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Abstract

Background:

To our knowledge, there is a lack of reports on the prevalence and risk factors of fish-borne zoonotic trematodiasis (FZTi) in humans in many regions of Vietnam.

Design and methods:

A cross-sectional study was performed in three communes located in the Red River Delta, northern Vietnam, where residents are reported to have a habit of eating raw freshwater fish, between June 2020 and December 2021. A total of 591 individuals were interviewed using structured questionnaires, and their stool samples were collected for the analysis of fishborne zoonotic trematode (FZT) egg presence using direct microscopic observation and the formalin-ether concentration method. Univariate and multivariable logistic regression analyses were employed to explore potential risk factors.

Results:

The prevalence of fish-borne zoonotic trematodiasis (FZTi) was 14.89% among the 591 participants, ranging from 1.52% to 39%. The average age of the participants was 48.31 ± 16.77 years (range: 7–86 years old), and the highest prevalence of FZT infection (17.36%) was observed in individuals aged 19–39 years, followed by those aged 40–59 (16.67%). The prevalence of FZT infectionwas higher in men (17.75%) than in women (11.07%). Factors independently associated with FZTi, obtained by multivariate analysis, included a history of eating raw freshwater fish and the study commune.

Conclusions:

The present study has revealed a wide-ranging prevalence of FZTi among humans in Vietnam’s Red River Delta. Sustained surveillance efforts for FZTi, as well as the implementation of long-term, practical control policies, and strategies for eliminating FZT in Vietnam, are still necessary.

Keywords

fish-borne zoonotic trematode prevalence risk factors Red River Delta Vietnam

Significance for public health

Fish-borne zoonotic trematodiasis (FZTi) is an important public health problem worldwide, capable of causing cholangiocarcinoma in humans. Efforts to reduce the prevalence of FZTi in recent years have had limited success. FZTi imposes a considerable burden on the Vietnam National Health Service. Monitoring FZTi prevalence could be a tool to track the evolution of the infection and understand its impact on human health in Vietnam. Our findings showed a wide-ranging prevalence of FZTi among humans in Vietnam’s Red River Delta, with a high frequency observed in Ninh Binh province. These findings suggest that routine FZT screening is still necessary for the development and implementation of sustainable and effective control policies aimed at eliminating FZT in Vietnam.

Introduction

Infections caused by fish-borne zoonotic trematodes pose a significant public health concern worldwide, especially in Asian countries such as China, Japan, South Korea, Lao PDR, Thailand, the Far East of Russia and Vietnam, where the local population consumes raw fish.^1–4 Recently, at least 59 species of FZTi have been identified as causing human infections, categorized into two main groups, the minute intestinal flukes (MIF) and the small liver flukes (SLF).^1,2,4 The life cycle of FZT involves three kinds of hosts: a definitive host (humans, several fish-eating mammals, and birds), a first intermediate host (freshwater snails), and a second intermediate host (freshwater fish).^1,2,4 According to the World Health Organization (WHO), in 2004, approximately half a billion people globally were evaluated to be at risk of FZTi.^5–7 FZT species belonging to SLF are believed to be the cause of cholangitis, gallstones, bile duct obstruction, hepatic fibrosis, and cholangiocarcinoma (a type of bile duct cancer) in humans.^4,8,9 Thus, the WHO and the International Agency for Research on Cancer (IARC) categorized SLF as group one carcinogenic pathogens for humans.^4,9,10

According to previous studies, seven fish-borne zoonotic trematode species have been found in Vietnamese populations including Clonorchis sinensis, Haplorchis pumilio, H. taichui, H. yokogawai, Stellantchasmus falcatus, and Centrocestus formosanus, which are reported to be endemic in the northern provinces, while Opisthorchis viverrini is found in the south and central provinces.^4,5,11,12 Several previous reports in Vietnam have indicated that at least 1 million people have been contaminated with either C. sinensis or O. viverrini.^4,13,14 Furthermore, previous reports have shown that the prevalence of FZTi varies across different studies and time periods, ranging from 0.2% to 53.0% for C. sinensis, and 0.3%–36.9% for O. viverrini.^4,14,15 However, the prevalence of MIF is rarely reported, although it is believed to be higher than that of SLF.^4,12,14

