Open access peer-reviewed chapter

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

Written By

Luciano Ritossa, Gustavo Viozzi and Verónica Flores

Submitted: October 26th, 2020 Reviewed: January 20th, 2021 Published: April 1st, 2021

DOI: 10.5772/intechopen.96125

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Abstract

In South America there are more dogs per person than in developed countries. Many owners allow their dogs to roam freely in public areas, which favours the spread of zoonotic diseases. 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 from urban and rural areas of southern South America (Argentina-Chile-Uruguay). Using three databases, we performed a systematic review of articles published between 2000 and 2020 in indexed journals. A total of 219 articles was evaluated for eligibility, and of these 67 were included in the final analysis; 48 correspond to Argentina, 17 to Chile, and 2 to Uruguay. The total number of parasite taxa recorded was 22, the most frequently occurring species being Toxocara canis, Ancylostoma sp., Trichuris vulpis and Echinococcus sp. Species richness was correlated with sample size and varied between 1 and 10 species. In addition, disease risk is not homogeneously distributed. Due to the high infection levels in dogs, urban and rural dwellers are at risk of infection with zoonotic diseases transmitted by these animals, therefore a One Health approach to public health would be advisable.

Keywords

  • Argentina
  • Chile
  • Uruguay
  • Helminths
  • Canine faeces
  • Toxocara canis
  • Echinococcus granulosus
  • Ancylostoma caninum
  • Trichuris vulpis
  • systematic bibliographic review
  • zoonotic risk

1. Introduction

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).

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2. Materials and methods

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.

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3. Results

From the search in the 3 databases, 29,450 scientific items were found. Of these, 24,517 belong to the period between 2000 and 2020. After analysing the titles and abstracts, 24,298 articles were excluded because they did not comply with the objectives or inclusion criteria, did not include helminths, did not correspond to the countries under study, or were not cross-sectional studies. A total of 219 articles were evaluated for eligibility. After removing the duplicates, 67 were included in the final analysis ( Table 1 ), and the full texts of these relevant articles were reviewed in depth. Forty-eight corresponded to Argentina, 17 to Chile, and 2 to Uruguay ( Figure 1 ). The data come from analysis of 32,300 dog faeces collected in urban or rural sites of the 3 countries. Sample sizes in the different studies ranged from 4 to 2,417, except for Uruguay where 5,356 faeces were analysed for the National Echinococcosis Control Programs, without considering the presence of other parasites ( Table 1 ).

Figure 1.

Flow diagram of epidemiologic studies on dog parasites for the systematic review.

