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 abyssinia–flowers, 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).

Over a period of years, investigation on the prevalence of Taenia saginata in human and C. bovis in beef with economic significance of the diseases has been done in different parts of Ethiopia (Feseha, 1995; Tembo, 2001; Dawit, 2004; Nigatu, 2004; Hailu, 2005; Abunna et al., 2007; Bedu et al., 2011; Mesfin and Nuradddis, 2012; Abay and Kumar, 2013; Terefe et al., 2014; Abate, 2014; Tolossa et al., 2015; Hiwot, 2016; Abdulaziz et al., 2016; Cheru and Zeryihun, 2017; Dereje, 2017; Tegegne et al., 2018; Tamirat et al., 2018) in the forms of fragment. The prevalence and spatial epidemiology of cysticercosis in slaughtered cattle from Brazil were assessed by Dutra et al. (2012).

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.

Table 1

Spatiotemporal distribution of bovine cysticercosis in some regions of Ethiopia [1990–2018].

Region/council	Location	Study method	Number of samples	Prevalence in %	Reference	Year¶
Oromia	Nekemt	PME	740	21.7	Issa, 1990	1990
Oromia	Bishoftu,	PME	396	13.85	Getachew, 1990	1990
Amhara	Bahir Dar	PME	486	19.4	Mulugeta, 1997	1997
Addis Ababa	A.A.C.	PME Serology	732	7.5	Nigatu, 2004	2004
Oromia	Mojo	PME,	768	17.6	Hailu, 2005	2005
SNNPR	Hawasa	PME	400	26.3	Abunna et al., 2007	2007
Oromia	Jimma	PME	500	4.4	Megersa et al., 2010	2010
Oromia	Ziway	PME	400	3.0	Bedu et al., 2011	2011
Addis Ababa	A.A.C*	PME	44,000	1.9	Deresse et al., 2012	2012
Oromia	Mojo	PME	17,000	8.5	Deresse et al., 2012	2012
SNNPR	W.S.T.**	PME	380	2.6	Dawit et al., 2012	2012
SNNPR	Yirgalem	PME	400	12.0	Abunna, 2013	2013
Tigray	Mekelle	PME	1023	7.2	Abay and Kumar, 2013	2013
Tigray	Shire	PME	439	5.2	Belay and Mekelle, 2014	2014
Harari	Harar	PME	898	19.7	Terefe et al., 2014	2014
Oromia	Bishoftu	PME	430	5.6	Emiru et al., 2014	2014
Ethiopia	Different	PCR	41	92.7	Hailemariam et al., 2014	2014
Oromia	Adama	PME	384	2.6	Tolossa et al., 2015	2015
Amhara	Gondar	PME	768	3.0	Motbaynor and Terefe, 2015	2015
Amahara	Gonder	PME	400	2.25	Kinfe et al., 2016	2016
Amahara	Gonder	PME	450	2.0	Adem and Alemneh, 2016	2016
Oromia	Bishoftu	PME	700	5.4	Hiwot, 2016	2016
Tigray	Mekelle	PME	1800	22.2	Getachew et al., 2017	2017
Oromia	Nekemt	PME	600	15.5	Dereje, 2017	2017
Oromia	West Arsi	PME	768	4.94	Kebede, 2017	2017
Ethio-Somali	Jijiga	PME	400	2.25	Biruk, 2017	2017
Amahara	Gonder	PME	400	5.5	Cheru and Zeryihun, 2017	2017
Amhara	Bahir Dar	PME	480	4.2	Tamirat et al., 2018	2018
Amhara	Kombolcha	PME	234	8.97	Tegegne et al., 2018	2018

Note: ¶Year = year of report; *A.A.C. = Addis Ababa City; **W.S.T = Wollayita Soddo Town.

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; Abunna et al., 2007; Bedu et al., 2011; Mesfin and Nuradddis, 2012; Abay and Kumar, 2013; Terefe et al., 2014; Abate, 2014; Tolossa et al., 2015; Hiwot, 2016; Abdulaziz et al., 2016; Cheru and Zeryihun, 2017; Dereje, 2017; Tegegne et al., 2018; Tamirat et al., 2018).

Except for Nigatu (2004) whose used detailed postmortem (PME) with Serology and Hailemariam et al. (2014) whose used PCR, almost all investigations in Ethiopia were based on detailed PME.

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.

Table 2

Spatiotemporal distribution of human taeniasis in some regions of Ethiopia [2001–2018].

