Current Status of Prevalence, Possible Control and Risk Factors Associated with Porcine Cysticercosis from Endemic Countries in Africa

Porcine cysticercosis (PC) caused by Taenia solium larvae is continuing being an important zoonotic neglected disease in many developing countries, is responsible for severe health disorders such as seizures and death in human and it poses a serious public health risk. In general estimated prevalence for porcine cysticercosis by Ag-ELISA was 29.7% (95% CI [4.8 58.2]), by EITB was 24.7% (95% CI [9.2 38.2]), by Tongue examination was 9.4% (95% CI [0.2 13.2]), and by postmortem examination was 15% (95% CI [0.2 27.4]). Average seroprevalence of human cysticercosis by circulating antibody detection (Ab-ELISA) was ranged from 1.3% to 45.3%. Average seroprevalence of human cysticercosis by circulating T. solium antigen detection (Ag-ELISA) was ranged from 4.6% to 11.9%. Average seroprevalence of human cysticercosis by EITB was ranged from 6.9% to 16.7%. Average prevalence of human cysticercosis by CT scan was ranged from 23.2% to 54.6%. A fundamental factor in the occurrence of infections in most of the article was lack of health education to the community on T. solium, cysticercosis and taeniasis complex as the key towards control and eradication. The major causal factors of the disease occurrence were free roaming pigs and poor sanitary conditions.


Introduction
Porcine cysticercosis is an infection of pigs with the larval form of Taenia solium [1].Pig production is an important economic activity to many poor families in developing countries [2] [3] [4] [5] [6] (Wilson, 2013).However, T. solium cysticercosis is being reported in these countries resulting in both agricultural and public health impacts [7]- [15].The parasite causes taeniosis in human, who is the definitive host and cysticercosis in pigs which are principal intermediate hosts.Human being acquires taeniosis following ingestion of raw or undercooked pork infected with viable T. solium cysticerci [16] [17] [18].The human being also can develop cysticercosis following accidental ingestion of T. solium eggs.Lodging of cysticerci of T. solium in the brain results in neurocysticercosis (NCC), one of the most important neurological parasitoses in human and the main preventable cause of acquired epilepsy in endemic areas [12] [19].Neurocysticercosis is now recognized as an important public health problem in both developing and developed countries [3].The study area consisted of 54 countries.The total population of pigs estimated in Africa in 2013 was 33,465,868, which was approximately 3.4% of the world pig population estimate 977,274,246 of 2013 [20].Out of the Africa regional pig population, approximately 0.23%, 6.07%, 41.3%, 17.3%, and 35.1% were reared in the northern countries, southern, western, central, and eastern Africa respectively.
Porcine cysticercosis has been reported in many sub-Saharan countries with prevalence rates as high as 18% to 64% [13] [21] [22] [23] [24] [25].In East African countries, the prevalence of cysticercosis infection among pigs in a number of areas reported being approximately 20% [13] [26] [27] [28].Endemicity of T. solium cysticercosis in developing countries have been associated with general poverty, free-ranging of pigs, poor sanitary conditions and poor knowledge about the parasite [13] [27] [29]- [34].In addition, home slaughters of pigs without inspection, and inadequate pork cooking before consumption were also found to be responsible for the reported prevalence [26].
In Africa pig keeping is the common and free-range type of pig management which is practiced [35].This review investigated the prevalence of porcine cysticercosis, distribution, possible control of disease and risk factors associated with T. solium cysticercosis transmission in Africa.The information is useful in planning parasite control measures in Africa to promote economic development through pig production.

Sites for Review Study
The search of the literature for this review was well organized pertaining to the prevalence of porcine cysticercosis and risk factors for T. solium in the district, country and regionally based studies carried out in endemic countries in Africa also few studies about human cysticercosis or taeniasis.And it was performed on lating antibody and antigen that detected by Enzyme-linked Immunoelectrotransfer Blot (EITB) or by enzyme-linked immunosorbent assay [36].
1) Antemortem (tongue palpation and small incision) and post mortem meat inspection were widely used in Africa for diagnosis of porcine cysticercosis.
However on the other hand, both methods are limited on sensitivity [37].
Antemortem by tongue examination/palpation to check for the presence of cysticerci.Because the prevalence of pigs with Tongue examination/palpation do relate to the prevalence of heavy infection.The data on this method were from [14] [26] [38] [39].

