The State of Knowledge on Intestinal Helminths in Free-Roaming Dogs in Southern South America

1.1 Dog populations

Humans and dogs share a long history and were probably associated with European early-modern humans [1], coexisting indoors and outdoors and colonising new environments, often in cooperation [2]. From ancient times dogs have been used by humans as tools for different purposes, such as hunting, gathering food, caring for livestock, protection, and more recently as detectors of explosives and drugs, as companion animals, or as assistants for people with various types of disease or disability [3, 4, 5]. Therefore, their coexistence has been wide-ranging, and has generated numerous opportunities for around 260 zoonotic diseases to emerge between dogs and humans [2, 6].

There are almost one billion dogs worldwide [7], but the relationship between the numbers of people and dogs varies according to the geographic area and socioeconomic conditions of each country or region [8]. In developed countries the human to dog ratio varies from 6 to 10:1 according to the World Health Organisation [9]; in Italy the human:dog ratio is 9:1 [10], and in the United States it is 3.6:1 [11]. The dog population in South America is very large, around 87.6 million. In Brazil in particular there are 44.9 million children aged under 14 years, and an estimated total of 52.2 million dogs, which means there are more dogs than children [12]. In Argentina, a survey carried out for food companies determined that there are approximately 9 million dogs, and that 78% of households have a dog, whose function is mainly exclusively companionship [13]. The situation in Chile is similar, where the dog population is around 3.5 million and 64% of households have at least one [14], while in Uruguay the dog population is 1.75 million and 72% of households own a dog [15].

To encourage responsible ownership of this large number of dogs, it was necessary to enact laws indicating what responsible dog care implies (Argentina: Decree 1088/11; Chile: No. 21.020/17; Uruguay: No. 1189/14). Animal welfare thus imposes obligations on the owner, which include vaccinations, deworming, neutering, adequate food, and keeping pets confined to the household or taking them outside on a lead, thus preventing them from roaming freely. It should be noted that in most localities of these countries these laws are not enforced effectively [16].

1.2 Dog care

Although national laws have been promulgated several years ago, knowledge of them and the care received by dogs is far from adequate [17, 18, 19, 20]. The biggest problem in these countries is that dogs are allowed to roam freely in public areas, and this is associated with education, socio-economic level, the idiosyncrasy and customs of each country, the role the dog plays within the family, and the low importance that people give to how their dog can affect other people or animals [21]. In addition, allowing dogs to roam freely is strongly correlated with other aspects of dog care, such as a lack of appropriate vaccination and deworming treatment [21]. The care given to dogs that roam freely is poorer than for dogs which are confined, and they are rarely taken to the vet due to the high cost that this represents [22]. In Chile, the average cost spent per pet for annual veterinary check-ups, diagnoses, vaccines and treatment is US$ 330 [4], while in Argentina this cost is around US$ 100 annually (personal observation). The percentage of vaccinated dogs is low, even when there is a possibility of rabies contagion [14, 23], and the frequency of deworming is in most cases inadequate considering that dogs can roam freely on public roads, becoming reinfected [23, 24, 25]. The percentage of animals that are neutered is also insufficient, despite the national or local neutering programs run in the three countries [21, 26, 27]. Neutered animals represent less than half the dog population [21, 23, 28] and the majority are older than 3 years; in many cases dogs are allowed to have at least one litter of offspring [23].

