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Keywords:

  • Taenia solium ;
  • Vietnam;
  • neurocysticercosis;
  • clinical signs;
  • burden

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Objectives

To describe the occurrence of cysticercosis in patients living in rural areas of Northern Vietnam presenting clinical signs of neurocysticercosis.

Methods

Serological antigen detection, reflecting current infection with viable larval stages of Taenia solium, was used to estimate the prevalence of active cysticercosis in this patient population.

Results

The seroprevalence in epileptic patient population was <10%. However, antigen detection cannot detect dead cysticerci, which may also cause clinical signs. Therefore, the seroprevalence figures shown here may underestimate the role of neurocysticercosis as a causal agent of epilepsy and headaches in this population.

Conclusions

Human and porcine cysticercosis remain public and veterinary public health problems in Northern Vietnam and probably in other parts of the country.

Objectifs

Décrire l'apparition de la cysticercose chez les patients vivant en milieu rural dans le nord du Vietnam qui présentent des signes cliniques de neurocysticercose.

Méthodes

La détection sérologique de l'antigène, reflétant une infection en cours avec des stades larvaires viables de Taenia solium, a été utilisée pour estimer la prévalence de cysticercose active dans ces populations.

Résultats

La séroprévalence dans les populations de patients épileptiques était <10%. Cependant, la détection d'antigènes ne peut pas détecter des cysticerques morts, qui peuvent également provoquer des signes cliniques. Par conséquent, les taux de séroprévalence présentés ici pourraient sous-estimer le rôle de la neurocysticercose comme agent causal de l’épilepsie et des maux de tête dans cette population.

Conclusions

La cysticercose porcine et humaine restent des problèmes de santé publique et vétérinaire dans le nord du Vietnam et probablement dans d'autres parties du pays.

Objetivos

Describir la presencia de cisticercosis en pacientes viviendo en zonas rurales del Norte de Vietnam que presentan signos clínicos de neurocisticercosis.

Métodos

Para calcular la prevalencia de cisticercosis activa en estas poblaciones se utilizó la detección del antígeno neurológico, como reflejo de la presencia de infección con estadios larvales viables de Taenia solium.

Resultados

La seroprevalencia en poblaciones de pacientes epilépticos era <10%. Sin embargo la detección del antígeno no se da en individuos con presencia de cisticercos muertos, que por otro lado si pueden provocar signos clínicos. Por lo tanto, los datos de seroprevalencia que aquí se presentan podrían estar subestimando el papel de la neurocisticercosis como agente causal de la epilepsia y de dolores de cabeza en esta población.

Conclusiones

La cisticercosis – humana y porcina – continúa siendo un problema de salud pública y veterinaria en el norte de Vietnam y probablemente en otras partes del país.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Like many other Asian countries, Vietnam is endemic for Taenia solium, a zoonotic parasite causing porcine and human cysticercosis (CC) (Erhart et al. 2002; Somers et al. 2007; Willingham et al. 2003; Somers et al. 2006). While CC in pigs may cause considerable economic losses, establishment of the larval stage of the parasite (cysticercus) in the human central nervous system (neurocysticercosis (NCC)) may cause severe neurological disorders, such as epilepsy and headaches (Prabhakar & Singh 2002; Carabin et al. 2006; Praet et al. 2009).

Data on the occurrence of T. solium in Asia are limited. Some studies conducted in Asian countries have reported a prevalence of porcine and human CC ranging from 0.01% to 70.4% and 1.7% to 18.5%, respectively (Willingham et al. 2010; Murrell 2005). However, these prevalence figures should be interpreted carefully because the diagnostic tools used to detect infected individuals differ among the studies, which may considerably influence the estimates (Praet et al. 2010a). Willingham et al. (2003) reviewed the available information on human and porcine CC and taeniasis in Vietnam. Although some information on CC is available at hospital level, community-based data, which would permit a clearer estimation of the burden of the disease in rural areas where the major risk factors prevail, are lacking. Such risk factors for parasite transmission are freely roaming pigs, lack of properly used latrines and the habit of eating raw pork (Erhart et al. 2002; Willingham et al. 2003). Through community-based surveys conducted in 2006 in villages of Northern Vietnam, Somers and colleagues demonstrated the presence of circulating cysticercus antigens, suggesting active infection with the parasite, in 5.3%, 0.6% and 0.0% of the sampled individuals from the mountainous, coastal and urban regions, respectively (Dorny et al. 2004; Somers et al. 2006).