AutorAñoCountryName Study LocalityCoordinatesSample sizeFixing methodof tection MethodsNo. Of detection methodsRURALURBANRichnessAncylostomidsAncylostomasp.Uncinariasp.Ascaris sp.Dibothriocephalussp.DipylidiumcaninumEchinococcussp.Eucoleus aerophilaEucoleus boehmiCapillaria sp.Taenia multicepssp.StrongyloideseggsSpirocercaTaenidaeTaenia hydatigenaTaenia ovisToxascarissp.Toxocarasp.Trichurissp.TrematodesOncicola canisPhysalopetrasp.
Acosta Jamett et al. [47]2010ChileTangue30°20'S, 71°34'W120ELISA1rural110
Acosta Jamett et al. [47]2010ChileGuanaqueros30°11'S, 71°25'W81ELISA1urban0
Acosta Jamett et al. [47]2010ChileCoquimbo29°57'S, 71°20'W128ELISA1urban115
Acosta Jamett et al. [48]2014ChileCombarbalá31°10′S, 71°03′W52CoproElisa1urban127
Andresiuk et al. [49]2007ArgentinaMar del Plata37°56'S, 57°35'W400Willis Flotation1urban362.813.946.75
Andresiuk et al. [50]2003ArgentinaMar del Plata38°00′S, 57°33′W125Flotation, sedimentation of Willis1urban462.9624.072.5622.2262.96
Andresiuk et al. [29]2004ArgentinaMar del Plata38°00′S, 57°33′W288Flotation, sedimentation of Willis1urban365.8314.1746.67
Archelli et al. [51]2018ArgentinaEnsenada34°51′S, 57°54′W217Formol 10%Sedimentation of Teleman and Flotation of Sheater2urban123.0
Arezo et al .[36]2020ArgentinaBariloche41°10’S, 71°18’W1780coproElisa Echinococcus1rural11
Arezo et al .[36]2020ArgentinaEl Bolson41°58′S, 71°32′WCoproElisa1rural
Arezo et al. [36]2020ArgentinaComallo41°02′S, 70°16′WCoproElisa1rural11
Arezo et al. [36]2020ArgentinaEl Cuy39°56′S, 68°20′WCoproElisa1rural11
Arezo et al. [36]2020ArgentinaIng. Jacobacci41°18′S, 69°35′WCoproElisa1rural11
Arezo et al. [36]2020ArgentinaMaquinchao41°15′S, 68°42′WCoproElisa1rural
Arezo et al. [36]2020ArgentinaLos Menucos40°50′S, 68°05′WCoproElisa1rural11
Arezo et al. [36]2020ArgentinaÑorquinco41°51′S, 70°54′WCoproElisa1rural11
Arezo et al. [36]2020ArgentinaPilcaniyeu41°07′S, 70°43′WCoproElisa1rural11
Arezo et al. [36]2020ArgentinaRamos Mexia40°30′S, 67°17′WCoproElisa1rural11
Arezo et al. [36]2020ArgentinaSierra Colorada40°35′S, 67°45′WCoproElisa1rural11
Arezo et al. [36]2020ArgentinaSierra Grande41°36′S, 65°21'WCoproElisa1rural
Arezo et al . [36]2020ArgentinaValcheta40°42′S, 66°09′WCoproElisa1rural11
Armstrong et al. [52]2011ChileTemuco37°24'S, 72°31'W196Flotation with zinc1urban49.34.712.44.7
Casas et al. [53]2013ArgentinaLa Quiaca22°06′S, 65°36′W89Copro, Elisa and WB2urban12.2
Castillo et al. [54]2000ChileSantiago de Chile33°27′S, 70°40′W288Formol salinoTelemann modified, using ethandl acetate1urban44.50.713.57.3
Chiodo et al. [55]2006ArgentinaGeneral Mansilla35°04'S, 57°44'W81Sedimentation of Teleman modified1rural16.17
Cociancic et al. [56]2017ArgentinaLa Plata34°56′S, 57°57′W78Sedimentation of Ritchie and Flotation of Willis2urban769.241.01.31.31.321.828.2
Cociancic et al. [32]2020ArgentinaUshuaia54°48′S, 68°18′W80Formol 5%Sedimentation and Flotac2urban71.32.55.01.3
De Costas et al. [57]2014ArgentinaTumbaya23°51′S, 65°28′W222Copro, Elisa and WB2111.7
De Costas et al. [57]2014ArgentinaHumahuaca23°12′S, 65°21′W18Copro, Elisa and WB2127.7
De Costas et al. [57]2014ArgentinaTilcara23°34′S, 65°23′W64Copro, Elisa and WB2114.0
De Costas et al. [57]2014ArgentinaCochinoca22°44′S, 65°53′W94Copro, Elisa and WB219.5
De Costas et al. [57]2014ArgentinaSusques23°24′S, 66°22′W50Copro, Elisa and WB212.0
De Costas et al. [57]2014ArgentinaSanta Catalina21°56′S, 66°03′W28Copro, Elisa and WB2110.7
De Costas et al. [57]2014ArgentinaYavi22°07′S, 65°27′W47Copro, Elisa and WB2114.8
Dopchiz et al. [58]2013ArgentinaLobos, Bs As35°10′S, 59°05'W42Formol 10%, freezadoSedimetation of Ritchie, Flotation of Sheater and CoproElisa3rural611.914.2919.0526.1926.19
Enriquez et al. [59]2019ArgentinaPampa del Indio, Chaco26°02′S, 59°55′W85SAF solutionFlotation with NaCl and Sedimentation2urban868.22.41.25.95.914.13.515.3
Flores et al. [35]2017ArgentinaBariloche41°10’S, 71°18’W118Sheater Flotation1urban947.016.90.89.35.12.511.912.739.0
Fontanarosa et al. [60]2006ArgentinaLanus34°22′S, 58°22′W262Sheater Flotation1urban59.10.0512.611
Fontanarosa et al. [60]2006ArgentinaAvellaneda34°39′S, 58°22′W547Sheater Flotation1urban58.90.814.25.4
