5
Hindawi Publishing Corporation e Scientific World Journal Volume 2013, Article ID 572089, 4 pages http://dx.doi.org/10.1155/2013/572089 Research Article Prevalence and Risk Factors Associated with Toxocara canis Infection in Children Camilo Romero Núñez, 1 Germán David Mendoza Martínez, 2 Selene Yañez Arteaga, 2 Martha Ponce Macotela, 3 Patricia Bustamante Montes, 4 and Ninfa Ramírez Durán 4 1 Centro Universitario Amecameca, Universidad Aut´ onoma del Estado de M´ exico, 56900 Amecameca, MEX, Mexico 2 Departamento de Producci´ on Agr´ ıcola y Animal, Universidad Aut´ onoma Metropolitana, 04960 Mexico City, DF, Mexico 3 Parasitolog´ ıa Experimental, Instituto Nacional de Pediatr´ ıa de M´ exico, 04530 Mexico City, DF, Mexico 4 Facultad de Medicina, Universidad Aut´ onoma del Estado de M´ exico, 50180 Toluca, MEX, Mexico Correspondence should be addressed to Ninfa Ram´ ırez Dur´ an; [email protected] Received 12 April 2013; Accepted 15 May 2013 Academic Editors: G. Cancrini and E. L. Jarroll Copyright © 2013 Camilo Romero N´ nez 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. e objective of this study was to determine seroprevalence and identify risk factors associated with Toxocara canis infection. A clinical and epidemiological questionnaire and body mass index were used to assess the risk factors associated with human toxocariasis in 108 children with an age range of 2–16 years. Antibodies against Toxocara canis were detected using an ELISA test kit. Chi-square analysis and odds ratio (OR) were used to identify risk factors associated with Toxocara canis seropositivity. e prevalence of antibodies against Toxocara canis was greater ( = 0.02) in males than females (28.84% and 16.07%, resp.). Chi-square analysis and odds ratio revealed just one variable with < 0.05, and OR > 1.0 was associated with seropositivity: the possession of dogs under one year old (OR = 1.78). Although not significant, the OR values suggest that other factors may be epidemiologically important for Toxocara presence such as not washing hands before meals, malnutrition, obesity, and use of public parks. Children in the age group >12 and <16 years old had higher seroprevalence to Toxocara canis (17.59%) than the >2 and <11 years old age group (4.62%). Toxocariosis infection needs to be prevented by pet deworming and hygienic measures aſter contact with dogs. 1. Introduction Toxocariasis is a parasitic zoonosis that causes significant morbidity worldwide. It is caused by nematodes of the genus Toxocara, which includes more than 30 species, of which two are important for humans: Toxocara canis and Toxocara cati [1]. Infection occurs in children by ingestion of eggs from T. canis via hands contaminated by direct contact with puppies, through the hair of the dog [2], or by ingestion of vegetables or soil contaminated with Toxocara eggs [3]. Consumption of raw liver from Toxocara-infected paratenic hosts is a less fre- quent source of contamination [4]. Seroprevalence in children is variable and can be as low as 1% reported in Spain [5] or as high as 67% reported in Argentina [6]; within each region or country prevalence can also vary widely, as in Brazil where there are locales with 8.7% and others up to 54.8% rates [7, 8]. Geophagia and the use of public parks have been recognized as risk factors for Toxocara in children but others have been poorly evaluated [9], so the objective of this study was to evaluate the seroprevalence of Toxocara canis in children and its association with several factors such as their health, hygiene practices, and pets. 2. Materials and Methods 2.1. Study Location. A cross-sectional study was carried out between August and September 2010 in the Municipality of Ecatepec of Morelos (Latitude 19 36 03 N and Longitude 99 03 09 W). Ecatepec is a city in the metropolitan area of Mexico City located in the north of the State of Mexico and north of the Mexican Valley; it has a mean altitude of 2,259 m above sea level and is an area with high population density and industrial zones. is district has a population of 1,656,107 inhabitants. Ecatepec has a temperate subhumid

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Page 1: Research Article Prevalence and Risk Factors Associated with Toxocara canis Infection ...downloads.hindawi.com/journals/tswj/2013/572089.pdf · 2019-07-31 · toxocariasis in children

Hindawi Publishing CorporationThe Scientific World JournalVolume 2013 Article ID 572089 4 pageshttpdxdoiorg1011552013572089

Research ArticlePrevalence and Risk Factors Associated with Toxocara canisInfection in Children

Camilo Romero Nuacutentildeez1 Germaacuten David Mendoza Martiacutenez2 Selene Yantildeez Arteaga2

Martha Ponce Macotela3 Patricia Bustamante Montes4 and Ninfa Ramiacuterez Duraacuten4

1 Centro Universitario Amecameca Universidad Autonoma del Estado de Mexico 56900 Amecameca MEX Mexico2Departamento de Produccion Agrıcola y Animal Universidad Autonoma Metropolitana 04960 Mexico City DF Mexico3 Parasitologıa Experimental Instituto Nacional de Pediatrıa de Mexico 04530 Mexico City DF Mexico4 Facultad de Medicina Universidad Autonoma del Estado de Mexico 50180 Toluca MEX Mexico

Correspondence should be addressed to Ninfa Ramırez Duran nramirezduaemexmx

Received 12 April 2013 Accepted 15 May 2013

Academic Editors G Cancrini and E L Jarroll

Copyright copy 2013 Camilo Romero Nunez et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

The objective of this study was to determine seroprevalence and identify risk factors associated with Toxocara canis infectionA clinical and epidemiological questionnaire and body mass index were used to assess the risk factors associated with humantoxocariasis in 108 children with an age range of 2ndash16 years Antibodies against Toxocara canis were detected using an ELISA testkit Chi-square analysis and odds ratio (OR) were used to identify risk factors associated with Toxocara canis seropositivity Theprevalence of antibodies againstToxocara caniswas greater (119875 = 002) inmales than females (2884 and 1607 resp) Chi-squareanalysis and odds ratio revealed just one variable with 119875 lt 005 and OR gt 10 was associated with seropositivity the possession ofdogs under one year old (OR = 178) Although not significant the OR values suggest that other factors may be epidemiologicallyimportant for Toxocara presence such as not washing hands before meals malnutrition obesity and use of public parks Childrenin the age group gt12 and lt16 years old had higher seroprevalence to Toxocara canis (1759) than the gt2 and lt11 years old age group(462) Toxocariosis infection needs to be prevented by pet deworming and hygienic measures after contact with dogs

1 Introduction

Toxocariasis is a parasitic zoonosis that causes significantmorbidity worldwide It is caused by nematodes of the genusToxocara which includes more than 30 species of which twoare important for humans Toxocara canis and Toxocara cati[1] Infection occurs in children by ingestion of eggs from Tcanis via hands contaminated by direct contact with puppiesthrough the hair of the dog [2] or by ingestion of vegetablesor soil contaminated with Toxocara eggs [3] Consumption ofraw liver from Toxocara-infected paratenic hosts is a less fre-quent source of contamination [4]

Seroprevalence in children is variable and can be as lowas 1 reported in Spain [5] or as high as 67 reported inArgentina [6] within each region or country prevalence canalso vary widely as in Brazil where there are locales with 87and others up to 548 rates [7 8] Geophagia and the use of

public parks have been recognized as risk factors forToxocarain children but others have been poorly evaluated [9] so theobjective of this study was to evaluate the seroprevalence ofToxocara canis in children and its association with severalfactors such as their health hygiene practices and pets