The Red River Delta encompasses 11 provinces located in the northern region of Vietnam, including Hanoi, Ha Nam, Vinh Phuc, Bac Ninh, Hung Yen, Hai Duong, Hai Phong, Quang Ninh, Nam Dinh, Thai Binh, and Ninh Binh. In some of these provinces, the local residents have a long-standing habit of consuming raw freshwater and undercooked fish.¹⁶ While several studies have highlighted the high prevalence of FZTi in specific areas of Nam Dinh (Nghia Lac, Nghia Phu, and Rang Dong communes in Nghia Hung district)^17,18 and Ninh Binh (Kim Tan and Kim Dong communes in Kim Son district; Gia Minh and Gia Thinh communes in Gia Vien district),^5,11,19 there is a lack of reports on FZTi in Ha Nam province. Furthermore, the prevalence of FZTi in Nam Dinh and Ninh Binh has been documented for a long time, warranting reassessment. To effectively control FZTi, it is essential to determine their current prevalence and potential risk factors. This information is then provided to health authorities to support the implementation of effective intervention and control programs, including public health education campaigns. Hence, the present study was conducted to identify the prevalence and risk factors for fish-borne zoonotic trematodiasis in three communes situated in the Red River Delta, Vietnam.

Materials and methods

Study sites

This work was performed in three communes: Nghia Hong (Nghia Hung district, Nam Dinh province), Kim Tan (Kim Son district, Ninh Binh province), and Thanh Thuy (Thanh Liem district, Ha Nam province), situated in northern Vietnam, within the Red River Delta. These provinces collectively host approximately 23,600 individuals living in 6899 households across 37 villages. The three surveyed communes are shown in Figure 1. Nghia Hong commune has a population of 9136 people living in 2783 households, Kim Tan commune has a population of 7237 people living in 1935 households, and Thanh Thuy commune has a population of 7262 people living in 2181 households. These communes were selected based on reports indicating a habitual practice of raw fish consumption among local residents.

Figure 1.

Study sites_three communes in Ha Nam, Nam Dinh, and Ninh Binh provinces.

Study design

A cross-sectional study was conducted from June 2020 to December 2021. All villages belonging to the three study communes were selected to obtain socio-demographic information, history of eating raw fish and previous examinations for FZTi, and other relevant data. In these villages, the number of participants for the survey was calculated proportionally based on their demographic weight. At the village level, one household member aged 7 years or older was randomly selected for a face-to-face interview conducted by researchers using a structured questionnaire. The inclusion criteria comprised individuals who were: (1) aged 7 years or older, (2) agreed to participate in the study, (3) provided written informed consent, (4) agreed to respond to the questionnaire, and (5) had been residents for at least 6 months. Individuals previously diagnosed with FZTi were excluded from the study. The reporting of the current study adheres to the STROBE statement.²⁰ The STROBE checklist of items was included in Supplemental Data.

Sample size

The sample size for this work was determined using the formula: $n = Z_{1 - α / 2}^{2} \frac{p (1 - p)}{d^{2}}$ ²¹ with a reference infection rate of 19.5%.¹¹ With a confidence interval of 95% and an acceptable margin of error of 6%, the minimum sample size required was 168 people per commune (504 people in total). However, a total of 591 people were enrolled, including 198 people in Nghia Hong commune, 200 people in Kim Tan commune, and 193 people in Thanh Thuy commune.

Data/sample collection

The trained research staff provided labeled plastic sample containers to the participants and instructed them on proper stool specimen collection and storage. The fecal samples were then brought back to the community health station the following day. For participants aged 7 to under 18 years, parents/guardians were requested to assist in completing the informed consent form. The individual’s name, age, address, and date of fecal collection were noted on the corresponding sample containers. After providing their stool sample, all selected individuals in this study were asked to complete a questionnaire that was partially adapted from a previous study¹⁵ to determine potential risk factors associated with FZTi. Participants were interviewed by trained research staff to obtain socio-demographic information, history of eating raw fish, and FZT examination history, among other data.

