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Research Article Parasitic Zoonoses in Humans and Their Dogs from a Rural Community of Tropical Mexico Antonio Ortega-Pacheco, 1 Juan F. J. Torres-Acosta, 1 Alejandro Alzina-López, 1 Eduardo Gutiérrez-Blanco, 1 Manuel E. Bolio-González, 1 Armando J. Aguilar-Caballero, 1 Roger I. Rodríguez-Vivas, 1 Edwin Gutiérrez-Ruiz, 1 Karla Y. Acosta-Viana, 2 Eugenia Guzmán-Marín, 2 Alberto Rosado-Aguilar, 1 and Matilde Jiménez-Coello 2 1 Departamento Salud Animal y Medicina Preventiva, Cuerpo Acad´ emico en Salud Animal, Facultad de Medicina Veterinaria y Zootecnia, Universidad Aut´ onoma de Yucat´ an, Km 15.5 Carr. M´ erida-Xmatkuil, AP 4-116, M´ erida, YUC, Mexico 2 Laboratorio de Biolog´ ıa Celular, CA Biomedicina de Enfermedades Infecciosas y Parasitarias. C.I.R. “Dr. Hideyo Noguchi”, Universidad Aut´ onoma de Yucat´ an, Avenida Itzaes, No. 490 x C. 59, 97000 M´ erida, YUC, Mexico Correspondence should be addressed to Antonio Ortega-Pacheco; [email protected] Received 1 July 2015; Revised 27 October 2015; Accepted 29 October 2015 Academic Editor: Marcel Tanner Copyright © 2015 Antonio Ortega-Pacheco et al. is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. A cross-sectional study was made on 89 inhabitants and their dogs from a rural community of Yucatan, Mexico, to determine the serological prevalence of some zoonotic parasitic agents. Samples were taken to monitor the presence and intensity of infection with gastrointestinal parasites in dogs. In humans, the serological prevalence of T. canis, T. gondii, and T. spiralis was 29.2%, 91.0%, and 6.7%, respectively. No associations were found between positive cases and studied variables. From the total of blood samples taken from dogs, 87 (97.6%) were seropositive to T. gondii; only 52 viable fecal samples were collected from dogs of which 46.2% had the presence of gastrointestinal parasites with low to moderate intensity; from those, 12% had the presence of T. canis. is study demonstrates the presence of the studied zoonotic agents in the area particularly T. gondii which suggest a common source of infection in dogs and humans and a high number of oocyts present in the environment. Preventive measures must be designed towards good prophylactic practices in domestic and backyard animals (T. canis and T. spiralis). Contaminated sources with T. gondii (food and water) should be further investigated in order to design effective control measures. 1. Introduction Dogs are the source of several zoonotic diseases and their close contact with humans may increase the risk of zoonotic disease transmission particularly when dogs are free to roam. Dogs in urban and rural areas can be used as sentinels in humans and wildlife to evaluate the diversity and environ- mental contamination with parasites [1]. Backyard pigs in tropical Mexico are important for domestic consumption [2, 3]. However, their sanitary management is very poor or nonexisting [3, 4] representing a risk for the transmission of zoonotic parasitic agents. e parasites Toxoplasma gondii and Toxocara spp. are capable of producing systemic and ocular disease in dogs and humans and share soil ingestion as common mode of exposure [5]. However, the protozoa T. gondii are more commonly transmitted by the ingestion of contaminated food or water. Domestic dogs are the principal animal reservoir hosts for Toxocara canis, a common nema- tode throughout the world producing severe anemia and systemic disease in puppies which in humans elicits various syndromes currently characterized as generalized (visceral larva migrans and covert toxocariasis) and compartmental- ized as well as ocular and neurologic [6], with more clinical manifestations on kids [7]. Diverse epidemiological studies have demonstrated that exposition to T. canis varies from countries and regions [8] reaching up to 83% of seropositivity in people from the Caribbean region [9]. Another important foodborne nematode Trichinella spiralis is transmitted to humans generally by the consumption of undercook contam- inated pork meat [10]. Hindawi Publishing Corporation Journal of Tropical Medicine Volume 2015, Article ID 481086, 6 pages http://dx.doi.org/10.1155/2015/481086
7

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Page 1: Research Article Parasitic Zoonoses in Humans and Their Dogs …downloads.hindawi.com/journals/jtm/2015/481086.pdf · larva migrans and covert toxocariasis) and compartmental-ized

Research ArticleParasitic Zoonoses in Humans and Their Dogs froma Rural Community of Tropical Mexico

Antonio Ortega-Pacheco1 Juan F J Torres-Acosta1 Alejandro Alzina-Loacutepez1

Eduardo Gutieacuterrez-Blanco1 Manuel E Bolio-Gonzaacutelez1 Armando J Aguilar-Caballero1

Roger I Rodriacuteguez-Vivas1 Edwin Gutieacuterrez-Ruiz1 Karla Y Acosta-Viana2

Eugenia Guzmaacuten-Mariacuten2 Alberto Rosado-Aguilar1 and Matilde Jimeacutenez-Coello2

1Departamento Salud Animal y Medicina Preventiva Cuerpo Academico en Salud Animal Facultad de Medicina Veterinaria yZootecnia Universidad Autonoma de Yucatan Km 155 Carr Merida-Xmatkuil AP 4-116 Merida YUC Mexico2Laboratorio de Biologıa Celular CA Biomedicina de Enfermedades Infecciosas y Parasitarias CIR ldquoDr Hideyo NoguchirdquoUniversidad Autonoma de Yucatan Avenida Itzaes No 490 x C 59 97000 Merida YUC Mexico

Correspondence should be addressed to Antonio Ortega-Pacheco opachecocorreouadymx

Received 1 July 2015 Revised 27 October 2015 Accepted 29 October 2015

Academic Editor Marcel Tanner

Copyright copy 2015 Antonio Ortega-Pacheco et alThis is an open access article distributed under theCreativeCommonsAttributionLicense which permits unrestricted use distribution and reproduction in anymedium provided the originalwork is properly cited

A cross-sectional study was made on 89 inhabitants and their dogs from a rural community of Yucatan Mexico to determine theserological prevalence of some zoonotic parasitic agents Samples were taken to monitor the presence and intensity of infectionwith gastrointestinal parasites in dogs In humans the serological prevalence of T canis T gondii and T spiralis was 292 910and 67 respectively No associations were found between positive cases and studied variables From the total of blood samplestaken from dogs 87 (976) were seropositive to T gondii only 52 viable fecal samples were collected from dogs of which 462had the presence of gastrointestinal parasites with low to moderate intensity from those 12 had the presence of T canis Thisstudy demonstrates the presence of the studied zoonotic agents in the area particularly T gondii which suggest a common sourceof infection in dogs and humans and a high number of oocyts present in the environment Preventive measures must be designedtowards good prophylactic practices in domestic and backyard animals (T canis and T spiralis) Contaminated sources with Tgondii (food and water) should be further investigated in order to design effective control measures

1 Introduction

Dogs are the source of several zoonotic diseases and theirclose contact with humans may increase the risk of zoonoticdisease transmission particularly when dogs are free to roamDogs in urban and rural areas can be used as sentinels inhumans and wildlife to evaluate the diversity and environ-mental contamination with parasites [1] Backyard pigs intropical Mexico are important for domestic consumption[2 3] However their sanitary management is very poor ornonexisting [3 4] representing a risk for the transmissionof zoonotic parasitic agents The parasites Toxoplasma gondiiand Toxocara spp are capable of producing systemic andocular disease in dogs and humans and share soil ingestionas common mode of exposure [5] However the protozoa T

gondii are more commonly transmitted by the ingestion ofcontaminated food or water Domestic dogs are the principalanimal reservoir hosts for Toxocara canis a common nema-tode throughout the world producing severe anemia andsystemic disease in puppies which in humans elicits varioussyndromes currently characterized as generalized (viscerallarva migrans and covert toxocariasis) and compartmental-ized as well as ocular and neurologic [6] with more clinicalmanifestations on kids [7] Diverse epidemiological studieshave demonstrated that exposition to T canis varies fromcountries and regions [8] reaching up to 83 of seropositivityin people from the Caribbean region [9] Another importantfoodborne nematode Trichinella spiralis is transmitted tohumans generally by the consumption of undercook contam-inated pork meat [10]

Hindawi Publishing CorporationJournal of Tropical MedicineVolume 2015 Article ID 481086 6 pageshttpdxdoiorg1011552015481086

2 Journal of Tropical Medicine

Information related to both animal and human zoonoticparasite infections in rural communities of Mexico is scarceTo establish an effective parasite prevention and controlstrategies it is necessary to understand the biology ofparasites circulating in endemic regions monitoring theirpresence and the risk factors associated in humans reservoiranimals and vectors for a better planning of strategies forprevention and control of zoonotic parasitic diseases Theobjective of this study was to determine the seroprevalenceof humans to T canis T gondii and T spiralis in a rural com-munity of Yucatan Mexico together with the seroprevalenceof T gondii and detection of T canis in their dogs

2 Methods

21 Area of Study The study was conducted in the ruralcommunity of Molas Yucatan Mexico (20∘491015840 and 20∘481015840Nand 89∘371015840 and 89∘381015840W) The community has 2014 inhabi-tants and 379 dwellings A sectional descriptive and prospec-tive study was conducted considering for convenience 90dwellings reporting tenure of at least one dog The commu-nity was divided into four sectors (north-south and east-west) 20 houses in each sector were selected

22 Sampling Each of the selected households was visitedand a directed questionnaire was applied Samples of bloodand feces of at least one dog per household were taken Indogs blood samples were obtained from the cephalic veinand were processed to obtain serum which was frozen atminus20∘Cuntil tested Feces were taken directly from the rectumthen rabies vaccine was applied and dogs were dewormedAdditionally blood samples from an adult person per house-hold were taken In humans blood samples were collected byvenipuncture of the brachial vein prior to written consent ofthe participants and according to the rules of the BioethicsCommittee of the Campus of Biological and AgriculturalSciences at the Autonomous University of Yucatan (CB-CCBA-I-20014-001) Sampleswere processed to obtain serumand frozen at minus20∘C A questionnaire was applied to allsampled persons including questions about their age feedinghabits water sources presence of eye lesions and previousdeworming procedures

23 Laboratory Analysis Fecal samples were processed bycentrifugation-flotation technique [11] positive samples wereexamined quantitatively by McMaster technique to estimatethe number of eggs per gram of feces (epg) with partic-ular attention to T canis Human sera were evaluated forthe measurement of IgG T canis and T spiralis antigensusing ELISA kit (DGR Laboratories International Inc USA)following the manufacturerrsquos instructions For T gondiithe presence of specific IgG antibodies was determined byindirect ELISA (International GmbH RE58241 HamburgGermany) containing tachyzoites of T gondii Serum sampleswere diluted to a ratio of 1 100 in PBS and secondary antibodyanti-human IgG HRP-labeled anti-human IgM HRP werealso marked

Table 1 Nematode infection intensity (epg) and Eucoccidiorida(oocysts per gram of feces) in 52 dogs from a rural community ofYucatan Mexico

Intestinal parasites Low Median HighAncylostoma caninum 458 250 00Toxocara canis 125 00 00Trichuris vulpis 83 42 00Eucoccidiorida 00 42 00Total 666 334 00Low 50ndash100 eg median 101ndash500 eg and high ge500 eg

24 Statistical Analysis The overall prevalence of intestinalparasites in dogs was estimated The intensity of infection(elimination of epg) was classified as low (50ndash100 epg)median (150ndash500 epg) or high (gt550 epg)The overall preva-lence of IgG-positive people to T canis T canis and Tspiralis was also estimated A primary screening of humansseropositive to T canis was assessed using 2 times 2 contingencytables of exposure variables odds ratio and confidenceinterval were determined Since very few negative cases of Tgondii in human and dogs and few positive cases of T spiraliswere found no statistical analysis was performedOdds ratios(OR) and 95 confidence intervals were calculated using Epi-Info software (version 60 CDCAtlanta GA USA)The levelof significance was set at 119875 lt 005

3 Results

A total of 52 viable fecal samples were collected from adultdogs of which 24 (462) had at least some orderspecieskind of intestinal nematode The nematode genera found indog feces wereAncylostoma caninum (708) Toxocara canis(125) Trichuris vulpis (125) and the order Eucoccidior-ida (42)

The intensity of infection of nematode orderspecies ispresented in Table 1 In most cases intensity of the infectionwas low followed by median intensity no cases of highinfection load were seen from the infected dogs all of themhad only a single orderspecies of nematode present

Regarding the serology from human samples 26 (292)from the 89 persons were positive to IgG anti-T canis(Table 2) None of the risk factors studied were significantlyassociated with seropositivity in humans (Table 3) All partic-ipants owned at least one dog and none of them collected thefeces from their animals From the questionnaire 36 personsclaim vision disorders such as cloudy vision and increasedtearing