2 Materials and Methods

21 Study Location A cross-sectional study was carried outbetween August and September 2010 in the Municipality ofEcatepec of Morelos (Latitude 19∘ 3610158400310158401015840N and Longitude99∘ 0310158400910158401015840W) Ecatepec is a city in the metropolitan areaof Mexico City located in the north of the State of Mexicoand north of the Mexican Valley it has a mean altitude of2259m above sea level and is an area with high populationdensity and industrial zones This district has a populationof 1656107 inhabitants Ecatepec has a temperate subhumid

2 The Scientific World Journal

climate with rains in summer with a mean temperature of138∘C (between 7 and 30∘C) and an average relative humidityof 35

22 Data Collection Interviews were carried out in theschools of participants with informed consent from a parentandor legal guardian and the assent of the children A totalof 108 subjects from 24 months to 16 years old participatedin this research with parental agreement for this study Thisresearch had the approval of the Ethical Research Committeeof the Graduate School of Medicine faculty UniversidadAutonoma del Estado de Mexico

Data from the questionnaires included risk factors andepidemiological data (age sex dog ownership dog presenceindoors dogs sleeping with people older dogs pet deworm-ing presence of other pets use of public parks history ofonychophagia not washing hands and eating undercookedmeat)The clinical data considered included respiratory signs(bronchospasm bronchitis and asthma) dermatologic signs(rash hives and itching) and BMI as ameasure of nutritionalstatus [10] Children with BMI less than 20 kgm2 wereconsidered underweight or malnourished those with BMIgreater than 30 kgm2 were categorized as overweight orobese and the rest were considered as having normal nutri-tion [11]

23 Laboratory Analyses Blood samples were collected forserology and assessment of eosinophils All sera were ana-lyzed by ELISA at the Parasitology Laboratory of theNationalInstitute of Pediatrics Mexico City DF using a commercialkit with Toxocara IgG (SCIMEDX Toxocara IgG) Values ofoptical density greater than 03 according to the serologicalELISA test were considered positive The numbers of circu-lating eosinophils were evaluated ldquoeosinophiliardquo was used todescribe those withmore than 10 eosinophils or an absolutevalue greater than 500 cells120583L of IgG [12]

24 Statistical Analysis Analysis was carried out using Chi-square and odds ratio (OR) tests in order to confirm themeandifferences between groups and association with seropreva-lence [13]The level of significance selected was119875 lt 005withan odds ratio gt10

3 Results

Twenty-four (2222) serum samples from the 108 examinedsera were T canis seropositive (Table 1) The prevalence ofantibodies against T canis was greater (119875 = 002) in malesthan females (2884 and 1607 resp) The seroprevalenceto T canis tended be lower in the youngest children (462)compared with the oldest group (1759) as shown in Table 1

Analysis of the signssymptoms suggested no relationshipbetween respiratory signs or symptoms (200) or cutaneoussigns (360) with Toxocariasis although the odds ratio wasgreater than 1 in the latter case (Table 2) Eosinophilia wasstatistically associated with positive serology (Table 2)

The analysis of risk factors evidenced that malnutritionobesity not washing hands before meals onicophagia and

Table 1 Seroprevalence of Toxocara canis in boys and girls from 2to 16 years of age

Age Seropositives119875-Fisher

Males (119899 = 52) Females (119899 = 56)2ndash11 years 3 2 03112ndash16 years 12 7 009Total 15 9 002

use of public parks all showed significant associations withseropositivity although theOR values (gt10) suggest that theymay be epidemiologically important for Toxocara presence(Table 3) Nevertheless the presence of dogs younger than 1year old within households showed a significant associationwith seropositivity (Table 3)

4 Discussion

The seroprevalence rate found (2222) was lower than thatreported in children from India (3286) [14] and two studiesfrom Argentina which reported 39 and 67 respectively[6 15] In Brazil it was found that children of 5ndash8 years oldweremore likely to be positive forToxocara canis [8] contraryto the findings in this study where the older group had moreseropositives Another study showed a higher prevalence ingroups from 1 to 10 years of age which was related to picaand contact with puppies [16]

In both age ranges boys were more prone to be infectedwith Toxocara canis than girls This has been observed inseveral studies with different degrees of magnitude In Indiaboys had double the infection rate (419) of girls (204) inthe 1 to 16 years old age group [14] which was similar to thatreported in children in Brazil with 667 prevalence in boysand 333 in girls [8]The eradication of dogs in Iceland dur-ing the forties resulted in the disappearance of Toxocariasis inhumans by the early eighties [17] A study in Brazil showed anassociation between increased levels of Toxocara antibodiesin children and the presence of young dogs and contact withtheir feces [7]

The presence of dogs in the household is considered a riskfactor for the presence of Toxocara seropositivity [18] In thisstudy the presence of dogs younger than one year of age wasfound to be a significant risk factor but this association is notalways detected [9] perhaps because in studies the age of thedog is not given and younger dogs are more susceptible totoxocariasis [14] A higher prevalence of Toxocara has alsobeen reported in unfenced houses indicating that the entryof dogs into the home is also a source of infection for children[14]

A lack of hand washing beforemeals was not significantlyassociated but had an OR of 173 It was found that 80of positive children did not wash their hands before eatingdoing nothing to prevent contamination after contact withpuppies or with soil or sand contaminated with Toxocaraeggs [19] A lack of washing of fruits and vegetables wasnot associated with serology positive however some studiesindicate that they can be sources of contaminationOnly a low

The Scientific World Journal 3

Table 2 Health problems and nutritional status associated with toxocariasis serology in children from Ecatepec Mexico

Problemnutrition status Positives (119899 = 24) Negatives (119899 = 84) Chi2 119901 OR (95 CI) 119875

Respiratory 5 21 029 058 073 0246ndash2212 058Dermatological 9 22 084 035 155 0602ndash4037 035Eosinophilia 15 21 104 0001 442 1728ndash11346 0001Normal nutrition 12 41 001 099 094 0386ndash2313 090Low weightmal nutrition 9 23 063 042 146 0568ndash3785 042Overweightobesity 6 17 014 070 122 0424ndash3543 0707lowastOR odds ratio CI confidence intervals p probability value for Chi-square P probability value for OR

Table 3 Some factors evaluated for their association with toxocariasis serology in children from Ecatepec Mexico

Factors Positives (119899 = 25) Negatives (119899 = 83) Chi2 p OR (95 CI) PNot washing hands 10 23 136 024 173 0683ndash4423 024Not washing fruits and vegetables 1 4 mdash mdash 082 0087ndash7718 086Consumption of raw meat 4 15 0057 081 086 0258ndash2885 081Onicophagia 13 38 029 058 128 0523ndash3141 058Use of public parks and gardens 19 54 195 030 170 0611ndash4729 030Ownership of dogs 18 70 193 016 047 0166ndash1371 016Ownership of dogs younger than 1 year 18 49 137 024 178 0672ndash4737 024Dog is not dewormed 6 17 014 070 122 04241ndash3548 070Dogs sleep with the owner 1 23 mdash mdash 010 0013ndash0850 003Frequent contact with dogs 11 45 080 037 066 0269ndash1632 037lowastOR odds ratio CI confidence intervals p probability value for Chi-square P probability value for OR

percentage (15) of raw vegetables used for salads was foundto be contaminatedwithToxocara spp [20]Theproblemmaybe larger as in Libya eggs were found to be contaminatedwith Toxocara canis and Toxocara cati in 11 to 48 of127 samples of raw salads [21] In Mexico contaminationwas demonstrated in carrots and radishes that were notdisinfected correctly [22]The consumption of raw vegetablesgrown in soils contaminated with Toxocara can be a source ofchronic infection [23]