Besides prevalence and incidence figures, estimates of the proportion of NCC-associated health outcomes (epilepsy and headaches) are urgently needed to assess the burden of T. solium CC. Unfortunately, these figures are often lacking because studies to measure the attribution rate of CC require a complicated and expensive study design. Recently, a systematic review estimated a proportion of 29.0% of NCC among people with epilepsy living in T. solium endemic areas (Ndimubanzi et al. 2010). Asia-specific estimates are scarce, but studies in India estimate a proportion ranging from 18.0% to 38.6% of NCC-associated epilepsy (Rajshekhar et al. 2006; Ndimubanzi et al. 2010; Raghava et al. 2010; Goel et al. 2011; Raina et al. 2012; Singh et al. 2012). Asian estimates of the proportion of NCC-associated headaches are inexistent. One study conducted in Mexico estimated that about 0.1% of the population suffers from severe headaches due to NCC (Bhattarai et al. 2012; Carabin et al. 2011).

We report here the results of investigative surveys conducted in seven provinces of Northern Vietnam to describe the occurrence of CC in selected epileptic, headache and subcutaneous cyst patient populations living in rural areas of Northern Vietnam.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Between 2007 and 2010, seven provinces (Bac Giang, Bac Ninh, Dien Bien, Ha Giang, Laichau, Lang Son and Tuyen Quang; Figure 1) were selected based on preliminary questionnaire surveys indicating the presence of the major risk factors for T. solium transmission, that is, free-roaming pigs, lack of properly used latrines and raw pork-eating habits (data not shown; Erhart et al. 2002; Willingham et al. 2003). First, the populations were screened for the presence of the three major CC clinical manifestations, namely epilepsy, chronic headaches and presence of subcutaneous cysts (Prabhakar & Singh 2002). Epileptic, chronic headache patients and patients presenting subcutaneous cysts were identified using available registers at health centres and local hospitals. After informed consent, patients who were willing to participate were blood sampled. Blood was allowed to clot and centrifuged, and the serum was kept at −20 °C until analysis. Serum samples were tested using ELISA for detection of circulating antigens of the larval stage of T. solium (Ag-ELISA; Dorny et al. 2004). A sensitivity of 90% and a specificity of 98% were determined for the diagnosis of active CC using Ag-ELISA (Praet et al. 2010a).

image

Figure 1. Map of Northern Vietnam showing the seven selected provinces where Taenia solium is endemic (shaded areas).

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Data were entered in Microsoft Excel software. For each NCC clinical manifestation, multivariate logistic regression analysis was used to identify significant relations between positivity to the Ag-ELISA (dependent variable) and age and sex (independent variables). The significance level was set at P < 0.05. Statistical analyses were conducted in STATA 11 ES software (Stata Corp., College Station, TX).

The study's protocol was approved by the Ethical Research Committee of the National Institute of Malariology, Parasitology and Entomology, Ministry of Health, Vietnam. Patients were included in the study upon written informed consent. A clinical follow-up of the Ag-ELISA positive patients was organised by the local health centres, and treatments were adjusted when needed.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

A total of 513, 758 and 83 patients suffering from epilepsy, chronic headaches and subcutaneous cysts, respectively, agreed to participate in the study. Patients were aged 6–89 years. The seroprevalence of CC in epileptic, headache and subcutaneous cyst patient populations and by province is detailed in Table 1.

Table 1. Seroprevalence of CC (based on Ag-ELISA) in epileptic, headache and subcutaneous cyst patient populations by province
Proportion of Ag-ELISA positives (95% CI)
ProvincesEpilepsyHeadachesSubcutaneous cysts
Bac Giang0.06 (0.02–0.12)0.08 (0.07–0.23)0.33 (0.00–0.91)
Bac Ninh0.12 (0.07–0.18)0.12 (0.06–0.20)0.04 (0.00–0.18)
Dien Bien0.04 (0.00–0.13)0.07 (0.03–0.14)0.09 (0.00–0.41)
Ha Giang0.07 (0.02–0.15)0.09 (0.03–0.19)0.18 (0.02–0.52)
Laichau0.11 (0.04–0.23)0.05 (0.02–0.10)0.00 (0.00–0.71)
Lang Son0.13 (0.05–0.27)0.05 (0.03–0.10)0.09 (0.11–0.29)
Tuyen Quang0.00 (0.00–0.21)0.03 (0.01–0.07)0.00 (0.00–0.52)
Mean Prev.0.09 (0.06–0.11)0.06 (0.05–0.08)0.08 (0.03–0.17)

Among patients suffering from epilepsy, 5% also had headaches and subcutaneous cysts, 58% had headaches only and 4% had only subcutaneous cysts. Logistic regression analysis did not show any significant difference of seroprevalence between males and females but revealed a positive correlation with age in both epileptic and headache patient populations (Figure 2).

image

Figure 2. Proportion of Ag-ELISA positives in both epileptic and headache patient populations by age category (9 age categories of 10 years).

