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Echinostoma revolutum infection in children, Pursat Province, Cambodia.

Echinostomes (family Echinostomatidae) are intestinal trematodes of birds and mammals, including humans. Echinostomiasis can result in severe epigastric or abdominal pain accompanied by diarrhea, easy fatigue, and malnutrition (1). Heavy worm loads may lead to death due to intestinal perforation or marked malnutrition and anemia, as has been reported for infection caused by an echinostome species, Artyfechinostomum malayanum (under the name Artyfechinostomum mehrai), in India (1).

A total of 20 species of echinostomes that belong to 8 genera (Echinostoma, Echinochasmus, Acanthoparyphium, Artyfechinostomum, Episthmium, Himasthla, Hypoderaeum, and Isthmiophora) infect humans worldwide (1). Echinostoma revolutum, the most widely distributed species, is found from Asia and Oceania to Europe and the Americas (1). The first reported human infection was in Taiwan in 1929 (2). The prevalence of E. revolutum flukes in Taiwan during 1929-1979 varied from 0.11% to 0.65% (3). Small E. revolutum-endemic foci or a few cases of human infection were discovered in the People's Republic of China, Indonesia, and Thailand until 1994 (4,5). However, no information is available about human E. revolutum infection after 1994, even in areas where the parasite was previously endemic.

In Cambodia, humans are commonly infected with intestinal nematodes and protozoa, including hookworms, Strongyloides stercoralis, Ascaris lumbricoides, Trichuris trichiura, and Giardia lamblia (6,7). However, with the exception of the blood fluke Schistosoma mekongi, infection with trematodes or cestodes has seldom been reported (8). Echinostomatid eggs have been detected in schoolchildren in 2 provinces, Battambang and Kampongcham (9,10), but adult worms were not collected for identification. The Korea Association of Health Promotion, South Korea, and The National Institute of Malaria, Entomology, and Parasitology, Ministry of Health, Cambodia, have been conducting an international collaboration to control intestinal helminthiases in schoolchildren in Cambodia (2006-2011). In June 2007, we conducted a fecal survey in 4 primary schools in Pursat Province, Cambodia, and found that an average of 11.9% of schoolchildren had positive test results for echinostome eggs. Adult worms recovered after the children received treatment with praziquantel and underwent purgation with magnesium salts were identified as E. revolutum. We report echinostomiasis as an endemic trematode infection among schoolchildren in Pursat.

The Study

The surveyed areas were lakeside (the Tonle Sap Lake) villages in Pursat Province (Figure 1) where [approximately equal to]12,000 persons, including 3,500 schoolchildren, live. For this study, 471 children (237 boys), 10-14 years of age, from 4 primary schools were selected. One fecal sample from each child was collected in June 2007. Samples were transported to the Malaria Station in Pursat within 2-3 days of collection and stored at 4[degrees]C until examination. The Kato-Katz thick smear technique was used to detect helminth eggs. Examination of feces and anthelmintic treatment were officially approved by the Ministry of Health, Cambodia, under the agreement of the Korea-Cambodia International Collaboration on Intestinal Parasite Control for Schoolchildren in Cambodia.

[FIGURE 1 OMITTED]

Four children who had positive test results for echinostomatid eggs and who had occasional, vague abdominal pain and discomfort were selected for anthelmintic treatment and adult worm recovery at the Malaria Station. After we obtained consent from their parents and the school guardian, the children's infections were treated with a single oral dose of 10 mg/kg praziquantel (Shinpoong Pharmceutical Co., Seoul, South Korea), and purged with 20 g magnesium sulfate. Whole diarrheic feces were collected 3-4 times and pooled individually. The diarrheic feces were processed as previously described (11). Worms were collected by using a wooden applicator and washed several times in water. They were fixed with 10% formalin under coverslip pressure, stained with acetocarmine, and identified by morphologic features.

A total of 17.4% of samples were positive for helminth eggs. Echinostomatid eggs were found most frequently, followed by hookworm and Trichuris trichiura eggs (Table 1). The percentages of echinostome eggs were significantly higher in school A than in schools B, C, and D (Table 1). However, prevalence did not differ significantly (p<0.01) between boys and girls (data not shown). A total of 20 echinostome adults (12, 3, 3, and 2 worms) were recovered from 4 children who showed 48-120 eggs per gram of feces (Table 2). The worms were leaflike, elongated (Figure 2), and an average of 8.8 mm long (8.0-9.5 mm) and 1.7 mm wide (1.2-2.1 mm) (n = 10). When first passed in the feces, they were pinkish red and coiled in a "c" or "e" shape. The eggs in uteri were an average of 105 Lim long (97-117 [micro]m) and 63 [micro]m wide (61-65 [micro]m) (n = 10). On the basis of these characteristics, the worms were identified as E. revolutum (Froelich, 1802) Looss, 1899.