Although there was no association of seropositives withrespiratory problems bronchospasm shortness of breathand cough have been reported in children with Toxocari-asis [24] Of the patients with positive serology 60 hadeosinophilia Among the causes of eosinophilia are parasiticand allergic diseases with the latter considered to be themaindiagnosis [23] An increase in eosinophils has been associatedwith Toxocara [12]

Although nutritional status was not associated with tox-ocariasis serology the odds ratio values indicate that lowweightmalnutrition (OR = 146) and overweightobesity(OR = 122) can be considered as potential risk factorsAn association between BMI and Toxocara has not beenreported however correlation between the presence ofhelminthes and nutritional status has been evaluated inVenezuela in a group of 257 children and adolescents whereintestinal parasites were associated with the presence ofmalnutrition with 435 of malnourished children para-sitized [25] In a study conducted in Argentina with 248

children 242 had some form of malnutrition (109 weremalnourished and 133were overweight) and 746 of thesehad parasites with the 89 of children with malnutritionand parasitism representing a slightly higher prevalence inmalnourished than in normally nourished children [10]

There is one study about seroprevalence for Toxocaraamong children along the Mexico-United States borderregion with 106 positives [26] however the infestationpotential is very high in the metropolitan area in the Stateof Mexico since the soils in public parks are highly contam-inated (303) as well as dog feces found in soil (281) orsampled from dogs with owners (398) [27] Environmentalcontamination and the high prevalence of parasitized dogsexplain the seropositivity found in this study and should beconsidered as important aspects for Toxocariasis preventionin children

5 Conclusions

It is concluded that boys had a greater presence of antibod-ies than girls and seroprevalence increased with age Themedium rate for Toxocariasis seroprevalence found in thisstudy in children could be the result of several factors how-ever the results indicate that ownership of younger dogs inthe home is the main risk factor associated with ToxocariasisOther factors including malnutrition obesity not washinghands before meals and use of public parks were not signifi-cantly associated with seropositivity to Toxocara canis in this

4 The Scientific World Journal

study however future studies should be conducted to betterassess the importance of these factors in this zoonotic disease

Acknowledgments

The authors extend their thanks to CONACYT for thescholarship for the graduate student This study is derivedfrom the thesis for the degree of Doctorate in Sciences ofHealth the Faculty of Medicine UAEM registered in thePNPC-CONACYT

References

[1] A Habluetzel G Traldi S Ruggieri et al ldquoAn estimation ofToxocara canis prevalence in dogs environmental egg contam-ination and risk of human infection in the Marche region ofItalyrdquo Veterinary Parasitology vol 113 no 3-4 pp 243ndash2522003

[2] M Aydenizoz-Ozkayhan B B Yagci and S Erat ldquoThe investi-gation ofToxocara canis eggs in coats of different dog breeds as apotential transmission route in human toxocariasisrdquoVeterinaryParasitology vol 152 no 1-2 pp 94ndash100 2008

[3] A Cianferoni L Schneider P M Schantz D Brown and L MFox ldquoVisceral larva migrans associated with earthworm inges-tion clinical evolution in an adolescent patientrdquo Pediatrics vol117 no 2 pp e336ndashe339 2006

[4] D Choi J Hoon D C Choi et al ldquoToxocariasis and ingestionof raw cow liver in patients with eosinophiliardquo Korean Journalof Parasitology vol 46 no 3 pp 139ndash143 2008

[5] A Guerra C Navarro andC L de Guevara ldquoSeroprevalence oftoxocariasis in children and a case of VLMrdquo European Journalof Epidemiology vol 11 no 6 pp 701ndash702 1995

[6] M A Lopez G Martin M C Chamorro and J M AlonsoldquoToxocariosis en ninos de una region subtropicalrdquo Medicinavol 65 no 3 pp 226ndash230 2005

[7] S D Figueiredo J A Taddei J J Menezes N F Novo E OSilva and H L Cristovao ldquoClinical-epidemiological study oftoxocariasis in a pediatric populationrdquo Jornal de Pediatria vol81 no 2 pp 126ndash132 2005

[8] C R Teixeira P P Chieffi S A Z Lescano et al ldquoFrequencyand risk factors for toxocariasis in children from a pediatricoutpatient center in Southeastern Brazilrdquo Revista do Instituto deMedicina Tropical de Sao Paulo vol 48 no 5 pp 251ndash255 2006

[9] WH Roldan Y A Cavero Y A Espinoza S Jimenez andC AGutierrez ldquoHuman toxocariasis a seroepidemiological surveyin the Amazonian City of Yurimaguas Perurdquo Revista do Insti-tuto de Medicina Tropical de Sao Paulo vol 52 no 1 pp 37ndash422010

[10] M L Zonta M Garraza L Castro et al ldquoPoverty Nutritionalstatus and child enteropasitoses a cross-sectional study inAristobulo del Valle Misiones Argentinardquo Nutricion ClınicaDietetica y Hospitalaria vol 31 no 2 pp 48ndash57 2011

[11] World Health Organization (WHO) ldquoPhysical status the useand interpretation of anthropometryrdquo World Technical Orga-nization Technical Reports Series 854 1995

[12] S Y Karadam S Ertug H Ertabaklar and P Okyay ldquoThecomparision of IgG antibodies specific to Toxocara spp amongeosinophilic and non-eosinophilic groupsrdquoNewMicrobiologicavol 31 no 1 pp 113ndash116 2008

[13] J L Fleiss Statistical Methods for Rates and Proportions JohnWiley amp Sons New York NY USA 1981

[14] Z Dar S Tanveer G Yattoo et al ldquoSeroprevalence of toxocari-asis in children in Kashmir J amp K State Indiardquo Iranian Journalof Parasitology vol 3 no 4 pp 45ndash50 2008

[15] N E Radman SMArchelli RD Fonrouge et al ldquoHuman tox-ocarosis Its seroprevalence in theCity of La PlatardquoMemorias doInstituto Oswaldo Cruz vol 95 no 3 pp 281ndash285 2000

[16] N Malla A K Aggarwal and R C Mahajan ldquoA serologicalstudy of human toxocariasis in North Indiardquo The NationalMedical Journal of India vol 15 no 3 pp 145ndash147 2002

[17] A W Woodruff D de Savigny and P M Hendy-Ibbs ldquoTox-ocaral and toxoplasmal antibodies in cat breeders and in Ice-landers exposed to cats but not to dogsrdquo BritishMedical Journalvol 284 no 6312 pp 309ndash310 1982

[18] C K Fan C W Liao T C Kao et al ldquoSero-epidemiologyof Toxocara canis infection among aboriginal schoolchildrenin the mountainous areas of North-Eastern Taiwanrdquo Annals ofTropical Medicine and Parasitology vol 99 no 6 pp 593ndash6002005

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

[20] E Kozan B Gonenc O Sarimehmetoglu and H AycicekldquoPrevalence of helminth eggs on raw vegetables used for saladsrdquoFood Control vol 16 no 3 pp 239ndash242 2005

[21] A K AbougrainMH Nahaisi N SMadiMM Saied and KS Ghenghesh ldquoParasitological contamination in salad vegeta-bles in Tripoli-Libyardquo Food Control vol 21 no 5 pp 760ndash7622010

