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Spatiotemporal distribution and economic loss associated with bovine cysticercosis and human taeniasis in Ethiopia

A metacestode stage (bovine cysticercosis) and adult stage Taenia saginata, accounted for zoonotic and economic losses from organ contamination and treatment cost. The objective of this paper is to assess the spatiotemporal distribution and economic loss from bovine cysticercosis and human taeniasis with treatment approach in different parts of Ethiopia. All available published research articles from Ethiopia on the disease were collected. The data were assessed using the current regional administrative, the locality and chronology of the reports for prevalence and economic loss with treatment trend. Prevalence ranging from 1.9% at Addis Ababa City to as high as of 26.3% Hawasa-SNNPR using postmortem examination. However, one study confirmed 92.7% of 41 isolates as bovine cysticercosis using polymerase chain reaction (PCR) method. Teaniasis was ranged from 7.8% in Modjo-Oromia to as high as 89.4% in Addis Ababa City. Except for 17.9% at Addis Ababa City, 29.0% at Mekele-Tigray and 19.0% at Halaba Kulito –SNNPR teaniasis in Ethiopia were greater than 30% over 2001–2018 years. Questionnaire survey and retrospective data were the major tools used for teaniasis reporting either pharmaceutical and/or traditional (herbs) medicines were used for teaniasis treatments. Niclosamide, mebendazole and praziquantel were pharmaceutical teaniacidal drugs used in Ethiopia until the years of 2009, uses of albendazole begins from 2011 to date (2018 year). Hagenica abyssinia “Kosso/Heto” flowers is still widely used in Ethiopia in that it contains Kosso-toxin, closely related to folic acid, are responsible for some cases of hepatic carcinoma and blindness. Only few data (reports) were available on spatiotemporal economic loss associated with bovine cysticercosis and Taenia saginata in Ethiopia showing an overall 4,052,278.16 ETB (212,202.76 USD) from five reports. Highest economic loss (88,500.00 USD) was registered at Yirgalem-SNNPR [2005–2009]. Study at Kombolcha-Amhara region during 2016 accounted 1,841,311.00ETB (73,652.44 USD) from C. bovis and teaniasis treatment cost. Total cost for the used pharmaceutical drugs accounted 921,112.00ETB over 2005–2016. The maximum drug expenditure was reported during the year 2013. Thus, bovine cysticercosis and Taenia saginata in Ethiopia indicating the health and economic challenges. It needs to Taenia saginata cycle interruption via stopping human open defecation with assessing the dynamics of the disease in the country.


Introduction
Taenia saginata (the adult in human intestine) and its Cysticercus bovis (the metacestode larval stage in active muscle of bovine) (Urquhart et al., 1996;OIE, 2000) occur throughout the world with variable degree of prevalence (Harrison and Sewell, 1991). Poor hygiene and sanitation, poor livestock husbandry practices and inadequate meat inspection and control as well as eating raw or insufficiently cooked meat can be the main risk factors for the spread of the disease (Cabaret et al., 2002). There are 77 million taeniasis patients of which 32 million are in Africa, 11 million in Asia and about 3 million in the new world. Highly endemic areas include Central and East African countries Ethiopia, Kenya, Argentina and in the Mediterranean Region (Syria, Lebanon and Yugoslavia) (Frolova, 1982). Cattle are infected by ingestion of pasture and drinking water contaminated with T. saginata eggs (Teka, 1997). The parasites appear to be specific to cattle, while wild animals play no part as intermediate hosts (Symth, 1994). Variability in degrees of awareness in human infection varies with age, sex, religion, educational level, presence and usage of sanitary facilities especially toilets (Megersa et al., 2010).
Based on routine carcass inspection, the infection rate of bovine cysticercosis is often around 30-60% in developing countries (Minozzo et al., 2002). The organs and tissues most commonly affected and condemned due to C. bovis are the heart, tongue, diaphragm and muscles of the jaw (Dorny et al., 2000;Maed et al., 1996). Besides human-animal health risk, high prevalence in Sub-Saharan Africa, causes an important economic loss due to partial or total condemnation of infected carcasses (Wayne et al., 2002;Tegegne et al., 2018), refrigeration and downgrading of infected carcasses (Fan, 1997) and the cost of drug for human treatment (Tegegne et al., 2018;Abunna, 2013). Chemotherapeutic, herbals medication or combinations of both were frequently used in Ethiopia (Tegegne et al., 2018;Abunna, 2013;Desta, 1995). Thus, different parts of various plants like Hagenica abyssiniaflowers, Cratonmacro satchyus-seed, Embelia schimperi-seed, or Cynadon dactylon-all parts are used. Some of them have certain draw backs and are responsible for hepatic carcinoma and blindness (Desta, 1995). Praziquantel is reported effective for human taeniasis but this is proved impractical because of high cost (Reniecke, 1983).
However, prevalence, spatial epidemiology and associated economic losses from bovine cysticercosis and human taeniasis in Ethiopia were not yet summarized. Therefore, the objective of this paper is to assess the spatiotemporal distribution and economic loss from bovine cysticercosis and human taeniasis with treatment approach in different parts of Ethiopia.

