Chapter Twenty-Eight - Global prevalence of Toxocara infection in dogs

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Abstract

Dogs serve as the most important definitive hosts for Toxocara canis—a causative agent of human toxocariasis and one of the most widespread zoonotic helminth worldwide. The present study was undertaken to assess the global prevalence of T. canis infection in dogs. PubMed, Scopus, Web of Science, EMBASE and SciELO were searched to identify relevant studies. A random-effects model was used to estimate the overall and the subgroup-pooled prevalences across studies, and heterogeneity was assessed via the I2 test. The data were categorized according to WHO-region, different types of dogs, risk factors and environmental variables. From a total of 4370 peer-reviewed publications, 229 articles that studied 13,010,004 dogs in 60 countries met the final inclusion criteria. The overall prevalence of Toxocara infection in dogs was 11.1% (95% CI, 10.6–11.7%). The estimated prevalence in the different WHO-regions ranged from 6.4% to 19.2%: Eastern Mediterranean (19.2%, 13.7–25.5%), Africa (18.5%, 13.7–23.9%), South-East Asia (11.9%, 6.8–18.2%), North America (11.1%, 10.6–11.7%), South America (10.9%, 7.6–14.6%), Europe (10.8%, 8.9–12.9%) and Western Pacific (6.4%, 3.3–10.2%). Young (< 1 year of age), stray, rural and male dogs had a significantly (P < 0.001) higher prevalence of infection than older, pet, urban or female dogs. The prevalence was higher in low income countries and regions at a low geographical latitude, close to the equator, characterized as having tropical climates. From this review, it is estimated that ≥ 100 million dogs are infected with Toxocara around the world. This highlights the need for an increased focus on implementing affordable, appropriate control programs to reduce the public health threat of toxocariasis as a zoonosis of global importance.

Introduction

Dogs (Canis familiaris) are ubiquitous and have the widest diversity of roles of any domesticated animal in human societies worldwide. They serve as companion, working or service animals, entertainment or show dogs, working dogs on farms, police or military dogs, shepherds, hunters, guardians, transport, and play an important role in a wide range of comparative animal medicine studies of diseases such as diabetes, narcolepsy and cancer. The dog is widely considered to be ‘man's best friend’ and has important roles in the psychological and physiological well-being of many people, particularly young children, as well as disabled and elderly people (Serpell and Barrett, 2016). The global dog population is estimated at 900 million (https://www.worldatlas.com), ~ 500 million of which are stray or feral animals (https://www.carodog.eu). These numbers probably underestimate the true numbers of dogs, as dogs are not registered in many countries. In 2017, the total number of pet dogs in the European Union was estimated at 85 million (https://www.statista.com). According to the 2017–2018 National Pet Owners Survey in the United States, ~ 60% of households owned a pet, and the number of pet dogs was estimated at 89 million (https://www.iii.org). In addition, according to a previous estimate, 361 million dogs were estimated to live in Asia, 102.2 million in Latin America and the Caribbean, and 87.6 million in Africa (Hughes and Macdonald, 2013).

Although many humans derive great benefits from dogs, these canids can also serve as reservoirs for a wide range of zoonotic pathogens, some of which are of major public health importance (Macpherson et al., 2013; Otranto et al., 2017). In many cases, stray dogs might harbour more infectious agents than pet dogs, such that they represent a significant risk to human populations (Otranto et al., 2017; Paoletti et al., 2015); nevertheless, direct contact of pet dogs with people is a significant risk factor (Dubná et al., 2007; Lucio-Forster et al., 2016; Overgaauw and van Knapen, 2013). Of the important zoonotic pathogens, ascaridoid nematodes of the genus Toxocara, including Toxocara canis and T. cati, are causative agents of human toxocariasis with a worldwide distribution (Aghamolaie et al., 2018; Fisher, 2003; Ma et al., 2018). Toxocariasis can cause four major clinical syndromes in humans, including visceral larva migrans (VLM), ocular larva migrans (OLM), neurotoxocariasis (NT) and common/covert toxocariasis (CT) (Aghaei et al., 2018; Ma et al., 2018; Mohammadzadeh et al., 2018; Rostami et al., 2019). Canids, including dogs, foxes, wolves and jackals serve as definitive hosts of T. canis, releasing eggs into the environment, where, under favourable conditions, they can embryonate and eventually become infective. Infective eggs containing third-stage (L3) larvae can be accidentally ingested by humans and other paratenic hosts via contaminated soil, unwashed raw vegetables, water, or occasionally from the fur of dogs (Ma et al., 2018).