[22] T Vazquez BMartinez Z Tay H Ruiz andT Perez ldquoVerdurasde consumo humano como probable fuente de infeccion deToxocara sp para el hombrerdquo Boletın Chileno de Parasitologıavol 52 no 3-4 pp 47ndash50 1997

[23] J F Magnaval L T Glickman P Dorchies and B MorassinldquoHighlights of human toxocariasisrdquoKorean Journal of Parasitol-ogy vol 39 no 1 pp 1ndash11 2001

[24] J M S Alderete C M A Jacob A C Pastorino et al ldquoPreva-lence of Toxocara Infection in Schoolchildren from the ButantaRegion Sao Paulo BrazilrdquoMemorias do Instituto Oswaldo Cruzvol 98 no 5 pp 593ndash597 2003

[25] L Solano I Acuna A Baron AMoron andA Sanchez ldquoInflu-encia de las parasitosis intestinales y otros antecedentes infec-ciosos sobre el estado nutricional antropometrico de ninos ensituacion de pobrezardquo Parasitologıa Latinoamericana vol 63no 1 pp 12ndash19 2008

[26] L Tinoco S Barrera V Lopez S Tamayo R Quiroz and TMelgarejo ldquoSeroprevalence of larva migrans of Toxocara canisand evaluation of associated risk factorrdquo International Journal ofApplied Research in Veterinary Medicine vol 6 no 2 pp 130ndash136 2008

[27] C Romero G Mendoza P Bustamante M Crosby and NRamırez ldquoPresencia y viabilidad de Toxocara spp en suelos deparques publicos jardines de casas y heces de perros en Nez-ahualcoyotl Mexicordquo Revista Cientıfica vol 21 no 3 pp 195ndash1201 2011

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Page 2: Research Article Prevalence and Risk Factors Associated with Toxocara canis Infection ...downloads.hindawi.com/journals/tswj/2013/572089.pdf · 2019-07-31 · toxocariasis in children

2 The Scientific World Journal

climate with rains in summer with a mean temperature of138∘C (between 7 and 30∘C) and an average relative humidityof 35

22 Data Collection Interviews were carried out in theschools of participants with informed consent from a parentandor legal guardian and the assent of the children A totalof 108 subjects from 24 months to 16 years old participatedin this research with parental agreement for this study Thisresearch had the approval of the Ethical Research Committeeof the Graduate School of Medicine faculty UniversidadAutonoma del Estado de Mexico

Data from the questionnaires included risk factors andepidemiological data (age sex dog ownership dog presenceindoors dogs sleeping with people older dogs pet deworm-ing presence of other pets use of public parks history ofonychophagia not washing hands and eating undercookedmeat)The clinical data considered included respiratory signs(bronchospasm bronchitis and asthma) dermatologic signs(rash hives and itching) and BMI as ameasure of nutritionalstatus [10] Children with BMI less than 20 kgm2 wereconsidered underweight or malnourished those with BMIgreater than 30 kgm2 were categorized as overweight orobese and the rest were considered as having normal nutri-tion [11]

23 Laboratory Analyses Blood samples were collected forserology and assessment of eosinophils All sera were ana-lyzed by ELISA at the Parasitology Laboratory of theNationalInstitute of Pediatrics Mexico City DF using a commercialkit with Toxocara IgG (SCIMEDX Toxocara IgG) Values ofoptical density greater than 03 according to the serologicalELISA test were considered positive The numbers of circu-lating eosinophils were evaluated ldquoeosinophiliardquo was used todescribe those withmore than 10 eosinophils or an absolutevalue greater than 500 cells120583L of IgG [12]

24 Statistical Analysis Analysis was carried out using Chi-square and odds ratio (OR) tests in order to confirm themeandifferences between groups and association with seropreva-lence [13]The level of significance selected was119875 lt 005withan odds ratio gt10

3 Results

Twenty-four (2222) serum samples from the 108 examinedsera were T canis seropositive (Table 1) The prevalence ofantibodies against T canis was greater (119875 = 002) in malesthan females (2884 and 1607 resp) The seroprevalenceto T canis tended be lower in the youngest children (462)compared with the oldest group (1759) as shown in Table 1

Analysis of the signssymptoms suggested no relationshipbetween respiratory signs or symptoms (200) or cutaneoussigns (360) with Toxocariasis although the odds ratio wasgreater than 1 in the latter case (Table 2) Eosinophilia wasstatistically associated with positive serology (Table 2)

The analysis of risk factors evidenced that malnutritionobesity not washing hands before meals onicophagia and

Table 1 Seroprevalence of Toxocara canis in boys and girls from 2to 16 years of age

Age Seropositives119875-Fisher

Males (119899 = 52) Females (119899 = 56)2ndash11 years 3 2 03112ndash16 years 12 7 009Total 15 9 002

use of public parks all showed significant associations withseropositivity although theOR values (gt10) suggest that theymay be epidemiologically important for Toxocara presence(Table 3) Nevertheless the presence of dogs younger than 1year old within households showed a significant associationwith seropositivity (Table 3)

4 Discussion

The seroprevalence rate found (2222) was lower than thatreported in children from India (3286) [14] and two studiesfrom Argentina which reported 39 and 67 respectively[6 15] In Brazil it was found that children of 5ndash8 years oldweremore likely to be positive forToxocara canis [8] contraryto the findings in this study where the older group had moreseropositives Another study showed a higher prevalence ingroups from 1 to 10 years of age which was related to picaand contact with puppies [16]

In both age ranges boys were more prone to be infectedwith Toxocara canis than girls This has been observed inseveral studies with different degrees of magnitude In Indiaboys had double the infection rate (419) of girls (204) inthe 1 to 16 years old age group [14] which was similar to thatreported in children in Brazil with 667 prevalence in boysand 333 in girls [8]The eradication of dogs in Iceland dur-ing the forties resulted in the disappearance of Toxocariasis inhumans by the early eighties [17] A study in Brazil showed anassociation between increased levels of Toxocara antibodiesin children and the presence of young dogs and contact withtheir feces [7]

The presence of dogs in the household is considered a riskfactor for the presence of Toxocara seropositivity [18] In thisstudy the presence of dogs younger than one year of age wasfound to be a significant risk factor but this association is notalways detected [9] perhaps because in studies the age of thedog is not given and younger dogs are more susceptible totoxocariasis [14] A higher prevalence of Toxocara has alsobeen reported in unfenced houses indicating that the entryof dogs into the home is also a source of infection for children[14]

A lack of hand washing beforemeals was not significantlyassociated but had an OR of 173 It was found that 80of positive children did not wash their hands before eatingdoing nothing to prevent contamination after contact withpuppies or with soil or sand contaminated with Toxocaraeggs [19] A lack of washing of fruits and vegetables wasnot associated with serology positive however some studiesindicate that they can be sources of contaminationOnly a low

The Scientific World Journal 3

Table 2 Health problems and nutritional status associated with toxocariasis serology in children from Ecatepec Mexico

Problemnutrition status Positives (119899 = 24) Negatives (119899 = 84) Chi2 119901 OR (95 CI) 119875

Respiratory 5 21 029 058 073 0246ndash2212 058Dermatological 9 22 084 035 155 0602ndash4037 035Eosinophilia 15 21 104 0001 442 1728ndash11346 0001Normal nutrition 12 41 001 099 094 0386ndash2313 090Low weightmal nutrition 9 23 063 042 146 0568ndash3785 042Overweightobesity 6 17 014 070 122 0424ndash3543 0707lowastOR odds ratio CI confidence intervals p probability value for Chi-square P probability value for OR