6) Porcine cysticercosis reports from the World Organisation for Animal
Health.
The understandable data about prevalence of porcine cysticercosis was collected to the accessible selected articles and there was no limitations meant for the diagnostic technique was made.Although it was well known that the porcine cysticercosis or taeniasis data would be biased by the technique used because of the difference of prevalence's results found such as Seroprevalence and other methods have large variations in their diagnostic performances.Ag-ELISA has

Selected Study
All countries where the selected studies took place were visualized using Google map.In the beginning we assessed every title and abstract prior to assess the full document/text; Authors of articles where full-text were inaccessible were contacted to gather scientific publications associated to porcine cysticercosis in each country and some we used Sci Hub; to remove barriers.When an appropriate article was encountered, required information such as diagnostic method, Results (disease magnitude), and sample size was recorded when accessible.
Available information were collected from 89 study locations which the study sites were located in 19 countries across Africa that reported the prevalence of whether documented as porcine cysticercosis, human cysticercosis, neurocysicercosis, taeniosis, or Taenia solium was included whether it was diagnosed by the following protocols/methods; epidemiological survey (questionnaires, environmental studies, antemortem, postmortem), and serological examination, for human cysticercosis or taeniasis by Ab-ELISA, Ag-ELISA and Coprology.Other criteria were; random sampling method for selection of pigs in the study or number of sample size, and authors for all the articles used were cited.The most up to date literature was preferred.

Excluded Study
The studies that performed and published before the year 2001 was excluded, all repeated studies from the title selection in the same country was excluded, studies based on questionnaire only were excluded for porcine cysticercosis prevalence [76].Also environmental only studies was excluded, Wrong parasite species e.g.[77], Studies performed in non-endemic countries or if based on experimental studies where location of infection could not be established, only clinical studies e.g.[37], Studies carried out for assessing laboratory tests performance, For human cysticercosis or taeniosisi Studies that focused on NCC only e.g.[15].Articles written in languages other than those spoken or understood by all authors of this review some articles in west Africa countries was written in French e.g.[78], if full-text was not available (Figure 1).

Data Collection
The following topics/items were collected and opened in a data base as of all preferred article: 1) Author(s) For example; Seria M.  In addition, if the study was conducted and associated with an analysis lying on porcine cysticercosis or associated with human taeniasis, the prevalence and the method used to diagnose cysticercosis and taeniasis were as well collected.

Statistical Analysis
The averages of prevalences in each method were used to estimate general prevalences.We calculated the average Seroprevalence of circulating antigens T. solium, Seroprevalence for antibodies, the prevalence of Tongue examination, and postmortem in each country of Africa that was selected in this review.Also average of Ninety five% Confidence Intervals (95% CI) were calculated for all reported prevalence's.The significant differences in estimated prevalences were evaluated using their 95% confidence intervals.The variations in prevalence between the selected countries were well thought out to be statistically significant if their 95% confidence intervals do not extend beyond.

Porcine Cysticercosis in Africa
From the sixty eight (68) 1.
By using the above results on Table 1 indicated that the estimated prevalence of porcine cysticercosis in Africa was low as there were no data or old data in some countries.

Prevalence of Human Cysticercosis in Some Countries in Africa
As summerised in Table 3, Twenty number of articles were included in this review for human cyaticercosis/taeniasis from ten countries from which; One (1) was studied for both methods (Ab-ELISA, Ag ELISA, EITB, and Coprology), Six (6) were studied for circulating antibody and antigen (Ab-ELISA and Ag-ELISA), Seven for only circulating antibody, One (1) was studied for only CT scan, and One (1) was studied for only Coprology.
Average seroprevalence of human cysticercosis by circulating antibody detection (Ab-ELISA) were ranged from 1.3% to 45.3%, Average seroprevalence of human cysticercosis by circulating T. soliumantigen detection (Ag-ELISA) were ranged from 4.6% to 11.9%.Average seroprevalence of human cysticercosis by EITB were ranged from 6.9% to 16.7%.Average Prevalence of human cysticercosis by CT scan was ranged from 23.2% to 54.6% (Table 3).

Risks Factors Associated with Active Human Cysticercosis
According to the study in Zambia by Mwape and colleagues 2015 [118] demonstrated that Seropositivity was significantly positively related to age but not related to gender.cysticercus antigens increased significantly in individuals above the age of 30.But Copro-Ag positivity was not related to age or gender.Many studies showed that significantly higher sero-Ag to the age of 60 years.Previous studies have indicated higher levels of active infection in elderly people, may be  due to a lowered host immune response [22].
The study in Tanzania by Mwanjali and colleagues 2013 [47] revealed that being older age had high risk for seropositivity with human cysticercosis in the regression model, because they found that Ag-ELISA was higher in the age groups 36 -45 years (OR = 2.5) and 46 -60 years (OR = 2.6) as compared to young people < 25 years.In contrast, human cysticercosis by Ab-ELISA in the regression model, the study demonstrated the risk for seropositivity that related to gender as was found to be significantly higher for males as compared to females and was related to family history as was found to be significantly higher for people using an unsafe source of water.