Regarding IgG anti-T gondii serological results from 89human blood samples collected 906 were positive to IgGT gondii (Table 2) For dogs 89 samples were obtained and976 were seropositive to T gondii Since very few negativecases were found no statistical inferences were feasible Fromthe interviews 93 drink water from commercial carafes 5drink tapwater and 2drink fromboth sources Participantsreported that the ingestion of meat is usually well cooked in82 of cases and 7 claim to eat semicooked meat 888 of

Journal of Tropical Medicine 3

Table 2 Serological frequency of zoonotic agents identified in 89persons from a rural community of Yucatan Mexico

Agent Positive cases (119899) T canis 26 292T gondii 81 910T spiralis 6 67T canis + T gondii 26 292T spiralis + T gondii 4 45

Table 3 Relationship between associated factors with T canisIgG seropositivity in humans from a rural community of YucatanMexico

119899 Positive Prevalence OR 95 CI 119875 valueAge (years)

20ndash40 29 8 276 15 054ndash426 042 (NS)gt40ndash75 55 11 200 mdash mdash mdash

SexMale 8 1 125 mdash mdash mdashFemale 76 18 237 446 005ndash39 041 (NS)

Eyes lesionsYes 52 16 308 13 049ndash36 056 (NS)No 32 8 255 mdash mdash mdash

DewormingYes 32 12 375 18 091ndash602 022 (NS)No 52 13 256 mdash mdash mdash119899 number of humans studied OR odds ratio CI confidence interval and119875 probabilityNS not significant

the interviewed persons eat sausages and from the 10 persons(112) who do not eat sausages 2 were seronegative

Only 6 (69) persons were found seropositive to Tspiralis (Table 2)

4 Discussion

The prevalence of dogs infected with gastrointestinal par-asites in this study is considered high and similar to thereported one in other regions of the world that is 524 inArgentina [12] 53 inHungary [13] and 68 in Nigeria [14]The high variation observed has been associated with variousweather conditions idiosyncrasies and sanitary control ofdogs A previous study in the same community was per-formed four years ago and prevalence of gastrointestinal par-asites in dogs was 80 with a high egg output of A caninumT canis and T vulpis found in this study deworming of dogswas performed and talks to children adolescents and adultsabout health management of dogs were given [15] Theseactions could explain the lower prevalence and intensityof infection reported at this time categorized between lowand medium intensity of infection In the specific case ofT canis a higher prevalence (125) was found comparedto previous studies in the same area where 62 was found[15] T canis mainly affects puppies with frequently fatalconsequences In adult dogs the infection is minor and

usually asymptomaticThe annual variation in the number ofinfected puppies in the regionmay influence the disposal andspreading of T canis eggs The presence of infected puppiescan increase the number of eggs and larvae deposited in theenvironment in which they can remain infective for severalmonths infecting other dogs andwith great potential to infecthumans especially children

Human toxocariasis is worldwide distributed and occurswhen embryonated eggs from the environment are ingestedThis is more critical when dog overpopulation is presentwithout the practice of preventive medicine (deworming)Children with pica are found at increased risk particularly inregions of low socioeconomic status and with proliferationof dogs andor those who have puppies at home [7] Adultsare also at risk of infection as shown by several studies whereprevalence of 268 in Brazil was reported [16] and 19 inLebanon was reported [17] In Argentina seroprevalence of20ndash38 in children and 10ndash39 in general population [18 19]is reported In Mexico 38 of people suffering from acutenongranulomatous uveitis were seropositive for T canis [20]with a prevalence of 46 to 1759 reported in children lessthan 16 years of age [21] Results of this study indicate a highspread of infective eggs in the rural community probablybecause of the high density of dogs having free access to thestreet and lack of health programs including a dewormingprogram

Although deworming has been introduced in healthmanagement of dogs in the studied community still spread-ing of infected eggs and contamination of the area are presentthus efforts to intensify the deworming of dog and cat arenecessary for better control results The ocular larva migranssyndrome is one of the major health problems associatedwith T canis [22] However eye lesions were not statisticallyassociated with seropositive persons this syndrome is morecritical in childrenwhere severe problems have been reported[7] so studies to evaluate the impact of this parasite on chil-dren should be designed and performedT canis andT gondiiare associated with eye lesions such as uveitis [23] Ocularlarva migrans in the case of toxocariasis may cause visualimpairment as a response of granulomatous inflammatoryreaction with consequences such as blindness and secondaryglaucoma [7 24] In the present study no association wasfound in patients seropositive toT canis and vision disordersHowever other symptoms not evaluated in the present studymay involve headache muscle pain influenza-like syndromeand diarrhea in seropositive patients [25] In a previousstudy conducted in Mexico T canis positive patients werehighly associated with ankylosing spondylitis [26] Youngchildren lt5 years are most affected with toxocariasis withclinical signs of fever abdominal pain (probably due tohepatomegaly) and lower respiratory symptoms [7] Furtherstudies should be focused on children in the studied regionexamining the different body systems to evaluate the impactof this zoonotic agent

The high prevalence of T gondii found in dogs andtheir owners demonstrates a high spread of oocysts in thestudied area with a probably common source of infectionThe prevalence found in dogs from Brazil was 269 witha higher risk for dogs over five years of age [27] However

4 Journal of Tropical Medicine

in the present study due to the very high prevalence foundall animals are expected to seroconvert since young ageswith frequent episodes of reinfection In Mexico dog fromshelters in Veracruz also showed a high seroprevalencereaching up to 673 [28] Free roaming dogs are indicatorsof the high contamination of the environment with T gondiioocysts as they may be sentinels of exposition In humanstoxoplasmosis has been reported previously in the Yucatanpeninsula with seroprevalence of 25 in non-cat owners[29] and also associated in patients with recent cases ofspontaneous abortion [30 31] Seroprevalence may reach upto 873 in humans from rural communities from Yucatan[32] In humans the main route of infection of T gondii is bythe ingestion of tissue cysts [33] In the present study the oralroute by consumption of undercooked meat (tissue cysts) ismore likely but also the ingestion of infective oocysts fromcontaminated water as previously demonstrated could occur[34] Considering the 100 T gondii seroprevalence found in50 studied cats from the same region [4] the density of catsand constant new born kittens in the village with excretion ofhigh numbers of oocysts probably occurred contaminatingthe environment and probable water sources Even when 93of the interviewed persons drank commercial bottled watertap water and water from artisanal wells are also used forseveral other activities and may be considered as a potentialsource of infection with T gondii oocysts However sincedogs in the studied area are fed with human leftovers [35]contaminated meat and sausages may also be involved in thetransmission cycle

T spiralis is a nematode capable of infecting anymammalingesting infected raw or undercooked meat Infection inhumans with this nematode is described worldwide andoutbreaks have been reported in developed countries infect-ing over 30 of people ingesting wild boar meat [36]Exposition of consumers to infected meat can reach up to651 of incidence especially when meat is not tested priorto consumption when slaughter is made in households [37]InMexico consumption of porkmeat coming from backyardis very common in rural villages without any kind of qualitytest [4] In Mexico the Ministry of Health (NOM-194-SSA1-2014)makes the inspection of porkmeat in search ofT spiraliscompulsory However this is rarely done at the abattoirsor before commercialization T spiralis in Mexico has beenreported since 1975 in Zacatecas state where several outbreakshave been reported in cases with mortality rates of 33in some cases in those outbreaks transmission was mostcommonly caused by the ingestion of raw pork productsor undercooked meat [38] More recently a prevalence of1 using ELISA was reported in semirural county areas ofMexico [39] In Yucatan no proper surveys of T spiralis havebeen performed in humans or animalsThis is the first reportof T spiralis serological presence in humans from YucatanHowever the Toxocara larval excretory antigen is normallyused in serological tests that may exhibit low specificitydue to cross-reaction between related helminthes includingT canis [40] Further research is needed to investigatethe epidemiology of these zoonotic helminthes using moreaccurate techniques for diagnosis including the search of theagent in farm and backyard pigs from the region

The main limitation of the present study was the smallsample size used and consequently results may be biased ormay not be representative of the rural communities from thestudied area However this study may be a good indicatorof the zoonotic situation and establish the bases for furtherstudies including a bigger and targeted sample size from bothanimals and humans

5 Conclusion

It is concluded that the dogs in a rural community of Yucatanare reservoirs of some helminthes parasites specially T canisThis implies a high risk of the presence of parasites in theenvironment of the village and a potential risk of infectionfor the human community It is important to improvethe dissemination and promotion of educational programson this important zoonosis and establish effective controlmeasures to reduce the emission of eggs and avoid contactof human with areas contaminated with dog feces Otherimportant zoonotic parasites (T gondii andT spiralis) are alsocirculating

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

This paper was financially supported by the Ministry ofEducation in Mexico through ldquoPRODEPrdquo (Programa parael Desarrollo Profesional Docente) as part of the projectldquoEpidemiologıa de Enfermedades Zoonoticas Transmitidaspor Vectores (ETVrsquoS) de Importancia en Salud Publicardquo

References

[1] A L Salb H W Barkema B T Elkin et al ldquoDogs as sourcesand sentinels of parasites in humans and wildlife NorthernCanadardquo Emerging Infectious Diseases vol 14 no 1 pp 60ndash632008

[2] J G Berdugo and C Franco ldquoGanaderia de traspatio en elEstado de Yucatanrdquo in Memorias de la Segunda Reunion SobreProduccion Animal Tropical M R Godoy J C Segura and AArellano Eds pp 114ndash120 Merida Yucatan Merida Mexico1991

[3] R Ku-Duperon W Trejo-Lizama A J Aguilar-Caballero etal ldquoGastrointestinal parasitism in the Mexican hairless pig inbackyard in the state of Yucatan Mexicordquo Revista Colombianade Ciencia Animal vol 6 pp 17ndash24 2013

[4] M Jimenez-Coello K Y Acosta-Viana E Guzman-Marin et alldquoThe occurrence of Toxoplasma gondii antibodies in backyardpigs and cats from an endemic tropical area ofMexicordquo Tropicaland Subtropical Agroecosystems vol 16 no 1 pp 89ndash92 2013

[5] J L Jones D Kruszon-Moran K Won M Wilson and P MSchantz ldquoToxoplasma gondii and Toxocara spp co-infectionrdquoAmerican Journal of Tropical Medicine and Hygiene vol 78 no1 pp 35ndash39 2008

Journal of Tropical Medicine 5

[6] L T Glickman and P M Schantz ldquoEpidemiology and patho-genesis of zoonotic toxocariasisrdquo Epidemiologic Reviews vol 3no 1 pp 230ndash250 1981

[7] D Despommier ldquoToxocariasis clinical aspects epidemiologymedical ecology and molecular aspectsrdquo Clinical MicrobiologyReviews vol 16 no 2 pp 265ndash272 2003

[8] H V Smith and R Noordin ldquoDiagnostic limitations and futuretrends in the serodiagnosis of human toxocariasisrdquo in ToxocaraThe Enigmatic Parasite C V Holland and H V Smith Edschapter 7 pp 89ndash112 CABI Publishing Wallingford UK 2006

[9] D EThompsonD A P Bundy E S Cooper and PM SchantzldquoEdidemiological characteristics of Toxocara canis zoonoticinfection of children in a Caribbean communityrdquo Bulletin of theWorld Health Organization vol 64 no 2 pp 283ndash290 1986

[10] J V Conlan K Vongxay B Khamlome et al ldquoPatterns and risksof Trichinella infection in humans and pigs in northern LaosrdquoPLoS Neglected Tropical Diseases vol 8 no 7 Article ID e30342014

[11] R I Rodrıguez-Vivas and L A Cob-Galera Tecnicas Diagnos-tico en Parasitologıa Veterinaria Universidad Autonoma deYucatan Merida Mexico 2nd edition 2005

[12] M F Fontanarrosa D Vezzani J Basabe and D F Eiras ldquoAnepidemiological study of gastrointestinal parasites of dogs fromSouthern Greater Buenos Aires (Argentina) age gender breedmixed infections and seasonal and spatial patternsrdquo VeterinaryParasitology vol 136 no 3-4 pp 283ndash295 2006

[13] E Fok V Szatmari K Busak and F Rozgonyi ldquoPrevalence ofintestinal parasites in dogs in some urban and rural areas ofHungaryrdquo Veterinary Quarterly vol 23 no 2 pp 96ndash98 2001

[14] B M Anene T O Nnaji and A B Chime ldquoIntestinal parasiticinfections of dogs in the Nsukka area of Enugu State NigeriardquoPreventive Veterinary Medicine vol 27 no 1-2 pp 89ndash94 1996