Table 3 Some factors evaluated for their association with toxocariasis serology in children from Ecatepec Mexico

Factors Positives (119899 = 25) Negatives (119899 = 83) Chi2 p OR (95 CI) PNot washing hands 10 23 136 024 173 0683ndash4423 024Not washing fruits and vegetables 1 4 mdash mdash 082 0087ndash7718 086Consumption of raw meat 4 15 0057 081 086 0258ndash2885 081Onicophagia 13 38 029 058 128 0523ndash3141 058Use of public parks and gardens 19 54 195 030 170 0611ndash4729 030Ownership of dogs 18 70 193 016 047 0166ndash1371 016Ownership of dogs younger than 1 year 18 49 137 024 178 0672ndash4737 024Dog is not dewormed 6 17 014 070 122 04241ndash3548 070Dogs sleep with the owner 1 23 mdash mdash 010 0013ndash0850 003Frequent contact with dogs 11 45 080 037 066 0269ndash1632 037lowastOR odds ratio CI confidence intervals p probability value for Chi-square P probability value for OR

percentage (15) of raw vegetables used for salads was foundto be contaminatedwithToxocara spp [20]Theproblemmaybe larger as in Libya eggs were found to be contaminatedwith Toxocara canis and Toxocara cati in 11 to 48 of127 samples of raw salads [21] In Mexico contaminationwas demonstrated in carrots and radishes that were notdisinfected correctly [22]The consumption of raw vegetablesgrown in soils contaminated with Toxocara can be a source ofchronic infection [23]

Although there was no association of seropositives withrespiratory problems bronchospasm shortness of breathand cough have been reported in children with Toxocari-asis [24] Of the patients with positive serology 60 hadeosinophilia Among the causes of eosinophilia are parasiticand allergic diseases with the latter considered to be themaindiagnosis [23] An increase in eosinophils has been associatedwith Toxocara [12]

Although nutritional status was not associated with tox-ocariasis serology the odds ratio values indicate that lowweightmalnutrition (OR = 146) and overweightobesity(OR = 122) can be considered as potential risk factorsAn association between BMI and Toxocara has not beenreported however correlation between the presence ofhelminthes and nutritional status has been evaluated inVenezuela in a group of 257 children and adolescents whereintestinal parasites were associated with the presence ofmalnutrition with 435 of malnourished children para-sitized [25] In a study conducted in Argentina with 248

children 242 had some form of malnutrition (109 weremalnourished and 133were overweight) and 746 of thesehad parasites with the 89 of children with malnutritionand parasitism representing a slightly higher prevalence inmalnourished than in normally nourished children [10]

There is one study about seroprevalence for Toxocaraamong children along the Mexico-United States borderregion with 106 positives [26] however the infestationpotential is very high in the metropolitan area in the Stateof Mexico since the soils in public parks are highly contam-inated (303) as well as dog feces found in soil (281) orsampled from dogs with owners (398) [27] Environmentalcontamination and the high prevalence of parasitized dogsexplain the seropositivity found in this study and should beconsidered as important aspects for Toxocariasis preventionin children

5 Conclusions

It is concluded that boys had a greater presence of antibod-ies than girls and seroprevalence increased with age Themedium rate for Toxocariasis seroprevalence found in thisstudy in children could be the result of several factors how-ever the results indicate that ownership of younger dogs inthe home is the main risk factor associated with ToxocariasisOther factors including malnutrition obesity not washinghands before meals and use of public parks were not signifi-cantly associated with seropositivity to Toxocara canis in this

4 The Scientific World Journal

study however future studies should be conducted to betterassess the importance of these factors in this zoonotic disease

Acknowledgments

The authors extend their thanks to CONACYT for thescholarship for the graduate student This study is derivedfrom the thesis for the degree of Doctorate in Sciences ofHealth the Faculty of Medicine UAEM registered in thePNPC-CONACYT

References

[1] A Habluetzel G Traldi S Ruggieri et al ldquoAn estimation ofToxocara canis prevalence in dogs environmental egg contam-ination and risk of human infection in the Marche region ofItalyrdquo Veterinary Parasitology vol 113 no 3-4 pp 243ndash2522003

[2] M Aydenizoz-Ozkayhan B B Yagci and S Erat ldquoThe investi-gation ofToxocara canis eggs in coats of different dog breeds as apotential transmission route in human toxocariasisrdquoVeterinaryParasitology vol 152 no 1-2 pp 94ndash100 2008

[3] A Cianferoni L Schneider P M Schantz D Brown and L MFox ldquoVisceral larva migrans associated with earthworm inges-tion clinical evolution in an adolescent patientrdquo Pediatrics vol117 no 2 pp e336ndashe339 2006

[4] D Choi J Hoon D C Choi et al ldquoToxocariasis and ingestionof raw cow liver in patients with eosinophiliardquo Korean Journalof Parasitology vol 46 no 3 pp 139ndash143 2008

[5] A Guerra C Navarro andC L de Guevara ldquoSeroprevalence oftoxocariasis in children and a case of VLMrdquo European Journalof Epidemiology vol 11 no 6 pp 701ndash702 1995

[6] M A Lopez G Martin M C Chamorro and J M AlonsoldquoToxocariosis en ninos de una region subtropicalrdquo Medicinavol 65 no 3 pp 226ndash230 2005

[7] S D Figueiredo J A Taddei J J Menezes N F Novo E OSilva and H L Cristovao ldquoClinical-epidemiological study oftoxocariasis in a pediatric populationrdquo Jornal de Pediatria vol81 no 2 pp 126ndash132 2005

[8] C R Teixeira P P Chieffi S A Z Lescano et al ldquoFrequencyand risk factors for toxocariasis in children from a pediatricoutpatient center in Southeastern Brazilrdquo Revista do Instituto deMedicina Tropical de Sao Paulo vol 48 no 5 pp 251ndash255 2006

[9] WH Roldan Y A Cavero Y A Espinoza S Jimenez andC AGutierrez ldquoHuman toxocariasis a seroepidemiological surveyin the Amazonian City of Yurimaguas Perurdquo Revista do Insti-tuto de Medicina Tropical de Sao Paulo vol 52 no 1 pp 37ndash422010

[10] M L Zonta M Garraza L Castro et al ldquoPoverty Nutritionalstatus and child enteropasitoses a cross-sectional study inAristobulo del Valle Misiones Argentinardquo Nutricion ClınicaDietetica y Hospitalaria vol 31 no 2 pp 48ndash57 2011

[11] World Health Organization (WHO) ldquoPhysical status the useand interpretation of anthropometryrdquo World Technical Orga-nization Technical Reports Series 854 1995

[12] S Y Karadam S Ertug H Ertabaklar and P Okyay ldquoThecomparision of IgG antibodies specific to Toxocara spp amongeosinophilic and non-eosinophilic groupsrdquoNewMicrobiologicavol 31 no 1 pp 113ndash116 2008

[13] J L Fleiss Statistical Methods for Rates and Proportions JohnWiley amp Sons New York NY USA 1981

[14] Z Dar S Tanveer G Yattoo et al ldquoSeroprevalence of toxocari-asis in children in Kashmir J amp K State Indiardquo Iranian Journalof Parasitology vol 3 no 4 pp 45ndash50 2008

[15] N E Radman SMArchelli RD Fonrouge et al ldquoHuman tox-ocarosis Its seroprevalence in theCity of La PlatardquoMemorias doInstituto Oswaldo Cruz vol 95 no 3 pp 281ndash285 2000

