Background
Infection with intestinal parasites, including soil-transmitted helminths (STHs), intestinal protozoa, and food-borne parasites (which can be diagnosed through the detection of eggs/cysts in human stool samples), occurs throughout the world and represents a widespread and serious public health problem in developing countries [
1]. The most common intestinal parasites within the group of helminths are STHs, including
Ascaris lumbricoides (roundworm),
Necator americanus and
Ancylostoma duodenale (hookworm), and
Trichuris trichiura (whipworm), which infect more than 1 billion people, with up to 5.3 billion people at risk of infection with at least one species [
2‐
4]. In China, the overall prevalence of STH infections in 2010 was 11.4%, with 6.8% of these infections caused by
Ascaris lumbricoides [
5]. Food-borne parasites are also an important cause of intestinal parasite infections, and liver flukes are the predominant food-borne parasitic human pathogen. There are an estimated 15.3 million cases of
Clonorchis sinensis(
C. sinensis)infection worldwide, and 80% of these infections are concentrated in China [
6,
7].
Intestinal parasite infections are important neglected tropical diseases. In general, infection with intestinal parasites causes diarrhea, iron deficiency anemia, growth retardation in children, and other physical and mental health problems [
8]. Furthermore, current studies have shown that chronic intestinal parasite infection can affect the spread, severity, and outcome of other infectious diseases, such as tuberculosis, malaria, and viral infections [
9‐
11]. However,
C. sinensis infection is primarily related to liver and biliary disorders, especially cholangiocarcinoma [
12,
13].
Several factors contribute to the high prevalence of intestinal parasites in tropical and sub-tropical countries, including climatic conditions, poor sanitation, and a lack of safe water and adequate toilet facilities [
14]. Furthermore, certain behaviors can lead to infection with specific pathogens; for instance, eating raw food can lead to infection with food-borne parasites, and barefooted agricultural work can lead to hookworm infection [
13,
15]. Strategies such as anthelmintic drug therapy and water, sanitation, and hygiene improvements can play a significant role in controlling intestinal parasite infections [
16,
17]. Also, providing health education and promoting positive health behaviors can help to decrease the incidence of intestinal parasitic infections [
14,
18].
Jiangsu is an eastern coastal province of the People’s Republic of China, and has the highest gross domestic product per capita of all of the Chinese provinces. The average temperature is − 1–4 °C in January and 26–29 °C in July, and the annual average rainfall is 800–1200 mm. Its environment is favorable for the transmission of intestinal parasites. The prevalence of intestinal parasite infections was as high as 71.75% in 1990, at which time 18 species of human parasites were present, with 51.5% of residents exhibiting infection with more than one parasite. The implementation of comprehensive control measures throughout the province, including mass drug administration and renovation of the water supply and sewage systems, resulted in a dramatic decrease in the prevalence of intestinal parasites over a 10-year period, to 9.28% in 2002 and nine species of human parasites were detected [
6]. In order to assess the current state of intestinal parasite infections in Jiangsu Province, we carried out a province-wide cross-sectional survey in 2015.
Methods
Survey design, participants, and organization
Two types of survey settings were selected: rural sites (for soil-transmitted parasites) and urban sites (for C. sinensis). A stratified random sampling method was used to select rural sites in Jiangsu Province, according to geographical features, income levels, and the epidemic characteristics of intestinal parasite diseases. A random sampling method was used to select urban sites in Jiangsu Province, according to local dietary habits, human-infection prevalence in 2002, and the epidemic characteristics of clonorchiasis.
One village or one community in a county (city or district) was randomly selected as a survey site, and at least 250 permanent residents (who had lived in the village or community for more than six months) were investigated according to the National Survey Programme of Important Human Parasitic Disease in China. Male and female participants in different age groups and with different occupations were included. More than 85% of the residents were surveyed at each study site.
Jiangsu Institute of Parasitic Diseases was responsible for supervision, data review, and quality control. Staff members from the parasitic diseases department of each municipal- and county-level Center for Disease Control were responsible for the study organization, sample collection, questionnaire administration, field-based testing, and initial data input.
