate or high heterogeneity if the value was 0%, ≤25%, 50% or ≥75%, respectively. Forest plots were generated to show the prevalence of Toxocara among the study subjects. Furthermore, subgroup analysis was carried out to assess the mean pooled prevalence estimates according to host types and regions within SSA. The Luis Furuya–Kanamori (LFK) index and funnel plot were used to assess the risks of publication bias (Barendregt & Doi, Reference Barendregt and Doi2016). We determined the symmetry of the Doi plots using the LFK index. An LFK value within the range of ‘±1’ was considered as ‘symmetrical’ and classified as absence of publication bias, while an LFK value within the range of ‘±2’ was considered as minor asymmetry with slight publication bias and an LFK value outside the range of ‘±2’ was considered as major asymmetry and high publication bias (Barendregt & Doi, Reference Barendregt and Doi2016).

Results

Search results

A total of 94 articles were obtained from the literature search, of which 11 articles were excluded after the title and abstract inspection. Articles were further read and assessed for inclusion. Eight studies were subsequently excluded due to lack of a valid diagnostic method to determine Toxocara species. Overall, 75 articles were included in the meta-analysis.

Study quality assessment

The quality index of the eligible articles selected ranged from 0.3 to 0.9. A variety of diagnostic methods used to detect Toxocara eggs in the studies are shown in the supplementary material (supplementary tables S1a–c, S2 and S3a, b). Different sampling methods for the study hosts were also used and sample sizes of the selected studies ranged from 200–384 (faecal) and 200–1502 (necropsy) in cats, 20–1647 (faecal) and 12–539 (necropsy) in dogs, to 40–601 (serology) in humans. Studies from the articles selected were conducted in Central Africa, East Africa, Southern Africa and West Africa within the SSA region. Data were derived from only 16 sub-Saharan countries, with most data from studies conducted in Nigeria (39). Other countries had less than ten studies (supplementary tables S1a–c, S2 and S3a, b).

Meta-analysis

Prevalence of T. canis

A total of 18,463 samples were examined for T. canis, and, of these, 16,857 were obtained from faecal, 1189 from necropsy and 417 from hair. Summaries of studies on the prevalence of T. canis in dogs in the SSA region are shown in the supplementary material (supplementary table S1a–c). Out of the total samples examined, 3717 (20.1%) (faecal = 3487; necropsy = 180; hair = 50) were positive for T. canis infection. Toxocara canis infection in the SSA region gave an overall prevalence of 19% (95% CI: 14–23%). Substantial heterogeneity was observed between studies (I 2 = 98%, P < 0.01). Among the regions within SSA, Central Africa had the highest prevalence of 35% (95% CI: 30–41%) for T. canis, followed by East Africa, which had a prevalence of 31% (95% CI: 20–43%). Southern Africa had the least prevalence of 11% (95% CI: 5–18%).

Prevalence of T. cati

Out of a total sample size of 2625 cases of T. cati, (faecal = 584; necropsy = 2041) that were examined, 266 (faecal = 101; necropsy = 165) were positive, with an overall prevalence estimate of 9% (95% CI: 0.00–28%). A summary of studies on the prevalence of T. cati in the SSA region is shown in the supplementary material (supplementary table S2). A high degree of heterogeneity was observed between studies (I 2 = 99%, P < 0.01). Regional subgroup analysis was not carried out, as only three studies mentioned the species of Toxocara.

Toxocara serology in humans

A summary of studies on Toxocara serology in humans in the SSA region is shown in the supplementary material (supplementary table S3a, b). Out of a total of 6014 serum samples that were examined, in humans in the SSA region, 2159 were positive for Toxocara serology, with an overall prevalence of 36% (95% CI: 24–49%). Central Africa had the highest prevalence of 73% (95% CI: 41–99%), followed by West Africa with a prevalence of 49% (95% CI: 25–72%). South Africa had the least prevalence of 11% (95% CI: 1–24%). Substantial heterogeneity was observed between studies (I 2 = 99%, P < 0.01).