[16] N Malla A K Aggarwal and R C Mahajan ldquoA serologicalstudy of human toxocariasis in North Indiardquo The NationalMedical Journal of India vol 15 no 3 pp 145ndash147 2002

[17] A W Woodruff D de Savigny and P M Hendy-Ibbs ldquoTox-ocaral and toxoplasmal antibodies in cat breeders and in Ice-landers exposed to cats but not to dogsrdquo BritishMedical Journalvol 284 no 6312 pp 309ndash310 1982

[18] C K Fan C W Liao T C Kao et al ldquoSero-epidemiologyof Toxocara canis infection among aboriginal schoolchildrenin the mountainous areas of North-Eastern Taiwanrdquo Annals ofTropical Medicine and Parasitology vol 99 no 6 pp 593ndash6002005

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

[20] E Kozan B Gonenc O Sarimehmetoglu and H AycicekldquoPrevalence of helminth eggs on raw vegetables used for saladsrdquoFood Control vol 16 no 3 pp 239ndash242 2005

[21] A K AbougrainMH Nahaisi N SMadiMM Saied and KS Ghenghesh ldquoParasitological contamination in salad vegeta-bles in Tripoli-Libyardquo Food Control vol 21 no 5 pp 760ndash7622010

[22] T Vazquez BMartinez Z Tay H Ruiz andT Perez ldquoVerdurasde consumo humano como probable fuente de infeccion deToxocara sp para el hombrerdquo Boletın Chileno de Parasitologıavol 52 no 3-4 pp 47ndash50 1997

[23] J F Magnaval L T Glickman P Dorchies and B MorassinldquoHighlights of human toxocariasisrdquoKorean Journal of Parasitol-ogy vol 39 no 1 pp 1ndash11 2001

[24] J M S Alderete C M A Jacob A C Pastorino et al ldquoPreva-lence of Toxocara Infection in Schoolchildren from the ButantaRegion Sao Paulo BrazilrdquoMemorias do Instituto Oswaldo Cruzvol 98 no 5 pp 593ndash597 2003

[25] L Solano I Acuna A Baron AMoron andA Sanchez ldquoInflu-encia de las parasitosis intestinales y otros antecedentes infec-ciosos sobre el estado nutricional antropometrico de ninos ensituacion de pobrezardquo Parasitologıa Latinoamericana vol 63no 1 pp 12ndash19 2008

[26] L Tinoco S Barrera V Lopez S Tamayo R Quiroz and TMelgarejo ldquoSeroprevalence of larva migrans of Toxocara canisand evaluation of associated risk factorrdquo International Journal ofApplied Research in Veterinary Medicine vol 6 no 2 pp 130ndash136 2008

[27] C Romero G Mendoza P Bustamante M Crosby and NRamırez ldquoPresencia y viabilidad de Toxocara spp en suelos deparques publicos jardines de casas y heces de perros en Nez-ahualcoyotl Mexicordquo Revista Cientıfica vol 21 no 3 pp 195ndash1201 2011

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Page 3: Research Article Prevalence and Risk Factors Associated with Toxocara canis Infection ...downloads.hindawi.com/journals/tswj/2013/572089.pdf · 2019-07-31 · toxocariasis in children

The Scientific World Journal 3

Table 2 Health problems and nutritional status associated with toxocariasis serology in children from Ecatepec Mexico

Problemnutrition status Positives (119899 = 24) Negatives (119899 = 84) Chi2 119901 OR (95 CI) 119875

Respiratory 5 21 029 058 073 0246ndash2212 058Dermatological 9 22 084 035 155 0602ndash4037 035Eosinophilia 15 21 104 0001 442 1728ndash11346 0001Normal nutrition 12 41 001 099 094 0386ndash2313 090Low weightmal nutrition 9 23 063 042 146 0568ndash3785 042Overweightobesity 6 17 014 070 122 0424ndash3543 0707lowastOR odds ratio CI confidence intervals p probability value for Chi-square P probability value for OR

Table 3 Some factors evaluated for their association with toxocariasis serology in children from Ecatepec Mexico

Factors Positives (119899 = 25) Negatives (119899 = 83) Chi2 p OR (95 CI) PNot washing hands 10 23 136 024 173 0683ndash4423 024Not washing fruits and vegetables 1 4 mdash mdash 082 0087ndash7718 086Consumption of raw meat 4 15 0057 081 086 0258ndash2885 081Onicophagia 13 38 029 058 128 0523ndash3141 058Use of public parks and gardens 19 54 195 030 170 0611ndash4729 030Ownership of dogs 18 70 193 016 047 0166ndash1371 016Ownership of dogs younger than 1 year 18 49 137 024 178 0672ndash4737 024Dog is not dewormed 6 17 014 070 122 04241ndash3548 070Dogs sleep with the owner 1 23 mdash mdash 010 0013ndash0850 003Frequent contact with dogs 11 45 080 037 066 0269ndash1632 037lowastOR odds ratio CI confidence intervals p probability value for Chi-square P probability value for OR

percentage (15) of raw vegetables used for salads was foundto be contaminatedwithToxocara spp [20]Theproblemmaybe larger as in Libya eggs were found to be contaminatedwith Toxocara canis and Toxocara cati in 11 to 48 of127 samples of raw salads [21] In Mexico contaminationwas demonstrated in carrots and radishes that were notdisinfected correctly [22]The consumption of raw vegetablesgrown in soils contaminated with Toxocara can be a source ofchronic infection [23]

Although there was no association of seropositives withrespiratory problems bronchospasm shortness of breathand cough have been reported in children with Toxocari-asis [24] Of the patients with positive serology 60 hadeosinophilia Among the causes of eosinophilia are parasiticand allergic diseases with the latter considered to be themaindiagnosis [23] An increase in eosinophils has been associatedwith Toxocara [12]

Although nutritional status was not associated with tox-ocariasis serology the odds ratio values indicate that lowweightmalnutrition (OR = 146) and overweightobesity(OR = 122) can be considered as potential risk factorsAn association between BMI and Toxocara has not beenreported however correlation between the presence ofhelminthes and nutritional status has been evaluated inVenezuela in a group of 257 children and adolescents whereintestinal parasites were associated with the presence ofmalnutrition with 435 of malnourished children para-sitized [25] In a study conducted in Argentina with 248

children 242 had some form of malnutrition (109 weremalnourished and 133were overweight) and 746 of thesehad parasites with the 89 of children with malnutritionand parasitism representing a slightly higher prevalence inmalnourished than in normally nourished children [10]

There is one study about seroprevalence for Toxocaraamong children along the Mexico-United States borderregion with 106 positives [26] however the infestationpotential is very high in the metropolitan area in the Stateof Mexico since the soils in public parks are highly contam-inated (303) as well as dog feces found in soil (281) orsampled from dogs with owners (398) [27] Environmentalcontamination and the high prevalence of parasitized dogsexplain the seropositivity found in this study and should beconsidered as important aspects for Toxocariasis preventionin children

5 Conclusions

It is concluded that boys had a greater presence of antibod-ies than girls and seroprevalence increased with age Themedium rate for Toxocariasis seroprevalence found in thisstudy in children could be the result of several factors how-ever the results indicate that ownership of younger dogs inthe home is the main risk factor associated with ToxocariasisOther factors including malnutrition obesity not washinghands before meals and use of public parks were not signifi-cantly associated with seropositivity to Toxocara canis in this

4 The Scientific World Journal

study however future studies should be conducted to betterassess the importance of these factors in this zoonotic disease