Types of parasite infection investigated
Human infections in each survey site were identified through the screening of fecal samples for the eggs of Ascaris lumbricoides, Necator americanus, Ancylostoma duodenale, Trichuris trichiura, Enterobius vermicularis, Taenia solium, Taenia saginata, Clonorchis sinensis, Paragonimus westermani, and other intestinal helminths. At the rural sites, cysts, oocysts, or trophozoites from Giardia lamblia, Cryptosporidium, Entamoeba histolytica, Entamoeba coli, Balantidium coli, and other intestinal protozoa were also identified. At urban sites, the prevalence of C. sinensis infection in animals, including secondary intermediate hosts (freshwater fish) and reservoir hosts (cats, dogs and pigs), was also investigated.
Specimen collection, detection, and registration
About 50 g of feces were collected from each participant. The Kato-Katz method was used to detect helminth eggs by microscopy, and the number of eggs and type of species were determined. Two slides were counted for each sample, and the number of eggs per gram was calculated by multiplying the average number of eggs per slide by 24. Hookworm species (
N. americanus or
A. duodenale) were identified by the filter paper culture method. Cultures were examined under low power magnification (100 ×) for emerging larvae each day starting on the third day to rule out the presence of filariform larvae. Species were identified by morphological characteristics [
19]. Intestinal protozoa were detected by Lugol’s Iodine Stain methodology using a microscope with an ocular micrometer. Species were identified according to the morphological characteristics and size of each cyst (oocysts) [
20]. For participants younger than six, a transparent tape test was used to detect pinworm (
E. vermicularis) eggs around the anus [
21].
To detect
C. sinensis infection among animals, at least 100 wild freshwater fish were collected from natural bodies of water (ponds, rivers, or streams) at each urban site, and the direct compression method was used to detect metacercaria in fish muscle tissue [
22]. Furthermore, fecal samples were collected from 20 of each type of animal investigated (including cats, dogs and pigs) at each site, and the Kato-Katz method was used to detect
C. sinensis eggs.
General information was recorded for each survey site, including geographical features (terrain, altitude, latitude, and longitude), population, and dietary habits. Also, general information for each participant was recorded, including name, gender, date of birth, nationality, occupation, education, and the presence or absence of intestinal parasites.
Questionnaires
Two different questionnaires were used in this study. Questionnaires were collected from legal guardians if participants were under six years old or from themselves in written format if participants were older than six years. Illiterate participants were informed of the content of questionnaires which were filled out by investigators on their behalf. One questionnaire was used for participants from rural sites and covered basic knowledge (knowledge regarding soil-transmitted parasites, infection routes, hazards, and prevention), attitudes (towards deworming treatments and the changing of habits that could lead to infection), and practices that could lead to becoming infected with soil-transmitted parasitic diseases (not washing hands before eating or after using the toilet, drinking non-boiled water, fertilizing soil with fresh excrement, and working in the fields barefoot). The other questionnaire was used for participants from urban sites, and covered basic knowledge (awareness of C. sinensis, hazards, infection routes, and prevention), attitudes (towards eating raw fish, seeking deworming treatment, and the changing of habits that could lead to infection), and practices that could lead to clonorchiasis (using the same chopping board for raw and cooked food, and eating raw freshwater fish/shrimp).
Data analysis
Epi Info software (version 6) was used to create the database. Double entry and recheck steps were used to ensure data accuracy. Pearson χ2 and Fisher’s exact tests were used to investigate associations among qualitative categorical variables using SPSS software (Version 19.0, SPSS Inc., Chicago, Illinois), and a p-value of less than 0.05 was considered to be statistically significant. The Bonferroni correction was used for each pairwise comparison.
Discussion
We carried out a cross-sectional survey of intestinal parasitic infections in Jiangsu Province in eastern China. We found that the human infection rate has decreased from 9.28 to 0.38% over the past 10 years. These data provide a better understanding of the current prevalence and characteristics of intestinal parasitic infections in this region, which can be used to inform the future implementation of control measures.