[15] R I Rodrıguez-Vivas E Gutierrez-Ruiz M E Bolio-Gonzalezet al ldquoAn epidemiological study of intestinal parasites of dogsfrom Yucatan Mexico and their risk to public healthrdquo Vector-Borne and Zoonotic Diseases vol 11 no 8 pp 1141ndash1144 2011

[16] G Rubinsky-Elefant M da Silva-Nunes R S MalafronteP T Muniz and M U Ferreira ldquoHuman toxocariasis inrural Brazilian Amazonia seroprevalence risk factors andspatial distributionrdquo American Journal of Tropical Medicine andHygiene vol 79 no 1 pp 93ndash98 2008

[17] Z A Kanafani A Skoury G F Araj et al ldquoSeroprevalence oftoxocariasis in Lebanon a pilot studyrdquo Parasitology vol 132 no5 pp 635ndash639 2006

[18] N E Radman S M Archelli R D Fonrouge M D V Guardisand O R Linzitto ldquoHuman toxocarosis Its seroprevalence inthe City of La Platardquo Memorias do Instituto Oswaldo Cruz vol95 no 3 pp 281ndash285 2000

[19] J M Alonso M V I Bojanich M Chamorro and J O Gorod-ner ldquoToxocara seroprevalence in children from a subtropicalcity in Argentinardquo Revista do Instituto de Medicina Tropical deSao Paulo vol 42 no 4 pp 235ndash237 2000

[20] F Jimenez-Balderas J Garcıa-Jaimes R Rıos et al ldquoIsolation ofIgG antibodies to Toxocara in ankylosing spondylitis patientswith acute anterior uveıtisrdquo Korean Journal of Ophthalmologyvol 28 no 3 pp 207ndash212 2014

[21] C Romero Nunez G D Mendoza Martınez S Yanez ArteagaM Ponce Macotela P Bustamante Montes and N RamırezDuran ldquoPrevalence and risk factors associated with toxocaracanis infection in childrenrdquo The Scientific World Journal vol2013 Article ID 572089 4 pages 2013

[22] D Woodhall M C Starr S P Montgomery et al ldquoOcular tox-ocariasis epidemiologic anatomic and therapeutic variationsbased on a survey of ophthalmic subspecialistsrdquo Ophthalmol-ogy vol 119 no 6 pp 1211ndash1217 2012

[23] S J Lim S E Lee S H Kim et al ldquoPrevalence of Toxoplasmagondii and Toxocara canis among patients with uveitisrdquo OcularImmunology and Inflammation vol 22 no 5 pp 360ndash366 2014

[24] S H Gillespie W J Dinning A Voller and N S CrowcroftldquoThe spectrum of ocular toxocariasisrdquo Eye vol 7 no 3 pp 415ndash418 1993

[25] D Antolava P Jarcuska M Janicko et al ldquoSeroprevalenceof human Toxocara infections in the Roma and non-Romapopulations of Eastern Slovakia a cross-sectional studyrdquo Epi-demiology and Infection vol 143 no 10 pp 1ndash10 2015

[26] F J Jimenez-Balderas A Camargo-Coronel J Gargia-Jaimes etal ldquoA study on parasites inMexican rheumatic disease patientsrdquoJournal of the Egyptian Society of Parasitology vol 42 no 2 pp271ndash280 2012

[27] H Langoni F Fornazari R C da Silva E T Monti and F BVilla ldquoPrevalence of antibodies against Toxoplasma gondii andNeospora caninum in dogsrdquo Brazilian Journal of Microbiologyvol 44 no 4 pp 1327ndash1330 2013

[28] C Alvarado-Esquivel D Romero-Salas A Cruz-Romero et alldquoHigh prevalence of Toxoplasma gondii antibodies in dogs inVeracruz Mexicordquo BMCVeterinary Research vol 10 article 1912014

[29] M Jimenez-Coello E Guzman-Marın A Ortega-Pacheco andK Y Acosta-Viana ldquoImmunological status against Toxoplasmagondii in non-cat owners from an endemic Region of MexicordquoVector-Borne and Zoonotic Diseases vol 11 no 8 pp 1057ndash10612011

[30] J Zavala-Velazquez E Guzman-Marın M Barrera-Perez andM E Rodrıguez-Felix ldquoToxoplasmosis and abortion in patientsat the OrsquoHoran Hospital of Merida Yucatanrdquo Salud Publica deMexico vol 31 no 5 pp 664ndash668 1989

[31] I A Vado-Solıs V Suarez-Solıs B Jimenez-Delgadillo J EZavala-Velazquez and J C Segura-Correa ldquoToxoplasma gondiipresence in women with spontaneous abortion in YucatanMexicordquoThe Journal of Parasitology vol 99 no 2 pp 383ndash3852013

[32] M Jimenez-Coello E Guzman-Marin M Rosado-Barrera Met al ldquoSeoprevalence of Toxoplasma gondii in a por ruralcommunity from Yucatan Mexicordquo in Memories from the 13thInternational Congress of Parasitology August 10ndash15 Mexico2014 2014

[33] A Kijlstra and E Jongert ldquoToxoplasma-safe meat close torealityrdquo Trends in Parasitology vol 25 no 1 pp 18ndash22 2009

[34] J L Jones and J P Dubey ldquoWaterborne toxoplasmosismdashrecentdevelopmentsrdquoExperimental Parasitology vol 124 no 1 pp 10ndash25 2010

[35] A Ortega-Pacheco J C Rodriguez-Buenfil M E Bolio-Gonzalez C H Sauri-Arceo M Jimenez-Coello and C LForsberg ldquoA survey of dog populations inUrban and rural areasof YucatanMexicordquoAnthrozoos vol 20 no 3 pp 261ndash274 2007

[36] M Faber S Schink A Mayer-Scholl et al ldquoOutbreak oftrichinellosis due to wild boar meat and evaluation of theeffectiveness of post exposure prophylaxis Germany 2013rdquoClinical Infectious Diseases vol 60 no 2 pp e98ndashe104 2015

[37] C Dobrescu H Hriscu M Emandi C Zamfir and C NemetldquoConsumption of untested pork contributed to over two-thousand clinical cases of human trichinellosis in RomaniardquoFolia Parasitologica vol 61 no 6 pp 558ndash560 2014

6 Journal of Tropical Medicine

[38] J Cabral-Soto H Villicana-Fuentes R Fragoso-Uribe and AContreras ldquoThe epidemiological profile of trichinosis in thestate of Zacatecasrdquo Salud Publica de Mexico vol 32 no 5 pp575ndash582 1990

[39] J L De-La-Rosa J G Aranda E Padilla andD Correa ldquoPreva-lence and risk factors associated with serum antibodies againstTrichinella spiralisrdquo International Journal for Parasitology vol28 no 2 pp 317ndash321 1998

[40] S Ozkoc S Bayram Delibas and C Akisu ldquoEvaluation ofTrichinella cross-reactions in the serological diagnosis of toxo-cariasisrdquoMikrobiyoloji Bulteni vol 46 no 3 pp 456ndash463 2012

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 2: Research Article Parasitic Zoonoses in Humans and Their Dogs …downloads.hindawi.com/journals/jtm/2015/481086.pdf · larva migrans and covert toxocariasis) and compartmental-ized

2 Journal of Tropical Medicine

Information related to both animal and human zoonoticparasite infections in rural communities of Mexico is scarceTo establish an effective parasite prevention and controlstrategies it is necessary to understand the biology ofparasites circulating in endemic regions monitoring theirpresence and the risk factors associated in humans reservoiranimals and vectors for a better planning of strategies forprevention and control of zoonotic parasitic diseases Theobjective of this study was to determine the seroprevalenceof humans to T canis T gondii and T spiralis in a rural com-munity of Yucatan Mexico together with the seroprevalenceof T gondii and detection of T canis in their dogs

2 Methods

21 Area of Study The study was conducted in the ruralcommunity of Molas Yucatan Mexico (20∘491015840 and 20∘481015840Nand 89∘371015840 and 89∘381015840W) The community has 2014 inhabi-tants and 379 dwellings A sectional descriptive and prospec-tive study was conducted considering for convenience 90dwellings reporting tenure of at least one dog The commu-nity was divided into four sectors (north-south and east-west) 20 houses in each sector were selected

22 Sampling Each of the selected households was visitedand a directed questionnaire was applied Samples of bloodand feces of at least one dog per household were taken Indogs blood samples were obtained from the cephalic veinand were processed to obtain serum which was frozen atminus20∘Cuntil tested Feces were taken directly from the rectumthen rabies vaccine was applied and dogs were dewormedAdditionally blood samples from an adult person per house-hold were taken In humans blood samples were collected byvenipuncture of the brachial vein prior to written consent ofthe participants and according to the rules of the BioethicsCommittee of the Campus of Biological and AgriculturalSciences at the Autonomous University of Yucatan (CB-CCBA-I-20014-001) Sampleswere processed to obtain serumand frozen at minus20∘C A questionnaire was applied to allsampled persons including questions about their age feedinghabits water sources presence of eye lesions and previousdeworming procedures

23 Laboratory Analysis Fecal samples were processed bycentrifugation-flotation technique [11] positive samples wereexamined quantitatively by McMaster technique to estimatethe number of eggs per gram of feces (epg) with partic-ular attention to T canis Human sera were evaluated forthe measurement of IgG T canis and T spiralis antigensusing ELISA kit (DGR Laboratories International Inc USA)following the manufacturerrsquos instructions For T gondiithe presence of specific IgG antibodies was determined byindirect ELISA (International GmbH RE58241 HamburgGermany) containing tachyzoites of T gondii Serum sampleswere diluted to a ratio of 1 100 in PBS and secondary antibodyanti-human IgG HRP-labeled anti-human IgM HRP werealso marked

Table 1 Nematode infection intensity (epg) and Eucoccidiorida(oocysts per gram of feces) in 52 dogs from a rural community ofYucatan Mexico

Intestinal parasites Low Median HighAncylostoma caninum 458 250 00Toxocara canis 125 00 00Trichuris vulpis 83 42 00Eucoccidiorida 00 42 00Total 666 334 00Low 50ndash100 eg median 101ndash500 eg and high ge500 eg

24 Statistical Analysis The overall prevalence of intestinalparasites in dogs was estimated The intensity of infection(elimination of epg) was classified as low (50ndash100 epg)median (150ndash500 epg) or high (gt550 epg)The overall preva-lence of IgG-positive people to T canis T canis and Tspiralis was also estimated A primary screening of humansseropositive to T canis was assessed using 2 times 2 contingencytables of exposure variables odds ratio and confidenceinterval were determined Since very few negative cases of Tgondii in human and dogs and few positive cases of T spiraliswere found no statistical analysis was performedOdds ratios(OR) and 95 confidence intervals were calculated using Epi-Info software (version 60 CDCAtlanta GA USA)The levelof significance was set at 119875 lt 005

3 Results

A total of 52 viable fecal samples were collected from adultdogs of which 24 (462) had at least some orderspecieskind of intestinal nematode The nematode genera found indog feces wereAncylostoma caninum (708) Toxocara canis(125) Trichuris vulpis (125) and the order Eucoccidior-ida (42)

The intensity of infection of nematode orderspecies ispresented in Table 1 In most cases intensity of the infectionwas low followed by median intensity no cases of highinfection load were seen from the infected dogs all of themhad only a single orderspecies of nematode present

Regarding the serology from human samples 26 (292)from the 89 persons were positive to IgG anti-T canis(Table 2) None of the risk factors studied were significantlyassociated with seropositivity in humans (Table 3) All partic-ipants owned at least one dog and none of them collected thefeces from their animals From the questionnaire 36 personsclaim vision disorders such as cloudy vision and increasedtearing

Regarding IgG anti-T gondii serological results from 89human blood samples collected 906 were positive to IgGT gondii (Table 2) For dogs 89 samples were obtained and976 were seropositive to T gondii Since very few negativecases were found no statistical inferences were feasible Fromthe interviews 93 drink water from commercial carafes 5drink tapwater and 2drink fromboth sources Participantsreported that the ingestion of meat is usually well cooked in82 of cases and 7 claim to eat semicooked meat 888 of

Journal of Tropical Medicine 3

Table 2 Serological frequency of zoonotic agents identified in 89persons from a rural community of Yucatan Mexico

Agent Positive cases (119899) T canis 26 292T gondii 81 910T spiralis 6 67T canis + T gondii 26 292T spiralis + T gondii 4 45

Table 3 Relationship between associated factors with T canisIgG seropositivity in humans from a rural community of YucatanMexico

119899 Positive Prevalence OR 95 CI 119875 valueAge (years)

20ndash40 29 8 276 15 054ndash426 042 (NS)gt40ndash75 55 11 200 mdash mdash mdash

