Epidemiology of Taenia Saginata Taeniosis/Cysticercosis: a Systematic Review of the Distribution in West and Central Africa Emilie Hendrickx1, Lian F
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Hendrickx et al. Parasites Vectors (2019) 12:324 https://doi.org/10.1186/s13071-019-3584-7 Parasites & Vectors REVIEW Open Access Epidemiology of Taenia saginata taeniosis/cysticercosis: a systematic review of the distribution in West and Central Africa Emilie Hendrickx1, Lian F. Thomas2,3, Pierre Dorny1,4, Branko Bobić5, Ufe Christian Braae6,7, Brecht Devleesschauwer8,9, Ramon M. Eichenberger10, Sarah Gabriël8, Anastasios Saratsis11, Paul R. Torgerson10, Lucy J. Robertson12 and Veronique Dermauw1* Abstract Background: The zoonotic tapeworm Taenia saginata, although causing only minor discomfort in humans, is responsible for considerable economic losses in the livestock sector due to condemnation or downgrading of infected beef carcasses. An overview of current knowledge on the distribution and prevalence of this parasite in West and Central Africa is lacking. Methods: We conducted a systematic review, collecting information on published and grey literature about T. sagi- nata taeniosis and bovine cysticercosis from 27 countries/territories in West and Central Africa, published between January 1st, 1990 and December 31st, 2017. Results: The literature search retrieved 1672 records, of which 51 and 45 were retained for a qualitative and quan- titative synthesis, respectively. Non-specifed human taeniosis cases were described for Nigeria, Cameroon, Senegal, Burkina Faso, Democratic Republic Congo, Guinea, and Ivory Coast (seven out of 27 countries/territories), while T. sagi- nata taeniosis specifcally was only reported for Cameroon. Most prevalence estimates for taeniosis ranged between 0–11%, while three studies from Nigeria reported prevalence estimates ranging between 23–50%. None of the studies included molecular confrmation of the causative species. The presence of bovine cysticercosis was reported for Benin, Burkina Faso, Cameroon, Central African Republic, Chad, Democratic Republic Congo, Ghana, Guinea, Ivory Coast, Mali, Niger, Nigeria, Senegal, and Tristan da Cunha (14 out of 27 countries/territories). Prevalence estimates ranged between 0–29%. Conclusions: Our systematic review has revealed that human taeniosis and bovine cysticercosis are seriously under- studied in West and Central Africa. The high prevalence estimates of both conditions suggest an active dissemination of this parasite in the region, calling for a concerted One Health action from public health, veterinary health and food surveillance sectors. Keywords: Taenia saginata, Cysticercosis, Cattle, Beef, Tapeworm, West Africa, Central Africa *Correspondence: [email protected] 1 Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium Full list of author information is available at the end of the article © The Author(s) 2019. 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. Hendrickx et al. Parasites Vectors (2019) 12:324 Page 2 of 10 Background while the semi-arid and sub-humid zones in the area are Te tapeworm Taenia saginata is one of three Taenia characterized by mixed crop-livestock farming systems species that infect humans as their defnitive host, with [8]. bovines serving as the intermediate host. Humans acquire As a summary of existing knowledge on the occur- T. saginata infection after consuming undercooked beef rence of T. saginata taeniosis and bovine cysticercosis in containing viable cysticerci. Te adult tapeworm resides the area is presently lacking, and as part of a coordinated in the small intestine, where it becomes patent within efort to document the global distribution of T. saginata approximately ten weeks. At that moment, the strobila [9–14], we undertook a systematic review of the occur- may have reached a length of up to three meters [1], and rence of this parasite in West and Central Africa. gravid proglottids can contain up to 100,000 taeniid eggs. Tese eggs are voided during and between defecation [2], Methods and have the potential to survive for a long time without Search strategy hatching. Eggs found in faecal material and eggs within We conducted a systematic review aiming to gather cur- soil have been documented to remain viable for up to 9.5 rent knowledge on the occurrence, prevalence and geo- months [3]. Contaminated pastures, water and feed are graphical distribution of human taeniosis and bovine a source of infection for cattle. Following ingestion, the cysticercosis in West and Central Africa, published early larval stages (oncospheres) hatch and the hexacanth between January 1st, 1990 and December 31st, 2017. A larvae migrate, utilising the lymphatic and blood system, complete study protocol is available in Additional fle 1: to the muscle tissue. Here the larvae mature into the Text S1. In the context of this study, West and Cen- metacestode stage, called cysticerci [4]. tral Africa was defned as the area covering the follow- Unlike Taenia solium, for which humans can also act as ing 27 countries/territories: Ascension, Benin, Burkina a dead-end intermediate host leading to the debilitating Faso, Cameroon, Cape Verde, Central African Republic, and stigmatising disease neurocysticercosis, human T. Chad, Republic of the Congo, Democratic Republic of saginata infections are restricted to the defnitive (adult the Congo (DR Congo), Equatorial Guinea, Gabon, Te tapeworm) stage, which has a more limited public health Gambia, Ghana, Guinea, Guinea-Bissau, Ivory Coast, burden. Taenia saginata taeniosis is generally asympto- Liberia, Mali, Mauritania, Niger, Nigeria, Saint Helena, matic or associated with mild abdominal discomfort, Sao Tome and Principe, Senegal, Sierra Leone, Togo although more serious complications, including appen- and Tristan da Cunha. Although Angola is classifed as dicitis, intestinal obstruction and gall bladder perforation being part of Central Africa, it is also classifed as being have occasionally been documented [3]. Bovine cyst- part of southern Africa, and data from this country were icercosis, however, may result in substantial economic included in an equivalent systematic review of southern losses generated for the food industry because of meat and eastern Africa [14]. condemnation, treatment processing costs and an over- Te international scientifc databases Web of Science all reduction in the product value [5]. Moreover, the meat (http://ipsci ence.thoms onreu ters.com/produ ct/web-of- inspection process itself requires substantial (veterinary) scien ce/) and PubMed (http://www.ncbi.nlm.nih.gov/ public health sector investment and there are costs asso- pubme d) were searched using the following combina- ciated with treatment seeking behaviour, diagnostics, and tion of key words: (cysticerc* OR cisticerc* OR “C. bovis” treatment of human taeniosis cases [5, 6]. OR taenia* OR tenia* OR saginata OR taeniosis OR Taenia saginata is considered to have a global distri- teniosis OR taeniasis OR ténia OR taeniid OR cysticer- bution, with higher prevalences in low-income regions que) AND (Ascension OR Benin OR “Burkina Faso” where sanitation standards may be poor, and the meat OR Cameroon OR “Cape Verde” OR “Central African inspectorate services are often poorly funded and Republic” OR Chad OR Congo-Brazzaville OR DRC OR understafed. Congo OR “Cote d’Ivoire” OR “Equatorial Guinea” OR In West and Central Africa, the cattle population Gabon OR Gambia OR Ghana OR Guinea OR Guinée amounts to 120 million heads [7]. While West Africa OR Guinea-Bissau OR Liberia OR Mali OR Mauritania mainly consists of arid (and to lesser degree semi-arid OR Niger OR Nigeria OR “Saint Helena” OR Sao Tome and sub-humid) agro-ecological zones, Central Africa OR Principe OR Senegal OR “Sierra Leone” OR Togo OR predominantly consists of humid zones (with some “Tristan da Cunha”). Moreover, databases for MSc/PhD sub-humid zones as well) [8]. In the purely humid agro- theses and grey literature (Additional fle 2: Text S2) were ecological zones, cattle production is not considered an searched using the same search phrase. Furthermore, the important economic activity due to the presence of dis- OIE databases “Help with World Animal Disease Sta- eases such as trypanosomiasis [8]. In the arid zones, pas- tus” (“Handistatus”, 1996–2004) [15] and “World Animal toralism is the most commonly cattle production system, Health Information System” (“WAHIS”, 2005) [16] were Hendrickx et al. Parasites Vectors (2019) 12:324 Page 3 of 10 consulted to extract data on bovine cysticercosis for the residents [18] both in Nigeria). Tree other studies per- study area. Finally, reference lists of relevant reviews were formed in Nigeria; however, they reported much higher screened for additional records. prevalence estimates: 23% in primary schoolchildren [19], 33% in rural schoolchildren [17] and even 50% in Selection criteria pre-school-age children (aged between 0 and 71 months) Te PRISMA guidelines were followed for reporting [20]. In four other studies, excluded from the quantita- the review (Additional fle 3: Table S1). Briefy, dupli- tive synthesis, the presence of T. saginata taeniosis was cate records