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Porcine Cysticercosis (Taenia Solium and Taenia Asiatica)

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Porcine Cysticercosis (Taenia Solium and Taenia Asiatica) Braae et al. Parasites & Vectors (2018) 11:613 https://doi.org/10.1186/s13071-018-3203-z RESEARCH Open Access Porcine cysticercosis (Taenia solium and Taenia asiatica): mapping occurrence and areas potentially at risk in East and Southeast Asia Uffe Christian Braae1* , Nguyen Manh Hung2, Fadjar Satrija3, Virak Khieu4, Xiao-Nong Zhou5 and Arve Lee Willingham1 Abstract Background: Due to the relative short life span and the limited spatial movement, porcine cysticercosis is an excellent indicator of current local active transmission. The aim of this study was to map at province-level, the occurrence of T. solium and T. asiatica in pigs and areas at risk of transmission to pigs in East and Southeast Asia, based on the density of extensive pig production systems and confirmed reports of porcine cysticercosis. Methods: This study covered East and Southeast Asia, which consist of the following countries: Brunei, Cambodia, China, East Timor, Indonesia, Japan, Laos, Malaysia, Mongolia, Myanmar, North Korea, Philippines, Singapore, South Korea, Thailand and Vietnam. Literature searches were carried out to identify current epidemiological data on the occurrence of porcine cysticercosis caused by T. solium and T. asiatica infections. Modelled densities of pigs in extensive production systems were mapped and compared to available data on porcine cysticercosis. Results: Porcine cysticercosis was confirmed to be present during the period 2000 to 2018 in eight out of the16countriesincludedinthisstudy.Taenia solium porcine cysticercosis was confirmed from all eight countries, whereas only one country (Laos) could confirm the presence of T. asiatica porcine cysticercosis. Province-level occurrence was identified in five countries (Cambodia, Indonesia, Laos, Myanmar, and Vietnam) across 19 provinces. Smallholder pig keeping is believed to be widely distributed throughout the region, with greater densities predicted to occur in areas of China, Myanmar, Philippines and Vietnam. Conclusions: The discrepancies between countries reporting taeniosis and the occurrence of porcine cysticercosis, both for T. solium and T. asiatica, suggests that both parasites are underreported. More epidemiological surveys are needed to determine the societal burden of both parasites. This study highlights a straightforward approach to determine areas at risk of porcine cysticercosis in the absence of prevalence data. Keywords: Taenia solium, Taenia asiatica, Mapping, Tapeworm, Neglected Tropical Disease (NTD), Zoonosis, Pigs, Cysticercosis, Taeniosis, East and Southeast Asia * Correspondence: [email protected] 1One Health Center for Zoonoses and Tropical Veterinary Medicine, Ross University School of Veterinary Medicine, Basseterre, Saint Kitts and Nevis Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Braae et al. Parasites & Vectors (2018) 11:613 Page 2 of 11 Background OR “porcine cysticercosis” OR “pig cysticercosis”)AND Pigs can become infected with Taenia solium or Taenia (“Brunei Darussalam” OR “Cambodia” OR “China” OR asiatica if eggs excreted from human tapeworm carriers “East Timor” OR “Hong Kong” OR “Indonesia” OR “Japan” are ingested. Although, both parasites cause human health OR “Laos” OR “Macau” OR “Malaysia” OR “Mongolia” OR concerns, only T. solium causes neurocysticercosis, which “Myanmar” OR “Burma” OR “Korea” OR “Philippines” OR is a major public health burden globally [1, 2]. In addition, “Singapore” OR “Taiwan” OR “Thailand” OR “Vietnam”). both parasites have an economic impact on livestock sec- The full search output is available in Additional file 1:Table tors. Taenia solium and T. asiatica share the same trans- S1. During the initial search phase, titles and abstracts were mission pathways from humans to pigs, and back to screened followed by full text review, based on the fol- humans again. Parasite transmission can therefore be ad- lowing exclusion criteria: (i) not dealing with porcine dressed with similar intervention approaches. cysticercosis (T. solium or T. asiatica); (ii) no geo- Taenia solium is present throughout the Americas [3], graphical reference provided; (iii) based on experimen- sub-Saharan Africa [4], and believed to be widely en- tal studies or solely on questionnaire surveys; and (iv) demic in East and Southeast Asia [5]. However, informa- data reported were from prior 2000. No language re- tion on the distribution