SexMale 8 1 125 mdash mdash mdashFemale 76 18 237 446 005ndash39 041 (NS)

Eyes lesionsYes 52 16 308 13 049ndash36 056 (NS)No 32 8 255 mdash mdash mdash

DewormingYes 32 12 375 18 091ndash602 022 (NS)No 52 13 256 mdash mdash mdash119899 number of humans studied OR odds ratio CI confidence interval and119875 probabilityNS not significant

the interviewed persons eat sausages and from the 10 persons(112) who do not eat sausages 2 were seronegative

Only 6 (69) persons were found seropositive to Tspiralis (Table 2)

4 Discussion

The prevalence of dogs infected with gastrointestinal par-asites in this study is considered high and similar to thereported one in other regions of the world that is 524 inArgentina [12] 53 inHungary [13] and 68 in Nigeria [14]The high variation observed has been associated with variousweather conditions idiosyncrasies and sanitary control ofdogs A previous study in the same community was per-formed four years ago and prevalence of gastrointestinal par-asites in dogs was 80 with a high egg output of A caninumT canis and T vulpis found in this study deworming of dogswas performed and talks to children adolescents and adultsabout health management of dogs were given [15] Theseactions could explain the lower prevalence and intensityof infection reported at this time categorized between lowand medium intensity of infection In the specific case ofT canis a higher prevalence (125) was found comparedto previous studies in the same area where 62 was found[15] T canis mainly affects puppies with frequently fatalconsequences In adult dogs the infection is minor and

usually asymptomaticThe annual variation in the number ofinfected puppies in the regionmay influence the disposal andspreading of T canis eggs The presence of infected puppiescan increase the number of eggs and larvae deposited in theenvironment in which they can remain infective for severalmonths infecting other dogs andwith great potential to infecthumans especially children

Human toxocariasis is worldwide distributed and occurswhen embryonated eggs from the environment are ingestedThis is more critical when dog overpopulation is presentwithout the practice of preventive medicine (deworming)Children with pica are found at increased risk particularly inregions of low socioeconomic status and with proliferationof dogs andor those who have puppies at home [7] Adultsare also at risk of infection as shown by several studies whereprevalence of 268 in Brazil was reported [16] and 19 inLebanon was reported [17] In Argentina seroprevalence of20ndash38 in children and 10ndash39 in general population [18 19]is reported In Mexico 38 of people suffering from acutenongranulomatous uveitis were seropositive for T canis [20]with a prevalence of 46 to 1759 reported in children lessthan 16 years of age [21] Results of this study indicate a highspread of infective eggs in the rural community probablybecause of the high density of dogs having free access to thestreet and lack of health programs including a dewormingprogram

Although deworming has been introduced in healthmanagement of dogs in the studied community still spread-ing of infected eggs and contamination of the area are presentthus efforts to intensify the deworming of dog and cat arenecessary for better control results The ocular larva migranssyndrome is one of the major health problems associatedwith T canis [22] However eye lesions were not statisticallyassociated with seropositive persons this syndrome is morecritical in childrenwhere severe problems have been reported[7] so studies to evaluate the impact of this parasite on chil-dren should be designed and performedT canis andT gondiiare associated with eye lesions such as uveitis [23] Ocularlarva migrans in the case of toxocariasis may cause visualimpairment as a response of granulomatous inflammatoryreaction with consequences such as blindness and secondaryglaucoma [7 24] In the present study no association wasfound in patients seropositive toT canis and vision disordersHowever other symptoms not evaluated in the present studymay involve headache muscle pain influenza-like syndromeand diarrhea in seropositive patients [25] In a previousstudy conducted in Mexico T canis positive patients werehighly associated with ankylosing spondylitis [26] Youngchildren lt5 years are most affected with toxocariasis withclinical signs of fever abdominal pain (probably due tohepatomegaly) and lower respiratory symptoms [7] Furtherstudies should be focused on children in the studied regionexamining the different body systems to evaluate the impactof this zoonotic agent

The high prevalence of T gondii found in dogs andtheir owners demonstrates a high spread of oocysts in thestudied area with a probably common source of infectionThe prevalence found in dogs from Brazil was 269 witha higher risk for dogs over five years of age [27] However

4 Journal of Tropical Medicine

in the present study due to the very high prevalence foundall animals are expected to seroconvert since young ageswith frequent episodes of reinfection In Mexico dog fromshelters in Veracruz also showed a high seroprevalencereaching up to 673 [28] Free roaming dogs are indicatorsof the high contamination of the environment with T gondiioocysts as they may be sentinels of exposition In humanstoxoplasmosis has been reported previously in the Yucatanpeninsula with seroprevalence of 25 in non-cat owners[29] and also associated in patients with recent cases ofspontaneous abortion [30 31] Seroprevalence may reach upto 873 in humans from rural communities from Yucatan[32] In humans the main route of infection of T gondii is bythe ingestion of tissue cysts [33] In the present study the oralroute by consumption of undercooked meat (tissue cysts) ismore likely but also the ingestion of infective oocysts fromcontaminated water as previously demonstrated could occur[34] Considering the 100 T gondii seroprevalence found in50 studied cats from the same region [4] the density of catsand constant new born kittens in the village with excretion ofhigh numbers of oocysts probably occurred contaminatingthe environment and probable water sources Even when 93of the interviewed persons drank commercial bottled watertap water and water from artisanal wells are also used forseveral other activities and may be considered as a potentialsource of infection with T gondii oocysts However sincedogs in the studied area are fed with human leftovers [35]contaminated meat and sausages may also be involved in thetransmission cycle

T spiralis is a nematode capable of infecting anymammalingesting infected raw or undercooked meat Infection inhumans with this nematode is described worldwide andoutbreaks have been reported in developed countries infect-ing over 30 of people ingesting wild boar meat [36]Exposition of consumers to infected meat can reach up to651 of incidence especially when meat is not tested priorto consumption when slaughter is made in households [37]InMexico consumption of porkmeat coming from backyardis very common in rural villages without any kind of qualitytest [4] In Mexico the Ministry of Health (NOM-194-SSA1-2014)makes the inspection of porkmeat in search ofT spiraliscompulsory However this is rarely done at the abattoirsor before commercialization T spiralis in Mexico has beenreported since 1975 in Zacatecas state where several outbreakshave been reported in cases with mortality rates of 33in some cases in those outbreaks transmission was mostcommonly caused by the ingestion of raw pork productsor undercooked meat [38] More recently a prevalence of1 using ELISA was reported in semirural county areas ofMexico [39] In Yucatan no proper surveys of T spiralis havebeen performed in humans or animalsThis is the first reportof T spiralis serological presence in humans from YucatanHowever the Toxocara larval excretory antigen is normallyused in serological tests that may exhibit low specificitydue to cross-reaction between related helminthes includingT canis [40] Further research is needed to investigatethe epidemiology of these zoonotic helminthes using moreaccurate techniques for diagnosis including the search of theagent in farm and backyard pigs from the region

The main limitation of the present study was the smallsample size used and consequently results may be biased ormay not be representative of the rural communities from thestudied area However this study may be a good indicatorof the zoonotic situation and establish the bases for furtherstudies including a bigger and targeted sample size from bothanimals and humans

5 Conclusion

It is concluded that the dogs in a rural community of Yucatanare reservoirs of some helminthes parasites specially T canisThis implies a high risk of the presence of parasites in theenvironment of the village and a potential risk of infectionfor the human community It is important to improvethe dissemination and promotion of educational programson this important zoonosis and establish effective controlmeasures to reduce the emission of eggs and avoid contactof human with areas contaminated with dog feces Otherimportant zoonotic parasites (T gondii andT spiralis) are alsocirculating

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

This paper was financially supported by the Ministry ofEducation in Mexico through ldquoPRODEPrdquo (Programa parael Desarrollo Profesional Docente) as part of the projectldquoEpidemiologıa de Enfermedades Zoonoticas Transmitidaspor Vectores (ETVrsquoS) de Importancia en Salud Publicardquo

References

[1] A L Salb H W Barkema B T Elkin et al ldquoDogs as sourcesand sentinels of parasites in humans and wildlife NorthernCanadardquo Emerging Infectious Diseases vol 14 no 1 pp 60ndash632008

[2] J G Berdugo and C Franco ldquoGanaderia de traspatio en elEstado de Yucatanrdquo in Memorias de la Segunda Reunion SobreProduccion Animal Tropical M R Godoy J C Segura and AArellano Eds pp 114ndash120 Merida Yucatan Merida Mexico1991

[3] R Ku-Duperon W Trejo-Lizama A J Aguilar-Caballero etal ldquoGastrointestinal parasitism in the Mexican hairless pig inbackyard in the state of Yucatan Mexicordquo Revista Colombianade Ciencia Animal vol 6 pp 17ndash24 2013

[4] M Jimenez-Coello K Y Acosta-Viana E Guzman-Marin et alldquoThe occurrence of Toxoplasma gondii antibodies in backyardpigs and cats from an endemic tropical area ofMexicordquo Tropicaland Subtropical Agroecosystems vol 16 no 1 pp 89ndash92 2013

[5] J L Jones D Kruszon-Moran K Won M Wilson and P MSchantz ldquoToxoplasma gondii and Toxocara spp co-infectionrdquoAmerican Journal of Tropical Medicine and Hygiene vol 78 no1 pp 35ndash39 2008

Journal of Tropical Medicine 5

[6] L T Glickman and P M Schantz ldquoEpidemiology and patho-genesis of zoonotic toxocariasisrdquo Epidemiologic Reviews vol 3no 1 pp 230ndash250 1981

[7] D Despommier ldquoToxocariasis clinical aspects epidemiologymedical ecology and molecular aspectsrdquo Clinical MicrobiologyReviews vol 16 no 2 pp 265ndash272 2003

[8] H V Smith and R Noordin ldquoDiagnostic limitations and futuretrends in the serodiagnosis of human toxocariasisrdquo in ToxocaraThe Enigmatic Parasite C V Holland and H V Smith Edschapter 7 pp 89ndash112 CABI Publishing Wallingford UK 2006

[9] D EThompsonD A P Bundy E S Cooper and PM SchantzldquoEdidemiological characteristics of Toxocara canis zoonoticinfection of children in a Caribbean communityrdquo Bulletin of theWorld Health Organization vol 64 no 2 pp 283ndash290 1986

[10] J V Conlan K Vongxay B Khamlome et al ldquoPatterns and risksof Trichinella infection in humans and pigs in northern LaosrdquoPLoS Neglected Tropical Diseases vol 8 no 7 Article ID e30342014

[11] R I Rodrıguez-Vivas and L A Cob-Galera Tecnicas Diagnos-tico en Parasitologıa Veterinaria Universidad Autonoma deYucatan Merida Mexico 2nd edition 2005

[12] M F Fontanarrosa D Vezzani J Basabe and D F Eiras ldquoAnepidemiological study of gastrointestinal parasites of dogs fromSouthern Greater Buenos Aires (Argentina) age gender breedmixed infections and seasonal and spatial patternsrdquo VeterinaryParasitology vol 136 no 3-4 pp 283ndash295 2006

[13] E Fok V Szatmari K Busak and F Rozgonyi ldquoPrevalence ofintestinal parasites in dogs in some urban and rural areas ofHungaryrdquo Veterinary Quarterly vol 23 no 2 pp 96ndash98 2001

[14] B M Anene T O Nnaji and A B Chime ldquoIntestinal parasiticinfections of dogs in the Nsukka area of Enugu State NigeriardquoPreventive Veterinary Medicine vol 27 no 1-2 pp 89ndash94 1996

[15] R I Rodrıguez-Vivas E Gutierrez-Ruiz M E Bolio-Gonzalezet al ldquoAn epidemiological study of intestinal parasites of dogsfrom Yucatan Mexico and their risk to public healthrdquo Vector-Borne and Zoonotic Diseases vol 11 no 8 pp 1141ndash1144 2011

[16] G Rubinsky-Elefant M da Silva-Nunes R S MalafronteP T Muniz and M U Ferreira ldquoHuman toxocariasis inrural Brazilian Amazonia seroprevalence risk factors andspatial distributionrdquo American Journal of Tropical Medicine andHygiene vol 79 no 1 pp 93ndash98 2008

[17] Z A Kanafani A Skoury G F Araj et al ldquoSeroprevalence oftoxocariasis in Lebanon a pilot studyrdquo Parasitology vol 132 no5 pp 635ndash639 2006

[18] N E Radman S M Archelli R D Fonrouge M D V Guardisand O R Linzitto ldquoHuman toxocarosis Its seroprevalence inthe City of La Platardquo Memorias do Instituto Oswaldo Cruz vol95 no 3 pp 281ndash285 2000