Discussion

Toxocariasis is a major public health challenge that poses a serious health concern in both developed and developing countries (Fakhri et al., Reference Fakhri, Gasser, Rostami, Fan, Ghasemi, Javanian, Bayani, Armoon and Moradi2018). The disease burden is high in SSA regions due to the existence of favourable transmission factors such as pet ownership with poor veterinary care, poor personal hygiene, socio-economic factors (poor sanitation level in disadvantaged areas) and favourable climatic conditions (humid and warm climate) for the embryonation and survival of Toxocara eggs (Liao et al., Reference Liao, Sukati and D'lamini2010; Gawor et al., Reference Gawor, Borecka, Marczyńska, Dobosz and Żarnowska-Prymek2015, Ma et al., Reference Ma, Holland, Wang, Hofmann, Fan, Maizels, Hotez and Gasser2018). This study revealed that only one-third of sub-Saharan countries have reported on the prevalence of Toxocara infections in dogs, cats and humans. The prevalence of Toxocara spp. in SSA has been associated with geographic regions with favourable climatic conditions (Fakhri et al., Reference Fakhri, Gasser, Rostami, Fan, Ghasemi, Javanian, Bayani, Armoon and Moradi2018), which probably explains the highest mean prevalence of Toxocara infections observed in Central Africa due to its location near the north of the equator, with optimum environmental conditions (Nguyen & Duvel, Reference Nguyen and Duvel2008). In the environment, the development of eggs of Toxocara spp. directly correlates with humidity (Gamboa, Reference Gamboa2005) and temperatures ranging between 23°C and 35°C, with limited development occurring at ≤17°C (Rocha et al., Reference Rocha, Pinto, Floriano, Teixeira, Bassili, Martinez, Costa and Caseiro2011).

Moreover, this review has revealed that T. canis is widely and more commonly reported in dogs than T. cati is in cats. Studies have established that dogs, mainly puppies in the close environment, are associated with the efficient transfer of T. canis (Glickman & Schantz, Reference Glickman and Schantz1981; Barriga, Reference Barriga1988; Macpherson, Reference Macpherson2013; Ferreira et al., Reference Ferreira, Pena, Azevedo, Labruna and Gennari2016; Panova & Khrustalev, Reference Panova and Khrustalev2018). Puppies acquire infections via transplacental and transmammary routes, and are capable of shedding millions of eggs per day in less than three weeks after birth, thereby making them epidemiological reservoirs of T. canis in the environment (da Cunha Amaral et al., Reference da Cunha Amaral, Rassier, Pepe, Gallina, Villela, De Oliveira Nobre, Scaini and Berne2010; Macpherson, Reference Macpherson2013; Ferreira et al., Reference Ferreira, Pena, Azevedo, Labruna and Gennari2016; McManus et al., Reference McManus, Hamilton and Holland2018). The efficient control of Toxocara infections, therefore, hinges upon control measures that target the elimination of the intestinal stage of T. canis populations in puppies and the sustained killing of the reservoir larvae in the tissues of bitches through the regular administration of effective anthelmintics (Barriga, Reference Barriga1988). However, the regular administration of anthelmintics may pose problems of cost to pet owners, making this a less feasible and efficient control measure; hence, an effective anti-T. canis vaccine has been proposed to become a reality in the foreseeable future (Barriga, Reference Barriga1988; Ma et al., Reference Ma, Holland, Wang, Hofmann, Fan, Maizels, Hotez and Gasser2018).