In the past decades, numerous studies have assessed the prevalence of T. canis infection in dogs, often in relatively small geographic regions. Consequently, there are significant gaps in the knowledge of the epidemiology of Toxocara infection/toxocariasis in many countries. Considering the public health implications of toxocariasis, a more comprehensive understanding of the occurrence and prevalence of Toxocara infection would be valuable. This paper provides the first systematic review and meta-analysis of the available data on the global prevalence of T. canis in dogs.

Section snippets

Methodology

This systematic literature search and meta-analysis study adhered to the protocol recommended by the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) (Moher et al., 2015).

Eligible studies, their characteristics and datasets

Fig. 1 shows a flow diagram for the selection of articles. The search strategy identified 4370 articles, 4064 of which were excluded after the removal of duplicates and the screening of titles and abstracts. A total of 306 articles with full-texts were assessed for eligibility. A total of 229 studies containing 275 datasets were included in this meta-analysis. These studies provided data on 13,010,004 dogs from 60 different countries in six WHO-regions. In total, 93 datasets were available for

Global and regional prevalence rates of Toxocara infection in dogs

The random-effects, pooled global prevalence of Toxocara infection in dogs was 11.1% (95% CI, 10.6–11.7%; 302,723/13,010,004), with a high heterogeneity among studies (I2 = 99.8). Prevalence was highest in the Eastern Mediterranean region (19.2%, 13.7–25.5%) and lowest in the Western Pacific region (6.4%, 3.3–10.2%). Pooled prevalences in other WHO-regions were 10.8–18%: Africa (18%, 13.7–23.9%), South-East Asia (11.9%, 6.8–18.2%), North America (11.1%, 10.6–11.7%), South America (10.9%,

Prevalence according to type of dogs, age, gender and area (rural vs urban)

In subgroup analyses, with respect to the type of dogs, the prevalences of Toxocara infection worldwide in pet, working and stray dogs were 8.9% (8.3–9.6%), 14.1% (10.1–18.7%) and 18.8% (14.7–23.2%), respectively (P < 0.001). In subgroup analyses, according to age and gender, the pooled prevalence of Toxocara infection was higher in dogs of ≤ 12 months of age (28.7%, 23.5–34.2%) and in male dogs (26.8%, 20.2–33.9%) than in dogs of > 12 months of age (12.9%, 9.6–16.6%) and female (21.7%, 15.4–28.7%)

Prevalence based on selected study characteristics

With respect to the type of samples, prevalence based on the detection of Toxocara eggs in faecal samples (10.9%, 10.3–11.5%) was lower than for the detection of such eggs on hairs (15.8%, 4.0–33.1%) and of Toxocara worms (adults) at postmortem (15.6%, 9.8–22.4%). Considering the diagnostic approach used, prevalence rates based on flotation, sedimentation, either flotation or sedimentation (unspecified), necropsy (to detect adult worm), and other (Kato–Katz or McMaster) techniques were 10.7%

Impact of socio-demographic, geographical and climatic parameters on prevalence

We also performed subgroup analyses with respect to socio-demographic, geographical and climate parameters, to establish the source of heterogeneity and also the effects of these parameters on the prevalence of Toxocara infection in dogs. With respect to the income level in a country, the highest and lowest prevalence rates were estimated for countries with low income levels (20.0%, 13.7–27.2%) and high income levels (7.7%, 7.2–8.3%), respectively. Prevalence rates in countries with lower-

Discussion and conclusions

This systematic review and meta-analysis of published prevalence studies on Toxocara in dogs found a global prevalence of 11.1%, suggesting that at least 100 million dogs are carriers of Toxocara worldwide. The results reveal that there are significant differences in prevalence among different regions of the world, which are associated with the type of dog, a country's GDP as well as geographical and climatic parameters. The high global prevalence of Toxocara infection is of public health

Acknowledgements

This research was supported by Health Research Institute at the Babol University of Medical Sciences (IR.MUBABOL.HRI.REC.1398.129), Babol, Iran (A.R.). RBG's research program is presently supported through funds from the National Health and Medical Research Council (NHMRC) of Australia, the Australian Research Council (ARC), Yourgene Health, Melbourne Water Corporation and The University of Melbourne.

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