Region/council	Locations of study	Study method	No. of sample	Prevalence in %	Reference	Year¶
Addis Ababa	A.A.C	Questionnaire	–	89.4	Tembo, 2001	2001
SNNPR	W.S.T	Questionnaire	–	62.5	Dawit, 2004	2005
SNNPR	Hawasa	Questionnaire	120	64.2	Abunna et al., 2007	2007
Oromia	Jimma	Questionnaire	60	56.7	Megersa et al., 2010	2010
Oromia	Ziway	Questionnaire	120	56.7	Bedu et al., 2011	2011
Oromia	Mojo	Stool exam.	90	7.8	Deresse et al., 2012	2012
Addis Ababa	A.A.C	Stool exam.	134	17.9	Deresse et al., 2012	2012
SNNPR	Hawassa	Questionnaire	192	44.0	Mesfin and Nuradddis, 2012	2012
Tigray	Mekelle	Questionnaire	7171	29.0	Abay and Kumar, 2013	2013
SNNPR	Yirgalem	Questionnaire	170	70.0	Abunna, 2013	2013
Harari	Harar	Questionnaire	300	60.7	Terefe et al., 2014	2014
Oromia	West Shoa	Questionnaire	110	63.6	Abate, 2014	2014
Oromia	Bishoftu	Questionnaire	100	64.0	Emiru et al., 2014	2014
Oromia	Adama	Questionnaire	200	45.5	Tolossa et al., 2015	2015
SNNPR	Halaba Kulito	Questionnaire	100	19.0	Abdulaziz et al., 2016	2016
Oromia	Bishoftu	Questionnaire	200	69.5	Hiwot, 2016	2016
Amahara	Gonder	Questionnaire	130	33.1	Cheru and Zeryihun, 2017	2017
Oromia	Assela	Questionnaire	125	71.2	Elemo et al., 2017	2017
Amhara	Gondar	Questionnaire	400	33.07	Cheru and Zeryihun, 2017	2017
Oromia	Nekemt	Questionnaire	80	60.0	Dereje, 2017.	2017
Amhara	Kombolcha	Questionnaire	110	31.82	Tegegne et al., 2018	2018
Amahara	Bahir Dar	Questionnaire	69	30.4	Tamirat et al., 2018	2018

Note: ¶Year = year of report; *A.A.C. = Addis Ababa City; **W.S.T = Wollayita Soddo Town; – = studied number of sample were not accessed; Stool Exam. = stool examination.

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).

Table 3

Major taeniacidal herbs used in Ethiopia.

Scientific name	Local name	Parts used	Traditional formulation/dosage forms
Hagenica abyssinia	Kosso	Flowers	Aqueous/hydroalchoholic extract
Cratonmacro satchyus	Bisanna	Seed	Paste in honey
Embelia schimperi	Enkoko	Fruits	Aqueous/hydroalchoholic extract
Cucurbita pepo	Dubafire	Seed	Fried and salted
Thymus serrulatus	Tosigne	Seed	Paste in honey
Cynadon dactylon	Serdo	All parts	Paste in honey
Myrsine africana	Kechemo	Flower	Aqueous
Glinus lotoides	Mettere	Flower	Aqueous

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).

Only few data (reports) were available on spatiotemporal economic loss associated with bovine cysticercosis and Taenia saginata in Ethiopia (Table 4) showing an overall 4,052,278.16 ETB (212,202.76 USD) from five reports (Abunna, 2013; Megersa et al., 2010; Tolossa et al., 2015; Cheru and Zeryihun, 2017; Tegegne et al., 2018). An annual losses due to treatment in USA was USD 100,000 (Roberts, 1985), in South Africa USD 428 million (Abdusslam, 1975). In Kenya and Botswana bovine cysticercosis resulted in annual losses of USD 4 million and USD 2 million respectively (Grindle, 1978). Highest economic loss (88,500.00 USD) was registered at Yirgalem-SNNPR. This could be due to five years [2005-2009] reports from teaniasis treatment cost only. However, in another study at Kombolcha-Amhara region during 2016 was the highest and accounted 1,841,311.00ETB (73,652.44 USD) (Tegegne et al., 2018) which could be due to economic loss from C. bovis and teaniasis treatment cost.

Table 4

Economic loss associated with taeniasis/cysticercosis in Ethiopia [2005–2016].

Region/councils	location	Year(s)	Total cost*		Remarks	Reference
			ETB	USD
SNNPR	Yirgalem	[2005–2008]	1,416,093.00	88,500.00	TcDC	Abunna, 2013
Oromia	Jimma	[2007–2008]	222,706.00	22,270.60	TcDC	Megersa et al., 2010
Oromia	Adama	[2011−2013]	378,609.66	18,379.11	TcDc	Tolossa et al., 2015
Amahara	Gonder	[2013–2014]	193,558.50	9400.61¶	TcDC	Cheru and Zeryihun, 2017
Amahara	Kombolcha	[2016]	1,841,311.00	73,652.44	TcDC + OC	Tegegne et al., 2018
Total			4,052,278.16	212,202.76

Note: *ETB to USD exchange currency varies with year; ¶calculated from Tolossa et al., 2015; TcDC = taeniacidal drugs cost; OC = organ condemnation.

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).

Table 5

Frequently used teaniacidal pharmaceutical drugs and the associated cost in Ethiopia [2005–2016].

Frequently used drugs	Abunna, 2013					Tolossa et al., 2015			Cheru and Zerihun, 2017		Tegegne et al., 2018	Total
	2005	2006	2007	2008	2009	2011	2012	2013	2013	2014	2016
Niclosamide	16,267	16,503	15,382	16,697	16,131	6448	7648	10,448	4764	4857	690	115,835
Mebendazole	69,502	66,759	69,736	68,671	68,717	54,541	55,410	164,256	4467	4898	12,155	639,112
Praziquantel	9943	9797	9975	9753	8180	1993	2786	3972	9756	8876	2326	77,357
Albendazole*	–	–	–	–	–	12,458	13,997	44,552	5354	7997	4450	88,808
Total	95,712	93,059	95,093	95,121	93,028	75,440	79,841	223,228	24,341	26,628	19,621	921,112

Note*: – = not reported.

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.