Fontanarosa et al. [60]2006ArgentinaAlte Brown34°50′S, 58°23′W458Sheater Flotation1urban5198.914.1
Fontanarosa et al. [60]2006ArgentinaE.Echeverria34°52′S, 58°28′W134Sheater Flotation1urban521.66.717.9
Fontanarosa et al. [60]2006ArgentinaLomas de Zamora34°45′S, 58°25′W499Sheater Flotation1urban5139.810.2
Fontanarosa et al. [60]2006ArgentinaQuilmes34°15′S, 58°15′W293Sheater Flotation1urban513.610.27.5
Gamboa et al. [61]2011ArgentinaLa Plata34°56′S, 57°53′W12Formol 10%Sedimentation of Ritchie and Flotation of Willis2urban41616168
Gamboa et al. [62]2009ArgentinaLa Plata Norte34°56′S, 57°57′W5Sedimentation of Ritchie and Carles Barthelemand, and Flotation of Fülleborn3urban416.716.716.78.3
Gamboa et al. [62]2009ArgentinaLa Plata Sur34°56′S, 57°57′W4Sedimentation of Ritchie and Carles Barthelemand, and Flotation of Fülleborn3urban233.38.3
Gamboa et al. [62]2009ArgentinaAristóbulo del Valle27°05′S, 54°53′W11Sedimentation of Ritchie and Carles Barthelemand, and Flotation of Fülleborn3urban490.99.127.39.1
Gonzalez Acuña et al. [63]2008ChileArchipiélago de Juan Fernández33°38′S, 78°50′w40SAF solutionTeuscher Methods or Flotation of Willis2rural330.03.915
Gorman et al. [31]2006ChileSantiago de Chile33°27′S, 70°40′W582Flotation zinc sulfate and Sedimentation of Teleman modified2urban55.32.12.49.18.6
Irabedra et al. [64]2016Uruguay5356CoproElisa13.6
Irabedra et al. [64]2016Uruguay1496CoproElisa17.35
La Sala et al. [65]2015aArgentinaBahía Blanca38°44′S, 62°16′W475Formol 10%Sedimentation of Ritchie1urban521.10.62.318.1
La Sala et al. [66]2015bArgentinaBahia Blanca38°43′S, 62°16′W475Direct observation1urban522.30.62.318.1
Lamberti et al . [67]2014ArgentinaGra. Pico35°39′S, 63°45′W785Flotation with ClNa1urban345.47.125.8
Lamberti et al. [68]2015ArgentinaGral Pico35°40′S, 63°44′W1229Flotation with ClNa and ZnSO42urban345.46.421.9
Larrieu et al. [69]2014ArgentinaEl Bolsón41°58′S, 71°32′W68Copro, Elisa and WB2rural111.8
Larrieu et al. [69]2014ArgentinaEl Cuy39°56′S, 68°20′W81Copro, Elisa and WB2rural16.1
Larrieu et al. [69]2014ArgentinaÑorquinco41°51′S, 70°54′W47Copro, Elisa and WB2rural16.4
Larrieu et al. [69]2014ArgentinaPilcaniyeu41°07′S, 70°43′W19Copro, Elisa and WB2rural15.3
Larrieu et al. [69]2014ArgentinaComallo41°02′S, 70°16′W12Copro, Elisa and WB2rural18.3
Larrieu et al. [69]2014ArgentinaIngeniero Jacobacci41°18′S, 69°35′W108Copro, Elisa and WB2rural17.4
Larrieu et al. [69]2014ArgentinaMaquinchao41°15′S, 68°42′W16Copro, Elisa and WB2rural112.5
Larrieu et al. [69]2014ArgentinaLos Menucos40°50′S, 68°05′W37Copro, Elisa and WB2rural15.4
Larrieu et al. [69]2014ArgentinaSierra Colorada40°35′S, 67°45′W42Copro, Elisa and WB2rural12.4
Larrieu et al. [69]2014ArgentinaValcheta40°42′S, 66°09′W106Copro, Elisa and WB2rural14.7
Larrieu et al. [69]2014ArgentinaSierra Grande41°36′S, 65°21'W14Copro, Elisa and WB2rural17.2
Lavallén et al. [70]2011ArgentinaGral Pueyrredon38°00′S, 57°33′W46Formol 10%Sediemtation of Ritchie and Flotation of Sheater and coproELISA3urban671.7441.38.617.3663.0445.65
Lopez et al. [71]2006ChileSantiago de Chile33°27′S, 70°40′W972PAF fenol, alcohol and formaldehídoBurrows Technique1urban71.82.20.41.411.18.91.2
Luzio et al. [72]2013ChileTomé36°37′S, 72°57′W223PAF fenol, alcohol and formaldehídoBurrows Technique1urban98.10.99.92.73.11.86.322.98.1
Luzio et al. [73]2015ChileSanta de los Angeles37°28'S, 72°21'W452PAF fenol, alcohol and formaldehídoBurrows Technique2urban74.20.442.60.441.61.39.3
Luzio et al. [74]2017ChileConcepcion36°49′S, 73°03′W64PAF fenol, alcohol and formaldehídoBurrows Technique1urban58.5294.56.329.7
Madrid et al. [75]2008ArgentinaMar del Plata38°00′S, 57°33′W358Flotation with NaCl1urban718.911.51.10.65.913.4
Marder et al. [76]2004ArgentinaCiudad de Corrientes27°25’S, 58°52’W900Flotation of Willis, Sheater and Faust3urban364.57.63.1
Martin et al. [77]2008ArgentinaParaná31°44′S, 60°31′W61Solución salina 5%Concentration methods1urban267.07.0
Martin et al. [77]2008ArgentinaSanta Fé31°38′S, 60°42′W200Solución salina 5%Concentration methods1urban314.062.012.0
Martin et al. [77]2008ArgentinaAvellaneda (Santa Fé)29°07′S, 59°39′W15Solución salina 5%Concentration methods1urban35.06.01.0
