A cross-sectional study of intestinal parasitic infections in a rural district of west China

Health and Anti-epidemic station (Centre for Disease Control and Prevention), Beibei, Chongqing, China Correspondence and reprints: Mr Ning Tang, present address in Australia:1/13 Gwynne Street, Gwynneville, Wollongong, New South Wales, Australia, 2500. Telephone (0061 2) 42253790, e-mail nt92@uow.edu.au. Permanent address in China: Health and Anti-epidemic Station (Centre for Disease Control and Prevention), Beibei, Chongqing, China, 400700. Telephone (001186 23) 68862799, 68863569, fax (001186 23) 68862799, e-mail nt920000@yahoo.com N Tang, NJ Luo. A cross-sectional study of intestinal parasitic enfections in a rural district of west China. Can J Infect Dis 2003;14(3):159-162

T he mortality and health problems parasitic diseases cause retard social and economic development in low-income countries (1).Parasitic diseases are also of concern in developed countries because of travel, immigration and an increasing population of immunocompromised people (2,3).Previous studies have reported a high prevalence of intestinal parasites in rural China (4,5), reaching 62.6% (95% CI 17.5% to 94.7%) in some areas (4).Trends observed have included a ©2003 Pulsus Group Inc.All rights reserved

ORIGINAL ARTICLE
decrease in Entamoeba histolytica, Fasciolopsis buski and soiltransmitted helminths, and an increase in food-transmitted parasitic diseases including trichinosis, Clonorchiasis, oriental lung fluke, cysticercosis, and hydatidosis (4).The present study describes the prevalence and characteristics of parasitic infestation in a rural district of western China, including our experience with a simple stool collection tool.

Study population
Beibei district has a population of 400,000 people, with one large urban area.For the present study, four rural quadrants were designated by East, West, South, and North coordinates, each including residents of different economic levels (high, intermediate and low).In each of the five areas (four rural and one urban), 500 to 550 people were randomly sampled.The total population that was approached to participate included 2644 people.
Ethics approval was obtained from town governments and the Beibei health bureau before the survey.All participants in the sample were assured of confidentiality, and advised that their participation was voluntary and that specimens would not be linked to individual identifiers.Each participant completed a short questionnaire that collected information including their residential area, sex, age, occupation and educational level.This information was linked by study number to the stool specimen and used only for analysis in the present study.

Laboratory methods
Each participant was provided with a standard fecal collection bag labelled with the participant's code and containing a dry plastic bag and a bamboo spike.Approximately 10 g of each participant's stool were collected and delivered to the laboratory within one day of collection.About 100 mg were filtered for the parasitological evaluation and 5 to 10 mg were smeared for direct microscopic detection.All samples were processed using five standard stool examination methods: iodine-stained smear for protozoal intestinal cysts, modified Kato-Katz thick smear (a semi-quantitative stool examination technique for detection of helminthic ova) (6,7), simple saline smear for intestinal protozoa trophozoites, a test tube filter paper culture method for detection of hookworm larvae (Ancylostoma duodenale and Necator americanus), and adhesive cellophane tape anal swab method for Enterobius vermicularis in children aged less than 12 years old.Stool specimens were initially read by two separate examiners, and reviewed by a third examiner if there was disagreement.

Statistical analysis
Standard statistical methods for categorical data were used.The significance level was P<0.05, and the calculation of 95% CIs followed standard methods.
The prevalence of parasites was higher in residents of the four rural communities (421 of 506 subjects [83.2%], 280 of 510