Methods used
All available published research articles on bovine cysticercosis in different time periods were assessed. Similarly published/ none-published reports on Taenia saginata in Ethiopia were assessed. The available data shows reported information on bovine cysticercosis from 1990 to 2018 and on Taenia saginata in Ethiopia from 2001 to 2018 years period different parties Ethiopia.
Focusing on spatiotemporal, treatment trend and associated cost, all reports were categorized. Thus, the current nine (9) administrative regions (Afar, Amhara, Benishangul-Gumiz, Ethio-Somali, Gambella, Harari, Oromia, South Nation Nationalities and People Regional Government (SNNPR) and Tigray Regional States) and the two councils (the Addis Ababa City and Dire Dawa town), the locality and chronology of the reports were considered. With regard to time, reports of bovine cysticercosis were categorized by years from 1990 to 2018 and that of Taenia saginata from 2001 to 2018.
Considering published/none-published date, Taenia saginata treatment trend and the types of drugs used were also assessed. Reported cost of organ and carcasses condemnation as well as treatment were assessed. Again the encored cost was categorized using spatiotemporal and expressed both by Ethiopian Birr (ETB) and United State of American Dollar (USD).

Spatiotemporal distribution of bovine cysticercosis in Ethiopia
Bovine cysticercosis is reported in various countries including Ethiopia, as a major parasite disease responsible for organ condemnation, and public health risk. Prevalence was reported in Ethiopia and showed variable with region, localities and years (Table 1). Except from the Afar, Benishangul-Gumiz and Gambella Regional States as well as the Dire Dawa town, bovine cysticercosis was reported from all other areas at different degrees of prevalence.
Prevalence ranging from 1.9% at Addis Ababa City (Deresse et al., 2012) to as high as of 26.3% Hawasa-SNNPR (Abunna et al., 2007) using postmortem examination. These reports from Ethiopia are below the 30-60% suggested in developing countries (Minozzo et al., 2002). However, Hailemariam et al. (2014) confirmed 92.7% of 41 isolates as bovine cysticercosis using polymerase chain reaction (PCR) method. In Ethiopia, the rural communities mainly raise cattle under extensive husbandry practices.  Existence of higher population density, raw meat consumption, low awareness, poor hygiene and sanitary infrastructures may facilitate transmission of the disease between animals and human beings in the rural area (Frolova, 1982;Feseha, 1995;Teka, 1997). However, variability in degrees of awareness in human infection varies with age, sex, religion, educational level, presence and usage of sanitary facilities especially toilets (Megersa et al., 2010). Using the organ and tissues suggested by Dorny et al. (2000) and Maed et al. (1996), the organs and tissues most commonly affected and condemned due to C. bovis were the heart, tongue, diaphragm and muscles of the jaw (Issa, 1990;Feseha, 1995;Tembo, 2001;Dawit, 2004;Nigatu, 2004;Hailu, 2005