Also, dogs’ hair, paws and their free-roaming habits (especially stray dogs) have been reported to largely contribute to environmental contamination with T. canis (Panova & Khrustalev, Reference Panova and Khrustalev2018; Sivajothi & Reddy, Reference Sivajothi and Reddy2018). Although studies have reported the recovery of T. canis eggs in the hair of both owned and stray dogs (Wolfe & Wright, Reference Wolfe and Wright2003; 2008; Aydenizöz-özkayhan et al., Reference Aydenizöz-özkayhan, Yağcı and Erat2008; Roddie et al., Reference Roddie, Stafford, Holland and Wolfe2008), these are probably acquired through the dogs’ habits of scent rolling on diarrheal stools (Keegan & Holland, Reference Keegan and Holland2010; Lee et al., Reference Lee, Schantz, Kazacos, Montgomery and Bowman2010; Merigueti et al., Reference Merigueti, Santarém, Ramires, Da Silveira Batista, Da Costa Beserra, Nuci and De Paula Esposte2017). However, most recovered eggs were less viable due to desiccation by direct sunlight (Overgaauw et al., Reference Overgaauw, Van Zutphen, Hoek, Yaya, Roelfsema, Pinelli, Van Knapen and Kortbeek2009). Low viability of Toxocara spp. eggs and their adhesive nature to dog or cat hair make them difficult to remove, which lessens the likelihood of them being accidentally swallowed by humans (Overgaauw et al., Reference Overgaauw, Van Zutphen, Hoek, Yaya, Roelfsema, Pinelli, Van Knapen and Kortbeek2009; Keegan & Holland, 2010). Generally, the observed prevalence of T. canis eggs from dogs in SSA obtained in this study 19% (95% CI: 14-23%) was higher than the 1.8–2.0% prevalence reported in the US (Lucio-Forster et al., Reference Lucio-Forster, Barbecho, Mohammed, Kornreich and Bowman2016). Thus, findings from this study underscore the role of dogs in the epidemiology of toxocariasis.

Similarly, studies have shown that cats are associated with a considerable level of environmental contamination with T. cati eggs (Fisher, Reference Fisher2003; Morgan et al., Reference Morgan, Azam and Pegler2013; Nijsse et al., Reference Nijsse, Mughini-Gras, Wagenaar, Franssen and Ploeger2015). Unlike dogs, cats do not show age-resistance and are more prey-eaters, which results in a direct development of egg-producing Toxocara worms without having a somatic migration (Overgaauw & van Knapen, Reference Overgaauw and van Knapen2013; Nijsse et al., Reference Nijsse, Ploeger, Wagenaar and Mughini-Gras2016). However, this study showed that studies on the epidemiology of T. cati are limited in SSA regions. This is consistent with the assumption that studies on helminth infections in cats are scarce (Fisher, Reference Fisher2003; Mircean et al., Reference Mircean, Titilincu and Vasile2010; Beugnet et al., Reference Beugnet, Bourdeau and Chalvet-Monfray2014; Nijsse et al., Reference Nijsse, Ploeger, Wagenaar and Mughini-Gras2016). The mean prevalence (9%) of T. cati observed in this study is lower than the mean prevalence (19.7%) reported in Europe (Beugnet et al., Reference Beugnet, Bourdeau and Chalvet-Monfray2014); however, it is comparable to the observed prevalence in the US (Gates & Nolan, Reference Gates and Nolan2009). The limited data on cats from this region may not imply a less contributory role in toxocariasis; rather, observed heterogeneity may be attributed to inaccessibility to cat faeces due to their defecation habit of burying faeces, thus making T. cati appear as less prevalent than T. canis (Nijsse et al., Reference Nijsse, Ploeger, Wagenaar and Mughini-Gras2016; Subrata et al., Reference Subrata, Oka and Agustina2017). A recent study conducted in the US observed the prevalence of T. cati in faecal samples from cats to be approximately 3% higher than in faecal samples from dogs in the same region (Lucio-Forster et al., Reference Lucio-Forster, Barbecho, Mohammed, Kornreich and Bowman2016). While this may not be generalized to all regions, it probably suggests that cats may be contributing more to toxocariasis than the available records in this review suggested.