FZT egg detection in fecal samples

Initially, FZT eggs in fecal specimens were examined using direct microscopic observation. Three smears were prepared and examined for each specimen to enhance the detection rate. Results were recorded for positive samples. Subsequently, approximately 2–3 g of each negative samples were analyzed for FZT eggs using the formol-ether method (formalin-ether concentration technique, FECT). FZT eggs were classified as small trematode eggs if their size was smaller than 50 μm.

Statistical analyses

In this study, SPSS software for Windows, version 22.0 (IBM; Chicago, IL, USA), was utilized for statistical analysis of the obtained data. To identify potential risk factors related to FZTi, univariate logistic regression analysis was employed to determine the relationship between FZTi and risk/indicator factors using either Fisher’s exact test or a Pearson chi-square test. Factors with a significance level of <0.05 in the single variables analysis were then included in a multivariable logistic regression model. An observational result was considered statistically significant if the p-value was less than 0.05.

Ethical approval

This work was approved by the Research Ethics Board of Vietnam National Institute of Malariology, Parasitology, and Entomology in January 2018 (ethics code: 113/QĐ-VSR) and Vietnam Military Medical University in April 2021 (ethics code: 1623/QĐ-HVQY) and was carried out following the principles of the Declaration of Helsinki and its subsequent amendments. Written informed consent was collected from all eligible participants or guardians before their enrollment in the research.

Results

Characteristics of the study population

In this work, three different communes in the Red River Delta were surveyed with 591 individuals enrolled, including 338 males (57.2%) and 253 females (42.8%). The mean age of participants was 48.31 years (range: 7–86, with a standard deviation (SD) of 16.77). All participants belonged to the Kinh ethnic group, with the majority being farmers (79.7%), and 53.5% reported ever eating raw fish (Figure 2). Additionally, more than three-quarters (77.5%) had an education level below secondary school (Table 1).

Figure 2.

A typical dish of raw fish served in a restaurant in Ninh Binh province.

Table 1.

Socio-demographic features of the study population.

	Commune (No; %)			Overall
Characteristics	Nghia Hong (n = 198; 33.5)	Kim Tan (n = 200; 33.8)	Thanh Thuy (n = 193; 32.7)	Overall
Gender
Male	108 (54.5)	143 (71.5)	87 (45.1)	338 (57.2)
Female	90 (45.5)	57 (28.5)	106 (54.9)	253 (42.8)
Age (years)	48.31 ± 16.77 (range: 7–86)
≤18	23 (11.6)	12 (6.0)	15 (7.8)	50 (8.5)
19–39	43 (21.7)	57 (28.5)	21 (10.9)	121 (20.5)
40–59	86 (43.4)	79 (39.5)	81 (42.0)	246 (41.6)
≥60	46 (23.2)	52 (26.0)	76 (39.4)	174 (29.4)
Ethnic group
Kinh	198 (100)	200 (100)	193 (100)	591 (100)
Other	0	0	0	0
Education
Primary school or no education	20 (10.1)	27 (13.5)	20 (10.4)	67 (11.3)
Secondary school	133 (67.2)	133 (66.5)	125 (64.8)	391 (66.2)
High school	34 (17.2)	35 (17.5)	40 (20.7)	109 (18.4)
Vocational and bachelor	11 (5.6)	5 (2.5)	8 (4.1)	24 (4.1)
Occupation
Farmer	141 (71.2)	184 (92.0)	146 (75.6)	471 (79.7)
Others	57 (28.8)	16 (8.0)	47 (24.4)	120 (20.3)
History of eating raw fish
Yes	106 (53.5)	173 (86.5)	37 (19.2)	316 (53.5)
No	92 (46.5)	27 (13.5)	156 (80.8)	275 (46.5)

Prevalence of fish-borne zoonotic trematode

Out of the 591 participants, 88 tested positive for FZT eggs (Figure 3), resulting in an overall prevalence of FZTi of 14.89%, while 503 tested negative. Notably, the highest FZT prevalence was found in Kim Tan commune (39.0%), followed by Thanh Thuy (3.63%), and Nghia Hong (1.52%). The carriage rate of FZTi was higher in men than in women (17.75% vs 11.07%), in farmers compared to other occupations (17.41% vs 5.0%), and was highest among individuals aged 19–39 years (17.36%).