DISCUSSION
Enteric parasites are common in this rural district of China.About one-half of the population had positive stool specimens, although the majority had only a single parasite identified.Ascaris species, Ancylostoma species and whipworm were the most common organisms.This is consistent with previous reports from rural China (4,5) and other developing countries (8)(9)(10).Most infections are asymptomatic, but roundworm infection may cause intestinal and respiratory symptoms, and is a cause of protein-energy malnutrition in undernourished children.Hookworm infection can cause anemia and hypoproteinemia (8).Multiple parasite infestations may not be independent because physiological, immunological or ecological factors that favour parasite infection may be specific to an individual (11).The prevalence rate in females was significantly higher than in males.Sex-specific differences have been suggested to be due to differences in parasite susceptibility between the sexes (12), perhaps due to the influence of sex hormones (13).Some parasitologists suggest that susceptibility to parasitic infections is greater in males and may contribute to malebiased mortality (14).The present study, however, found a higher prevalence of parasitic infestation in women.The infection rate of female foreign workers in northern Taiwan was also reported to be 3-fold higher than that of males (15).A major contributor to parasitic diseases in the developing world is inadequate water and sanitation.Obtaining water for houshold use in most rural areas is done by women, and women spend more time actually working in the water, washing clothes and cooking.This increases exposure to waterborne diseases and may explain the increased prevalence observed in women (16).
Two species, roundworm and hookworm, were detected in all age groups.However, the infection rates did not correlate with increased age -rates were highest in the groups aged 15 to 19 years and over 80 years, and lowest in the groups aged 30 to 39 years and 70 to 79 years.Children may have higher rates of infection because of greater exposure, while the elderly may have greater rates of infection because of an age-associated decline in their immune systems (17).The prevalence of infection is higher and occurs at a younger age when the transmission rate is high.When the transmission rate is low, the peak prevalence is lower and occurs at an older age -a `peak shift' (18).Our observations would be consistent with a lower rate of transmission.
The prevalence of infestations in farmers was 8.3-fold higher than in all other occupational groups.Traditional life and farm labour practices, including irrigation and inappropriate fecal disposal, increase parasitic infectious risk in rural areas (19).The infection rate for farmers living in hilly terrains was higher than in mountainous areas.Disposal of human excreta is inadequate in some rural areas.In hilly land, sewage flows or leaks more easily to wells.Water drains more rapidly in mountainous areas, perhaps reducing infection rates.A recent World Health Organization report estimates that over 700 million Chinese people drink water contaminated with levels of animal and human waste exceeding government standards for safe water (28).The rates we observed were lower with increased education levels, similar to observations from Shanghai, China (21), although not all reports have confirmed this (10).The infectious rates were not, however, significantly associated with income.
Direct microscopy is widely used for the diagnosis of parasitic infections.Serial simple stool examinations may be a suitable method to detect pathogenic intestinal parasites.Only single samples were obtained for the present study, which may have underestimated the infection rates.Other, more sensitive and rapid techniques, such as polymerase chain reation (22), latex agglutination tests (23), serologic and intradermal tests (24), antigen detection tests and parasitic test kits (25,26) were not used.Though the direct microscopy approach needs experienced microscopists and is labour intensive and time consuming for accurate diagnosis, the procedure is relatively cheap and applicable for the diagnosis of parasitic infections in developing countries.
In 1990, major parasitic diseases were estimated to account for 11.7% of the disease burden from communicable diseases.In many nations, parasitic infections are the most frequent causes of disease attributed to contaminated drinking water.Parasitic cysts are resistant to chlorination and require water  filtration for removal, and the number of cysts required for infection may be very small (27).Thus, preventing drinking water contamination at the source is important in limiting transmission of these parasites (28).Improving private wells, based on national or provincial drinking water standards, and establishing safe public drinking water systems in rural areas may decrease parasitic density.Appropriate health education and management, and the improvement of toilets and stool disposal or personal hygiene, are also important to control parasitic infestations.

CONCLUSIONS
The present study reports a high prevalence of enteric parasites in one area of West China.The study demonstrates the usefulness of fecal examinations in developing countries, particularly in rural areas, because these examinations are easily performed at a low cost.Monitoring the prevalence of enteric parasites may be useful in assessing the effectiveness of public health interventions, particularly improvement in drinking water quality.
Mr Nian Ji Luo was responsible for the detection of parasites and for administration of the study.
Tang and LuoCan J Infect Dis Vol 14 No 3 May/June 2003 160 Intestinal parasitic infections in a rural district of west ChinaCan J Infect Dis Vol 14 No 3 May/June 2003 161