[19] J M Alonso M V I Bojanich M Chamorro and J O Gorod-ner ldquoToxocara seroprevalence in children from a subtropicalcity in Argentinardquo Revista do Instituto de Medicina Tropical deSao Paulo vol 42 no 4 pp 235ndash237 2000

[20] F Jimenez-Balderas J Garcıa-Jaimes R Rıos et al ldquoIsolation ofIgG antibodies to Toxocara in ankylosing spondylitis patientswith acute anterior uveıtisrdquo Korean Journal of Ophthalmologyvol 28 no 3 pp 207ndash212 2014

[21] C Romero Nunez G D Mendoza Martınez S Yanez ArteagaM Ponce Macotela P Bustamante Montes and N RamırezDuran ldquoPrevalence and risk factors associated with toxocaracanis infection in childrenrdquo The Scientific World Journal vol2013 Article ID 572089 4 pages 2013

[22] D Woodhall M C Starr S P Montgomery et al ldquoOcular tox-ocariasis epidemiologic anatomic and therapeutic variationsbased on a survey of ophthalmic subspecialistsrdquo Ophthalmol-ogy vol 119 no 6 pp 1211ndash1217 2012

[23] S J Lim S E Lee S H Kim et al ldquoPrevalence of Toxoplasmagondii and Toxocara canis among patients with uveitisrdquo OcularImmunology and Inflammation vol 22 no 5 pp 360ndash366 2014

[24] S H Gillespie W J Dinning A Voller and N S CrowcroftldquoThe spectrum of ocular toxocariasisrdquo Eye vol 7 no 3 pp 415ndash418 1993

[25] D Antolava P Jarcuska M Janicko et al ldquoSeroprevalenceof human Toxocara infections in the Roma and non-Romapopulations of Eastern Slovakia a cross-sectional studyrdquo Epi-demiology and Infection vol 143 no 10 pp 1ndash10 2015

[26] F J Jimenez-Balderas A Camargo-Coronel J Gargia-Jaimes etal ldquoA study on parasites inMexican rheumatic disease patientsrdquoJournal of the Egyptian Society of Parasitology vol 42 no 2 pp271ndash280 2012

[27] H Langoni F Fornazari R C da Silva E T Monti and F BVilla ldquoPrevalence of antibodies against Toxoplasma gondii andNeospora caninum in dogsrdquo Brazilian Journal of Microbiologyvol 44 no 4 pp 1327ndash1330 2013

[28] C Alvarado-Esquivel D Romero-Salas A Cruz-Romero et alldquoHigh prevalence of Toxoplasma gondii antibodies in dogs inVeracruz Mexicordquo BMCVeterinary Research vol 10 article 1912014

[29] M Jimenez-Coello E Guzman-Marın A Ortega-Pacheco andK Y Acosta-Viana ldquoImmunological status against Toxoplasmagondii in non-cat owners from an endemic Region of MexicordquoVector-Borne and Zoonotic Diseases vol 11 no 8 pp 1057ndash10612011

[30] J Zavala-Velazquez E Guzman-Marın M Barrera-Perez andM E Rodrıguez-Felix ldquoToxoplasmosis and abortion in patientsat the OrsquoHoran Hospital of Merida Yucatanrdquo Salud Publica deMexico vol 31 no 5 pp 664ndash668 1989

[31] I A Vado-Solıs V Suarez-Solıs B Jimenez-Delgadillo J EZavala-Velazquez and J C Segura-Correa ldquoToxoplasma gondiipresence in women with spontaneous abortion in YucatanMexicordquoThe Journal of Parasitology vol 99 no 2 pp 383ndash3852013

[32] M Jimenez-Coello E Guzman-Marin M Rosado-Barrera Met al ldquoSeoprevalence of Toxoplasma gondii in a por ruralcommunity from Yucatan Mexicordquo in Memories from the 13thInternational Congress of Parasitology August 10ndash15 Mexico2014 2014

[33] A Kijlstra and E Jongert ldquoToxoplasma-safe meat close torealityrdquo Trends in Parasitology vol 25 no 1 pp 18ndash22 2009

[34] J L Jones and J P Dubey ldquoWaterborne toxoplasmosismdashrecentdevelopmentsrdquoExperimental Parasitology vol 124 no 1 pp 10ndash25 2010

[35] A Ortega-Pacheco J C Rodriguez-Buenfil M E Bolio-Gonzalez C H Sauri-Arceo M Jimenez-Coello and C LForsberg ldquoA survey of dog populations inUrban and rural areasof YucatanMexicordquoAnthrozoos vol 20 no 3 pp 261ndash274 2007

[36] M Faber S Schink A Mayer-Scholl et al ldquoOutbreak oftrichinellosis due to wild boar meat and evaluation of theeffectiveness of post exposure prophylaxis Germany 2013rdquoClinical Infectious Diseases vol 60 no 2 pp e98ndashe104 2015

[37] C Dobrescu H Hriscu M Emandi C Zamfir and C NemetldquoConsumption of untested pork contributed to over two-thousand clinical cases of human trichinellosis in RomaniardquoFolia Parasitologica vol 61 no 6 pp 558ndash560 2014

6 Journal of Tropical Medicine

[38] J Cabral-Soto H Villicana-Fuentes R Fragoso-Uribe and AContreras ldquoThe epidemiological profile of trichinosis in thestate of Zacatecasrdquo Salud Publica de Mexico vol 32 no 5 pp575ndash582 1990

[39] J L De-La-Rosa J G Aranda E Padilla andD Correa ldquoPreva-lence and risk factors associated with serum antibodies againstTrichinella spiralisrdquo International Journal for Parasitology vol28 no 2 pp 317ndash321 1998

[40] S Ozkoc S Bayram Delibas and C Akisu ldquoEvaluation ofTrichinella cross-reactions in the serological diagnosis of toxo-cariasisrdquoMikrobiyoloji Bulteni vol 46 no 3 pp 456ndash463 2012

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 3: Research Article Parasitic Zoonoses in Humans and Their Dogs …downloads.hindawi.com/journals/jtm/2015/481086.pdf · larva migrans and covert toxocariasis) and compartmental-ized

Journal of Tropical Medicine 3

Table 2 Serological frequency of zoonotic agents identified in 89persons from a rural community of Yucatan Mexico

Agent Positive cases (119899) T canis 26 292T gondii 81 910T spiralis 6 67T canis + T gondii 26 292T spiralis + T gondii 4 45

Table 3 Relationship between associated factors with T canisIgG seropositivity in humans from a rural community of YucatanMexico

119899 Positive Prevalence OR 95 CI 119875 valueAge (years)

20ndash40 29 8 276 15 054ndash426 042 (NS)gt40ndash75 55 11 200 mdash mdash mdash

SexMale 8 1 125 mdash mdash mdashFemale 76 18 237 446 005ndash39 041 (NS)

Eyes lesionsYes 52 16 308 13 049ndash36 056 (NS)No 32 8 255 mdash mdash mdash

DewormingYes 32 12 375 18 091ndash602 022 (NS)No 52 13 256 mdash mdash mdash119899 number of humans studied OR odds ratio CI confidence interval and119875 probabilityNS not significant

the interviewed persons eat sausages and from the 10 persons(112) who do not eat sausages 2 were seronegative

Only 6 (69) persons were found seropositive to Tspiralis (Table 2)

4 Discussion

The prevalence of dogs infected with gastrointestinal par-asites in this study is considered high and similar to thereported one in other regions of the world that is 524 inArgentina [12] 53 inHungary [13] and 68 in Nigeria [14]The high variation observed has been associated with variousweather conditions idiosyncrasies and sanitary control ofdogs A previous study in the same community was per-formed four years ago and prevalence of gastrointestinal par-asites in dogs was 80 with a high egg output of A caninumT canis and T vulpis found in this study deworming of dogswas performed and talks to children adolescents and adultsabout health management of dogs were given [15] Theseactions could explain the lower prevalence and intensityof infection reported at this time categorized between lowand medium intensity of infection In the specific case ofT canis a higher prevalence (125) was found comparedto previous studies in the same area where 62 was found[15] T canis mainly affects puppies with frequently fatalconsequences In adult dogs the infection is minor and

usually asymptomaticThe annual variation in the number ofinfected puppies in the regionmay influence the disposal andspreading of T canis eggs The presence of infected puppiescan increase the number of eggs and larvae deposited in theenvironment in which they can remain infective for severalmonths infecting other dogs andwith great potential to infecthumans especially children

Human toxocariasis is worldwide distributed and occurswhen embryonated eggs from the environment are ingestedThis is more critical when dog overpopulation is presentwithout the practice of preventive medicine (deworming)Children with pica are found at increased risk particularly inregions of low socioeconomic status and with proliferationof dogs andor those who have puppies at home [7] Adultsare also at risk of infection as shown by several studies whereprevalence of 268 in Brazil was reported [16] and 19 inLebanon was reported [17] In Argentina seroprevalence of20ndash38 in children and 10ndash39 in general population [18 19]is reported In Mexico 38 of people suffering from acutenongranulomatous uveitis were seropositive for T canis [20]with a prevalence of 46 to 1759 reported in children lessthan 16 years of age [21] Results of this study indicate a highspread of infective eggs in the rural community probablybecause of the high density of dogs having free access to thestreet and lack of health programs including a dewormingprogram

Although deworming has been introduced in healthmanagement of dogs in the studied community still spread-ing of infected eggs and contamination of the area are presentthus efforts to intensify the deworming of dog and cat arenecessary for better control results The ocular larva migranssyndrome is one of the major health problems associatedwith T canis [22] However eye lesions were not statisticallyassociated with seropositive persons this syndrome is morecritical in childrenwhere severe problems have been reported[7] so studies to evaluate the impact of this parasite on chil-dren should be designed and performedT canis andT gondiiare associated with eye lesions such as uveitis [23] Ocularlarva migrans in the case of toxocariasis may cause visualimpairment as a response of granulomatous inflammatoryreaction with consequences such as blindness and secondaryglaucoma [7 24] In the present study no association wasfound in patients seropositive toT canis and vision disordersHowever other symptoms not evaluated in the present studymay involve headache muscle pain influenza-like syndromeand diarrhea in seropositive patients [25] In a previousstudy conducted in Mexico T canis positive patients werehighly associated with ankylosing spondylitis [26] Youngchildren lt5 years are most affected with toxocariasis withclinical signs of fever abdominal pain (probably due tohepatomegaly) and lower respiratory symptoms [7] Furtherstudies should be focused on children in the studied regionexamining the different body systems to evaluate the impactof this zoonotic agent

The high prevalence of T gondii found in dogs andtheir owners demonstrates a high spread of oocysts in thestudied area with a probably common source of infectionThe prevalence found in dogs from Brazil was 269 witha higher risk for dogs over five years of age [27] However

4 Journal of Tropical Medicine

in the present study due to the very high prevalence foundall animals are expected to seroconvert since young ageswith frequent episodes of reinfection In Mexico dog fromshelters in Veracruz also showed a high seroprevalencereaching up to 673 [28] Free roaming dogs are indicatorsof the high contamination of the environment with T gondiioocysts as they may be sentinels of exposition In humanstoxoplasmosis has been reported previously in the Yucatanpeninsula with seroprevalence of 25 in non-cat owners[29] and also associated in patients with recent cases ofspontaneous abortion [30 31] Seroprevalence may reach upto 873 in humans from rural communities from Yucatan[32] In humans the main route of infection of T gondii is bythe ingestion of tissue cysts [33] In the present study the oralroute by consumption of undercooked meat (tissue cysts) ismore likely but also the ingestion of infective oocysts fromcontaminated water as previously demonstrated could occur[34] Considering the 100 T gondii seroprevalence found in50 studied cats from the same region [4] the density of catsand constant new born kittens in the village with excretion ofhigh numbers of oocysts probably occurred contaminatingthe environment and probable water sources Even when 93of the interviewed persons drank commercial bottled watertap water and water from artisanal wells are also used forseveral other activities and may be considered as a potentialsource of infection with T gondii oocysts However sincedogs in the studied area are fed with human leftovers [35]contaminated meat and sausages may also be involved in thetransmission cycle

