Human Taeniasis and Cysticercosis and Related Factors in Phu Tho Province, Northern Vietnam

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Korean J Parasito. 2021;59(4):369-376

Publication date (electronic) : 2021 August 18

doi : https://doi.org/10.3347/kjp.2021.59.4.369

Vu Thi Lam Binh^1,†, Do Trung Dung^1,†, Hoang Quang Vinh¹, Van Hul Anke², Praet Nicolas^2,4, Dorny Pierre^2,3, Dermauw Veronique^2,

¹National Institute of Malariology, Parasitology and Entomology (NIMPE), No 34 Trung Van, Nam Tu Liem, Ha Noi, Vietnam

²Department of Biomedical Sciences, Institute of Tropical Medicine, Nationalestraat 155, 2000 Antwerpen, Belgium

³Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium

⁴The Janssen Pharmaceutical Companies of Johnson & Johnson, Beerse, Belgium

^*Corresponding author (vdermauw@itg.be)

^†

These authors contributed equally to this work.

Received 2021 February 25; Revised 2021 July 11; Accepted 2021 July 19.

Abstract

INTRODUCTION

Taenia solium was reported as the most important foodborne parasite in a risk assessment by the World Health Organization and the Food and Agricultural Organisation [1]. The parasite is endemic in many developing countries, including Vietnam. When consuming undercooked measled pork, humans can become infected with the adult tapeworm in their intestine, this condition is called taeniasis. When ingesting eggs by consuming contaminated vegetables, water or through bad hand hygiene [2], humans can acquire cysticercosis, infection with the cysticercus. Cysticerci can establish in the muscle, skin, and central nervous system [3]. Neurocysticercosis (NCC) is a serious cause of acquired epilepsy and accompanied symptoms in endemic countries [3,4]. Humans also act as the final host of T. saginata and T. asiatica. However, the occurrence of human cysticercosis is unique for T. solium infections [5].

In Vietnam, human taeniasis/cysticercosis cases have been reported in 60 of the 63 provinces [6,7]. Nevertheless, epidemiological data on human taeniasis and cysticercosis only became available after 2000. Using classical coprology, the prevalence of taeniasis was estimated to range between 0 and 1.2% [8–10]. Using more sensitive techniques such as copro-antigen detecting ELISA (coproAg-ELISA) and copro-PCR, prevalence estimates ranged between 0 and 6.7% [10,11]. Apart from T. solium, T. asiatica and T. saginata infections are known to occur in the country [11,12], complicating the prevalence estimation of tapeworm carriers for the 3 separate species. Data on human cysticercosis are even more scarce for Vietnam. Each year, 200–300 cysticercosis patients have been treated in the referral clinic of the National Institute of Malariology, Parasitology and Entomology in Hanoi [13]. In northern Vietnam, the prevalence of circulating cysticercus antigens was reported to range between 0% and 5.7% [9,10]. Among patients suffering from epilepsy in the North, the prevalence of active cysticercosis was estimated at 9% [14], while antibodies were measured in 5.0% of surveyed individuals in South and Central Vietnam [11,15].

Vietnam has several factors presumed to facilitate the transmission of Taenia spp., such as the culinary habit to consume raw beef and pork [11], and the use of night soil to fertilize crops and vegetable fields [8]. Nevertheless, few epidemiological studies were conducted to investigate risk factors for Taenia spp. infections in Vietnam. It was reported that regular raw vegetable consumption, outdoor defecation, and drinking water from stream, lake, or pond are risk factors for cysticercosis, whereas being male and consuming undercooked pork or beef are for taeniasis [11]. In local reports, allowing pigs to roam freely, poor sanitation, lack of hygienic latrines, use of human feces as a fertilizer in agriculture, and no or inadequate meat inspection were identified as risk factors for taeniasis/cysticercosis [16].