There is poor understanding of the global impact and economic cost of human toxocariasis due to insufficient clinical awareness and unclear repository for the efficacy of clinical, laboratory and treatment interventions (Smith et al., Reference Smith, Holland, Taylor, Magnaval, Schantz and Maizels2009). Most of the studies on Toxocara serology were associated with epilepsy and asthma and, as such, results were reported as odds ratios (Quattrocchi et al., Reference Quattrocchi, Nicoletti, Marin, Bruno, Druet-Cabanac and Preux2012; Aghaei et al., Reference Aghaei, Riahi, Rostami, Mohammadzadeh, Javanian, Tohidi, Foroutan and Dooki2018). The highest seroprevalence estimate observed in Central Africa could be explained as a statistical bias arising from limited studies from the region. The seroprevalence estimate of 49% observed in West Africa may, however, be attributed to risk factors such as geophagia, older age of study subjects, lack of potable water, consumption of raw vegetables, inadequate hygiene, contacts with pets and keeping pets (Kyei et al., Reference Kyei, Ayi, Boampong and Turkson2015; Lötsch et al., Reference Lötsch, Vingerling, Spijker and Grobusch2017). Findings from this study are comparable with other results from the sub-Saharan region (Lötsch et al., Reference Lötsch, Vingerling, Spijker and Grobusch2017). A lack of focused studies on Toxocara serology in humans and the lack of a test to distinguish T. canis and T. cati infections indicate a public health underestimation of the Toxocara parasite in the SSA region. Such studies are needed to evaluate the relationship between exposure, seroprevalence and disease symptoms in human toxocariasis in SSA.

This analysis showed a substantial heterogeneity between studies and subgroups, which may be attributed to varying sampling techniques adopted by different studies, sociocultural beliefs, hygiene practices of people, level of awareness, degree of pet care, host age, human and animal bonding (Fakhri et al., Reference Fakhri, Gasser, Rostami, Fan, Ghasemi, Javanian, Bayani, Armoon and Moradi2018; Ma et al., Reference Ma, Holland, Wang, Hofmann, Fan, Maizels, Hotez and Gasser2018). The implication of this is that, despite the epidemiological information on Toxocara prevalence provided by this review, it may not be representing the true prevalence of Toxocara in the SSA region due to factors such as limited studies from some regions in SSA as well as unequal distribution of studies across the regions.

This study revealed a paucity of information on the prevalence of Toxocara spp. in a wide variety of hosts including food animals such as poultry, pigs, lamb, goats and cattle in SSA regions. Food animals are known to be zoonotic agents of several helminths of public health importance, including Toxocara spp. (Karshima, Reference Karshima2019). This transmission route is particularly of concern among communities with a cultural habit of consuming raw or undercooked meat viscera, thereby contributing significantly to the prevalence of human toxocariasis (Robertson et al., Reference Robertson, Sprong, Ortega, Van Der Giessen and Fayer2014). Therefore, understanding the epidemiology of Toxocara spp. in food animals and diverse hosts will be of importance in devising and implementing toxocariasis control measures.

Limitations

The major diagnostic methods employed in faecal analysis were mainly qualitative and, as a result, the intensity of infections could not be ascertained in the meta-analysis. Also, the lack of application of molecular techniques in identifying Toxocara spp. to species level resulted in the exclusion of some studies; thereby, the epidemiology of Toxocara spp. in the environment could not be determined.

Conclusions

Despite these limitations, this study revealed that the prevalence of Toxocara infections in the SSA region are under-reported, and underscores the need to intensify awareness on and the need to practice good hygiene and adequate cooking of vegetables and meat, which are imperative in toxocariasis control. Also, there is the need to embark on more epidemiological studies in order to provide more insight into the transmission routes of Toxocara spp., understand disease prevalence and spatial distribution. Furthermore, policies that ensure proper care for pets are imperative to avoid stray animals contaminating the environment, as well as regular anthelmintic treatment of pets. The application of molecular techniques in species identification is imperative in order to understand the epidemiology of Toxocara spp. Lastly, there is a need for focused and collaborative studies in order to measure exposure in the human population, disease states and reservoirs of infection in animals and the environment through a ‘One Health’ approach across SSA countries.

Supplementary material

To view supplementary material for this article, please visit https://doi.org/10.1017/S0022149X19000889.

Acknowledgement

The authors would like to thank the National Research Foundation of South Africa who awarded A.O.O. a bursary for her PhD studies.

Financial support

This study is based on the research supported wholly by the National Research Foundation of South Africa (Grant Numbers: 113036).

Conflicts of interest

None.