1.3 Dogs, parasites and diseases

One Health is recognised as a valuable paradigm for global health management, and seeks the integration of human and animal health. The risk of transmission of a zoonotic disease from dogs to humans is related to the abundance of infectious forms in the environment, climatic conditions, whether dogs roam freely, and the behaviour of humans that exposes them to infective sources [29, 30]. It has been observed that free-roaming dogs are more exposed and prone to acquiring parasites [24, 31, 32, 33]. In Chile, rural dogs are associated with agricultural and livestock activities. They are unsupervised, have freedom to roam and are given limited veterinary care [34]. In Argentina, parasite richness and prevalence are positively associated with free-roaming animals, and only a small proportion of dogs (17%) is subjected to some degree of movement restriction [20]. In the cities of Argentinian Patagonia, another important factor that promotes infection by zoonotic parasites, mainly cystic echinococcosis, is the domestic slaughter of small ruminants for human consumption. This practice occurs frequently in rural areas and the peripheral low-income neighbourhoods of cities, where dogs are fed with the raw offal of sheep and goats [35, 36]. The vast majority of parasites registered in South America are cosmopolitan zoonotic parasites transmitted through dog faeces, such as Toxocara canis, Ancylostoma caninum, Toxascaris leonina, Echinococcusspp., and Dipylidium caninum, which are common parasites in dogs worldwide [12]. Zoonotic parasitic infections in dogs are a public health issue not only in developing countries but also in developed nations, such as in the USA and European countries [37, 38]. Other parasites like Trichuris vulpisare distributed worldwide, but are rarely transmitted to humans [39]. Some human parasites like Ascaris lumbricoides and Strongyloides stercoralisare occasionally reported in dogs [40, 41]. Therefore, worldwide, dogs may harbour zoonotic parasites that affect the health and wellbeing of humans, their distribution being linked to poverty, poor knowledge of sanitary practices, insufficient hygiene and problems with unconfined and untreated dogs [42]. Pet diseases may pose risks to human health but are rarely included in surveillance systems. Although pet-borne infections have become increasingly relevant to human health, systematic notification of these infections is not currently conducted, except for rabies and Echinococcosis in some countries [22, 43].

Southern South America is a region with varied geography and climate and marked altitudinal and latitudinal differences; for example, plains (Pampas in Argentina and Uruguay), arid plateaus (Patagonia), forests (Patagonia and northeastern Argentina), and mountains of high altitude between Argentina and Chile (the Andes). The climate ranges from humid tropical in northern Argentina and Uruguay, arid in northern Chile, to humid cold in the south of Argentina and Chile. This climatic variety favours the distribution and occurrence of different parasites. On the other hand, the socio-economic condition of a large part of the population is characterised by poverty and a low-income economy. This scenario is accompanied by a lack of parasitological studies, surveillance and zoonosis control plans on the part of public health organisations [44].

The objective of this work is to describe, through bibliographic analysis, the occurrence, prevalence, species richness, and distribution of intestinal helminth parasites found in dog faeces in urban and rural areas of southern South America (Argentina-Chile-Uruguay).

2.1 Search approach

Three databases (PubMed, Google Scholar and Scopus) were searched for studies published between 2000 and 2020. The search terms were “dog AND parasite AND Argentina”; “dog AND parasite AND Chile”; and “dog AND parasite AND Uruguay”.

The Google Scholar search in particular returned a large number of results, of which the first 700 titles were read (and in some cases the abstract); however, it was observed that after the first 200 no results were found that met the search requirements.

2.2 Paper assortment

The studies to be included were identified independently by two reviewers, and were confirmed by a third reviewer following standardised methodology [45]. The studies included met the following criteria: (1) full text articles available online; (2) published between 2000 and 2020; (3) peer-reviewed, original papers published either in English or Spanish; (4) cross-sectional studies that assessed the prevalence of any intestinal helminth parasite of dogs in Argentina, Chile or Uruguay; (5) studies that detected parasite infection in faeces using at least one parasitological, serological and/or molecular method; (6) studies that reported sample sizes, and the prevalence of each parasite species. Reviews and case reports were excluded. The following data were extracted from each article: authors, publication year, country, localities (coordinates), type of locality (rural/urban), sample size, detection method, prevalence of each parasite, number of parasite species.

2.3 Parasite distribution

The distribution maps were constructed using the Free and Open Source Geographic Information System (QGis system). The coordinates for the site locations were taken from the selected works or were completed using Google Earth. The prevalence values shown on the maps were obtained from the studies included in the bibliographic review. The map of South America was obtained from shape files from Instituto Geográfico Nacional[46].

2.4 Statistical analysis

Spearman’s rank Correlation Tests were performed to analyse the relation between richness, with sample size and latitude. All sites with richness = 1 were excluded, since they searched for only one parasite.