The major sources of E. revolutum infection in humans are freshwater clams (Corbicula producta) in Taiwan and snails (Physa occidentalis or Lymnaea sp.) in Thailand (1,5). According to school personnel, the children were fond of eating undercooked snails or clams of unidentified species sold on the road to their homes after school. They stated that the mollusks are caught near Tonle Sap Lake. Reasons for the higher prevalence in school A than schools B, C and D are unclear.

Conclusions

Of the schoolchildren living near Tonle Sap Lake, Pursat Province, Cambodia, who participated in this study, 7.5%-22.4%, depending on school, were infected with E. revolutum. E. revolutum trematodes are endemic parasites in this area of Cambodia and a likely source of infection is freshwater snails or clams from the lake. The public health significance of echinostomiasis and educational and prevention efforts should be highlighted.

Echinostomiasis is not only an endemic infectious disease in Asian countries, including Cambodia, but also can be imported by overseas travelers from the United States or Europe. An outbreak of echinostomiasis was reported among US travelers returning from Kenya and Tanzania, although the source of infection was uncertain (12). This diagnosis should also be considered in patients with abdominal pain and diarrhea who have traveled to Southeast Asia and eaten snails or clams.

Despite the dangerous nature of echinostomes, the study of echinostomiasis has been neglected for many decades (13,14), possibly because physicians and laboratory personnel lack knowledge about this trematode parasite. In addition, no easy diagnostic technique is available to detect echinostome eggs, except for routine fecal examination. However, some microscopists seem to overlook or misinterpret the presence of echinostome eggs, particularly in Kato-Katz fecal smears. Even if echinostome eggs are detected, the specific diagnosis is not possible unless the adult worm is collected and identified. Thus, both the training of microscopists and emphasis on the clinical significance of echinostomiasis are urgently needed.

[FIGURE 2 OMITTED]

DOI: 10.3201/eid1701.100920

Acknowledgments

We thank the staffs of the National Institute of Malaria, Entomology, and Parasitology, Ministry of Health, Cambodia, for preparing the Kato-Katz smears for the schoolchildren. We also thank Hyun-Mi Kim, Yu-Jung Kim, Jae-Young Park, Geun-Hoon Lee, Hoo-Gn Jeong, and Chong-Kyun Shin, Korea Association of Health Promotion, for their help in reading Kato-Katz fecal smears.

References

(1.) Chai JY. Echinostomes in humans. In: Fried B, Toledo R, editors. The biology of echinostomes. New York: Springer; 2009. p. 147-83.

(2.) Anazawa K. On a human case of Echinostoma revolutum and its infection route [in Japanese]. Taiwan Igakkai Zasshi. 1929;288:221-41.

(3.) Lu SC. Echinostomiasis in Taiwan. Int J Zoonoses. 1982;9:33-8.

(4.) Radomyos P, Radomyos B, Tungtrongchitr A. Multi-infection with helminthes in adults from northeast Thailand as determined by posttreatment fecal examination of adult worms. Trop Med Parasitol. 1994;45:133-5.

(5.) Yu SH, Mott KE. Epidemiology and morbidity of food-borne intestinal trematode infections. Trop Dis Bull. 1994;91:R125-52.

(6.) Sinuon M, Anantaphruti MT, Socheat D. Intestinal helminthic infections in schoolchildren in Cambodia. Southeast Asian J Trop Med Public Health. 2003;34:254-8.

(7.) Copelovitch L, Ol OS, Taraquinio S, Chanpheaktra N. Childhood nephrotic syndrome in Cambodia: an association with gastrointestinal parasites. J Pediatr. 2010;156:76-81. DOI: 10.1016/j.jpeds.2009.06.049

(8.) Ohmae H, Sinuon M, Kirinoki M, Matsumoto J, Chigusa Y, Socheat D, et al. Schistosomiasis mekongi: from discovery to control. Parasitol Int. 2004;53:135-42. DOI: 10.1016/j.parint.2004.01.004

(9.) Lee KJ, Bae YT, Kim DH, Deung YK, Ryang YS, Kim HJ, et al. Status of intestinal parasites infection among primary school children in Kampongcham, Cambodia. Korean J Parasitol. 2002;40:153-5. DOI: 10.3347/kjp.2002.40.3.153

(10.) Park SK, Kim DH, Deung YK, Kim HJ, Yang EJ, Lim SJ, et al. Status of intestinal parasite infections among children in Bat Dambang, Cambodia. Korean J Parasitol. 2004;42:201-3. DOI: 10.3347/ kjp.2004.42.4.201

(11.) Chai JY, Park JH, Han ET, Guk SM, Shin EH, Lin A, et al. Mixed infections with Opisthorchis viverrini and intestinal flukes in residents of Vientiane Municipality and Saravane Province in Laos. J Helminthol. 2005;79:283-9. DOI: 10.1079/JOH2005302

(12.) Poland GA, Navin TR, Sarosi GA. Outbreak of parasitic gastroenteritis among travelers returning from Africa. Arch Intern Med. 1985;145:2220-1. DOI: 10.1001/archinte.145.12.2220

(13.) Graczyk TK, Fried B. Echinostomiasis: a common but forgotten food-borne disease. Am J Trop Med Hyg. 1998;58:501-4.