To address the scarcity of epidemiological data on human taeniasis and cysticercosis in the country, we conducted a study in 3 communes in Phu Tho Province, representative for northern Vietnam. This area is mountainous, inhabited predominantly by ethnic minorities farming pigs, both traditional and commercial types. The local people have a habit of eating raw pork and vegetables. The purpose of our study was to determine the prevalence of taeniasis and cysticercosis and to assess the risk factors associated with T. solium infection.

MATERIALS AND METHODS

Study design and area

A cross-sectional survey was conducted from August 2012 to December 2012 in 3 communes of Phu Tho Province, 120 km away from Hanoi, capital of Vietnam (Fig. 1). Thu Ngac commune comprises of 15 hamlets and 5,552 inhabitants in 1,150 households. Long Coc commune, bordering with Thu Ngac commune, has 8 hamlets, and 3,133 people in 766 households. Xuan Vien commune consists of 13 hamlets, with 4,596 people in 1,173 households. Citizens in the 3 communes are predominantly Muong (95–99%) ethnic minority group. Commune selection was based on a high number of neurocysticercosis (NCC) patients treated at NIMPE, the presence of taeniasis cases, and the habit of eating undercooked pork in the area (unpublished survey data).

Fig. 1

Map of Vietnam showing Phu Tho Province and the surveyed communes.

RESULTS

A total of 1,185 people (515 men and 670 women) participated in this study (Table 1). All but 26 individuals belonged to the Muong ethnic minority (97.8%), the others to the Kinh group. The majority of participants were 21–50 years old (56.7%), and their main occupation was farming (76.7%). Commune and demographic characteristics were significantly associated (P>0.05), except for ethnicity (P=0.462). All 1,185 participants responded to the questionnaire, while serum samples were collected from 1,151 individuals. Stool samples were collected from 1,036 participants, of which 925 were examined using the copro-Ag-ELISA.

Table 1

Demographic characteristics of participants in Phu Tho Province, Vietnam (n=1,185)

A large majority of participants declared to consume raw meat and/or vegetables (76.9%) (Table 2). Fifteen cases (1.3%) reported having subcutaneous nodules, while 15.4% participants had observed proglottids in their stools. A total of 32 participants (2.7%) mentioned that they were suffering from epilepsy. In Thu Ngac, a high percentage of participants reported having seen proglottids in their stools, or reported suffering from epilepsy, in comparison with the other two communes. An association between questionnaire response and commune was observed for eating raw meat/vegetables, proglottids seen in faeces, and reporting to suffer from epilepsy (all P<0.05).

Table 2

Questionnaire results of participants in Phu Tho Province, Vietnam (n=1,185)

Taenia spp. eggs were found in 1.5% of the stool samples (Table 3). No participant was found infected with Taenia spp. in Xuan Vien commune, while there were 1.7% and 3.1% infected cases in Long Coc and Thu Ngac communes, respectively. Almost all taeniasis cases were males (81.3%), and they were all over 10 years old.

Table 3

Coproscopic results of participants in Phu Tho Province, Vietnam (n=1,036)

Positive copro-Ag-ELISA results were found in 2.9% of participants, 3.8% in males, 2.3% in females (Table 4). No association was found between commune, gender or age group and copro-Ag-ELISA result (all P>0.05). A strong association was found between eating raw meat and/or vegetables and having a positive result in the copro-Ag-ELISA. There was a high uncertainty around this estimate (OR=8.6, 95% CI: 1.16–63.9, P=0.01) (Table 4). No significant associations were found between having observed proglottids in feces and positivity in copro-Ag-ELISA (P>0.05), although there was a trend in that direction (OR=2.2, 95% CI: 0.93–5.1). For 24 out of 25 cases with positive copro-Ag-ELISA, there was a negative coproscopy result, whereas 14 out of 15 people with a positive coproscopy result had a negative copro-Ag-ELISA result.

Table 4

Association between copro-Ag-ELISA results and questionnaire responses in Phu Tho Province, Vietnam (n=885)

The antigen positive prevalence in sera, indicating infections with viable cysticerci, was 4.6%, 3.6% in males and 5.4% in females (Table 5). No association was found between communes, genders or age groups, and Ag-ELISA results (all P>0.05). No significant associations were found between questionnaire responses and the positivity of Ag-ELISA (all P>0.05).