References

Aghaei, S, Riahi, SM, Rostami, A, Mohammadzadeh, I, Javanian, M, Tohidi, E, Foroutan, M and Dooki, ME (2018) Toxocara spp. infection and risk of childhood asthma: a systematic review and meta-analysis. Acta Tropica 182, 298–304.Google Scholar
Antolová, D, Reiterová, K, Stanko, M, Zalesny, G, Fričová, J and Dvorožňáková, E (2013) Small mammals: paratenic hosts for species of Toxocara in eastern Slovakia. Journal of Helminthology 87, 52–58.Google Scholar
Aydenizöz-özkayhan, M, Yağcı, B and Erat, S (2008) The investigation of Toxocara canis eggs in coats of different dog breeds as a potential transmission route in human toxocariasis. Veterinary Parasitology 152, 94–100.Google Scholar
Barendregt, JJ and Doi, SA (2016) MetaXL user guide. Version 4, 2011–2016.Google Scholar
Barriga, OO (1988) A critical look at the importance, prevalence and control of toxocariasis and the possibilities of immunological control. Veterinary Parasitology 29, 195–234.Google Scholar
Beugnet, F, Bourdeau, P, Chalvet-Monfray, K, et al. (2014) Parasites of domestic owned cats in Europe: co-infestations and risk factors. Parasites & Vectors 7, 291.Google Scholar
Choi, D, Lim, JH, Choi, D-C, Lee, KS, Paik, SW, Kim, S-H, Choi, Y-H and Huh, S (2012) Transmission of Toxocara canis via ingestion of raw cow liver: a cross-sectional study in healthy adults. The Korean Journal of Parasitology 50(1), 23–27.Google Scholar
Cooper, AE, Ahonen, S, Rowlan, JS, Duncan, A, Seppälä, EH, Vanhapelto, P, Lohi, H and Komáromy, AM (2014) A novel form of progressive retinal atrophy in Swedish Vallhund dogs. PloS One 9(9), 1–10.Google Scholar
da Cunha Amaral, HL, Rassier, GL, Pepe, MS, Gallina, T, Villela, MM, De Oliveira Nobre, M, Scaini, CJ and Berne, MEA (2010) Presence of Toxocara canis eggs on the hair of dogs: a risk factor for Visceral Larva Migrans. Veterinary Parasitology 174(1-2), 115–118.Google Scholar
Dillon, AR, Tillson, D, Hathcock, J, et al. (2013) Lung histopathology, radiography, high-resolution computed tomography, and bronchio-alveolar lavage cytology are altered by Toxocara cati infection in cats and is independent of development of adult intestinal parasites. Veterinary Parasitology 193, 413–426.Google Scholar
Fakhri, Y, Gasser, R, Rostami, A, Fan, C, Ghasemi, S, Javanian, M, Bayani, M, Armoon, B and Moradi, B (2018) Toxocara eggs in public places worldwide-A systematic review and meta-analysis. Environmental Pollution 242, 1467–1475.Google Scholar
Fan, C-K, Holland, CV, Loxton, K and Barghouth, U (2015) Cerebral toxocariasis: silent progression to neurodegenerative disorders? Clinical Microbiology Reviews 28(3), 663–686.Google Scholar
Ferreira, JIGDS, Pena, HFJ, Azevedo, SS, Labruna, MB and Gennari, SM (2016) Occurrences of gastrointestinal parasites in fecal samples from domestic dogs in São Paulo, SP, Brazil. Revista Brasileira de Parasitologia Veterinária 25(4), 435–440.Google Scholar
Fialho, PMM and Corrêa, CRS (2016) A systematic review of toxocariasis: a neglected but high-prevalence disease in Brazil. The American Journal of Tropical Medicine and Hygiene 94, 1193–1199.Google Scholar
Fisher, M (2003) Toxocara cati: an underestimated zoonotic agent. Trends in Parasitology 19(4), 167–170.Google Scholar
Fisher, M (2014) Update on Toxocara spp. and toxocarosis. Companion Animal 19(9), 465–468.Google Scholar
Gamboa, M (2005) Effects of temperature and humidity on the development of eggs of Toxocara canis under laboratory conditions. Journal of Helminthology 79(4), 327–331.Google Scholar