Acknowledgments

The authors extend their thanks to CONACYT for thescholarship for the graduate student This study is derivedfrom the thesis for the degree of Doctorate in Sciences ofHealth the Faculty of Medicine UAEM registered in thePNPC-CONACYT

References

[1] A Habluetzel G Traldi S Ruggieri et al ldquoAn estimation ofToxocara canis prevalence in dogs environmental egg contam-ination and risk of human infection in the Marche region ofItalyrdquo Veterinary Parasitology vol 113 no 3-4 pp 243ndash2522003

[2] M Aydenizoz-Ozkayhan B B Yagci and S Erat ldquoThe investi-gation ofToxocara canis eggs in coats of different dog breeds as apotential transmission route in human toxocariasisrdquoVeterinaryParasitology vol 152 no 1-2 pp 94ndash100 2008

[3] A Cianferoni L Schneider P M Schantz D Brown and L MFox ldquoVisceral larva migrans associated with earthworm inges-tion clinical evolution in an adolescent patientrdquo Pediatrics vol117 no 2 pp e336ndashe339 2006

[4] D Choi J Hoon D C Choi et al ldquoToxocariasis and ingestionof raw cow liver in patients with eosinophiliardquo Korean Journalof Parasitology vol 46 no 3 pp 139ndash143 2008

[5] A Guerra C Navarro andC L de Guevara ldquoSeroprevalence oftoxocariasis in children and a case of VLMrdquo European Journalof Epidemiology vol 11 no 6 pp 701ndash702 1995

[6] M A Lopez G Martin M C Chamorro and J M AlonsoldquoToxocariosis en ninos de una region subtropicalrdquo Medicinavol 65 no 3 pp 226ndash230 2005

[7] S D Figueiredo J A Taddei J J Menezes N F Novo E OSilva and H L Cristovao ldquoClinical-epidemiological study oftoxocariasis in a pediatric populationrdquo Jornal de Pediatria vol81 no 2 pp 126ndash132 2005

[8] C R Teixeira P P Chieffi S A Z Lescano et al ldquoFrequencyand risk factors for toxocariasis in children from a pediatricoutpatient center in Southeastern Brazilrdquo Revista do Instituto deMedicina Tropical de Sao Paulo vol 48 no 5 pp 251ndash255 2006

[9] WH Roldan Y A Cavero Y A Espinoza S Jimenez andC AGutierrez ldquoHuman toxocariasis a seroepidemiological surveyin the Amazonian City of Yurimaguas Perurdquo Revista do Insti-tuto de Medicina Tropical de Sao Paulo vol 52 no 1 pp 37ndash422010

[10] M L Zonta M Garraza L Castro et al ldquoPoverty Nutritionalstatus and child enteropasitoses a cross-sectional study inAristobulo del Valle Misiones Argentinardquo Nutricion ClınicaDietetica y Hospitalaria vol 31 no 2 pp 48ndash57 2011

[11] World Health Organization (WHO) ldquoPhysical status the useand interpretation of anthropometryrdquo World Technical Orga-nization Technical Reports Series 854 1995

[12] S Y Karadam S Ertug H Ertabaklar and P Okyay ldquoThecomparision of IgG antibodies specific to Toxocara spp amongeosinophilic and non-eosinophilic groupsrdquoNewMicrobiologicavol 31 no 1 pp 113ndash116 2008

[13] J L Fleiss Statistical Methods for Rates and Proportions JohnWiley amp Sons New York NY USA 1981

[14] Z Dar S Tanveer G Yattoo et al ldquoSeroprevalence of toxocari-asis in children in Kashmir J amp K State Indiardquo Iranian Journalof Parasitology vol 3 no 4 pp 45ndash50 2008

[15] N E Radman SMArchelli RD Fonrouge et al ldquoHuman tox-ocarosis Its seroprevalence in theCity of La PlatardquoMemorias doInstituto Oswaldo Cruz vol 95 no 3 pp 281ndash285 2000

[16] N Malla A K Aggarwal and R C Mahajan ldquoA serologicalstudy of human toxocariasis in North Indiardquo The NationalMedical Journal of India vol 15 no 3 pp 145ndash147 2002

[17] A W Woodruff D de Savigny and P M Hendy-Ibbs ldquoTox-ocaral and toxoplasmal antibodies in cat breeders and in Ice-landers exposed to cats but not to dogsrdquo BritishMedical Journalvol 284 no 6312 pp 309ndash310 1982

[18] C K Fan C W Liao T C Kao et al ldquoSero-epidemiologyof Toxocara canis infection among aboriginal schoolchildrenin the mountainous areas of North-Eastern Taiwanrdquo Annals ofTropical Medicine and Parasitology vol 99 no 6 pp 593ndash6002005

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

[20] E Kozan B Gonenc O Sarimehmetoglu and H AycicekldquoPrevalence of helminth eggs on raw vegetables used for saladsrdquoFood Control vol 16 no 3 pp 239ndash242 2005

[21] A K AbougrainMH Nahaisi N SMadiMM Saied and KS Ghenghesh ldquoParasitological contamination in salad vegeta-bles in Tripoli-Libyardquo Food Control vol 21 no 5 pp 760ndash7622010

[22] T Vazquez BMartinez Z Tay H Ruiz andT Perez ldquoVerdurasde consumo humano como probable fuente de infeccion deToxocara sp para el hombrerdquo Boletın Chileno de Parasitologıavol 52 no 3-4 pp 47ndash50 1997

[23] J F Magnaval L T Glickman P Dorchies and B MorassinldquoHighlights of human toxocariasisrdquoKorean Journal of Parasitol-ogy vol 39 no 1 pp 1ndash11 2001

[24] J M S Alderete C M A Jacob A C Pastorino et al ldquoPreva-lence of Toxocara Infection in Schoolchildren from the ButantaRegion Sao Paulo BrazilrdquoMemorias do Instituto Oswaldo Cruzvol 98 no 5 pp 593ndash597 2003

[25] L Solano I Acuna A Baron AMoron andA Sanchez ldquoInflu-encia de las parasitosis intestinales y otros antecedentes infec-ciosos sobre el estado nutricional antropometrico de ninos ensituacion de pobrezardquo Parasitologıa Latinoamericana vol 63no 1 pp 12ndash19 2008

[26] L Tinoco S Barrera V Lopez S Tamayo R Quiroz and TMelgarejo ldquoSeroprevalence of larva migrans of Toxocara canisand evaluation of associated risk factorrdquo International Journal ofApplied Research in Veterinary Medicine vol 6 no 2 pp 130ndash136 2008

[27] C Romero G Mendoza P Bustamante M Crosby and NRamırez ldquoPresencia y viabilidad de Toxocara spp en suelos deparques publicos jardines de casas y heces de perros en Nez-ahualcoyotl Mexicordquo Revista Cientıfica vol 21 no 3 pp 195ndash1201 2011

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Page 4: Research Article Prevalence and Risk Factors Associated with Toxocara canis Infection ...downloads.hindawi.com/journals/tswj/2013/572089.pdf · 2019-07-31 · toxocariasis in children

4 The Scientific World Journal

study however future studies should be conducted to betterassess the importance of these factors in this zoonotic disease

Acknowledgments

The authors extend their thanks to CONACYT for thescholarship for the graduate student This study is derivedfrom the thesis for the degree of Doctorate in Sciences ofHealth the Faculty of Medicine UAEM registered in thePNPC-CONACYT