Table 5

Association between Ag-ELISA results and questionnaire responses in Phu Tho Province, Vietnam (n=1,151)

DISCUSSION

A higher prevalence of taeniasis was observed in the study areas compared to the earlier studies [8–10]. Using the more sensitive copro-PCR test, a higher taeniasis prevalence was reported [11] in Central Vietnam. In contrast to the higher prevalence of taeniasis, a lower prevalence of soil-transmitted helminths (STH) was observed than in earlier studies [8–10]. This disparate trend for taeniasis versus other parasites, could point to a general improvement in hygienic conditions and/or mass drug administration programmes in the area, yet with continued risky behavior in terms of culinary habits consuming raw meat.

There was a marked difference in taeniasis prevalence based on coproscopy and copro-Ag-ELISA. This is due to disparity in test sensitivity, for coproscopy at 52.4% and for copro-Ag-ELISA at 84.5% [23]. Furthermore, test specificity might be problematic for the copro-Ag-ELISA [23] due to the presence of cross-reactions with other parasites, although earlier work failed to detect such cross-reactions [19,24]. In addition, Praet et al. [23] pointed to the ability of the copro-Ag-ELISA to detect immature tapeworm stages. These 3 hypotheses might explain why 24 out of 25 stool samples with a positive copro-Ag-ELISA result, had a negative coproscopy result. On the other hand, 14 out of 15 people with a positive coproscopy result had a negative copro-Ag-ELISA result. This disagreement might be explained by the presence of T. saginata and/or T. asiatica infections, which produce weaker reactions in the current copro-Ag-ELISA [26], thus causing a negative copro-Ag-ELISA result, but positive coproscopy result. In the current study, we did not differentiate Taenia spp., so we could not investigate whether the presence of T. saginata and/or T. asiatica infections played a role in this difference in test results.

The prevalence of active cysticercosis as examined by Ag-ELISA was in line with earlier reports in rural and mountainous regions in northern Vietnam [9,10]. Prevalence of cysticercosis antibodies was 5.0% in Central Vietnam [11] and 4.9% in South Vietnam [15,27]. Prevalence of active cysticercosis in Vietnamese patients suffering from epilepsy was estimated at 9% [14], showing that a significant proportion of epilepsy cases could be attributed to neurocysticercosis. In this study, 2.7% of participants reported epilepsy, no significant association with Ag-ELISA results was found. This could be due to the small number of participants reporting epilepsy.

In Vietnam, being male, consuming undercooked pork or beef, and having observed proglottids in the stool were significantly associated with taeniasis [11], confirmed in our study. Moreover, regular consumption of raw vegetables, outdoor defecation, drinking from streams, lakes, or ponds all were found to be significantly associated with the presence of antibodies [11], while no factors were significantly associated with active cysticercosis in our study. These findings point to the need to perform more in-depth studies investigated on risk factors for taeniasis/cysticercosis in North Vietnam, in order to adequately address both conditions in the region.

Our study has some limitations. First, the lack of species identification is hampering an in-depth insight on Taenia spp. epidemiology in the region. In Vietnam, 3 Taenia spp. cause human taeniasis, T. solium, T. saginata, and T. asiatica, and a recent study has also confirmed the presence of T. asiatica in pigs in Phu Tho Province [28]. This problem should be addressed in future studies by using molecular techniques. Furthermore, the pooled questions about raw vegetable and meat consumption might impact study conclusions.

In conclusion, notwithstanding the improvement of hygienic standards and living conditions in Vietnam in last decades, our study has shown that T. solium transmission still occurs in communities in Phu Tho Province. The consumption of raw pork and vegetables combined with traditional pig husbandry systems, poor meat inspection procedures [28,29], and the common habit of using night soil on agricultural lands [8] are likely to perpetuate the transmission of tapeworm infections. Health education campaigns are needed in this area to inform the population on those infection risks.

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