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Brief Communication

Intestinal Parasite Infections in Pigs and Beef Cattle in Rural Areas of Chungcheongnam-do, Korea

Hassan Ahmed Hassan Ahmed Ismail1, Hyung-Kyu Jeon2, Yong-Man Yu3, Changhee Do4, Young-Ha Lee1
The Korean Journal of Parasitology 2010;48(4):347-349.
Published online: December 16, 2010

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Corresponding author (yhalee@cnu.ac.kr)
• Received: June 16, 2010   • Revised: November 22, 2010   • Accepted: November 23, 2010

© 2010, Korean Society for Parasitology

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  • The present study was performed to investigate the infection status of intestinal parasites in pigs and beef cattle in rural areas of Chungcheongnam-do, Korea. From November 2009 to April 2010, a total of 241 fecal samples of pigs and beef cattle (136 and 105, respectively) were examined by direct smear and centrifugal sedimentation methods. The overall positive rates of intestinal parasites among pigs and beef cattle were 73.5% and 4.8%, respectively, and the double-infection rate was 10.3% in pigs. Of 136 specimens from pigs, Balantidium coli, Ascaris suum, and Entamoeba spp. infections were found in 88 (64.7%), 24 (17.6%), and 5 cases (3.7%), respectively. Of 105 beef cattle, Entamoeba spp. infections were detected in 5 cases (4.8%). From these results, it is shown that pigs raised on rural farms in Chungcheongnam-do had a high B. coli infection rate and a moderate A. suum infection rate. These results demonstrate that environmentally resistant cysts or eggs could be widespread on the farms examined, and thus an effective hygienic management system is needed to prevent them from serving as the source of infection for human beings.
  • Key words: prevalence, intestinal parasites, beef cattle, pigs
Zoonoses can be transmitted directly by contact with an animal, via contaminated environment, or food, and they can be transmitted indirectly via vectors. The diseases they cause in humans range from mild and self-limiting to fatal. Livestock, such as pigs and cattle, are known to be important sources of zoonoses. Parasitic infections of pigs and cattle, such as Toxoplasma gondii, Cryptosporidium spp., Ascaris suum, and Balantidium coli, are increasingly attracting attention due to their pathogenic and zoonotic impacts [1]. The prevalence of intestinal parasites in Korea in the 1980s was 55.4% for Entamoeba spp., 66.6% for B. coli, 25.6% for A. suum, 55.4% for Eimeria and Isospora spp., and 1.0% for Giardia lamblia [2]. Furthermore, the infection rates of nematodes, coccidia, and trematodes in cattle were 49.0%, 10.9%, and 14.6%, respectively [3].
However, environments for keeping pigs and cattle have undergone major changes in the past few decades. For example, pigs are now kept confined in pigpens with concrete as opposed to earth floors. Thus, pigs now have a lower risk of direct contact with arthropods harboring parasites or soil contaminated with environmentally resistant forms of parasites. In addition, cattle are raised on hay with concrete floors. Furthermore, drug and vaccine treatments for animals, breeding programs intended to introduce resistance to pathogenic microorganisms, and cleaning of sheds with disinfectants are now commonplace. Although the number of pig and cattle farmers in Korea is now decreasing, the number of animals per farmer is increasing. The high number of animals per farm is an important factor in the outbreak and persistence of infectious diseases. Insufficient information exists regarding parasitic infections among pigs and cattle in Korea, despite the implementation of many environmental changes in raising the animals. Thus, we tried to estimate the prevalence of intestinal parasites in pigs and beef cattle raised on farms in Chungcheongnam-do using a coproscopic approach.
We surveyed the farms of 6 villages of Chungcheongnam-do, Korea between November 2009 and April 2010. Of 241 fecal samples collected, 136 were from pigs and 105 were from beef cattle. The samples were stored at 4℃ and examined within 5 days of sample collection. Fecal samples were examined for the presence of helminth eggs and protozoan cysts, oocysts, and/or trophozoites using direct smear and centrifugal sedimentation methods. The centrifugal sedimentation method was performed according to Zajac and Conboy [1]. Briefly, 1 g of fecal material was diluted in 9 ml of tap water in a 15-ml centrifugal tube and centrifuged at 800 g for 5 min. After centrifugation, 10 ml of 10% formalin solution was added to the sediment and mixed with 4 ml of ethyl acetate followed by centrifugation at 800 g for 5 min. Sediment on the bottom was recovered and placed onto a glass slide. The entire smear was examined by light microscopy at magnifications of 200 × or 400 ×. An animal was determined to be infected with an intestinal parasite if at least one egg, oocyst, cyst, or trophozoite was found in the fecal smear.