Figure 3.

Eggs of small trematodes were found in the feces of a patient in Ninh Binh province.

Risk factors for fish-borne zoonotic trematode infection

Based on the univariate logistic regression analysis, participants who belonged to Kim Tan commune, males (OR = 1.73; 95% CI: 1.07–2.81; p = 0.025), individuals with a low level of education (OR = 2.01; 95% CI: 1.06–3.81; p = 0.034), farmers (OR = 4.01; 95% CI: 1.70–9.47; p = 0.001), and those with a history of eating raw freshwater fish (OR = 9.85; 95% CI: 4.84–20.07; p < 0.001), as well as those who had ever undergone FZT examination (OR = 1.92; 95% CI: 1.19–30.9; p = 0.008) were at a higher risk of FZTi. However, multivariate analysis revealed that only those with a history of eating raw freshwater fish and those belonging to Kim Tan commune were identified as risk factors for FZTi (Table 2).

Table 2.

Associations of FZT infection with socio-demographic, behavioral factors of the study population.

Characteristics	N	n (Pos)	% (Pos)	Univariate analysis		Multivariate analysis
Characteristics	N	n (Pos)	% (Pos)	OR (95% CI)	p-Value	OR (95% CI)	p-Value
Age	591	88	14.89	1 (0.99–1.01)	0.932
Age groups
≤18	50	4	8.0	Reference
19–39	121	21	17.36	0.41 (0.13–1.28)	0.124
40–59	246	41	16.67	0.44 (0.15–1.27)	0.129
≥60	174	22	12.64	0.60 (0.20–1.83)	0.371
Commune
Kim Tan	200	78	39.0	Reference		1
Thanh Thuy	198	7	3.63	16.99 (7.59–38.05)	<0.001	7.96 (3.06–20.67)	<0.001
Nghia Hong	193	3	1.52	41.56 (12.83–134.6)	<0.001	30.13 (9.06–100.21)	<0.001
Gender
Female	253	28	11.07	Reference		1
Male	338	60	17.75	1.73 (1.07–2.81)	0.025	0.94 (0.52–1.69)	0.836
Education
Higher than high school	133	12	9.02	Reference
Lower than secondary school	458	76	16.59	2.01 (1.06–3.81)	0.034	2.03 (0.98–4.24)	0.058
Occupation
Farmer	471	82	17.41	4.01 (1.70–9.47)	0.001	1.54 (0.58–4.05)	0.383
Others	120	6	5.0	Reference		1
Family size
≤4 members	484	69	14.26	Reference
>4 members	107	19	17.76	1.30 (0.74–2.27)	0.358
Toilet type
Hygienic	577	84	14.56	Reference
Unhygienic	14	4	28.57	2.35 (0.72–7.66)	0.157
History of eating raw fish
No	275	9	3.27	Reference		1
Yes	316	79	25.0	9.85 (4.84–20.07)	<0.001	4.03 (1.73–9.38)	0.001
FZT examination history
Yes	153	33	21.57	Reference		1
No	438	55	12.56	1.92 (1.19–30.9)	0.008	0.78 (0.44–1.39)	0.401

FZT: fish-borne zoonotic trematode; OR: odds ratios; (Pos): positive; 95% CI: 95% confidence intervals.