Martin et al. [77]2008ArgentinaReconquista (Santa Fé)29°09′S, 59°39′W10Solución salina 5%Concentration methods1urban25.05.0
Martin et al. [77]2008ArgentinaCalchaquí (Santa Fé)29°53′S, 60°16′W17Solución salina 5%Concentration methods1urban32.05.01.0
Martin et al. [77]2008ArgentinaHersilia (Santa Fé)30°00′S, 61°51′W12Solución salina 5%Concentration methods1urban34.05.01.0
Martin et al. [77]2008ArgentinaSan Carlos Centro (Santa Fé)31°44′S, 61°06′W24Solución salina 5%Concentration methods1urban38.06.03.0
Martin et al. [77]2008ArgentinaSanto Tomé (Santa Fé)31°40′S, 60°46′W54Solución salina 5%Concentration methods1urban39.05.02.0
Mercado et al. [78]2004ChileArica18°28′S, 70°19′W50Sedimentation and Harada, Mori2urban224
Mercado et al. [78]2004ChileAntofagasta23°38′S, 70°23′W50Sedimentation and Harada, Mori2urban22
Mercado et al. [78]2004ChileIllapel31°37′S, 71°10′W50Sedimentation and Harada, Mori2urban27.210
Mercado et al. [78]2004ChileViña del Mar33°01′S, 71°33′W27Sedimentation and Harada, Mori2urban2
Mercado et al. [78]2004ChileValparaiso33°02′S, 71°37′W40Sedimentation and Harada, Mori2urban21012.5
Mercado et al. [78]2004ChileSan Felipe32°45′S, 70°43′W44Sedimentation and Harada, Mori2urban26.8
Mercado et al. [78]2004ChileSantiago de Chile33°27′S, 70°40′W54Sedimentation and Harada, Mori2urban21.9
Mercado et al. [78]2004ChileRancagua34°09′S, 70°44′W27Sedimentation and Harada, Mori2urban27.4
Mercado et al. [78]2004ChileSan Fernando34°35′S, 70°59′W50Sedimentation and Harada, Mori2urban2248
Mercado et al. [78]2004ChileConcepcion36°49′S, 73°03′W49Sedimentation and Harada, Mori2urban28.26.1
Mercado et al. [78]2004ChileTemuco38°44′S, 72°35′W50Sedimentation and Harada, Mori2urban2404
Mercado et al. [78]2004ChileValdivia39°48′S, 73°14′W50Sedimentation and Harada, Mori2urban2204
Mercado et al. [78]2004ChilePunta Arenas53°09′S, 70°54′W54Sedimentation and Harada, Mori2urban21.9
Milano et al. [79]2005ArgentinaCiudad de Corrientes27°25’S, 58°52’W61Formol 10%Sedimentation and flotation of Willis2urban432.81.626.33.3
Milano et al. [79]2005ArgentinaCiudad de Corrientes27°25’S, 58°52’W40Formol 10%Sedimentation and flotation of Willis2urban435.02.517.52.5
Milano et al. [79]2005ArgentinaCiudad de Corrientes27°25’S, 58°52’W40Formol 10%Sedimentation and flotation of Willis2urban435.012.512.510.0
Milano et al. [79]2005ArgentinaCiudad de Corrientes27°25’S, 58°52’W32Formol 10%Sedimentation and flotation of Willis2urban350.015.69.4
Milano et al. [79]2005ArgentinaCiudad de Corrientes27°25’S, 58°52’W40Formol 10%Sedimentation and flotation of Willis2urban445.02.520.02.5
Milano et al. [79]2005ArgentinaCiudad de Corrientes27°25’S, 58°52’W33Formol 10%Sedimentation and flotation of Willis2urban348.26.03.0
Milano et al. [79]2005ArgentinaCiudad de Corrientes27°25’S, 58°52’W34Formol 10%Sedimentation and flotation of Willis2urban338.217.65.9
Milano et al. [79]2005ArgentinaCiudad de Corrientes27°25’S, 58°52’W44Formol 10%Sedimentation and flotation of Willis2urban443.24.56.8
Milano et al. [79]2005ArgentinaCiudad de Corrientes27°25’S, 58°52’W38Formol 10%Sedimentation and flotation of Willis2urban450.02.615.87.9
Motta et al . [80]2019ArgentinaRio Cuarto33°07′S, 64°20′W493Formol 10%Flotation of Willis, and Sheather, and Sedimentation3urban530.830.611.426.99.94
Natalini et al . [81]2020ArgentinaParque Nac Mburucuya27°58′S, 57°59′W28Formol 10%Flotation Sheater and sedimentation of Ritchie2rural644471444
Natalini et al . [81]2020ArgentinaSan Nicolás NP27°59′S, 57°35′W23Formol 10%Flotation Sheater and Sedimentation of Ritchie2rural35299
Oku et al. [82]2004UruguayTacuarembo31°42′S, 55°58′W79Necropsy1urban4382318
Oku et al. [82]2004Uruguay31°45′S, 55°58′W-31.75Necropsy1rural61303.494233
Olivares et al. [83]2014ChileTemuco37°24'S, 72°36'W102Flotation and Sedimentation of Teuscher1urban421.512.721.535.2
Opazo et al. [84]2019ChileValparaiso33°02′S, 71°37′W30PAF fenol, alcohol and formaldehídoBurrows Technique1rural67131717403
Oyarzun et al. [85]2019ChileContulmo38°00′S, 73°14′W270AlcoholSedimentation and Flotation of Teuscher1rural525.5453.930.515.6
Parra et al. [86]2017ArgentinaAncajuli26°35′S, 65°33′W43CoproElisa1rural113
Parra et al. [86]2017ArgentinaAnfama26°45′S, 65°34′W22CoproElisa1rural17