Continent Distributions of the Endemic Countries Where Studies Were Held
Prevalence of Porcine Cysticercosis, Human Taeniosis/Cysticercosis data reported using different diagnostic techniques, of the checked information; Forty three (43) studies were from nine countries in east Africa, Three (3) studies were from one (1) country in Southern Africa, Ten studies were from five countries in west Africa, Two (2) studies were from one (1) country in Northern Africa, Seven studies were from four (4) countries in Central Africa.In these studies, clear prevalence on porcine cysticercosis varied from 0.2% to 56% as results shown in Table 1.

Risk Factors for Porcine Cysticercosis and Human Cysticercosis in Africa Countries
Of the 161 articles selected out of it 72 Articles were reported risk factors for the In rural areas pig production can be classified into three main categories [103] scavenging/free range system where the pig finds most of its own food, and semi-intensive and intensive systems where the majority of the food consists of domestic kitchen waste.About 90% of pigs are reared under scavenging/free range and semi-intensive in Western and Central African countries

Discussion
Generally, pork or pig-meat products are consumed in Africa, but in Islamic countries it is prohibited and there were few or no data in Islamic countries.
Many counties of Africa Continent well liked keeping pigs, though, there has been no study that has evidently described the outline overall status of porcine cysticercosis and overall clear outline of pig production in Africa continent [8] [153].In actuality, porcine or swine cysticercosis is the result of pig ingesting Taenia solium egg coming from human feces containing tapeworm egg that may perhaps have acquired the cyst from pork meat either locally produced or transported from other endemic regions [154] [155] [156] [157].For that reason this review was important in order to understand the currency prevalence of porcine cysticercosis in the continent as well as pig production, in view of the fact that, Africa is one of the continents where the full cycle of T. solium is taking place because of the favorable environmental situation or behavioral conditions enhancing egg distribution and survival and also because of poverty, which holds back application of efficient control measures for the parasite, because the presence of circulating antigens at a population level is the outcome of viable cysticerci in pigs.The predicted prevalence of porcine cysticercosisin circulating antigens and antibodies detection test in each country were higher than the predicted Prevalence of porcine cysticercosis using tongue examination and postmortem in the same country, but this difference was only statistically significant for Tanzania, Kenya, Uganda, South Africa, and Mozambique.There was observation of a significantly higher seroprevalence of porcine cysticercosis by antigen and antibody detection for studies that carried out both Tongue examination, postmortem, antigen and antibody detection tests.This distinct difference in the seroprevalence of circulating antigens or antibodies with Tongue examination or postmortem as observed by [59] [63] [72] [73] as shown in Table 3.
In this review, free range pig rearing, insufficient latrines or poor use of latrines [13] [33] [89], insufficiency sanitary [144], lack of health education to the community were reported as a significant risk factor both for the presence of circulating antigens and/or antibodies, Tongue examination and postmortem Table 3.Most studies revealed that the presence of pigs and the consumption of pork were also acknowledged as significant risk factors in favor of introduction of disease in the area [160].
At the time of writing this review there were no data about pigs reported for Djibouti, Comoros, Mauritania, Eritrea, Libya, Sudan, and Southern Sudan.This suggesting probably absence of pigs or insignificant pig rearing in the countries could be due to lack of professional for animal data collection in the country, or This review demonstrated the prevalence of porcine and human cysticercosis and exposure to the parasite in endemic countries in Africa, suggests that further studies have to be done in Africa to develop rapid tests serviceable at the farm level so that to detect infected animals in farms in order to offer safe meat for neighborhood demand.We recommend for additional studies because there is limited information on the prevalence of porcine cysticercosis in some countries in Africa because of non-availability of appropriate diagnostic facilities in various settings where these infections are widespread and no published articles on pig population and porcine cysticercosis from northern Africa.Most countries have old information such as Senegal, Gambia, Zimbabwe and Togo (e.g.[161] for Togo) therefore this study suggests that T. solium infection is more widespread than these data reported here because of insufficiency data as many countries with unknown data.The rapid epidemiological tool for evaluation of the prevalence of porcine cysticercosis is tongue examination for cyst, although further justification and refinement is necessary using standardized data sets.
High prevalence of porcine cysticercosis was observed in many articles in Africa with traditional pig rearing practices and villages with lack knowledge of the disease.In order to be successful, veterinary and medical public health services be supposed to find out foci of the disease transmission and work out on control strategies such as research, surveillance and control activities although will be needy on the presence of appropriate infrastructure.Therefore exposure was mostly related to environmental factors which varied from country to country.
The appropriate method to eliminate the problem is by using combination treatment by drugs or vaccine that expel parasitic worms (antworms) so that can eliminate existing infections in pigs and human, combined with increasing awareness as discussed about the risk factors.