T spiralis is a nematode capable of infecting anymammalingesting infected raw or undercooked meat Infection inhumans with this nematode is described worldwide andoutbreaks have been reported in developed countries infect-ing over 30 of people ingesting wild boar meat [36]Exposition of consumers to infected meat can reach up to651 of incidence especially when meat is not tested priorto consumption when slaughter is made in households [37]InMexico consumption of porkmeat coming from backyardis very common in rural villages without any kind of qualitytest [4] In Mexico the Ministry of Health (NOM-194-SSA1-2014)makes the inspection of porkmeat in search ofT spiraliscompulsory However this is rarely done at the abattoirsor before commercialization T spiralis in Mexico has beenreported since 1975 in Zacatecas state where several outbreakshave been reported in cases with mortality rates of 33in some cases in those outbreaks transmission was mostcommonly caused by the ingestion of raw pork productsor undercooked meat [38] More recently a prevalence of1 using ELISA was reported in semirural county areas ofMexico [39] In Yucatan no proper surveys of T spiralis havebeen performed in humans or animalsThis is the first reportof T spiralis serological presence in humans from YucatanHowever the Toxocara larval excretory antigen is normallyused in serological tests that may exhibit low specificitydue to cross-reaction between related helminthes includingT canis [40] Further research is needed to investigatethe epidemiology of these zoonotic helminthes using moreaccurate techniques for diagnosis including the search of theagent in farm and backyard pigs from the region

The main limitation of the present study was the smallsample size used and consequently results may be biased ormay not be representative of the rural communities from thestudied area However this study may be a good indicatorof the zoonotic situation and establish the bases for furtherstudies including a bigger and targeted sample size from bothanimals and humans

5 Conclusion

It is concluded that the dogs in a rural community of Yucatanare reservoirs of some helminthes parasites specially T canisThis implies a high risk of the presence of parasites in theenvironment of the village and a potential risk of infectionfor the human community It is important to improvethe dissemination and promotion of educational programson this important zoonosis and establish effective controlmeasures to reduce the emission of eggs and avoid contactof human with areas contaminated with dog feces Otherimportant zoonotic parasites (T gondii andT spiralis) are alsocirculating

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

This paper was financially supported by the Ministry ofEducation in Mexico through ldquoPRODEPrdquo (Programa parael Desarrollo Profesional Docente) as part of the projectldquoEpidemiologıa de Enfermedades Zoonoticas Transmitidaspor Vectores (ETVrsquoS) de Importancia en Salud Publicardquo

References

[1] A L Salb H W Barkema B T Elkin et al ldquoDogs as sourcesand sentinels of parasites in humans and wildlife NorthernCanadardquo Emerging Infectious Diseases vol 14 no 1 pp 60ndash632008

[2] J G Berdugo and C Franco ldquoGanaderia de traspatio en elEstado de Yucatanrdquo in Memorias de la Segunda Reunion SobreProduccion Animal Tropical M R Godoy J C Segura and AArellano Eds pp 114ndash120 Merida Yucatan Merida Mexico1991

[3] R Ku-Duperon W Trejo-Lizama A J Aguilar-Caballero etal ldquoGastrointestinal parasitism in the Mexican hairless pig inbackyard in the state of Yucatan Mexicordquo Revista Colombianade Ciencia Animal vol 6 pp 17ndash24 2013

[4] M Jimenez-Coello K Y Acosta-Viana E Guzman-Marin et alldquoThe occurrence of Toxoplasma gondii antibodies in backyardpigs and cats from an endemic tropical area ofMexicordquo Tropicaland Subtropical Agroecosystems vol 16 no 1 pp 89ndash92 2013

[5] J L Jones D Kruszon-Moran K Won M Wilson and P MSchantz ldquoToxoplasma gondii and Toxocara spp co-infectionrdquoAmerican Journal of Tropical Medicine and Hygiene vol 78 no1 pp 35ndash39 2008

Journal of Tropical Medicine 5

[6] L T Glickman and P M Schantz ldquoEpidemiology and patho-genesis of zoonotic toxocariasisrdquo Epidemiologic Reviews vol 3no 1 pp 230ndash250 1981

[7] D Despommier ldquoToxocariasis clinical aspects epidemiologymedical ecology and molecular aspectsrdquo Clinical MicrobiologyReviews vol 16 no 2 pp 265ndash272 2003

[8] H V Smith and R Noordin ldquoDiagnostic limitations and futuretrends in the serodiagnosis of human toxocariasisrdquo in ToxocaraThe Enigmatic Parasite C V Holland and H V Smith Edschapter 7 pp 89ndash112 CABI Publishing Wallingford UK 2006

[9] D EThompsonD A P Bundy E S Cooper and PM SchantzldquoEdidemiological characteristics of Toxocara canis zoonoticinfection of children in a Caribbean communityrdquo Bulletin of theWorld Health Organization vol 64 no 2 pp 283ndash290 1986

[10] J V Conlan K Vongxay B Khamlome et al ldquoPatterns and risksof Trichinella infection in humans and pigs in northern LaosrdquoPLoS Neglected Tropical Diseases vol 8 no 7 Article ID e30342014

[11] R I Rodrıguez-Vivas and L A Cob-Galera Tecnicas Diagnos-tico en Parasitologıa Veterinaria Universidad Autonoma deYucatan Merida Mexico 2nd edition 2005

[12] M F Fontanarrosa D Vezzani J Basabe and D F Eiras ldquoAnepidemiological study of gastrointestinal parasites of dogs fromSouthern Greater Buenos Aires (Argentina) age gender breedmixed infections and seasonal and spatial patternsrdquo VeterinaryParasitology vol 136 no 3-4 pp 283ndash295 2006

[13] E Fok V Szatmari K Busak and F Rozgonyi ldquoPrevalence ofintestinal parasites in dogs in some urban and rural areas ofHungaryrdquo Veterinary Quarterly vol 23 no 2 pp 96ndash98 2001

[14] B M Anene T O Nnaji and A B Chime ldquoIntestinal parasiticinfections of dogs in the Nsukka area of Enugu State NigeriardquoPreventive Veterinary Medicine vol 27 no 1-2 pp 89ndash94 1996

[15] R I Rodrıguez-Vivas E Gutierrez-Ruiz M E Bolio-Gonzalezet al ldquoAn epidemiological study of intestinal parasites of dogsfrom Yucatan Mexico and their risk to public healthrdquo Vector-Borne and Zoonotic Diseases vol 11 no 8 pp 1141ndash1144 2011

[16] G Rubinsky-Elefant M da Silva-Nunes R S MalafronteP T Muniz and M U Ferreira ldquoHuman toxocariasis inrural Brazilian Amazonia seroprevalence risk factors andspatial distributionrdquo American Journal of Tropical Medicine andHygiene vol 79 no 1 pp 93ndash98 2008

[17] Z A Kanafani A Skoury G F Araj et al ldquoSeroprevalence oftoxocariasis in Lebanon a pilot studyrdquo Parasitology vol 132 no5 pp 635ndash639 2006

[18] N E Radman S M Archelli R D Fonrouge M D V Guardisand O R Linzitto ldquoHuman toxocarosis Its seroprevalence inthe City of La Platardquo Memorias do Instituto Oswaldo Cruz vol95 no 3 pp 281ndash285 2000

[19] J M Alonso M V I Bojanich M Chamorro and J O Gorod-ner ldquoToxocara seroprevalence in children from a subtropicalcity in Argentinardquo Revista do Instituto de Medicina Tropical deSao Paulo vol 42 no 4 pp 235ndash237 2000

[20] F Jimenez-Balderas J Garcıa-Jaimes R Rıos et al ldquoIsolation ofIgG antibodies to Toxocara in ankylosing spondylitis patientswith acute anterior uveıtisrdquo Korean Journal of Ophthalmologyvol 28 no 3 pp 207ndash212 2014

[21] C Romero Nunez G D Mendoza Martınez S Yanez ArteagaM Ponce Macotela P Bustamante Montes and N RamırezDuran ldquoPrevalence and risk factors associated with toxocaracanis infection in childrenrdquo The Scientific World Journal vol2013 Article ID 572089 4 pages 2013

[22] D Woodhall M C Starr S P Montgomery et al ldquoOcular tox-ocariasis epidemiologic anatomic and therapeutic variationsbased on a survey of ophthalmic subspecialistsrdquo Ophthalmol-ogy vol 119 no 6 pp 1211ndash1217 2012

[23] S J Lim S E Lee S H Kim et al ldquoPrevalence of Toxoplasmagondii and Toxocara canis among patients with uveitisrdquo OcularImmunology and Inflammation vol 22 no 5 pp 360ndash366 2014

[24] S H Gillespie W J Dinning A Voller and N S CrowcroftldquoThe spectrum of ocular toxocariasisrdquo Eye vol 7 no 3 pp 415ndash418 1993

[25] D Antolava P Jarcuska M Janicko et al ldquoSeroprevalenceof human Toxocara infections in the Roma and non-Romapopulations of Eastern Slovakia a cross-sectional studyrdquo Epi-demiology and Infection vol 143 no 10 pp 1ndash10 2015

[26] F J Jimenez-Balderas A Camargo-Coronel J Gargia-Jaimes etal ldquoA study on parasites inMexican rheumatic disease patientsrdquoJournal of the Egyptian Society of Parasitology vol 42 no 2 pp271ndash280 2012

[27] H Langoni F Fornazari R C da Silva E T Monti and F BVilla ldquoPrevalence of antibodies against Toxoplasma gondii andNeospora caninum in dogsrdquo Brazilian Journal of Microbiologyvol 44 no 4 pp 1327ndash1330 2013

[28] C Alvarado-Esquivel D Romero-Salas A Cruz-Romero et alldquoHigh prevalence of Toxoplasma gondii antibodies in dogs inVeracruz Mexicordquo BMCVeterinary Research vol 10 article 1912014

[29] M Jimenez-Coello E Guzman-Marın A Ortega-Pacheco andK Y Acosta-Viana ldquoImmunological status against Toxoplasmagondii in non-cat owners from an endemic Region of MexicordquoVector-Borne and Zoonotic Diseases vol 11 no 8 pp 1057ndash10612011

[30] J Zavala-Velazquez E Guzman-Marın M Barrera-Perez andM E Rodrıguez-Felix ldquoToxoplasmosis and abortion in patientsat the OrsquoHoran Hospital of Merida Yucatanrdquo Salud Publica deMexico vol 31 no 5 pp 664ndash668 1989

[31] I A Vado-Solıs V Suarez-Solıs B Jimenez-Delgadillo J EZavala-Velazquez and J C Segura-Correa ldquoToxoplasma gondiipresence in women with spontaneous abortion in YucatanMexicordquoThe Journal of Parasitology vol 99 no 2 pp 383ndash3852013

[32] M Jimenez-Coello E Guzman-Marin M Rosado-Barrera Met al ldquoSeoprevalence of Toxoplasma gondii in a por ruralcommunity from Yucatan Mexicordquo in Memories from the 13thInternational Congress of Parasitology August 10ndash15 Mexico2014 2014

[33] A Kijlstra and E Jongert ldquoToxoplasma-safe meat close torealityrdquo Trends in Parasitology vol 25 no 1 pp 18ndash22 2009

[34] J L Jones and J P Dubey ldquoWaterborne toxoplasmosismdashrecentdevelopmentsrdquoExperimental Parasitology vol 124 no 1 pp 10ndash25 2010

[35] A Ortega-Pacheco J C Rodriguez-Buenfil M E Bolio-Gonzalez C H Sauri-Arceo M Jimenez-Coello and C LForsberg ldquoA survey of dog populations inUrban and rural areasof YucatanMexicordquoAnthrozoos vol 20 no 3 pp 261ndash274 2007

[36] M Faber S Schink A Mayer-Scholl et al ldquoOutbreak oftrichinellosis due to wild boar meat and evaluation of theeffectiveness of post exposure prophylaxis Germany 2013rdquoClinical Infectious Diseases vol 60 no 2 pp e98ndashe104 2015

[37] C Dobrescu H Hriscu M Emandi C Zamfir and C NemetldquoConsumption of untested pork contributed to over two-thousand clinical cases of human trichinellosis in RomaniardquoFolia Parasitologica vol 61 no 6 pp 558ndash560 2014

6 Journal of Tropical Medicine

[38] J Cabral-Soto H Villicana-Fuentes R Fragoso-Uribe and AContreras ldquoThe epidemiological profile of trichinosis in thestate of Zacatecasrdquo Salud Publica de Mexico vol 32 no 5 pp575ndash582 1990

[39] J L De-La-Rosa J G Aranda E Padilla andD Correa ldquoPreva-lence and risk factors associated with serum antibodies againstTrichinella spiralisrdquo International Journal for Parasitology vol28 no 2 pp 317ndash321 1998

[40] S Ozkoc S Bayram Delibas and C Akisu ldquoEvaluation ofTrichinella cross-reactions in the serological diagnosis of toxo-cariasisrdquoMikrobiyoloji Bulteni vol 46 no 3 pp 456ndash463 2012

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 4: Research Article Parasitic Zoonoses in Humans and Their Dogs …downloads.hindawi.com/journals/jtm/2015/481086.pdf · larva migrans and covert toxocariasis) and compartmental-ized