References

[1] A Habluetzel G Traldi S Ruggieri et al ldquoAn estimation ofToxocara canis prevalence in dogs environmental egg contam-ination and risk of human infection in the Marche region ofItalyrdquo Veterinary Parasitology vol 113 no 3-4 pp 243ndash2522003

[2] M Aydenizoz-Ozkayhan B B Yagci and S Erat ldquoThe investi-gation ofToxocara canis eggs in coats of different dog breeds as apotential transmission route in human toxocariasisrdquoVeterinaryParasitology vol 152 no 1-2 pp 94ndash100 2008

[3] A Cianferoni L Schneider P M Schantz D Brown and L MFox ldquoVisceral larva migrans associated with earthworm inges-tion clinical evolution in an adolescent patientrdquo Pediatrics vol117 no 2 pp e336ndashe339 2006

[4] D Choi J Hoon D C Choi et al ldquoToxocariasis and ingestionof raw cow liver in patients with eosinophiliardquo Korean Journalof Parasitology vol 46 no 3 pp 139ndash143 2008

[5] A Guerra C Navarro andC L de Guevara ldquoSeroprevalence oftoxocariasis in children and a case of VLMrdquo European Journalof Epidemiology vol 11 no 6 pp 701ndash702 1995

[6] M A Lopez G Martin M C Chamorro and J M AlonsoldquoToxocariosis en ninos de una region subtropicalrdquo Medicinavol 65 no 3 pp 226ndash230 2005

[7] S D Figueiredo J A Taddei J J Menezes N F Novo E OSilva and H L Cristovao ldquoClinical-epidemiological study oftoxocariasis in a pediatric populationrdquo Jornal de Pediatria vol81 no 2 pp 126ndash132 2005

[8] C R Teixeira P P Chieffi S A Z Lescano et al ldquoFrequencyand risk factors for toxocariasis in children from a pediatricoutpatient center in Southeastern Brazilrdquo Revista do Instituto deMedicina Tropical de Sao Paulo vol 48 no 5 pp 251ndash255 2006

[9] WH Roldan Y A Cavero Y A Espinoza S Jimenez andC AGutierrez ldquoHuman toxocariasis a seroepidemiological surveyin the Amazonian City of Yurimaguas Perurdquo Revista do Insti-tuto de Medicina Tropical de Sao Paulo vol 52 no 1 pp 37ndash422010

[10] M L Zonta M Garraza L Castro et al ldquoPoverty Nutritionalstatus and child enteropasitoses a cross-sectional study inAristobulo del Valle Misiones Argentinardquo Nutricion ClınicaDietetica y Hospitalaria vol 31 no 2 pp 48ndash57 2011

[11] World Health Organization (WHO) ldquoPhysical status the useand interpretation of anthropometryrdquo World Technical Orga-nization Technical Reports Series 854 1995

[12] S Y Karadam S Ertug H Ertabaklar and P Okyay ldquoThecomparision of IgG antibodies specific to Toxocara spp amongeosinophilic and non-eosinophilic groupsrdquoNewMicrobiologicavol 31 no 1 pp 113ndash116 2008

[13] J L Fleiss Statistical Methods for Rates and Proportions JohnWiley amp Sons New York NY USA 1981

[14] Z Dar S Tanveer G Yattoo et al ldquoSeroprevalence of toxocari-asis in children in Kashmir J amp K State Indiardquo Iranian Journalof Parasitology vol 3 no 4 pp 45ndash50 2008

[15] N E Radman SMArchelli RD Fonrouge et al ldquoHuman tox-ocarosis Its seroprevalence in theCity of La PlatardquoMemorias doInstituto Oswaldo Cruz vol 95 no 3 pp 281ndash285 2000

[16] N Malla A K Aggarwal and R C Mahajan ldquoA serologicalstudy of human toxocariasis in North Indiardquo The NationalMedical Journal of India vol 15 no 3 pp 145ndash147 2002

[17] A W Woodruff D de Savigny and P M Hendy-Ibbs ldquoTox-ocaral and toxoplasmal antibodies in cat breeders and in Ice-landers exposed to cats but not to dogsrdquo BritishMedical Journalvol 284 no 6312 pp 309ndash310 1982

[18] C K Fan C W Liao T C Kao et al ldquoSero-epidemiologyof Toxocara canis infection among aboriginal schoolchildrenin the mountainous areas of North-Eastern Taiwanrdquo Annals ofTropical Medicine and Parasitology vol 99 no 6 pp 593ndash6002005

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

[20] E Kozan B Gonenc O Sarimehmetoglu and H AycicekldquoPrevalence of helminth eggs on raw vegetables used for saladsrdquoFood Control vol 16 no 3 pp 239ndash242 2005

[21] A K AbougrainMH Nahaisi N SMadiMM Saied and KS Ghenghesh ldquoParasitological contamination in salad vegeta-bles in Tripoli-Libyardquo Food Control vol 21 no 5 pp 760ndash7622010

[22] T Vazquez BMartinez Z Tay H Ruiz andT Perez ldquoVerdurasde consumo humano como probable fuente de infeccion deToxocara sp para el hombrerdquo Boletın Chileno de Parasitologıavol 52 no 3-4 pp 47ndash50 1997

[23] J F Magnaval L T Glickman P Dorchies and B MorassinldquoHighlights of human toxocariasisrdquoKorean Journal of Parasitol-ogy vol 39 no 1 pp 1ndash11 2001

[24] J M S Alderete C M A Jacob A C Pastorino et al ldquoPreva-lence of Toxocara Infection in Schoolchildren from the ButantaRegion Sao Paulo BrazilrdquoMemorias do Instituto Oswaldo Cruzvol 98 no 5 pp 593ndash597 2003

[25] L Solano I Acuna A Baron AMoron andA Sanchez ldquoInflu-encia de las parasitosis intestinales y otros antecedentes infec-ciosos sobre el estado nutricional antropometrico de ninos ensituacion de pobrezardquo Parasitologıa Latinoamericana vol 63no 1 pp 12ndash19 2008

[26] L Tinoco S Barrera V Lopez S Tamayo R Quiroz and TMelgarejo ldquoSeroprevalence of larva migrans of Toxocara canisand evaluation of associated risk factorrdquo International Journal ofApplied Research in Veterinary Medicine vol 6 no 2 pp 130ndash136 2008

[27] C Romero G Mendoza P Bustamante M Crosby and NRamırez ldquoPresencia y viabilidad de Toxocara spp en suelos deparques publicos jardines de casas y heces de perros en Nez-ahualcoyotl Mexicordquo Revista Cientıfica vol 21 no 3 pp 195ndash1201 2011

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology

Page 5: Research Article Prevalence and Risk Factors Associated with Toxocara canis Infection ...downloads.hindawi.com/journals/tswj/2013/572089.pdf · 2019-07-31 · toxocariasis in children

Submit your manuscripts athttpwwwhindawicom

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Anatomy Research International

PeptidesInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporation httpwwwhindawicom

International Journal of

Volume 2014

Zoology

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Molecular Biology International

GenomicsInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

The Scientific World JournalHindawi Publishing Corporation httpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioinformaticsAdvances in

Marine BiologyJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Signal TransductionJournal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

BioMed Research International

Evolutionary BiologyInternational Journal of

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Biochemistry Research International

ArchaeaHindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Genetics Research International

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Advances in

Virolog y

Hindawi Publishing Corporationhttpwwwhindawicom

Nucleic AcidsJournal of

Volume 2014

Stem CellsInternational

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

Enzyme Research

Hindawi Publishing Corporationhttpwwwhindawicom Volume 2014

International Journal of

Microbiology