Parra et al. [86]2017ArgentinaChaquivil26°41′S, 65°36′W7CoproElisa1rural14
Parra et al. [86]2017ArgentinaLa Hoyada26°41′S, 65°31′W5CoproElisa1rural13
Parra et al. [86]2017ArgentinaMala Mala26°47′S, 65°33′W9CoproElisa1rural16
Parra et al. [86]2017ArgentinaSan José de Chasquivil26°41′S, 65°36′W17CoproElisa1rural18
Perez et al. [87]2006ArgentinaRio Negro40°48′S, 63°00′W416Copro, Elisa and WB224.614.9
Quilodrán-González et al. [88]2018ChileCabrero37°2'S, 72°24'W83Flotation of Sheater1urban1414.84.813.3
Quilodrán-González et al. [88]2018ChileCabrero37°2'S, 72°24'W10Flotation of Sheater1rural26010
Radman et al. [89]2006ArgentinaCapital Federal34°34S, 58°31W125Flotation of Fülleborn1urban151.2
Rivero et al. [90]2015ArgentinaPuerto Iguazú y alrededres25°35′S, 54°34′W405Formol 10%Flotation of Sheater and Sedimentation of Telemann2rural10.49
Rivero et al. [91]2017ArgentinaPuerto Iguazú y alrededres25°35′S, 54°34′W530Formol 10%Direct with lugol, Flotation of Sheater and Sedimentation of Teleman3urban80.90.91.355.60.43.913.412.1
Rodriguez et al. [92]2005ArgentinaMar del Plata38°00′S, 57°33′W171Flotation and Sedimentation2urban667.842.41.55.66.852.2
Roth et al. [93]2018ArgentinaBariloche41°08′S, 71°27′W118FreezadoFlotation of Sheater and Sedimentation of Telemann2urban116.9
Rubel et al. [94]2003ArgentinaCapital Federal34°34S, 58°31W31Formol 5%Sedimentation of Teleman1urban114.0
Rubel et al. [95]2005ArgentinaCapital Federal34°34S, 58°31’W2417Formol 5%Sedimentation of Teleman1urban433.50.713.032.0
Rubel et al. [96]2010ArgentinaCapital Federal34°34’S, 58°31’W421Formol 5%Flotation of Willis1urban726.00.60.90.60.21.74.0
Rubel et al. [97]2019ArgentinaBuenos Aires34°37′S, 58°25′W112Centrifugation and Flotation of Sheater2urban420.50.91.83.6
Sánchez et al. [98]2003ArgentinaComodoro Rivadavia y Rada Tilly45°S, 68°W481Formol 5%Sedimentation de Teleman and Flotation de Willis2urban61.00.20.22.63.617.9
Sánchez Thevenet et al. [99]2003ArgentinaComodoro Rivadavia45°S, 68°W163Formol 5%Sedimentation of Teleman and Flotation of Willis2urban60.80.31.61.48.8
Semenas et al. [100]2014ArgentinaBariloche41°10’S, 71°18’W54Sedimentation of Teleman and Flotation of Sheater2urban101.83.712.83.61.812.87.31.811.029.3
Soriano et al. [101]2010ArgentinaNeuquen rural38°14′S, 69°46′W1298Formol 5%Flotation and Sedimentation2rural80.150.150.1517.870.8416.41.30.3
Soriano et al. [101]2010ArgentinaNeuquén urbano (neuquen y chos malal37°23′S, 70°17′W646Formol 5%Flotation and Sedimentation2urban60.930.312.1716.115.63
Souto et al. [102]2016ArgentinaEl Chalía (Chubut)45°41′S, 70°59′W22Formol 10%Sedimentation of Teleman, Flotation of Willis and copro, Elisa3rural213.69.1
Taranto et al. [103]2000ArgentinaFortín Dragones y Misión Chaqueña23°15’S, 63°20’W106Directo, Flotation of Willis and centrifugation3urban469.81.917.27.5
Torres et al. [104]2004ChilePanguipulli39°38′S, 72°20′W109PAF fenol, alcohol y formaldehídoSedimentation1urban11.8
Torres et al. [104]2004ChileChoshuenco39°50′S, 72°04′W22PAF fenol, alcohol y formaldehídoSedimentation1urban14.5
Vargas et al. [105]2016ChileNiebla39°48'S, 73°14'W78Formol salinoSedimentation of Telemann modified, Flotation Sulphate Zinc, método cuantitativo3115.4
Vargas et al. [105]2016ChileValdivia39°48'S, 73°14'W77Formol salinoSedimentation of Telemann modified, Flotation Sulphate Zinc, método cuantitativo3urban115.6
Winter et al. [106]2018ArgentinaViedma40°48’S, 62°59’W531Flotation de Sheater1urban633.82.20.72.922.840.4
Zonta et al [107]2019ArgentinaClorinda (Formosa)25°17'S, 57°43'W16FormolSedimentation of Ritchie and Flotation of Willis2urban462.537.5
Zunino et al. [108]2000ArgentinaComodoro Rivadavia45°S, 68°W31Formol 5%Flotation of Willis1urban29.73.3
Zunino et al. [108]2000ArgentinaTrelew43°15′S, 65°18′W30Formol 5%Flotation of Willis1urban33.33.333.3
Zunino et al. [108]2000ArgentinaPuerto Madryn42°46′S, 65°02′W29Formol 5%Flotation of Willis1urban110.3
Zunino et al. [108]2000ArgentinaSarmiento45°36′S, 69°05′29Formol 5%Flotation of Willis1urban36.96.924.1
Zunino et al. [108]2000ArgentinaEsquel42°54′S, 71°19'W29Formol 5%Flotation of Willis1urban36.93.413.8
Zunino et al. [108]2000ArgentinaLago Puelo42°09′S, 71°38′W30Formol 5%Flotation of Willis1urban316.76.920.0