4 Journal of Tropical Medicine

in the present study due to the very high prevalence foundall animals are expected to seroconvert since young ageswith frequent episodes of reinfection In Mexico dog fromshelters in Veracruz also showed a high seroprevalencereaching up to 673 [28] Free roaming dogs are indicatorsof the high contamination of the environment with T gondiioocysts as they may be sentinels of exposition In humanstoxoplasmosis has been reported previously in the Yucatanpeninsula with seroprevalence of 25 in non-cat owners[29] and also associated in patients with recent cases ofspontaneous abortion [30 31] Seroprevalence may reach upto 873 in humans from rural communities from Yucatan[32] In humans the main route of infection of T gondii is bythe ingestion of tissue cysts [33] In the present study the oralroute by consumption of undercooked meat (tissue cysts) ismore likely but also the ingestion of infective oocysts fromcontaminated water as previously demonstrated could occur[34] Considering the 100 T gondii seroprevalence found in50 studied cats from the same region [4] the density of catsand constant new born kittens in the village with excretion ofhigh numbers of oocysts probably occurred contaminatingthe environment and probable water sources Even when 93of the interviewed persons drank commercial bottled watertap water and water from artisanal wells are also used forseveral other activities and may be considered as a potentialsource of infection with T gondii oocysts However sincedogs in the studied area are fed with human leftovers [35]contaminated meat and sausages may also be involved in thetransmission cycle

T spiralis is a nematode capable of infecting anymammalingesting infected raw or undercooked meat Infection inhumans with this nematode is described worldwide andoutbreaks have been reported in developed countries infect-ing over 30 of people ingesting wild boar meat [36]Exposition of consumers to infected meat can reach up to651 of incidence especially when meat is not tested priorto consumption when slaughter is made in households [37]InMexico consumption of porkmeat coming from backyardis very common in rural villages without any kind of qualitytest [4] In Mexico the Ministry of Health (NOM-194-SSA1-2014)makes the inspection of porkmeat in search ofT spiraliscompulsory However this is rarely done at the abattoirsor before commercialization T spiralis in Mexico has beenreported since 1975 in Zacatecas state where several outbreakshave been reported in cases with mortality rates of 33in some cases in those outbreaks transmission was mostcommonly caused by the ingestion of raw pork productsor undercooked meat [38] More recently a prevalence of1 using ELISA was reported in semirural county areas ofMexico [39] In Yucatan no proper surveys of T spiralis havebeen performed in humans or animalsThis is the first reportof T spiralis serological presence in humans from YucatanHowever the Toxocara larval excretory antigen is normallyused in serological tests that may exhibit low specificitydue to cross-reaction between related helminthes includingT canis [40] Further research is needed to investigatethe epidemiology of these zoonotic helminthes using moreaccurate techniques for diagnosis including the search of theagent in farm and backyard pigs from the region

The main limitation of the present study was the smallsample size used and consequently results may be biased ormay not be representative of the rural communities from thestudied area However this study may be a good indicatorof the zoonotic situation and establish the bases for furtherstudies including a bigger and targeted sample size from bothanimals and humans

5 Conclusion

It is concluded that the dogs in a rural community of Yucatanare reservoirs of some helminthes parasites specially T canisThis implies a high risk of the presence of parasites in theenvironment of the village and a potential risk of infectionfor the human community It is important to improvethe dissemination and promotion of educational programson this important zoonosis and establish effective controlmeasures to reduce the emission of eggs and avoid contactof human with areas contaminated with dog feces Otherimportant zoonotic parasites (T gondii andT spiralis) are alsocirculating

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgments

This paper was financially supported by the Ministry ofEducation in Mexico through ldquoPRODEPrdquo (Programa parael Desarrollo Profesional Docente) as part of the projectldquoEpidemiologıa de Enfermedades Zoonoticas Transmitidaspor Vectores (ETVrsquoS) de Importancia en Salud Publicardquo

References

[1] A L Salb H W Barkema B T Elkin et al ldquoDogs as sourcesand sentinels of parasites in humans and wildlife NorthernCanadardquo Emerging Infectious Diseases vol 14 no 1 pp 60ndash632008

[2] J G Berdugo and C Franco ldquoGanaderia de traspatio en elEstado de Yucatanrdquo in Memorias de la Segunda Reunion SobreProduccion Animal Tropical M R Godoy J C Segura and AArellano Eds pp 114ndash120 Merida Yucatan Merida Mexico1991

[3] R Ku-Duperon W Trejo-Lizama A J Aguilar-Caballero etal ldquoGastrointestinal parasitism in the Mexican hairless pig inbackyard in the state of Yucatan Mexicordquo Revista Colombianade Ciencia Animal vol 6 pp 17ndash24 2013

[4] M Jimenez-Coello K Y Acosta-Viana E Guzman-Marin et alldquoThe occurrence of Toxoplasma gondii antibodies in backyardpigs and cats from an endemic tropical area ofMexicordquo Tropicaland Subtropical Agroecosystems vol 16 no 1 pp 89ndash92 2013

[5] J L Jones D Kruszon-Moran K Won M Wilson and P MSchantz ldquoToxoplasma gondii and Toxocara spp co-infectionrdquoAmerican Journal of Tropical Medicine and Hygiene vol 78 no1 pp 35ndash39 2008

Journal of Tropical Medicine 5

[6] L T Glickman and P M Schantz ldquoEpidemiology and patho-genesis of zoonotic toxocariasisrdquo Epidemiologic Reviews vol 3no 1 pp 230ndash250 1981

[7] D Despommier ldquoToxocariasis clinical aspects epidemiologymedical ecology and molecular aspectsrdquo Clinical MicrobiologyReviews vol 16 no 2 pp 265ndash272 2003

[8] H V Smith and R Noordin ldquoDiagnostic limitations and futuretrends in the serodiagnosis of human toxocariasisrdquo in ToxocaraThe Enigmatic Parasite C V Holland and H V Smith Edschapter 7 pp 89ndash112 CABI Publishing Wallingford UK 2006

[9] D EThompsonD A P Bundy E S Cooper and PM SchantzldquoEdidemiological characteristics of Toxocara canis zoonoticinfection of children in a Caribbean communityrdquo Bulletin of theWorld Health Organization vol 64 no 2 pp 283ndash290 1986

[10] J V Conlan K Vongxay B Khamlome et al ldquoPatterns and risksof Trichinella infection in humans and pigs in northern LaosrdquoPLoS Neglected Tropical Diseases vol 8 no 7 Article ID e30342014

[11] R I Rodrıguez-Vivas and L A Cob-Galera Tecnicas Diagnos-tico en Parasitologıa Veterinaria Universidad Autonoma deYucatan Merida Mexico 2nd edition 2005

[12] M F Fontanarrosa D Vezzani J Basabe and D F Eiras ldquoAnepidemiological study of gastrointestinal parasites of dogs fromSouthern Greater Buenos Aires (Argentina) age gender breedmixed infections and seasonal and spatial patternsrdquo VeterinaryParasitology vol 136 no 3-4 pp 283ndash295 2006

[13] E Fok V Szatmari K Busak and F Rozgonyi ldquoPrevalence ofintestinal parasites in dogs in some urban and rural areas ofHungaryrdquo Veterinary Quarterly vol 23 no 2 pp 96ndash98 2001

[14] B M Anene T O Nnaji and A B Chime ldquoIntestinal parasiticinfections of dogs in the Nsukka area of Enugu State NigeriardquoPreventive Veterinary Medicine vol 27 no 1-2 pp 89ndash94 1996

[15] R I Rodrıguez-Vivas E Gutierrez-Ruiz M E Bolio-Gonzalezet al ldquoAn epidemiological study of intestinal parasites of dogsfrom Yucatan Mexico and their risk to public healthrdquo Vector-Borne and Zoonotic Diseases vol 11 no 8 pp 1141ndash1144 2011

[16] G Rubinsky-Elefant M da Silva-Nunes R S MalafronteP T Muniz and M U Ferreira ldquoHuman toxocariasis inrural Brazilian Amazonia seroprevalence risk factors andspatial distributionrdquo American Journal of Tropical Medicine andHygiene vol 79 no 1 pp 93ndash98 2008

[17] Z A Kanafani A Skoury G F Araj et al ldquoSeroprevalence oftoxocariasis in Lebanon a pilot studyrdquo Parasitology vol 132 no5 pp 635ndash639 2006

[18] N E Radman S M Archelli R D Fonrouge M D V Guardisand O R Linzitto ldquoHuman toxocarosis Its seroprevalence inthe City of La Platardquo Memorias do Instituto Oswaldo Cruz vol95 no 3 pp 281ndash285 2000

[19] J M Alonso M V I Bojanich M Chamorro and J O Gorod-ner ldquoToxocara seroprevalence in children from a subtropicalcity in Argentinardquo Revista do Instituto de Medicina Tropical deSao Paulo vol 42 no 4 pp 235ndash237 2000

[20] F Jimenez-Balderas J Garcıa-Jaimes R Rıos et al ldquoIsolation ofIgG antibodies to Toxocara in ankylosing spondylitis patientswith acute anterior uveıtisrdquo Korean Journal of Ophthalmologyvol 28 no 3 pp 207ndash212 2014

[21] C Romero Nunez G D Mendoza Martınez S Yanez ArteagaM Ponce Macotela P Bustamante Montes and N RamırezDuran ldquoPrevalence and risk factors associated with toxocaracanis infection in childrenrdquo The Scientific World Journal vol2013 Article ID 572089 4 pages 2013

[22] D Woodhall M C Starr S P Montgomery et al ldquoOcular tox-ocariasis epidemiologic anatomic and therapeutic variationsbased on a survey of ophthalmic subspecialistsrdquo Ophthalmol-ogy vol 119 no 6 pp 1211ndash1217 2012

[23] S J Lim S E Lee S H Kim et al ldquoPrevalence of Toxoplasmagondii and Toxocara canis among patients with uveitisrdquo OcularImmunology and Inflammation vol 22 no 5 pp 360ndash366 2014

[24] S H Gillespie W J Dinning A Voller and N S CrowcroftldquoThe spectrum of ocular toxocariasisrdquo Eye vol 7 no 3 pp 415ndash418 1993

[25] D Antolava P Jarcuska M Janicko et al ldquoSeroprevalenceof human Toxocara infections in the Roma and non-Romapopulations of Eastern Slovakia a cross-sectional studyrdquo Epi-demiology and Infection vol 143 no 10 pp 1ndash10 2015

[26] F J Jimenez-Balderas A Camargo-Coronel J Gargia-Jaimes etal ldquoA study on parasites inMexican rheumatic disease patientsrdquoJournal of the Egyptian Society of Parasitology vol 42 no 2 pp271ndash280 2012

[27] H Langoni F Fornazari R C da Silva E T Monti and F BVilla ldquoPrevalence of antibodies against Toxoplasma gondii andNeospora caninum in dogsrdquo Brazilian Journal of Microbiologyvol 44 no 4 pp 1327ndash1330 2013

[28] C Alvarado-Esquivel D Romero-Salas A Cruz-Romero et alldquoHigh prevalence of Toxoplasma gondii antibodies in dogs inVeracruz Mexicordquo BMCVeterinary Research vol 10 article 1912014

[29] M Jimenez-Coello E Guzman-Marın A Ortega-Pacheco andK Y Acosta-Viana ldquoImmunological status against Toxoplasmagondii in non-cat owners from an endemic Region of MexicordquoVector-Borne and Zoonotic Diseases vol 11 no 8 pp 1057ndash10612011

[30] J Zavala-Velazquez E Guzman-Marın M Barrera-Perez andM E Rodrıguez-Felix ldquoToxoplasmosis and abortion in patientsat the OrsquoHoran Hospital of Merida Yucatanrdquo Salud Publica deMexico vol 31 no 5 pp 664ndash668 1989

[31] I A Vado-Solıs V Suarez-Solıs B Jimenez-Delgadillo J EZavala-Velazquez and J C Segura-Correa ldquoToxoplasma gondiipresence in women with spontaneous abortion in YucatanMexicordquoThe Journal of Parasitology vol 99 no 2 pp 383ndash3852013

[32] M Jimenez-Coello E Guzman-Marin M Rosado-Barrera Met al ldquoSeoprevalence of Toxoplasma gondii in a por ruralcommunity from Yucatan Mexicordquo in Memories from the 13thInternational Congress of Parasitology August 10ndash15 Mexico2014 2014

[33] A Kijlstra and E Jongert ldquoToxoplasma-safe meat close torealityrdquo Trends in Parasitology vol 25 no 1 pp 18ndash22 2009

[34] J L Jones and J P Dubey ldquoWaterborne toxoplasmosismdashrecentdevelopmentsrdquoExperimental Parasitology vol 124 no 1 pp 10ndash25 2010

[35] A Ortega-Pacheco J C Rodriguez-Buenfil M E Bolio-Gonzalez C H Sauri-Arceo M Jimenez-Coello and C LForsberg ldquoA survey of dog populations inUrban and rural areasof YucatanMexicordquoAnthrozoos vol 20 no 3 pp 261ndash274 2007