The results of the pig fecal examinations are shown in Table 1. Of 136 pigs, 100 (73.5%) had parasite eggs and/or cysts in their feces. B. coli cysts were found in 88 (64.7%), and A. suum eggs and Entamoeba spp. cysts were detected in 24 (17.6%) and 5 animals (3.7%), respectively. Of the 100 infected pigs, more than 2 species of parasites were observed in 14 (10.3%) (A. suum and B. coli: 12 cases; A. suum and Entamoeba spp: 3 cases; B. coli and Entamoeba spp: 5 cases; A. suum, B. coli, and Entamoeba spp: 3 cases). Parasites were detected in the pigs from all farms examined. The highest positive rate was seen in the pigs from Tancheon-myeon, Gongju-si (80.6%), followed by Gwangcheon-eup, Hongseong-gun (73.5%). On the cattle coprological examinations, 5 of 105 beef cattle (4.8%) examined were infected with Entamoeba spp. (Table 2).
B. coli is the largest protozoan parasite and the only ciliate parasitic to humans. Ingestion of B. coli cysts from pig feces through water and food intake results in transmission [4,5]. Its prevalence among pigs has been reported as 47.2% in China [6] and 1.6% in Turkey [7], but the highest prevalence is found in tropical and subtropical regions of the world [4,5]. In a study from Denmark, the prevalence of B. coli was found to increase from 57% to 100% with increasing age [8]. The prevalence of B. coli was 64.7% in the present study, which is higher than that in other studies [6,7]. It is thought that contaminated feed buckets or pens as well as a lack of careful treatment of feces from infected animals are the reasons for the high prevalence of these parasites. Further study is needed to evaluate the key factors involved in the high prevalence of B. coli in pigs. Estimates of the worldwide prevalence of B. coli infection are usually less than 1% [4,5]. However, the infection rates among swine herders and slaughterhouse workers are as high as 28% in Papua New Guinea [9]. In recent years, there have been some reports of B. coli infection in immunocompromised patients, including HIV/AIDS patients, patients with malignancies, and patients who have undergone organ transplantations [10].
A. suum is a causative agent of visceral larva migrans in humans. Humans with liver and lung lesions as well as cases and epidemics of eosinophilic pneumonia have been reported, and A. suum-specific antibodies were present in all cases [11-13]. In Japan and Turkey, 14.7% and 3.7% of pigs, respectively, were estimated to be infected with A. suum [7,14]. The prevalence of A. suum infection in the present study was 17.6%, which was lower than that in a previous report in Korea by Jang [2]. However, Ascaris in pigs is an important zoonotic parasite, as genetic analysis has indicated that pig Ascaris may infect humans [11-13]. Thus, we need a detailed epidemiological survey to clarify the relationship between environmental factors and the prevalence of parasites on farms.
Cattle are known to be important sources of zoonotic parasites, such as C. parvum. Matsubayashi et al. [14] recently reported that the prevalence of parasite infections in cattle were 76.5% for Eimeria spp., 7.0% for Capillaria bovis, and 3.8% for Trichuris spp. The prevalence of cryptosporidiosis in Korea was 8.9-98.2% in cattle and 9.9-47.7% in pigs [15]. In this study, we found Amoeba spp. in 5 beef cattle in Chungcheongnam-do, which was a lower parasite infection rate than that previously reported in Korea [3]. The prevalence of infectious diseases in animals is related to several factors, including types of food and water, food supply systems, hygienic conditions, location of pens, administration of drugs or vaccinations, and so on. We examined hygienically well-managed beef cattle on farms. However, cysts of Cryptosporidium spp. were not detected in either pigs or beef cattle because acid-fast staining was not performed on the feces.