Table 1.

Data extracted from the 67 articles selected for analysis.

The number of copro-parasitological techniques used in each study varied between 1 and 3, with a total of 15 different methods ( Table 1 ). The most commonly used techniques were Willis flotation (20 reports), Sheater flotation (15 reports) and Telemann sedimentation (14 reports). In Uruguay only two methods were used: necropsy of stray dogs and coproELISA for Echinococcussp., whereas in Argentina and Chile the techniques in common were Faust, Sheater, Telemann, Willis, and coproELISA for Echinococcussp. Chilean researchers also used a modification of Faust (Teuscher), Burrows, and Harada-Mori for larvae. Other methods used only in Argentina were Füllerborn, Mini Flotac; Ritchie, Carles Barthelemy, direct observation with lugol; and Western Blot and PCR molecular techniques for E. granulosus.

More than 140 sites were analysed in Chile and Argentina ( Figure 2 , Table 1 ); however, the number of sites analysed in Uruguay could not be determined as this information is not given in the 2 selected studies. In Argentina and Chile, a total of 104 urban sites and 43 rural areas were considered ( Table 2 ).

Figure 2.

Distribution of collection sites and species richness in each site.

CountryNumber of studies analysedNumber of sites analysedRural SitesUrban SitesTotal collected faeces (range)Richness (Range)Number of Techniques used
Argentina48110387618,812 (4–2417)17 (1–10)13
Chile19335284,574 (10–972),14 (1–9)11
Uruguay2not reportednot reportednot reported7,134 (79–5356)6 (1–6)2

Table 2.

Summary of studies: Total number of reports analysed for the three countries, number of rural and urban sites, collected samples, techniques used, and species richness.

A total of 22 parasite taxa was recorded ( Table 3 ): 1 trematode (Trematoda sp.), 7 cestodes (Dibothriocephalussp., Dipylidium caninum, Echinococcussp., Taenidae, Taenia multiceps, Taenia hydatigena, Taenia ovis), 13 nematodes (Trichuris vulpis, Eucoleus aerophila, Eucoleus boehmi, Capillariasp., Strongyloidessp., Ancylostomatidae sp., Ancylostomasp., Uncinariasp., Ascarissp., Toxascaris leonina, Toxocara canis, Spirocercasp., and Physalopterasp.), and 1 acanthocephalan species (Oncicola canis). In Argentina the presence of Ancylostomawas recorded up to genus level, whereas in Chile they were recorded only as Ancylostomatidae sp., so while it is likely that there are some shared species, this cannot be established from the records analysed. The distribution of the species is presented in Figures 3 5 , which show that most of the parasitic records are located in the central zone of Chile, while in Argentina there are records at all latitudes, except in an arid zone in the northwest, close to the Andes mountains. Species richness was correlated only with sample size (R = 0.44809, p < 0.05) and varied between sites, from 1 to 10 species (Argentina 1 to 10; Chile 1 to 9; Uruguay 1 to 6) ( Figure 2 ).

