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Original Article

Prevalence and Associated Risk Factors of Toxocara vitulorum Infections in Buffalo and Cattle Calves in Three Provinces of Central Cambodia

Pierre Dorny1,2,*, Brecht Devleesschauwer1, Valérie Stoliaroff1, Meas Sothy3, Rortana Chea3, Bunthon Chea3, Hor Sourloing3, Sum Samuth3, Seth Kong3, Koemseang Nguong3, San Sorn4, Davun Holl4, Jozef Vercruysse1
The Korean Journal of Parasitology 2015;53(2):197-200.
Published online: April 22, 2015

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*Corresponding author (pdorny@itg.be)
• Received: November 25, 2014   • Revised: January 21, 2015   • Accepted: March 12, 2015

© 2015, Korean Society for Parasitology and Tropical Medicine

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  • The prevalence and associated risk factors of Toxocara vitulorum infection in buffalo and cattle calves was studied in 3 provinces in central Cambodia. Fecal samples were collected from 517 calves between the age of 1-15 weeks and processed for nematode egg counts by a modified McMaster method. A total of 64 calves were found to excrete T. vitulorum eggs in their feces (12.4%; 95% exact CI: 9.7-15.5). The mean fecal egg count was 2,798 EPG (SD=16,351; range=0-224,400). A multivariable generalized linear mixed model showed higher odds of T. vitulorum infection for buffalo versus cattle, for animals aged 4-8 weeks versus younger and older ones, and for animals with strongyle infection. There was no association with fecal consistency. Farmers should be aware of the potential impact of T. vitulorum, and treat their calves at the age of 2-3 weeks with anthelmintics such as benzimidazoles or pyrantel.
  • Key words: Toxocara vitulorum, cattle, buffalo, prevalence, risk factor, Cambodia
Toxocara vitulorum is an intestinal ascarid parasite of cattle and water buffaloes (Bubalus bubalis). Although the parasite may occur worldwide, it is of particular economic importance in tropical and subtropical regions, mainly due to lacking or inefficient control [1]. T. vitulorum causes morbidity and mortality in calves, which typically become infected early post-partum by ingesting larvae excreted in the colostrum and milk [2]. After a prepatent period of 3-4 weeks, the ingested larvae have matured to adult worms in the calf’s duodenum that produce a large number of eggs, during a patent period of about 4 weeks. At the age of 8 weeks, most infected calves are able to clear the parasite due to strengthened and acquired immunity [3].
Cambodia, a Southeast Asian country, has a tropical climate characterized by distinct rainy and dry seasons. Agriculture is the major work sector in Cambodia, and within this sector, livestock is the third largest subsector, behind crop production and fisheries [4]. Cattle (mainly Bos indicus) and water buffaloes (Bubalus bubalis) provide draught power, manure used as fertilizer or biogas, and increasingly, animal protein and income from trade [5]. Nevertheless, the ruminant sector is characterized by smallholder farmers rearing limited numbers of animals in traditional production systems. As a result, the animals are highly susceptible to endemic diseases, including T. vitulorum and other gastrointestinal parasites [6], resulting in substandard agricultural output.
The aim of this study was to investigate the prevalence and associated risk factors of T. vitulorum infection in buffalo and cattle calves in Cambodia.
Study design
The study was conducted in 3 provinces, i.e., Pursat, Kampong Chnnang, and Kampong Cham, located in central Cambodia from June till October 2011. In each province, 6 communes were randomly selected and local farmers were asked for their cooperation. Fecal samples were collected from calves between the age of 1 and 15 weeks. The age of the animals was registered as either ≤28 days, 28-56 days, or >56 days.
Fecal examination