The results of the present study demonstrate that pigs raised on farms in Chungcheongnam-do had a high B. coli infection rate and a moderate A. suum infection rate, whereas the prevalence of intestinal parasite infections in beef cattle was low. These results demonstrate that environmentally resistant cysts or eggs could be widespread on the farms examined, and pig feces may serve as a source for a group of parasites capable of infecting human beings. Thus, an effective hygienic management system must be based on appropriate knowledge of the epidemiological conditions of the prevailing parasitic infections. This survey is meaningful as a farm-based study to reveal the prevalence of intestinal parasite infection in the rural areas of Korea. However, the study has some limitations in its determination of the exact prevalence of intestinal parasites in pigs and beef cattle, such as excluding the acid-fast staining of feces. Further surveys from various areas will be necessary to clarify the exact prevalence.
This work was carried out with the support of "Cooperative Research Program for Agriculture Science & Technology Development (Project No. PJ006600)" Rural Development Administration, Republic of Korea.
  • 1. Zajac AM, Conboy GA. Veterinary Clinical Parasitology. 2006. 7th ed. Iowa, USA. Blackwell Publishing Co; p. 3-147.
  • 2. Jang DH. Survey for internal parasites of swine in Korea. Korean J Vet Res 1975;15:309-314.
  • 3. Lee CS, Lee JH, Byun MD, Park CK, Lee HS, Moon MH. Incidence of parasitic infections and diseases in rearing and fattening cattle raising in Gyeongbuk District. Korean J Vet Res 1980;20:179-197.
  • 4. Schuster FL, Ramirez-Avila L. Current world status of Balantidium coli. Clin Microbiol Rev 2008;21:626-638.
  • 5. Solaymani-Mohammadi S, Petri WA Jr. Zoonotic implications of the swine-transmitted protozoal infections. Vet Parasitol 2006;140:189-203.
  • 6. Weng YB, Hu YJ, Li Y, Li BS, Lin RQ, Xie DH, Gasser RB, Zhu XQ. Survey of intestinal parasites in pigs from intensive farms in Guangdong Province, People's Republic of China. Vet Parasitol 2005;127:333-336.
  • 7. Uysal HK, Boral O, Metiner K, Ilgaz A. Investigation of intestinal parasites in pig feces that are also human pathogens. Turkiye Parazitol Derg 2009;33:218-221.
  • 8. Hindsbo O, Nielsen CV, Andressen J, Willingham AL, Bendixen M, Nielsen M, Nielsen NO. Age-dependent occurrence of the intestinal ciliate Balantidium coli in pigs at a Danish research farm. Acta Vet Scand 2000;41:79-83.
  • 9. Barnish G, Ashford RW. Occasional parasitic infections of man in Papua New Guinea and Irian Jaya (New Guinea). Ann Trop Med Parasitol 1989;83:121-135.
  • 10. Cermeno JR, Hernandez de Cuesta I, Uzcategui O, Paez J, Rivera M, Baliachi N. Balantidium coli in a HIV-infected patient with chronic diarrhea. AIDS 2003;17:941-942.
  • 11. Inatomi Y, Murakami T, Tokunaga M, Ishiwata K, Nawa Y, Uchino M. Encephalopathy caused by visceral larva migrans due to Ascaris suum. J Neurol Sci 1999;164:195-199.
  • 12. Kakihara D, Yoshimitsu K, Ishigami K, Irie H, Aibe H, Tajima T, Shinozaki K, Nishie A, Nakayama T, Hayashida K, Nakamuta M, Nawata H, Honda H. Liver lesions of visceral larva migrans due to Ascaris suum infection: CT findings. Abdom Imaging 2004;29:598-602.
  • 13. Maruyama H, Nawa Y, Noda S, Mimori T, Choi WY. An outbreak of visceral larva migrans due to Ascaris suum in Kyushu, Japan. Lancet 1996;347:1766-1767.
  • 14. Matsubayashi M, Kita T, Narushima T, Kimata I, Tani H, Sasai K, Baba E. Coprological survey of parasitic infections in pigs and cattle in slaughterhouse in Osaka, Japan. J Vet Med Sci 2009;71:1079-1083.
  • 15. Yu JR, Lee JK, Seo M, Kim SI, Sohn WM, Huh S, Choi HY, Kim TS. Prevalence of cryptosporidiosis among the villagers and domestic animals in several rural areas of Korea. Korean J Parasitol 2004;42:1-6.
Table 1.
Prevalence of intestinal parasites infection in pigs examined by the direct smear method and the centrifugal sedimentation method in Chungcheongnam-do, Korea
Table 1.
Localities No. exam. No. of positive (%)
As Bc Ep As+Bc As+Ep Bc+Ep As+Bc+Ep Subtotal
Gyeryong-myeon, Gongju-si 66 24 (36.4) 34 (51.5) 3 (4.5) 12 (18.2) 3 (4.5) 3 (4.5) 3 (4.5) 46 (69.7)
Tancheon-myeon, Gongju-si 36 0 (0.0) 29 (80.6) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 29 (80.6)
Gwangcheon-eup, Hongseong-gun 34 0 (0.0) 25 (73.5) 2 (5.9) 0 (0.0) 0 (0.0) 2 (5.9) 0 (0.0) 25 (73.5)
Total 136 24 (17.6) 88 (64.7) 5 (3.7) 12 (8.8) 3 (4.5) 5 (3.7) 3 (2.2) 100 (73.5)