Parasite speciesTotal Number of SitesMean prevalence (SD)Number of positive urban sitesMean prevalence in urban sites (SD)Number of positive rural sitesMean prevalence in rural sites (SD)
Dibothriocephalussp.145.7 ± 6.2107.8 ± 6.340.6 ± 0.4
Dipylidium caninum215.6 ± 10.3164.1 ± 9.3510.5 ± 12.8
Echinococcus granulosus527.9 ± 7.11412.9 ± 9.9386 ± 4.7
Taenidae165.1 ± 5.9123.4 ± 4.2410.3 ± 7.5
Taenia hydatigena99 ± 10.573.9 ± 2.7226.8 ± 5.3
Taenia multiceps22.5 ± 2.11114
Taenia ovis1313
Trichuris vulpis6014.7 ± 14.75315.3 ± 15.3710.3 ± 8.7
Eucoleus aerophila414.9 ± 8.8117.4314.1 ± 10.5
Eucoleus boehmi21.8 ± 0.621.8 ± 0.6
Capillariasp.113.9 ± 6.1113.9 ± 6.1
Strongyloidessp.1912 ± 16.1145.6 ± 4.2530.1 ± 22.7
Ancylostomatidae624.2 ± 23.5316 ± 21.7332.3 ± 26.6
Ancylostomasp.6629 ± 23.46229.7 ± 23.3321.4 ± 27.2
Uncinariasp.2117.3 ± 18.51718 ± 20.2414.2 ± 8.8
Ascarissp.87.6 ± 6.269.3 ± 6.122.5 ± 2.2
Toxascaris leonina132.7 ± 3.2112.7 ± 3.522.4 ± 2.2
Toxocara canis8613.6 ± 11.68013.4 ± 11.5615.9 ± 12.8
Spirocercasp.33.4 ± 2.333.4 ± 2.3
Physalopetrasp.11.211.2
Oncicola canis10.310.3

Table 3.

Species recorded in the studies analysed, their distribution (urban versus rural) and mean intensity.

Figure 3.

Distribution of Cestoda collected in Argentina, Chile and Uruguay. A.:Dibothriocephalussp.; B.:Dipilidium caninum; C.:Echinococcussp.; D.: Taenids.

Figure 4.

Distribution of Nematoda (part 1) in Argentina, Chile and Uruguay. A.: Ancylostomatidae.; B.:Ascaris sp.;C.:Strongyloides; D.:Eucocleusspp. andCapillariasp.

Figure 5.

Distribution of Nematoda (part 2) in Argentina, Chile and Uruguay. A.:Toxocara canisandToxascaris leonina.; B.:Trichuris vulpis; C.:Spirocerca; D.:Physalopetra,Trematodasp.andOncicola canis.

The most frequently recorded species was T. canis(86 sites), followed by Ancylostomasp. (66); Trichuris vulpis(60 sites), and Echinococcussp. (52) ( Table 3 ; Figure 4A , 5B , 3E , respectively); others were recorded only once, e.g.: Trematoda sp. and O. canisin Argentina, and Physalopterasp. in Chile. The species detected in Uruguay, except for Echinococcussp., correspond to different taeniid cestodes. Argentina and Chile shared 10 helminth species: Dibothriocephalussp., D. caninumsp., Echinococcussp., Ascarissp., Capillariasp., Strongyloidessp., T. leonina, T. canis, T. vulpis, and Uncinariasp.

The species richness in urban areas (20 species) was slightly higher than in rural areas (17 species) ( Table 3 ). In addition, a higher number of zoonotic species was recorded in urban areas, species such as Uncinaria sp., Ancylostomasp. and Echinococcussp. being widespread and prevalent in the cities ( Table 3 ). Many parasite species showed greater prevalence in urban areas than in rural ones. The only exception to this was T. caniswhich had higher values in the rural areas ( Table 3 ). In Chile 8 species were registered in rural areas and 14 in urban locations, whereas in Argentina the species richness was 10 and 16, respectively ( Table 4 ).

CountryUrbanRural
Richness (Range)Mean richnessMost widespread speciesRichness (Range)Mean richnessMost widespread speciesSimilarity
Argentina16 (1–10)3.8Toxocara canis, Ancylostomasp. Trichuris vulpis10 (1–8)1.7Echinococcussp.7/17
Chile14 (1–9)2.8Toxocara canis, Ancylostomasp. Trichuris vulpis8 (1–6)3Echinococcussp.7/14

Table 4.

Characterisation of urban and rural areas in terms of richness and most widespread species, present in Argentina and Chile.

Of the total taxa recorded, 14 (63.6%) have been registered in humans: Dibothriocephalussp., D. caninum, Echinococcus(sensu lato), Taenidae, T. multiceps, T. hydatigena, Ancylostomatidae sp., Ancylostomasp., Uncinariasp., Ascarissp., E. aerophila, E. boehmi, T. leonina,and T. canis.Some of these species are only occasionally recorded infecting humans, such as D. caninum, Taenia multiceps, E. aerophila, E. boehmiand T. leonina.

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4. Discussion

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.