Each fecal sample was examined for the presence of eggs of T. vitulorum and strongyle eggs and Eimeria spp. oocysts by the McMaster technique with a sensitivity of 50 eggs per gram of feces (EPG) [7]. The consistency of the fecal sample was scored as being either normal, or soft, or watery.
Statistical analysis
T. vitulorum prevalence and corresponding exact 95% confidence intervals (CI) were calculated for the entire sample and for the different provinces, species, age groups, fecal consistencies, and co-infection categories. Additionally, the results of the T. vitulorum fecal egg counts were summarized by their arithmetic mean and SD.
Association of T. vitulorum prevalence with species, age group, fecal consistency, and co-infection category was assessed with a generalized linear mixed model for binary data, using adaptive Gaussian quadrature with 25 quadrature points. Commune was included as a random effect. A final multivariable model was obtained through a backwards selection procedure, at a significance level for removal of 5%. The analysis was performed in R 3.0.2 using the lme4 package [8,9].
A total of 517 animals were subjected in this study. Of these, 64 were found to excrete T. vitulorum eggs in their feces (12.4%; 95% exact CI: 9.7-15.5). The mean fecal egg count was 2,798 EPG (SD=16,351; range=0-224,400). Table 1 shows descriptive statistics by the province, species, age group, fecal consistency, and co-infection category.
The final multivariable generalized linear mixed model showed a higher odds of T. vitulorum infection for buffalo versus cattle, for animals aged 4-8 weeks versus younger and older ones, and for animals with strongyle infection (Table 2). There was no association with fecal consistency.
To our knowledge, this is the first report on T. vitulorum infections in buffalo and cattle calves from Cambodia. Prevalence estimates of T. vitulorum in neighboring countries also appear to be rare. Compared to those countries, the prevalence observed in our study is relatively low (12.4%). In Thailand, Srikitjakarn et al. [10] found a T. vitulorum prevalence of 58% in calves during their first 3 months of life. More recently, Holland et al. [11] observed a prevalence of 8% in Vietnamese calves aged 1-2 months, and Rast et al. [1] found a prevalence of 22.6% in buffalo and cattle calves aged <3 months in northern Lao PDR.
In our study, the main risk factors for T. vitulorum infection appeared to be host species and, not surprisingly, age. The apparent association with strongyle prevalence might be explained as an artefact due to the collinearity between strongyle infection and age (results not shown). Indeed, strongyle infections tend to be more common in older animals.
Roberts [12] reported clinical signs in toxocariasis, especially in buffalo calves. They included, poor hair coat, eczema, stools resembling white scour and having a foul smell, inappetency with intermittent colic and bloat [12]. More recent literature reports that calves with toxocariasis could have either pale colored or black diarrhea, or could be asymptomatic [13,14]. In our study, there was no association between T. vitulorum infection and fecal consistency. Further studies are needed to determine the contribution of T. vitulorum towards the overall clinical impact of disorders in calves of less than 3 months.
In conclusion, T. vitulorum is important in Cambodia, especially in buffalo cattle and animals between 4-8 weeks of age. Farmers should be aware of the potential impact of this parasite, and treat their animals appropriately. Anthelmintic treatment with either pyrantel or benzimidazoles at the age of 2-3 weeks has proved to be very effective in eliminating T. vitulorum both in cattle and buffalo calves in Cambodia (data not shown) and should be recommended to livestock owners in order to prevent potential pathologies caused by this parasite.