4.1 State of knowledge and distribution

Although three databases were used, this work could have some bias due to the exclusion of grey literature, like technical reports, congress abstracts or thesis manuscripts, so some sites or negative data may be excluded in the analysis [109]. The systematic bibliographic review carried out shows that the published and available knowledge of the occurrence and distribution of helminths in dogs is scarce in southern South America; in countries such as Uruguay there are no records other than those obtained within the Echinococcosis National Programmes. Furthermore, in Argentina there are arid regions near the Andes, such as the northwest of the country, where there are no records of parasites in dogs. The same was observed for Chile south to 40°s, except for one record in Punta Arenas, the southernmost city in Chile. Most of the records are associated with large cities and their surroundings, such as Buenos Aires and La Plata in Argentina, and in the area of Santiago de Chile, Concepción, and Temuco in Chile.

Although sample size is the only factor that significantly affected richness, other factors to consider could be the analytical methods used and whether the sample was fixed or not. Sample size affects the results, generating deviations in the number of species and in their prevalence, especially in places where the sample size was too low. On the other hand, a lack of methodological specifications can be observed in the techniques used. This could imply potential biases in the reporting and/or interpretation of data. In order to obtain data of higher quality, a general consensus should be reached on the techniques to be applied. It is also desirable to apply molecular techniques that allow parasite identification to species level, thus solving records identified to family level, such as “Ancylostomatidae” or “Strongylids”, or the recording of species outside their natural range of distribution, like Dibothriocephalusin the northeast of Argentina.

The presence of a greater number of species, most of which have zoonotic potential, in urban areas than rural ones is probably due to the fact that dogs can roam freely. Dogs spread the parasite eggs, thereby these areas will function as contagion points for both other dogs and humans. A further problem is that deworming in these countries is insufficient [21]. A similar situation has been detected in parks in the United States, where it has been suggested that dogs are at risk of infection with parasites at these sites, and it has been recommended that preventive strategies be considered [30, 110]. Some parasitic infections could become increasingly urbanised, and an estimation for 2050 indicates that up to two-thirds of the global population will live in megacities. The slums of these megacities would concentrate high levels of intestinal helminth. Toxocariasis and other urban soil-transmitted helminths are important, yet little studied, health issues in the cities of the Americas [111].

The zoonotic broad tapeworm, Dibothriocephalussp., is found in dogs from the endemic zone of the disease, the Andean Patagonia of Argentina and Chile [93, 104]. The records from the northeastern region of Argentina require revision, as there are no molecular studies confirming the identity of these parasites, and there are no records of fish infected by plerocercoids in this zone. Although Dibothriocephalussp., is not transmitted to humans by dogs, they can act as disseminators of the disease and are often used as sentinel species for the spread of the disease in some areas. Ascarissp. in dogs is distributed mainly in subtropical regions of Argentina, where this parasite is most prevalent in humans [107]. Some parasites are distributed throughout all the latitudes regardless of the type of climate, like T. canis., T. vulpis, and Ancylostomatids, as observed in other parts of the world [112, 113, 114]. Echinococcussp. is distributed across almost all rural areas of the three countries, although has recently also been registered in cities [35, 47, 64, 115].

4.2 Zoonoses and human cases reported

The high percentage of parasites with zoonotic potential reinforces the need to establish effective prevention measures, not only with regard to parasitosis in animals but also to transmission to humans. This situation highlights the need for better integration between specialists in animal and human health [74]. A few diseases transmitted by dogs have surveillance mechanisms in humans, but there are many other important zoonoses worldwide, with numerous human cases, which are not kept watch on. Some of these have been recorded in Argentina and Chile, such as those caused by T. canis, Ancylostomasp., A. caninum, Uncinariasp., and Strongyloidessp. [30]. Of the main zoonoses recorded in dogs in the three countries, cystic echinococcosis is the only one which has to be reported to the health authorities, since it is of major sanitary importance [115]. The others, like toxocariasis, hookworm and strongyloidiasis are not reported, and records of human cases in these countries are scarce. The status of these zoonoses in humans from southern South America is analysed below.