Gates, MC and Nolan, TJ (2009) Endoparasite prevalence and recurrence across different age groups of dogs and cats. Veterinary Parasitology 166, 153–158.Google Scholar
Gawor, J, Borecka, A, Marczyńska, M, Dobosz, S and Żarnowska-Prymek, H (2015) Risk of human toxocarosis in Poland due to Toxocara infection of dogs and cats. Acta Parasitologica 60, 99–104.Google Scholar
Glickman, LT and Schantz, PM (1981) Epidemiology and pathogenesis of zoonotic toxocariasis. Epidemiologic Reviews 3, 230–250.Google Scholar
González-García, T, Muñoz-Guzmán, M, Sánchez-Arroyo, H, Prado-Ochoa, M, Cuéllar-Ordaz, J and Alba-Hurtado, F (2017) Experimental transmission of Toxocara canis from Blattella germanica and Periplaneta americana cockroaches to a paratenic host. Veterinary Parasitology 246, 5–10.Google Scholar
Holland, CV and Hamilton, CM (2013) The significance of cerebral toxocariasis: a model system for exploring the link between brain involvement, behaviour and the immune response. Journal of Experimental Biology 216, 78–83.Google Scholar
Karshima, S (2019) Helminths of zoonotic importance in slaughtered food animals in Nigeria: a systematic review and meta-analysis. Journal of Helminthology 93(3), 295–305.Google Scholar
Keegan, JD and Holland, CV (2010) Contamination of the hair of owned dogs with the eggs of Toxocara spp. Veterinary Parasitology 173(1-2), 161–164.Google Scholar
Kyei, G, Ayi, I, Boampong, J and Turkson, P (2015) Sero-epidemiology of Toxocara canis infection in children attending four selected health facilities in the central region of Ghana. Ghana Medical Journal 49(2), 77–83.Google Scholar
Lee, AC, Schantz, PM, Kazacos, KR, Montgomery, SP and Bowman, DD (2010) Epidemiologic and zoonotic aspects of ascarid infections in dogs and cats. Trends in Parasitology 26, 155–161.Google Scholar
Lee, RM, Moore, LB, Bottazzi, ME and Hotez, PJ (2014) Toxocariasis in North America: a systematic review. PLoS Neglected Tropical Diseases 8(8), e3116.Google Scholar
Liao, C-W, Sukati, H, D'lamini, P, et al. (2010) Seroprevalence of Toxocara canis infection among children in Swaziland, southern Africa. Annals of Tropical Medicine & Parasitology 104, 73–80.Google Scholar
Lötsch, F, Vingerling, R, Spijker, R and Grobusch, MP (2017) Toxocariasis in humans in Africa–A systematic review. Travel Medicine and Infectious Diseases 20, 15–25.Google Scholar
Lucio-Forster, A, Barbecho, JSM, Mohammed, HO, Kornreich, BG and Bowman, DD (2016) Comparison of the prevalence of Toxocara egg shedding by pet cats and dogs in the USA, 2011–2014. Veterinary Parasitology: Regional Studies and Reports 5, 1–13.Google Scholar
Luna, J, Cicero, CE, Rateau, G et al. (2018) Updated evidence of the association between toxocariasis and epilepsy: Systematic review and meta-analysis. PLoS Neglected Tropical Diseases 12(7), e0006665.Google Scholar
Ma, G, Holland, CV, Wang, T, Hofmann, A, Fan, C-K, Maizels, RM, Hotez, PJ and Gasser, RB (2018) Human toxocariasis. The Lancet Infectious Diseases 18(1), e14–e24.Google Scholar
Machado, ER, De Araujo, LB and De Leão E Neves Eduardo, A (2017) Human toxocariasis: secondary data analysis. Annals of Clinical Cytolology and Pathology 3(6), 1075.Google Scholar
Macpherson, CN (2013) The epidemiology and public health importance of toxocariasis: a zoonosis of global importance. International Journal for Parasitology 43(12-13), 999–1008.Google Scholar
Magnaval, J-F, Michault, A, Calon, N and Charlet, J-P (1994) Epidemiology of human toxocariasis in La Reunion. Transactions of the Royal Society of Tropical Medicine and Hygiene 88(5), 531–533.Google Scholar