We have no conflict of interest related to this work.

This study was carried out within the framework of the Parasitology Project in Cambodia funded by the Flemish Interuniversity Council (VLIR) and implemented at the Royal University of Agriculture (RUA) and the National Veterinary Research Institute (NaVRI) in Phnom Penh. The authors would like to express their gratitude to the cattle owners for their kind cooperation, as well as to the technicians and students from RUA and NaVRI for their assistance during the field sampling and the laboratory analysis.
Table 1.
Descriptive statistics of Toxocara vitulorum infection in Cambodian calves per province, host species, age group, faecal consistency, and co-infection category
Table 1.
Variable Sample size (%) Positive (%; 95% exact CI) Mean EPG (SD)
Province
 Pursat 239 (46.2) 34 (14.2; 10.1-19.3) 3,638 (17,942)
 Kampong Chnnang 155 (30.0) 14 (9.0; 5.0-14.7) 1,154 (7,148)
 Kampong Cham 123 (23.8) 16 (13.0; 7.6-20.3) 3,237 (20,815)
Species
 Buffalo 169 (27.8) 34 (20.1; 14.4-27.0) 6,053 (22,038)
 Cattle 348 (72.1) 30 (8.6; 5.9-12.1) 1,218 (12,440)
Age (days)
 ≤ 28 59 (11.4) 7 (11.9; 5.0-22.9) 1,943 (10,778)
 28-56 143 (27.7) 32 (22.4; 15.8-30.1) 7,756 (28,499)
 > 56 315 (60.9) 25 (8.0; 5.2-11.5) 708 (5,906)
Faecal consistency
 Normal 374 (72.5) 44 (11.8; 8.7-15.5) 2,757 (14,883)
 Soft 117 (22.7) 18 (15.4; 9.4-23.2) 2,953 (21,306)
 Watery 25 (4.8) 2 (8.0; 1.0-26.0) 2,804 (10,530)
Strongyle infection
 No 182 (35.2) 39 (21.4; 15.7-28.1) 5,846 (25,234)
 Yes 335 (64.8) 25 (7.5; 4.9-10.8) 1,142 (7,755)
Eimeria infection
 No 272 (52.6) 35 (12.9; 9.1-17.4) 3,453 (19,398)
 Yes 245 (47.4) 29 (11.8; 8.1-16.6) 2,071 (12,102)

CI, confidence interval; SD, standard deviation.

Table 2.
Estimates of generalized linear mixed model
Table 2.
Variable Estimate (SE) OR (95% Wald CI) P-value
Species
 Buffalo reference - -
 Cattle -1.295 (0.3127) 0.273 (0.148-0.504) < 0.001
Age (days)
 ≤ 28 -0.874 (0.4919) 0.417 (0.159-1.094) 0.076
 28-56 reference - -
 > 56 -1.150 (0.3203) 0.317 (0.169-0.593) < 0.001
Strongyle infection
 No reference - -
 Yes -1.225 (0.3059) 0.294 (0.161-0.535) < 0.001

SE, standard error; OR, odds ratio; CI, confidence interval.