(14.) Carney WP, Sudomo M. Purnomo. Echinostomiasis: a disease that disappeared. Trop Geogr Med. 1980;32:101-5.

Author affiliations: Gyeongsang National University School of Medicine, Jinju, South Korea (W.-M. Sohn); Seoul National University College of Medicine, Seoul, South Korea (J.-Y. Chai, S.-H. Lee); Korea Association of Health Promotion, Seoul (J.-Y. Chai, C.-H. Yoon); Yonsei University College of Medicine, Seoul (T.-S. Yong); Chungbuk National University College of Medicine, Cheongju, South Korea (K.S. Eom); and Center for National Malaria Control, Phnom Penh, Cambodia (M. Sinuon, D. Socheat)

Address for correspondence: Jong-Yil Chai, Department of Parasitology and Tropical Medicine, Seoul National University College of Medicine, Seoul 110-799, South Korea; email: cjy@snu.ac.kr

Dr Sohn is a professor in the Department of Parasitology and Institute of Health Sciences, Gyeongsang National University School of Medicine, Jinju, South Korea. His major research area is foodborne zoonotic parasites, including echinostomes, heterophyids, and gnathostomes.
Table 1. Prevalence of intestinal helminths among schoolchildren,
Pursat Province, Cambodia, June 2007 *

                         No. (%) positive results for helminth eggs;
                                95% CI egg positive rate
         No. children
School     examined     Echinostomes ([dagger])        Hookworms

A            116         26 (22.4); 14.8-30.0#     4 (3.4); 0.1-6.7
B            117         12 (10.3); 4.8-15.8#     12 (10.3); 4.8-15.8
C            118          9 (7.6); 2.8-12.4#               0
D            120          9 (7.5); 2.8-12.2#            7 (5.8)

Total        471          56 (11.9); 9.0-14.8      23 (4.9); 3.0-6.8

             No. (%) positive results for helminth eggs;
                    95% CI egg positive rate

School   Trichuris trichuira eggs   Others ([double dagger])

A            1 (0.9); 0.0-2.6           1 (0.9); 0.0-2.6
B                   0                   3 (2.6); 0.0-5.5
C                   0                   1 (0.8); 0.0-2.4
D                   0                          0

Total        1 (0.2); 0.0-0.6           5 (1.1); 0.2-2.0

         No. (%) positive results
            for helminth eggs;
         95% CI egg positive rate

School      Total ([section])

A          31 (26.7); 18.6-34.8
B          26 (22.2); 14.7-29.7
C           10 (8.5); 3.5-13.5
D          15 (12.5); 6.6-17.2

Total      82 (17.4); 14.0-20.8

* Determined by examination of feces using the Kato-Katz
technique. Boldface indicates significant differences between
schools A and B (p = 0.01); A and C (p = 0.004), and A and D
(p = 0.004), as analyzed by z test.CI, confidence interval.

([dagger]) Most of these are presumed to be eggs of Echinostoma
revolutum worms.

([double dagger]) Includes eggs of Enterobius vermicularis
(schools A and B) and Hymenolepis nana (school C) worms.

([section]) Total no. of schoolchildren positive for [greater
than or equal to] 1 helminth species.

Note: Boldface indicates significant differences between schools
A and B (p = 0.01) are indicated with #.

Table 2. Recovery of Echinostoma revolutum worms from
schoolchildren, Pursat Province, Cambodia, June 2007 *

                                          No. E. revolutum
                      No. echinostome    specimens recovered
Child no.   Age, y   eggs/g ([dagger])    ([double dagger])

1             13             48                  12
2             13            120                   3
3             10            120                   3
4             13             96                   2

* All children were female. Fecal samples were collected
individually 2-3 hours after administration of MgS[O.sub.4].

([dagger]) Eggs/g of feces; amount in a typical sample was
assumed to be 41.7 mg.

([double dagger]) All recovered worms were adult worms that
contained eggs.
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Article Details
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Author:Sohn, Woon-Mok; Chai, Jong-Yil; Yong, Tai-Soon; Eom, Keeseon S.; Yoon, Cheong-Ha; Sinuon, Muth; Soch
Publication:Emerging Infectious Diseases
Article Type:Report
Geographic Code:9CAMB
Date:Jan 1, 2011
Words:2088
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