Figure 1 . 8 )
Figure 1.A flow chart for the inclusion process of literatures analyzed.
presence of Taenia solium as causes of porcine Cysticercosis and human cysticercosis.The management systems used by pig farmers in Africa are dogged by an assortment of causes as well as the source of feed, Deficient of financial resource for animal houses, feeding and health concern obligations[8] [13] [30] [70] [76] [88] [89] [90] [120] [125] [139] [140] [141] [142].The famous risk factors for the presence of porcine Cysticercosis and human taeniosis/cysticercosis were: Inadequate research attention and investments in pig production [76],Free range pig rearing(Penrith et al., 2007), insufficient latrines or poor use of latrines because of foul odors, flies, latrine deluging and lack of privacy as no an exceptional concern to be given to construction of latrines to be easy to people with disabilities, old people and children[13] [33] [104] [114] [133], insufficiency sanitary for example Poor sanitation carried out in slaughterhouses [42] [46] [143] [144] health education to the community [104] [143] [145].Keeping pig for long time as increased risk with age [31] [35] [57] [59] [74] [98] [107][120][146] lack of potable water and poor personal and house hygiene[15] undercooked pork consumption, Free-roaming of pigs and Poor sanitary conditions acknowledged as significant risk factors for porcine cysticercosis are habitually associated to the low level of education stuck between the pig farmers that limits their knowledge on the management of pigs[30] [125].Almost absolute unawareness of the T. solium life cycle concerning pigs and humans (taeniosis and neurocysticercosis) has been reported within studies carried out in Africa[33] [34]  [59][147].Good numbers of farmers in endemic areas are familiar with on the subject of the cysts in infected pigs, although a small number of farmers are conscious of how pigs acquire the infection[32] [33] [47] [57][108] [147][148].

[ 13 ]
[15] [37] [60][149].In these pig production systems, poor sanitary conditions play an important role in the circulation of T. solium infection[14].A free-range production system for pigs combined with open field defecation by humans are the conditions in which the animals can gain access to human faeces[28] [32] [33] [75] [146] [150].Intensive pig production systems do not always eliminate T. solium transmission because in Cameroon for instance some farmers are known to defecate directly in the pigsties [151].The characteristics of traditional pig production systems favoring T. solium taeniosis/cysticercosis in Eastern and Southern African countries are largely similar to those reported in West and Central Africa [9] [27] [30] [32] [71] [125].Pig keeping is predominantly of the smallholder, traditional type, characterized by a free-range management system [12] [30] [72] [114] [125] [152] South Africa and Ethiopia.

Table 1 .
Summery showing population of pig, prevalence of porcine cysticercosis recorded in each country in Africa from year 2001 to 2017.
DOI: 10.4236/wjv.2018.8300660 World Journal of Vaccines about 378 articles about Taenia solium but, no more than 161 studies were included, since some data were too old to be included in this review.More than 2 S. M. Shonyela et al.DOI: 10.4236/wjv.2018.8300661 World Journal of Vaccines studies were selected from each country in Africa.

Table 2 .
Diagnostic tests used for the estimating prevalence of porcine cysticercosis in Africa were.

Table 3 .
Summery prevalence of human cysticercosis/taeniosis in Africa from few selected studies.
The information presented in this review assessed a number of literatures details of the current status of porcine cysticercosis in each country of Africa based on available scientific literature on: tongue/lingual palpation, postmortem and seroprevalence.The outcome of this review allowed us to estimate the preva- circulating antigens and antibodies not recorded in whichever other part of the Africa (57%, 56.6% and 41.2%,, respectively).The statistics recommend a higher incidence of porcine cysticercosis in Tanzania, Kenya, Uganda, South Africa, Zambia, Mozambique and Democratic Republic of Congo (DRC), at the same time as compare to Senegal, Gambia, Zimbabwe, Madagascar and Burundi.
drought such as northern Africa region, also likely because most of the inhabitants in the region are Muslims.In the northern Africa countries there was no data available with regard to prevalence of porcine cysticercosis possibly because of non-availability of proper diagnostic facilities in the area or no pigs.Some countries had old data such as Togo, Egypt, Senegal, Gambia, Togo, and Guinea and Central African Republic.Not all the studies offered details of the studied in sequence such as number of pigs in representativeness of each age group, health status of the pig such as presence of other pathogens that could have interfered when characterizing and comparing prevalence figures.Also were no studies selected for this review reported the presence of adult tapeworms in pigs' even postmortem studies concentrated only on muscle diagnosis but not intestinal diagnosis.