4.2.1 Cystic echinococcosis

Cystic echinococcosis or hydatidosis, produced by Echinococcus granulosus sensu lato, is a highly endemic parasitic zoonosis in South American countries, especially in Argentina, Chile, Uruguay and Brazil. It is associated with rural areas dedicated mainly to goat and sheep breeding, and causes significant economic losses [47, 69, 116, 117, 118]. From 2009 to 2014, a total of 29,559 new human cases of cystic echinococcosis were registered in these countries. The average fatality rate across the three countries was 2.9%, suggesting that the disease causes approximately 880 deaths annually. The most affected are children <15 years of age, which is indicative of a persistent environmental risk leading to new cases [69, 115]. In the countries analysed, Government Control Programmes have been addressed, and surveillance of the disease from a holistic perspective based on Primary Health Care has been implemented [64, 69, 115, 117]. The number of human cases has a heterogeneous geographical distribution in Chile and Argentina, showing an increase towards the south [116, 118].

4.2.2 Toxocariasis

Toxocariasis is an infection that has a worldwide distribution and is a very important zoonosis due to its frequent occurrence in humans [119]. The estimate of the overall worldwide prevalence of T. canisin dogs of 11.1% represents 100 million dogs, which should alert Public Health experts and policy makers to the need for effective intervention programs [114, 120]. This parasite species has high biotic potential since its eggs contaminate water, soil, grass, and pet fur [51]. The results presented here regarding T. canisin dogs of southern South America show higher prevalence values (around 13%) than the overall prevalence registered worldwide. Also, the risk of infection is similar in urban and rural areas, as suggested in Chile [105]. In Argentina, numerous studies that analysed the seroprevalence of toxocariasis in both children and adults from urban and rural areas reported results varying between 28% and 80% [51, 121, 122]. In Chile, the seroprevalence of this parasitosis varies between 1.3% and 25.4% [105]. Although in Uruguay there are no published records of seroprevalence in humans [123], a recently published work reported that from 2014 to 2018, 20 children had been treated in the public health system for ocular and visceral larva migranssyndrome [123].

4.2.3 Ancylostomiasis

Dog hookworms are Ancylostoma caninum, Ancylostoma braziliense, and Uncinaria stenocephala,and their eggs can be found in faeces. The larvae of these parasites can cause cutaneous larva migransin humans [124]. The main causal agent of larva migransworldwide is A. braziliense; however, the causative agents vary among geographical areas, even within a single country. This disease is mainly endemic to tropical and subtropical developing countries with high average annual temperatures and humid climates, predominating in America from the southern United States, through Mexico, Central, and reaching South America. It is especially prevalent in areas where dogs roam freely, and on sandy, wet soils, such as beaches and playgrounds [124]. In Argentina, records of human cutaneous larva migranscorrespond to the Wichiaboriginal communities in the subtropics of the northwest of the country [103], or to people who had travelled to Brazil [125]. In Chile, there are also few reports of this disease, and they correspond to a 3-year-old patient who acquired the disease in an urban area [126], and to an adult who had been infected on a trip to Brazil [127].

4.2.4 Strongyloidiasis

Strongyloidiasis is prevalent in remote socioeconomically disadvantaged communities around the world, and dogs can act as reservoirs of human strongyloidiasis [128]. This parasitosis is registered in the north of Argentina, with similar infection values in both rural and urban populations and an overall seroprevalence of 19.6% [129, 130]. In Chile, the seroprevalence is much lower (0.25%) in blood donors from Arica and La Union. Human infections by S. stercoralisin this country are therefore endemic, with very low frequency in apparently healthy individuals [131].

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5. General conclusions

This review shows that knowledge of canine helminths in southern South America is scarce. The studies published on dog parasites are not equally distributed across the three countries, with Uruguay presenting the least amount of available information. Data on dog parasites in southern South America is still too incipient for identification of a clear distribution pattern. Homogenisation of criteria would be beneficial, since the methods used are diverse and heterogeneous, some studies using only flotation or sedimentation techniques. Numerous parasitic species were recorded, many of which are zoonotic and widely distributed throughout both urban and rural areas of these countries. The risk of dogs becoming infected is high given the number of parasites present and the style of pet ownership in the communities of these countries, where dogs are allowed to roam freely, and veterinary care is scarce. The high percentage of zoonotic helminths reinforces the need to establish effective prevention measures, not only for parasitosis in animals but also for transmission to humans. Considering that people in both urban and rural areas are at risk of being infected with zoonoses transmitted by dogs, given the high levels of infection they present in their faeces, a One Health approach to public health would be desirable, such that humans and dogs should be treated concomitantly to control the parasites. Furthermore, it would be desirable to implement measures such as control of the canine population, mass treatment of dogs with anthelmintics, education programmes and healthcare alert systems.

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Acknowledgments

This work was funded by PICT 1385–2017 and UNCo B225.

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Written By

Luciano Ritossa, Gustavo Viozzi and Verónica Flores

Submitted: October 26th, 2020 Reviewed: January 20th, 2021 Published: April 1st, 2021