[36] M Faber S Schink A Mayer-Scholl et al ldquoOutbreak oftrichinellosis due to wild boar meat and evaluation of theeffectiveness of post exposure prophylaxis Germany 2013rdquoClinical Infectious Diseases vol 60 no 2 pp e98ndashe104 2015

[37] C Dobrescu H Hriscu M Emandi C Zamfir and C NemetldquoConsumption of untested pork contributed to over two-thousand clinical cases of human trichinellosis in RomaniardquoFolia Parasitologica vol 61 no 6 pp 558ndash560 2014

6 Journal of Tropical Medicine

[38] J Cabral-Soto H Villicana-Fuentes R Fragoso-Uribe and AContreras ldquoThe epidemiological profile of trichinosis in thestate of Zacatecasrdquo Salud Publica de Mexico vol 32 no 5 pp575ndash582 1990

[39] J L De-La-Rosa J G Aranda E Padilla andD Correa ldquoPreva-lence and risk factors associated with serum antibodies againstTrichinella spiralisrdquo International Journal for Parasitology vol28 no 2 pp 317ndash321 1998

[40] S Ozkoc S Bayram Delibas and C Akisu ldquoEvaluation ofTrichinella cross-reactions in the serological diagnosis of toxo-cariasisrdquoMikrobiyoloji Bulteni vol 46 no 3 pp 456ndash463 2012

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 5: Research Article Parasitic Zoonoses in Humans and Their Dogs …downloads.hindawi.com/journals/jtm/2015/481086.pdf · larva migrans and covert toxocariasis) and compartmental-ized

Journal of Tropical Medicine 5

[6] L T Glickman and P M Schantz ldquoEpidemiology and patho-genesis of zoonotic toxocariasisrdquo Epidemiologic Reviews vol 3no 1 pp 230ndash250 1981

[7] D Despommier ldquoToxocariasis clinical aspects epidemiologymedical ecology and molecular aspectsrdquo Clinical MicrobiologyReviews vol 16 no 2 pp 265ndash272 2003

[8] H V Smith and R Noordin ldquoDiagnostic limitations and futuretrends in the serodiagnosis of human toxocariasisrdquo in ToxocaraThe Enigmatic Parasite C V Holland and H V Smith Edschapter 7 pp 89ndash112 CABI Publishing Wallingford UK 2006

[9] D EThompsonD A P Bundy E S Cooper and PM SchantzldquoEdidemiological characteristics of Toxocara canis zoonoticinfection of children in a Caribbean communityrdquo Bulletin of theWorld Health Organization vol 64 no 2 pp 283ndash290 1986

[10] J V Conlan K Vongxay B Khamlome et al ldquoPatterns and risksof Trichinella infection in humans and pigs in northern LaosrdquoPLoS Neglected Tropical Diseases vol 8 no 7 Article ID e30342014

[11] R I Rodrıguez-Vivas and L A Cob-Galera Tecnicas Diagnos-tico en Parasitologıa Veterinaria Universidad Autonoma deYucatan Merida Mexico 2nd edition 2005

[12] M F Fontanarrosa D Vezzani J Basabe and D F Eiras ldquoAnepidemiological study of gastrointestinal parasites of dogs fromSouthern Greater Buenos Aires (Argentina) age gender breedmixed infections and seasonal and spatial patternsrdquo VeterinaryParasitology vol 136 no 3-4 pp 283ndash295 2006

[13] E Fok V Szatmari K Busak and F Rozgonyi ldquoPrevalence ofintestinal parasites in dogs in some urban and rural areas ofHungaryrdquo Veterinary Quarterly vol 23 no 2 pp 96ndash98 2001

[14] B M Anene T O Nnaji and A B Chime ldquoIntestinal parasiticinfections of dogs in the Nsukka area of Enugu State NigeriardquoPreventive Veterinary Medicine vol 27 no 1-2 pp 89ndash94 1996

[15] R I Rodrıguez-Vivas E Gutierrez-Ruiz M E Bolio-Gonzalezet al ldquoAn epidemiological study of intestinal parasites of dogsfrom Yucatan Mexico and their risk to public healthrdquo Vector-Borne and Zoonotic Diseases vol 11 no 8 pp 1141ndash1144 2011

[16] G Rubinsky-Elefant M da Silva-Nunes R S MalafronteP T Muniz and M U Ferreira ldquoHuman toxocariasis inrural Brazilian Amazonia seroprevalence risk factors andspatial distributionrdquo American Journal of Tropical Medicine andHygiene vol 79 no 1 pp 93ndash98 2008

[17] Z A Kanafani A Skoury G F Araj et al ldquoSeroprevalence oftoxocariasis in Lebanon a pilot studyrdquo Parasitology vol 132 no5 pp 635ndash639 2006

[18] N E Radman S M Archelli R D Fonrouge M D V Guardisand O R Linzitto ldquoHuman toxocarosis Its seroprevalence inthe City of La Platardquo Memorias do Instituto Oswaldo Cruz vol95 no 3 pp 281ndash285 2000

[19] J M Alonso M V I Bojanich M Chamorro and J O Gorod-ner ldquoToxocara seroprevalence in children from a subtropicalcity in Argentinardquo Revista do Instituto de Medicina Tropical deSao Paulo vol 42 no 4 pp 235ndash237 2000

[20] F Jimenez-Balderas J Garcıa-Jaimes R Rıos et al ldquoIsolation ofIgG antibodies to Toxocara in ankylosing spondylitis patientswith acute anterior uveıtisrdquo Korean Journal of Ophthalmologyvol 28 no 3 pp 207ndash212 2014

[21] C Romero Nunez G D Mendoza Martınez S Yanez ArteagaM Ponce Macotela P Bustamante Montes and N RamırezDuran ldquoPrevalence and risk factors associated with toxocaracanis infection in childrenrdquo The Scientific World Journal vol2013 Article ID 572089 4 pages 2013

[22] D Woodhall M C Starr S P Montgomery et al ldquoOcular tox-ocariasis epidemiologic anatomic and therapeutic variationsbased on a survey of ophthalmic subspecialistsrdquo Ophthalmol-ogy vol 119 no 6 pp 1211ndash1217 2012

[23] S J Lim S E Lee S H Kim et al ldquoPrevalence of Toxoplasmagondii and Toxocara canis among patients with uveitisrdquo OcularImmunology and Inflammation vol 22 no 5 pp 360ndash366 2014

[24] S H Gillespie W J Dinning A Voller and N S CrowcroftldquoThe spectrum of ocular toxocariasisrdquo Eye vol 7 no 3 pp 415ndash418 1993

[25] D Antolava P Jarcuska M Janicko et al ldquoSeroprevalenceof human Toxocara infections in the Roma and non-Romapopulations of Eastern Slovakia a cross-sectional studyrdquo Epi-demiology and Infection vol 143 no 10 pp 1ndash10 2015

[26] F J Jimenez-Balderas A Camargo-Coronel J Gargia-Jaimes etal ldquoA study on parasites inMexican rheumatic disease patientsrdquoJournal of the Egyptian Society of Parasitology vol 42 no 2 pp271ndash280 2012

[27] H Langoni F Fornazari R C da Silva E T Monti and F BVilla ldquoPrevalence of antibodies against Toxoplasma gondii andNeospora caninum in dogsrdquo Brazilian Journal of Microbiologyvol 44 no 4 pp 1327ndash1330 2013

[28] C Alvarado-Esquivel D Romero-Salas A Cruz-Romero et alldquoHigh prevalence of Toxoplasma gondii antibodies in dogs inVeracruz Mexicordquo BMCVeterinary Research vol 10 article 1912014

[29] M Jimenez-Coello E Guzman-Marın A Ortega-Pacheco andK Y Acosta-Viana ldquoImmunological status against Toxoplasmagondii in non-cat owners from an endemic Region of MexicordquoVector-Borne and Zoonotic Diseases vol 11 no 8 pp 1057ndash10612011

[30] J Zavala-Velazquez E Guzman-Marın M Barrera-Perez andM E Rodrıguez-Felix ldquoToxoplasmosis and abortion in patientsat the OrsquoHoran Hospital of Merida Yucatanrdquo Salud Publica deMexico vol 31 no 5 pp 664ndash668 1989

[31] I A Vado-Solıs V Suarez-Solıs B Jimenez-Delgadillo J EZavala-Velazquez and J C Segura-Correa ldquoToxoplasma gondiipresence in women with spontaneous abortion in YucatanMexicordquoThe Journal of Parasitology vol 99 no 2 pp 383ndash3852013

[32] M Jimenez-Coello E Guzman-Marin M Rosado-Barrera Met al ldquoSeoprevalence of Toxoplasma gondii in a por ruralcommunity from Yucatan Mexicordquo in Memories from the 13thInternational Congress of Parasitology August 10ndash15 Mexico2014 2014

[33] A Kijlstra and E Jongert ldquoToxoplasma-safe meat close torealityrdquo Trends in Parasitology vol 25 no 1 pp 18ndash22 2009

[34] J L Jones and J P Dubey ldquoWaterborne toxoplasmosismdashrecentdevelopmentsrdquoExperimental Parasitology vol 124 no 1 pp 10ndash25 2010

[35] A Ortega-Pacheco J C Rodriguez-Buenfil M E Bolio-Gonzalez C H Sauri-Arceo M Jimenez-Coello and C LForsberg ldquoA survey of dog populations inUrban and rural areasof YucatanMexicordquoAnthrozoos vol 20 no 3 pp 261ndash274 2007

[36] M Faber S Schink A Mayer-Scholl et al ldquoOutbreak oftrichinellosis due to wild boar meat and evaluation of theeffectiveness of post exposure prophylaxis Germany 2013rdquoClinical Infectious Diseases vol 60 no 2 pp e98ndashe104 2015

[37] C Dobrescu H Hriscu M Emandi C Zamfir and C NemetldquoConsumption of untested pork contributed to over two-thousand clinical cases of human trichinellosis in RomaniardquoFolia Parasitologica vol 61 no 6 pp 558ndash560 2014

6 Journal of Tropical Medicine

[38] J Cabral-Soto H Villicana-Fuentes R Fragoso-Uribe and AContreras ldquoThe epidemiological profile of trichinosis in thestate of Zacatecasrdquo Salud Publica de Mexico vol 32 no 5 pp575ndash582 1990

[39] J L De-La-Rosa J G Aranda E Padilla andD Correa ldquoPreva-lence and risk factors associated with serum antibodies againstTrichinella spiralisrdquo International Journal for Parasitology vol28 no 2 pp 317ndash321 1998

[40] S Ozkoc S Bayram Delibas and C Akisu ldquoEvaluation ofTrichinella cross-reactions in the serological diagnosis of toxo-cariasisrdquoMikrobiyoloji Bulteni vol 46 no 3 pp 456ndash463 2012

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 6: Research Article Parasitic Zoonoses in Humans and Their Dogs …downloads.hindawi.com/journals/jtm/2015/481086.pdf · larva migrans and covert toxocariasis) and compartmental-ized

6 Journal of Tropical Medicine

[38] J Cabral-Soto H Villicana-Fuentes R Fragoso-Uribe and AContreras ldquoThe epidemiological profile of trichinosis in thestate of Zacatecasrdquo Salud Publica de Mexico vol 32 no 5 pp575ndash582 1990

[39] J L De-La-Rosa J G Aranda E Padilla andD Correa ldquoPreva-lence and risk factors associated with serum antibodies againstTrichinella spiralisrdquo International Journal for Parasitology vol28 no 2 pp 317ndash321 1998

[40] S Ozkoc S Bayram Delibas and C Akisu ldquoEvaluation ofTrichinella cross-reactions in the serological diagnosis of toxo-cariasisrdquoMikrobiyoloji Bulteni vol 46 no 3 pp 456ndash463 2012

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom

Page 7: Research Article Parasitic Zoonoses in Humans and Their Dogs …downloads.hindawi.com/journals/jtm/2015/481086.pdf · larva migrans and covert toxocariasis) and compartmental-ized

Submit your manuscripts athttpwwwhindawicom

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

MEDIATORSINFLAMMATION

of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Behavioural Neurology

EndocrinologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Disease Markers

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

OncologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Oxidative Medicine and Cellular Longevity

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

PPAR Research

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Immunology ResearchHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Journal of

ObesityJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Computational and Mathematical Methods in Medicine

OphthalmologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Diabetes ResearchJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Research and TreatmentAIDS

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Gastroenterology Research and Practice

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Parkinsonrsquos Disease

Evidence-Based Complementary and Alternative Medicine

Volume 2014Hindawi Publishing Corporationhttpwwwhindawicom