Discussion

FZTi is part of a group of food-borne zoonotic infections and are commonly found circulating in certain areas of the world, mainly distributed in China, Korea, Lao PDR, Vietnam, Thailand, and the Russian Far East.^22–24 Findings from previous studies show that the prevalence of FZTi in humans varies across different regions,^5,19,25 and depend on socio-demographic features (gender and age groups), different times of the year, study populations, and detection methods.^26,27 Globally, at least 500 million people are at potential risk of FZTi.^13,28 Epidemiological data from various areas worldwide have shown that the prevalence of FZTi among humans varies widely, ranging from 0.08% to 75.0%.^29–31

In this investigation, the prevalence of FZTi among the study population across three communes was found to be 14.89%. The infection rate varied considerably, ranging from 1.52% in Nghia Hong commune to 39.0% in Kim Tan commune. Consequently, the prevalence of FZTi observed in our research population was within the reported range. Our findings also indicated that FZTi was widespread in Kim Tan commune (Kim Son district, Ninh Binh province), but less common in Nghia Hong commune (Nghia Hung district, Nam Dinh province) and Thanh Thuy commune (Thanh Liem district, Ha Nam province). In Vietnam, lower FZT prevalence was found in some provinces such as Da Nang (0.3%), Khanh Hoa (1.4%), Quang Nam (4.6%), Dak Lak (7.6%), and Binh Dinh (11.9%). Conversely, higher prevalences were previously reported in Nghia Hung district, Nam Dinh province (22.72% and 64.9%) ^12,18; Kim Son, Yen Khanh and Gia Vien districts, Ninh Binh province (20.1% and 26.1%, 18.91%, and 20.5%, respectively),^5,11,32 Nga Son and Ha Trung districts, Thanh Hoa province (17.2% and 34.41%),^15,33 and Yen Binh district, Yen Bai province (44.85%).¹⁵ Epidemiological data from some regions in Phu Yen and Quang Tri provinces also observed a higher prevalence of FZTi in humans than in the current research (36.9% and 32% vs 14.89%).³⁴ The reasons for these variations are due to the prevalence of FZTi depending on eating behavior characteristics (consumption of raw fish), gender (male), social demographics, and different regions of the understudied population.^5,19,25

Notably, the prevalence of FZTi in Kim Son district in this study was significantly higher than in Nghia Hong district (Nam Dinh province) and Thanh Liem district (Ha Nam province; 39.0% vs 3.63% and 1.52%, respectively), and also higher than that in previous surveys carried out in Kim Son district by Tran et al. (19.5%),¹¹ and Dang et al. (26.1%).³² Previously, a high prevalence of FZTi in humans has been documented in Nam Dinh (26.0–37.5%) and Ninh Binh (23.5–31.0%) provinces.^14,15,34 Our findings indicated that the prevalence of FZTi in Kim Son district not only did not decrease but also tended to increase. In contrast, FZTi in Nghia Hung district (Nam Dinh province) and Thanh Liem district (Ha Nam province) was quite low and seemed to have a decreasing trend. These differences may be attributed to the higher prevalence of raw freshwater fish consumption (86.5%) among residents in Kim Son district compared to those in Nghia Hung and Thanh Liem districts. Therefore, more large-scale surveys are needed to determine the prevalence of FZTi in these provinces.

The results from various studies have shown a c conflicting relationship between FZTi and gender, age, education level, occupation, toilet type, and FZT examination history. For example, in this study, there was no association between FZTi and gender. Similar findings were also observed in previous investigations in Kamalasai district (Kalasin province, Thailand)³⁵ and Yen Binh district (Yen Bai province, Vietnam).⁴ Conversely, previous studies conducted by Hung et al.,⁵ Tran et al.,¹¹ Nguyen et al.,¹⁵ and Xu et al.³⁶ revealed that men had a higher risk of FZTi than women. Similarly, conflicting results regarding the relationship between age, occupation, and FZT examination history and FZTi were also observed in many reported studies.^4,19,35,37 Notably, education level and occupation were identified as risk factors for FZTi in some previous studies in Vietnam.^15,19 This may be attributed to misconceptions about the FZT transmission and prevention among certain populations. Furthermore, in many rural areas of Vietnam, farmers still use animal manure in fish ponds as part of integrated agricultural systems, which combine gardens, fish ponds, and animal sheds - a practice historically promoted by the Ministry of Agriculture.¹⁵ However, in recent years, Vietnam has experienced substantial socio-economic development and infrastructure improvements, gradually reducing disparities in public awareness. These advancements may help explain the inconsistent findings regarding the associations between education level, occupation, and FZTi.