McManus, R, Hamilton, CM and Holland, CV (2018) Toxocara spp. in: Rose JB and Jiménez-Cisneros B (Eds) Global Water Pathogen Project. http://www.waterpathogens.org (Robertson L (Eds) Part 4 Helminths) http://www.waterpathogens.org/book/toxocara Michigan State University, E. Lansing, MI, UNESCO.Google Scholar
Merigueti, YFFB, Santarém, VA, Ramires, LM, Da Silveira Batista, A, Da Costa Beserra, LV, Nuci, AL and De Paula Esposte, TM (2017) Protective and risk factors associated with the presence of Toxocara spp. eggs in dog hair. Veterinary Parasitology 244, 39–43.Google Scholar
Mircean, V, Titilincu, A and Vasile, C (2010) Prevalence of endoparasites in household cat (Felis catus) populations from Transylvania (Romania) and association with risk factors. Veterinary Parasitology 171(1-2), 163–166.Google Scholar
Morgan, E, Azam, D and Pegler, K (2013) Quantifying sources of environmental contamination with Toxocara spp. eggs. Veterinary Parasitology 193(4), 390–397.Google Scholar
Mukaratirwa, S and Taruvinga, M (1999) A survey on environmental contamination of suburban parks and playgrounds in Harare, Zimbabwe, with canine helminths of zoonotic significance. Journal of the South African Veterinary Association 70(3), 119–121.Google Scholar
Munn, Z, Moola, S, Lisy, K, Riitano, D and Tufanaru, C (2015) Methodological guidance for systematic reviews of observational epidemiological studies reporting prevalence and cumulative incidence data. International Journal of Evidence-Based Health Care 13(3), 147–153.Google Scholar
Nguyen, H and Duvel, JP (2008) Synoptic wave perturbations and convective systems over equatorial Africa. Journal of Climate 21, 6372–6388.Google Scholar
Nijsse, R, Mughini-Gras, L, Wagenaar, JA, Franssen, F and Ploeger, HW (2015) Environmental contamination with Toxocara eggs: a quantitative approach to estimate the relative contributions of dogs, cats and foxes, and to assess the efficacy of advised interventions in dogs. Parasites & Vectors 8, 397.Google Scholar
Nijsse, R, Ploeger, H, Wagenaar, J and Mughini-Gras, L (2016) Prevalence and risk factors for patent Toxocara infections in cats and cat owners’ attitude towards deworming. Parasitology Research 115(12), 4519–4525.Google Scholar
Okewole, E (2016) The prevalence, pathogenesis and control of canine and human toxocariosis in Ibadan, Nigeria. Sokoto Journal of Veterinary Sciences 14(2), 34–42.Google Scholar
Overgaauw, PA and van Knapen, F (2013) Veterinary and public health aspects of Toxocara spp. Veterinary Parasitology 193(4), 398–403.Google Scholar
Overgaauw, PA, Van Zutphen, L, Hoek, D, Yaya, FO, Roelfsema, J, Pinelli, E, Van Knapen, F and Kortbeek, LM (2009) Zoonotic parasites in fecal samples and fur from dogs and cats in The Netherlands. Veterinary parasitology 163(1-2), 115–122.Google Scholar
Pahari, T and Sasmal, N (1991) Experimental infection of Japanese quail with Toxocara canis larvae through earthworms. Veterinary Parasitology 39(3-4), 337–340.Google Scholar
Panova, OA and Khrustalev, AV (2018) Dog walking brings Toxocara eggs to people's homes. Veterinary Parasitology 262, 16–19.Google Scholar
Poulsen, CS, Skov, S, Yoshida, A, Skallerup, P, Maruyama, H, Thamsborg, SM and Nejsum, P (2015) Differential serodiagnostics of Toxocara canis and Toxocara cati–is it possible? Parasite Immunology 37(4), 204–207.Google Scholar
Quattrocchi, G, Nicoletti, A, Marin, B, Bruno, E, Druet-Cabanac, M and Preux, P-M (2012) Toxocariasis and epilepsy: systematic review and meta-analysis. PLoS Neglected Tropical Diseases 6(8), e1775.Google Scholar