Three cross-sectional surveys carried out approximately every ten years, show that the rate of human infection has decreased dramatically over the last 30 years [
6]. Comprehensive measures including mass drug administration, renovation of the water supply and sewage systems, and health education were implemented in this province in the 1990s. As of 2015, approximately 115.96 million deworming treatments and prophylactic chemotherapy regimens (albendazole and mebendazole) have been administered throughout Jiangsu Province (Data not published). Furthermore, the government has continuously promoted the renovation of the water supply and sewage systems, especially in rural areas. In addition, a public sewage system was in place in 87.52% of rural areas in Jiangsu Province by the end of 2015 (Data not published). Data from this study indicates that the implementation of these measures has had a marked effect on intestinal parasite control.
Previous studies have shown that factors such as gender, age, education, and occupation, may influence the rate of intestinal parasite infections. Our data show that female participants in rural areas had a higher rate of infection than men; this may be because they are more likely to engage in agricultural work and come into contact with soil [
19]. We also observed a negative correlation between education, socioeconomic level, and infection rates. This may be explained by healthier habits or better living conditions for participants who had high education levels or were from wealthy areas [
24,
25]. We did not observe any significant differences in infection rate between participants based on age and occupation.
The mass migration of rural laborers into urban areas means that the population of rural areas of Jiangsu is primarily comprised of children and the elderly; these groups are at high risk for infection with intestinal parasites, especially STHs. Our data show that elderly individuals are more likely to be infected than individuals from other age groups. The most common parasite identified in this study was the hookworm A. duodenale. It is reasonable to presume that this is due to the relatively low awareness of hookworm infection routes and the relatively common practice of peforming agricultural work barefoot, as reported in the questionnaire responses.
Clonorchiasis is endemic in southern (Guangdong and Guangxi Province) and northeastern (Heilongjiang and Jilin Province) China, due to frequent consumption of raw fish and shrimp [
12,
13]. Clonorchiasis is also endemic in Jiangsu Province, although at low rates (< 0.1% historically), especially in northern parts of the province. Our data confirmed this low rate of infection (only four positive cases were detected); however, other stages of the life cycle of
C. sinensis were still found in animals.
Unfortunately, a relatively low level of knowledge about C. sinensis and a high rate of risky behaviors (using the same chopping board for raw and cooked food) were observed in this study. Furthermore, dietary habits including eating raw/uncooked freshwater fish or shrimp were prevalent among participants. Therefore, there is a potentially significant risk of human infection in this province, and further health education and food safety risk monitoring should be carried out in the near future.
Traditional pathogen-detecting methods are useful for field studies of parasitic infections as they are low-cost and simple to perform. Several traditional pathogen-detecting methods were used in this study, including the Kato-Katz method for parasite egg detection, Lugol’s Iodine Stain method for protozoa detection, and the direct compression method for detecting metacercaria in fish muscle tissue. The sensitivity of these methods may be lower in the context of low infection rates and mild infections [
26,
27]. Thus, some cases may have been missed, even though two slides were prepared from each fecal sample for detection by the Kato-Katz method.
Several molecular methods based on the detection of parasite-specific nucleotide sequences have been developed in recent years, and these methods have satisfactory sensitivity and specificity for detecting parasitic infections [
28‐
30]. Disadvantages such as high cost and the need for a professional operator and specialized equipment, limit their usefulness in the field. An alternative method with high sensitivity and specificity that is simple to perform and low-cost should be developed for parasitic infection surveillance in areas with low levels of infection (such as Jiangsu).
Conclusion
The prevalence of intestinal parasite infections in Jiangsu Province in eastern China has decreased from 71.57% in 1990 to 0.38% in 2015. Next-step control measures should focus on parasitic infections in children and the elderly, health education (promotion), food safety risk monitoring for food-borne parasites, and the development of alternative detection methods.
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