Spatiotemporal distribution of Taenia saginata in Ethiopia
Globally, there were 77 million human carriers of taeniasis of which 40% live in Africa (WHO, 2013). In developed countries even if the disease has very low prevalence, the problem with the removal and treatment facilities in their sewage system plays a great role in the distribution of eggs that can survive longer in sewages (Gracey and Collins, 1992). Due to the habit of eating raw or undercooked beef dishes, habit of defecating in the open grazing fields, human taeniasis is common in Ethiopia (Tolossa et al., 2015;Megersa et al., 2010;Deresse et al., 2012;Teka, 1997). It is highly associated with poor sanitary condition in general and inappropriate human excreta disposal in particular.
Published work on Taenia saginata in Ethiopia was collected and summarized based on the current administrative regions, districts, study methodology and chronological order of the reports (Table 2). Except from the Afar, Benishangul-Gumiz, Gambella and Ethio-Somali Regional States as well as the Dire Dawa town, bovine cysticercosis was reported from all other areas at different degrees of prevalence. This could be due to parallel investigation of both the bovine cysticercosis and Taenia saginata. Teaniasis was ranged from 7.8% in Modjo-Oromia (Deresse et al., 2012) to as high as 89.4% in Addis Ababa City (Tembo, 2001). Except for 17.9% (Deresse et al., 2012) at Addis Ababa City, 29.0% (Abay and Kumar, 2013) at Mekele-Tigray and 19.0% (Abdulaziz et al., 2016) at Halaba Kulito -SNNPR, teaniasis in Ethiopia was greater than 30% over 2001-2018 years. Except for Deresse et al. (2012) who's used stool examination, almost all of the reports were using Questioner survey and retrospective data reports.

Human taeniasis treatment trend in Ethiopia
Still taeniasis in Ethiopia is under-reported, missing many infections owing to the tradition of self-treatment using modern or traditional plant medicines. Tegegne et al. (2018) reported out of the 35 taeniasis patients 19 (54.3%) used pharmaceutical, while 28.6% uses the traditional (herbs) medicine and the remaining 17.2% uses both. Of pharmaceutical, a single dose of praziquantel (10 mg/kg body weight) is effective. Other drugs, albendazole or mebendazole can also be given but they are considered not fully effective (Soulsby, 1982). The uses of niclosamide, mebendazole, praziquantel, albendazole (Abunna, 2013;Megersa et al., 2010;Tolossa et al., 2015;Cheru and Zeryihun, 2017;Tegegne et al., 2018) and vermox (Megersa et al., 2010) in Ethiopia have been reported. Among several traditional drugs (Table 3), Hagenica abyssinia "Kosso/Heto" flowers is still widely used in Ethiopia.
Hagenica abyssinia contains Kosso-toxin, closely related to folic acid, are responsible for some cases of hepatic carcinoma and blindness (Desta, 1995).

Spatiotemporal economic loss from bovine cysticercosis and human taeniasis in Ethiopia
Economic losses from bovine cysticercosis are determined by disease prevalence, grade of animal infected, potential market price of cattle and treatment cost for detainee carcasses. Cysticercosis in domestic animals is a significant food safety problem and causes economic loss in food production. This will be particularly important where export industries are involved, since most importing countries have stringent regulation designed to prevent the importation of infected meat (Harrison and Sewell, 1991). The cost implication can be broken down into those involved in treating human taeniasis and cattle carcasses (costs of freezing, boiling) or condemned, as well as the costs involved in the inspection procedures amount to millions of dollars (Mann, 1984).
Although niclosamide, mebendazole and praziquantel were pharmaceutical teaniacidal drugs used in Ethiopia until the years of 2009, uses of albendazole were began from 2011 to date (2018 year). The total treatment cost for these drugs accounted 921,112.00ETB over 2005-2016 in Ethiopia (Table 5). The maximum drug expenditure was during the year 2013 (Tolossa et al., 2015;Cheru and Zeryihun, 2017).

Conclusion and recommendations
Bovine cysticercosis and its adult (Taenia saginata) are public health and economically significant cestode parasite prevalent in reported regions of Ethiopia. But low area coverage investigations were observed. Mostly postmortem meat inspection in cases of bovine cysticercosis and questioner survey in cases Taenia saginata was implanted as tools of investigation which need other methods like serology and molecular techniques. Although the uses of herbal mediation were reported in Ethiopia, pharmacognosy and dosage formulation of those plants extract could reduce toxicity, replace chemotherapy, prevent associated drug resistance and uses of new drug for Taenia saginata treatment. Taenia saginata cycle interruption via stopping human open defecation could prevent such challenges. (1), 25-30. Abunna, F., Tilahun, G., Megersa, B., Regassa, A., Kumsa, B., 2007. Bovine cysticercosis in cattle slaughtered at Hawassa municipal abattoir, Ethiopia: prevalence, cyst viability, distribution and its public health implication. East Afr. J. Public Health. 4 (2), 73-79. Note*: -= not reported.