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Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Taenia solium is endemic in Vietnam, but few studies allowed estimating the prevalence of the disease in the country. Moreover, little is known about the role of the parasite as a causal agent of epilepsy and headaches. The present study aimed at describing the occurrence of CC in selected epileptic, headache and subcutaneous cyst patient populations living in rural areas of Northern Vietnam. The Ag-ELISA, reflecting current infection with viable larval stages of the parasite, was used to estimate the prevalence of active CC in these populations, where risk factors for transmission are still present. The seroprevalence of CC in the epileptic patient population was relatively low (<10%) but within the range of values found in other countries (1.9% to 38.3%; Prado-Jean et al. 2007; Nitiéma et al. 2012; Willingham et al. 2010). A lower proportion of Ag-ELISA positives among epileptic patient may be linked to a lower overall CC prevalence in the region. However, as T. solium, T. saginata and T. asiatica are sympatric in South-east Asian countries; interspecific parasite competition may moderate T. solium transmission in this region, as suggested by Conlan et al. (2009). Yet, even though Gabriël et al. (2012) demonstrated that antigen detection can be of added value for diagnosing NCC in patients with epilepsy, one has to keep in mind that the Ag-ELISA is not able to detect dead cysticerci, which may also be responsible of clinical signs. Therefore, our seroprevalence figures probably underestimate the role of NCC as a causal agent of epilepsy and headaches in these populations. In contrast, using the Ag-ELISA may also overestimate the latter figure because the serological assay detects active CC and not exclusively NCC.

Data on the proportion of NCC-associated headaches are dramatically lacking, which precludes an accurate assessment of the burden of T. solium cysticercosis (Carabin et al. 2006, 2011; Praet et al. 2009; Bhattarai et al. 2012). Providing estimates of the proportion of active NCC among patients suffering from headaches in Northern Vietnamese provinces is a first attempt to fill this gap.

Our study indicates that human and porcine CC still remain public and veterinary public health problems in Northern Vietnam and probably in other parts of the country and neighbouring countries sharing the same pig breeding and raw pork-eating habits, and lacking functioning sanitations. The prevalence of CC in both epileptic and headache patient populations significantly increased with age of the patients. This observation could indicate that susceptibility to become infected increases with age as hypothesised in other studies (Fleury et al. 2004; Cavellani et al. 2007; Praet et al. 2010b).

The design of this study has limitations mainly due to the selection of patients, which is based on registers at health centres and local hospitals. Therefore, the number of patients suffering from CC symptoms may have been underestimated. Moreover, due to the lack of appropriate tools at local level, the diagnosis of epilepsy, chronic headaches and subcutaneous cysts may be inaccurate. However, this study underlines the importance of conducting community-based studies in the region using available serological tools to study the relation between clinical manifestations of CC and infection with the parasite. Further investigations should include the use of imaging techniques such as Magnetic Resonance Imaging and/or Computed Tomography scan allowing to determine the role of NCC as causal agent of epilepsy and headaches. These neuroimaging methods are starting to become available in hospitals in Vietnam, also at the provincial level. Adult tapeworm detection tests such as coprology, coproantigen ELISA, tapeworm recovery after treatment and molecular identification should be simultaneously used with CC detection tools to fully understand the transmission dynamics of the parasite in this Taenia spp. co-endemic region, to assess its impact on public and veterinary public health and to combat CC (Willingham et al. 2010; Murrell 2005).

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The authors would like to acknowledge the staff of the Preventive Medical Centers of the provinces, districts and communes for their collaboration in the present study. This work was supported by the Belgian Cooperation in the framework of the Institutional Collaboration between the Institute of Tropical Medicine in Antwerp, Belgium and the National Institute of Malariology, Parasitology and Entomology, Ministry of Health in Hanoi, Vietnam.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
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