Robertson, LJ, Sprong, H, Ortega, YR, Van Der Giessen, JW and Fayer, R (2014) Impacts of globalisation on foodborne parasites. Trends in Parasitology 30(1), 37–52.Google Scholar
Rocha, S, Pinto, RMF, Floriano, AP, Teixeira, LH, Bassili, B, Martinez, A, Costa, SOPD and Caseiro, MM (2011) Environmental analyses of the parasitic profile found in the sandy soil from the Santos municipality beaches, SP, Brazil. Revista do Instituto de Medicina Tropical de São Paulo 53(5), 277–281.Google Scholar
Roddie, G, Stafford, P, Holland, C and Wolfe, A (2008) Contamination of dog hair with eggs of Toxocara canis. Veterinary Parasitology 152(1-2), 85–93.Google Scholar
Salem, G and Schantz, P (1992) Toxocaral visceral larva migrans after ingestion of raw lamb liver. Clinical Infectious Diseases 15(4), 743–744.Google Scholar
Schnieder, T, Laabs, E-M and Welz, C (2011) Larval development of Toxocara canis in dogs. Veterinary Parasitology 175(3-4), 193–206.Google Scholar
Selek, MB, Karagoz, E and Baylan, O (2016) Toxocariasis: a review. Medicine Science 5(4), 1063–1067.Google Scholar
Sivajothi, S and Reddy, BS (2018) Investigation on Toxocara spp. eggs in hair coat of dogs in YSR Kadapa district of Andhra Pradesh, India. Journal of Parasitic Diseases 42(4), 550–553.Google Scholar
Smith, H and Noordin, R (2006) Diagnostic limitations and future trends in the serodiagnosis of human toxocariasis. pp. 89–112 in Toxocara: The enigmatic parasite. Trowbridge, Cromwell Press.Google Scholar
Smith, H, Holland, C, Taylor, M, Magnaval, J, Schantz, P and Maizels, R (2009) How common is human toxocariasis? Towards standardizing our knowledge. Trends in Parasitology 25(4), 182–188.Google Scholar
Sprent, J (1956) The life history and development of Toxocara cati (Schrank 1788) in the domestic cat. Parasitology 46(1-2), 54–78.Google Scholar
Strube, C, Heuer, L and Janecek, E (2013) Toxocara spp. infections in paratenic hosts. Veterinary Parasitology 193(4), 375–389.Google Scholar
Subrata, IM, Oka, IBM and Agustina, KK (2017) Prevalence of intestinal worm in free ranging domestic cats in Bali (PREVALENSI CACING USUS PADA KUCING PELIHARAAN YANG BEBAS BERKELIARAN DI BALI). Jurnal Veteriner 18(3), 441–445.Google Scholar
Taira, K, Saeed, I, Permin, A and Kapel, C (2004) Zoonotic risk of Toxocara canis infection through consumption of pig or poultry viscera. Veterinary Parasitology 121(1-2), 115–124.Google Scholar
Walsh, MG and Haseeb, M (2012) Reduced cognitive function in children with toxocariasis in a nationally representative sample of the United States. International Journal for Parasitology 42(13-14), 1159–1163.Google Scholar
Wolfe, A and Wright, I (2003) Human toxocariasis and direct contact with dogs. Veterinary Record 152(14), 419–422.Google Scholar
Yoshida, A, Hombu, A, Wang, Z and Maruyama, H (2016) Larva migrans syndrome caused by Toxocara and Ascaris roundworm infections in Japanese patients. European Journal of Clinical Microbiology & Infectious Diseases 35(9), 1521–1529.Google Scholar
Yoshikawa, M, Nishiofuku, M, Moriya, K et al. (2008) A familial case of visceral toxocariasis due to consumption of raw bovine liver. Parasitology International 57(4), 525–529.Google Scholar
Zibaei, M, Sadjjadi, S and Maraghi, S (2017) The occurrence of Toxocara species in naturally infected broiler chickens revealed by molecular approaches. Journal of Helminthology 91, 633–636.Google Scholar
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