  • 1. Rast L, Lee S, Nampanya S, Toribio JA, Khounsy S, Windsor PA. Prevalence and clinical impact of Toxocara vitulorum in cattle and buffalo calves in northern Lao PDR. Trop Anim Health Prod 2013;45:539-546.
  • 2. Roberts JA, Fernando ST, Sivanathan S. Toxocara vitulorum in the milk of buffalo (Bubalus bubalis) cows. Res Vet Sci 1990;49:289-291.
  • 3. Roberts JA. The life cycle of Toxocara vitulorum in Asian buffalo (Bubalus bubalis). Int J Parasitol 1990;20:833-840.
  • 4. Young JR, O'Reilly RA, Ashley K, Suon S, Leoung IV, Windsor PA, Bush R.D. Impacts on rural livelihoods in Cambodia following adoption of best practice health and husbandry interventions by smallholder cattle farmers. Transbound Emerg Dis 2014;61(suppl 1):11-24.
  • 5. Nampanya S, Suon S, Rast L, Windsor PA. Improvement in smallholder farmer knowledge of cattle production, health and biosecurity in Southern Cambodia between 2008 and 2010. Transbound Emerg Dis 2012;59:117-127.
  • 6. Dorny P, Stoliaroff V, Charlier J, Meas S, Sorn S, Chea B, Holl D, Van Aken D, Vercruysse J. Infections with gastrointestinal nematodes, Fasciola and Paramphistomum in cattle in Cambodia and their association with morbidity parameters. Vet Parasitol 2011;175:293-299.
  • 7. Thienpont D, Rochette F, Vanparijs OFJ. Diagnosing helminthiasis by coprological examination. Beerse, Belgium. Janssen Research Foundation; 1986. p 205.
  • 8. R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria; 2014 205 http://www.R-project.org/
  • 9. Bates D, Maechler M, Bolker B, Walker S. lme4: linear mixed-effects models using Eigen and S4. R package version 1.0-6; 2014 http://CRAN.R-project.org/package=lme4
  • 10. Srikitjakarn L, Löhr KF, Leidl K, Hörchner F. Metaphylactic deworming program for buffalo calves (Bubalis bubalis) in North-East Thailand. Trop Med Parasitol 1987;38:191-193.
  • 11. Holland WG, Luong TT, Nguyen LA, Do TT, Vercruysse J. The epidemiology of nematode and fluke infections in cattle in the Red River Delta in Vietnam. Vet Parasitol 2000;93:141-147.
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Prevalence and Associated Risk Factors of Toxocara vitulorum Infections in Buffalo and Cattle Calves in Three Provinces of Central Cambodia
Korean J Parasitol. 2015;53(2):197-200.   Published online April 22, 2015
DOI: https://doi.org/10.3347/kjp.2015.53.2.197
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Prevalence and Associated Risk Factors of Toxocara vitulorum Infections in Buffalo and Cattle Calves in Three Provinces of Central Cambodia
Korean J Parasitol. 2015;53(2):197-200.   Published online April 22, 2015
DOI: https://doi.org/10.3347/kjp.2015.53.2.197
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Prevalence and Associated Risk Factors of Toxocara vitulorum Infections in Buffalo and Cattle Calves in Three Provinces of Central Cambodia
Prevalence and Associated Risk Factors of Toxocara vitulorum Infections in Buffalo and Cattle Calves in Three Provinces of Central Cambodia
Variable Sample size (%) Positive (%; 95% exact CI) Mean EPG (SD)
Province
 Pursat 239 (46.2) 34 (14.2; 10.1-19.3) 3,638 (17,942)
 Kampong Chnnang 155 (30.0) 14 (9.0; 5.0-14.7) 1,154 (7,148)
 Kampong Cham 123 (23.8) 16 (13.0; 7.6-20.3) 3,237 (20,815)
Species
 Buffalo 169 (27.8) 34 (20.1; 14.4-27.0) 6,053 (22,038)
 Cattle 348 (72.1) 30 (8.6; 5.9-12.1) 1,218 (12,440)
Age (days)
 ≤ 28 59 (11.4) 7 (11.9; 5.0-22.9) 1,943 (10,778)
 28-56 143 (27.7) 32 (22.4; 15.8-30.1) 7,756 (28,499)
 > 56 315 (60.9) 25 (8.0; 5.2-11.5) 708 (5,906)
Faecal consistency
 Normal 374 (72.5) 44 (11.8; 8.7-15.5) 2,757 (14,883)
 Soft 117 (22.7) 18 (15.4; 9.4-23.2) 2,953 (21,306)
 Watery 25 (4.8) 2 (8.0; 1.0-26.0) 2,804 (10,530)
Strongyle infection
 No 182 (35.2) 39 (21.4; 15.7-28.1) 5,846 (25,234)
 Yes 335 (64.8) 25 (7.5; 4.9-10.8) 1,142 (7,755)
Eimeria infection
 No 272 (52.6) 35 (12.9; 9.1-17.4) 3,453 (19,398)
 Yes 245 (47.4) 29 (11.8; 8.1-16.6) 2,071 (12,102)
Variable Estimate (SE) OR (95% Wald CI) P-value
Species
 Buffalo reference - -
 Cattle -1.295 (0.3127) 0.273 (0.148-0.504) < 0.001
Age (days)
 ≤ 28 -0.874 (0.4919) 0.417 (0.159-1.094) 0.076
 28-56 reference - -
 > 56 -1.150 (0.3203) 0.317 (0.169-0.593) < 0.001
Strongyle infection
 No reference - -
 Yes -1.225 (0.3059) 0.294 (0.161-0.535) < 0.001
Table 1. Descriptive statistics of Toxocara vitulorum infection in Cambodian calves per province, host species, age group, faecal consistency, and co-infection category

CI, confidence interval; SD, standard deviation.

Table 2. Estimates of generalized linear mixed model

SE, standard error; OR, odds ratio; CI, confidence interval.

Table 1.

Table 2.

PHD : Parasites, Hosts and Diseases

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