The consumption of raw fish has been previously shown to be the most important risk factor associated with FZTi in both cross-sectional studies^3,11,12 and cohort studies.^4,38 In the current study, individuals who had ever consumed uncooked fish dishes had 4.03 times higher risk of FZTi than those who had not eaten raw freshwater fish dishes (95% CI: 1.73–9.38), which was consistent with findings from previous studies in Thailand,^10,35 China,^27,36,39 Korea,⁴⁰ Philippines,⁴¹ and Vietnam.^{3,4,11,12,15,19,37} The result of this study also indicated that more than fifty percent of participants had ever eaten raw fish dishes. Although many efforts have been made to reduce raw fish consumption, this habit seems almost unchanged.¹¹ The reason for this situation is that it is very hard to change the habit of consuming raw freshwater fish among local people,¹¹ and the misconception that praziquantel can easily eliminate parasites.¹⁰ Therefore, public health interventions aimed at raising awareness, educating local residents on the risks of FZTi, and promoting behavioral changes are crucial to reducing its prevalence in the community.^19,42

This investigation had some limitations, including a lack of comprehensive clinical information, the absence of specific data on C. sinensis and MIF infections, and no assessment of FZT egg density in feces. Additionally, the potential for recall bias during the interview process may have affected the accuracy of participants’ self-reports on raw fish consumption, which is also considered a limitation of the study.

Conclusion

The results of the current study have revealed a wide-ranging prevalence of FZTi among humans in Vietnam’s Red River Delta. Risk factors for FZT infection in humans, obtained through multivariate analysis, included a history of eating raw freshwater fish and the study commune. The findings of this study not only enrich the existing epidemiological data but also provide practical evidence for improving prevention strategies, designing health education programs, and implementing suitable diagnostic tools for early detection and control of FZT infections in endemic areas.

Supplemental Material

sj-docx-1-phj-10.1177_22799036251345939 – Supplemental material for Prevalence and risk factors of fish-borne zoonotic trematode infections in a rural community: A cross-sectional study in the Red River Delta of Vietnam

Supplemental material, sj-docx-1-phj-10.1177_22799036251345939 for Prevalence and risk factors of fish-borne zoonotic trematode infections in a rural community: A cross-sectional study in the Red River Delta of Vietnam by Hoang Dinh Canh, Cao Ba Loi, Nguyen Van Tuan, Nguyen Van Thoai, Nguyen Duc Tan, Nguyen Thi Nhu Quynh, Vu Van Du and Do Ngoc Anh in Journal of Public Health Research

Footnotes

Acknowledgements

We gratefully thank all the study participants in this work. We appreciate the Centre Disease Control and Prevention (CDC) of Ninh Binh, Nam Dinh, and Ha Nam provinces as well as the three health stations in Kim Tan, Nghia Hong, and Thanh Thuy communes. We are also grateful to the Department of Medical Parasitology (Military Medical University, Vietnam) for providing research staff and equipment for sample analysis.

ORCID iDs

Hoang Dinh Canh

Do Ngoc Anh

Author contributions

HDC, CBL, NVT and DNA conceived and designed the study, drafted the article, and critically revised the article; NVT, NTNQ, and DNA collected stool samples, recorded participants’ information, and tested the collected specimens. NVT, NVTh, NDT, VVD, and DNA contributed to statistical analysis, data interpretation, and prepared Tables 1 and 2 and Figures 1 –. All authors read and approved the ﬁnal manuscript.

Funding

The author(s) disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was partially supported by The Institute for Veterinary Research and Development of Central Vietnam, Khanh Hoa province, Vietnam (Grant no. 46/QĐ-VTY-KHĐT to NVT).

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Data availability statement

All data in this work are obtainable from the corresponding author upon reasonable request.

Supplemental material

Supplemental material for this article is available online.

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