As, Ascaris suum; Bc, Balantidium coli; Ep, Entamoeba spp.

Table 2.
Prevalence of intestinal parasites infection in beef cattle examined by the direct smear method and the centrifugal sedimentation method in Chungcheongnam-do, Korea
Table 2.
Localities No. of exam. No. of positive (%)
Entamoeba spp. Subtotal
Jeongan-myeon, Gongju-si 35 0 (0.0) 0 (0.0)
Uidang-myeon, Gongju-si 30 2 (6.6) 2 (6.6)
Bujeok-myeon, Nonsan-si 35 3 (8.6) 3 (8.6)
Total 105 5 (4.8) 5 (4.8)

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Intestinal Parasite Infections in Pigs and Beef Cattle in Rural Areas of Chungcheongnam-do, Korea
Korean J Parasitol. 2010;48(4):347-349.   Published online December 16, 2010
DOI: https://doi.org/10.3347/kjp.2010.48.4.347
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Intestinal Parasite Infections in Pigs and Beef Cattle in Rural Areas of Chungcheongnam-do, Korea
Korean J Parasitol. 2010;48(4):347-349.   Published online December 16, 2010
DOI: https://doi.org/10.3347/kjp.2010.48.4.347
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Intestinal Parasite Infections in Pigs and Beef Cattle in Rural Areas of Chungcheongnam-do, Korea
Localities No. exam. No. of positive (%)
As Bc Ep As+Bc As+Ep Bc+Ep As+Bc+Ep Subtotal Gyeryong-myeon, Gongju-si 66 24 (36.4) 34 (51.5) 3 (4.5) 12 (18.2) 3 (4.5) 3 (4.5) 3 (4.5) 46 (69.7) Tancheon-myeon, Gongju-si 36 0 (0.0) 29 (80.6) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 0 (0.0) 29 (80.6) Gwangcheon-eup, Hongseong-gun 34 0 (0.0) 25 (73.5) 2 (5.9) 0 (0.0) 0 (0.0) 2 (5.9) 0 (0.0) 25 (73.5) Total 136 24 (17.6) 88 (64.7) 5 (3.7) 12 (8.8) 3 (4.5) 5 (3.7) 3 (2.2) 100 (73.5) Localities No. of exam. No. of positive (%)
Entamoeba spp. Subtotal Jeongan-myeon, Gongju-si 35 0 (0.0) 0 (0.0) Uidang-myeon, Gongju-si 30 2 (6.6) 2 (6.6) Bujeok-myeon, Nonsan-si 35 3 (8.6) 3 (8.6) Total 105 5 (4.8) 5 (4.8)
Table 1. Prevalence of intestinal parasites infection in pigs examined by the direct smear method and the centrifugal sedimentation method in Chungcheongnam-do, Korea

As, Ascaris suum; Bc, Balantidium coli; Ep, Entamoeba spp.

Table 2. Prevalence of intestinal parasites infection in beef cattle examined by the direct smear method and the centrifugal sedimentation method in Chungcheongnam-do, Korea

Table 1.

Table 2.

PHD : Parasites, Hosts and Diseases

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