of porcine cysticercosis within strictions were imposed. Only the baseline data from East and Southeast Asia, whether due to T. solium or T. studies testing intervention approaches were extracted. asiatica, is sparse. Due to the relative short life span and Due to the cross-reaction with Taenia hydatigena the limited spatial movement, porcine cysticercosis in- when using serology, data based on serological testing fected pigs are excellent indicators of current local active were omitted if data from tongue or carcass inspection transmission. Keeping pigs in extensive production sys- from the same country were available. Country reports tems whereby access to human waste is more accessible of porcine cysticercosis (T. solium)presence(i.e.“dis- compared to intensive production systems, is considered ease present” or “limited distribution”)intheperiod the main risk factor for porcine cysticercosis in many re- 2005–2017 were also extracted from the OIE database gions [6]. The presence of pigs in extensive systems WAHID Interface [7]. could therefore be used as a first indicator of areas at During the second phase, backward reference searches risk of porcine cysticercosis transmission [3]. The aim of for potential references of epidemiological studies this study was to map, at first-level administrative sub- reporting data from 2000–2018 in any of the target division level, the occurrence of T. solium and T. asia- countries were conducted on all review articles and eli- tica in pigs and areas at risk of transmission to pigs in gible articles found during the first search. Collabora- East and Southeast Asia, based on the occurrence of tors and known researchers from the respective smallholder pig production systems and confirmed re- countries were contacted in efforts to obtain grey lit- ports of porcine cysticercosis (T. solium and T. asiatica). erature containing epidemiological data from the re- quested period. Figure 1 shows a flow diagram of the Methods applied search strategies. Study area In the third phase, if no data on porcine cysticercosis This study covered East and Southeast Asia, which con- could be obtained from a respective target country, a sist of the following countries: Brunei (Negara Brunei country-specific PubMed search was carried out. The Darussalam), Cambodia, China, East Timor, Indonesia, country-specific search was performed to confirm the Japan, Laos, Malaysia, Mongolia, Myanmar, North presence of the parasites in human hosts within the Korea, Philippines, Singapore, South Korea, Thailand respective country during the study period by obtain- and Vietnam. ing reports of human cysticercosis, T. solium taeniosis, or T. asiatica taeniosis, respectively. The country-spe- Data extraction from published and grey literature cific search was performed using the same date restric- Literature searches were carried out to identify epi- tion as previously and using the term, e.g. demiological field surveys or routine slaughter surveys (“neurocysticercosis” OR “cysticercosis” OR “taeniosis” with current data (from year 2000) on the occurrence of OR “taeniasis” OR “Taenia solium” OR “Taenia asia- porcine cysticercosis caused by T. solium and T. asiatica tica”)AND(“Country name”). Only the newest reports infections in East and Southeast Asia. Thus, porcine cys- of human cysticercosis, T. solium taeniosis and T. ticercosis in this paper only concerns T. solium and T. asiatica taeniosis cases were retained, and the data asiatica unless otherwise stated. We performed a litera- only used as national level confirmation of presence if ture search using PubMed (http://www.ncbi.nlm.nih.- the authors provided sufficient evidence to conclude gov/pubmed/) with a date restriction from 1st January the cases were autochthonous. Furthermore, taeniosis 2000 to 30th June 2018, and the search term: (“Taenia cases were only included if infection was determined solium” OR “Taenia asiatica” OR “swine cysticercosis” to the species level. Braae et al. Parasites & Vectors (2018) 11:613 Page 3 of 11 Fig. 1 Flow diagram of the search strategy for epidemiological studies on Taenia solium or Taenia asiatica in pigs Pigs in extensive production systems porcine cysticercosis, and eight of them had sufficient data The distribution of pigs raised in extensive production to provide information on province level distribution systems (smallholder pig keeping) was mapped using (Additional file 1: Table S2). geographical information systems based on modelled Both T. solium taeniosis and T. solium cysticercosis in data
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