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  • Review
  • Open Access

Epidemiology of Taenia saginata taeniosis/cysticercosis: a systematic review of the distribution in southern and eastern Africa

Parasites & Vectors201811:578

https://doi.org/10.1186/s13071-018-3163-3

  • Received: 26 July 2018
  • Accepted: 22 October 2018
  • Published:

Abstract

Background

The beef tapeworm, Taenia saginata, causing cysticercosis in bovines and taeniosis in humans, is thought to have a global distribution. In eastern and southern Africa, cattle production plays a crucial role in the economy, but a clear overview of the prevalence of T. saginata in the region is still lacking. This review aims to summarize existing knowledge on T. saginata taeniosis and bovine cysticercosis distribution in eastern and southern Africa.

Methods

A systematic review was conducted, that gathered published and grey literature, including OIE reports, concerning T. saginata taeniosis and bovine cysticercosis in eastern and southern Africa published between January 1st, 1990 and December 31st, 2017.

Results

A total of 1232 records were initially retrieved, with 78 full text articles retained for inclusion in the database. Unspecified taeniosis cases were reported for Angola, Ethiopia, Kenya, Madagascar, Malawi, South Africa, Tanzania, Uganda and Zambia, whereas T. saginata taeniosis cases were found for Ethiopia, Kenya, South Africa, Tanzania, Zambia and Zimbabwe. The prevalence of taeniosis ranged between 0.2–8.1% based on microscopy, and between 0.12–19.7% based on coproAg-ELISA. In Ethiopia, the percentage of tapeworm self-reporting was high (45.0–64.2%), and a substantial number of anthelmintic treatments were reported to be sold in towns. The presence of bovine cysticercosis was reported in all 27 countries/territories included in the study, except for Rwanda and Somalia, Comoros, Madagascar, Mauritius, Mayotte, Seychelles and Socotra. The prevalence of cysticercosis ranged between 0.02–26.3% based on meat inspection, and between 6.1–34.9% based on Ag-ELISA.

Conclusions

Although T. saginata has been reported in the majority of countries/territories of the study area, T. saginata taeniosis/cysticercosis remains a largely ignored condition, probably due to the absence of symptoms in cattle, the lack of data on its economic impact, and the fact that human taeniosis is considered a minor health problem. However, the occurrence of bovine cysticercosis is a clear sign of inadequate sanitation, insufficient meat inspection, and culinary habits that may favour transmission. Measures to reduce transmission of T. saginata are therefore warranted and the infection should be properly monitored.

Keywords

  • Taenia saginata
  • Cestode
  • Beef tapeworm
  • Taeniosis
  • Bovine cysticercosis
  • Eastern Africa
  • Southern Africa

Background

The beef tapeworm, Taenia saginata, utilizes bovines as intermediate hosts and humans as final hosts. Although tapeworm infections have been reported since ancient times [1], it was not until 1782 [2] that differentiation of T. saginata from the other well-known meat-transmitted human tapeworm, Taenia solium, was established. Furthermore, it was not until 1871 that the role of cattle as intermediate hosts for the parasite was established, with “measly” beef being reported as the source of infection in patients [3].

Ingestion of raw or undercooked infected beef is indeed the mode of transmission of this zoonotic parasite to humans, in whom it develops to its adult form, a several metres long segmented worm consisting of a scolex with four suckers, neck and strobila, i.e. a chain of proglottids [4]. In contrast to T. solium, the gravid proglottids of T. saginata, which contain thousands of embryonated eggs, are mobile and can migrate from the anus independently of, as well as during, defaecation [5]. Eggs are then shed into the environment, and cattle become infected through grazing contaminated pastures, or ingesting contaminated fodder or water. After hatching, and penetration of the intestinal wall, the oncospheres reach the general circulation, distributing them throughout the body where they develop into cysticerci [4]. Common predilection sites for T. saginata cysticerci include the heart and masseter muscles [6].

In both intermediate and definitive hosts, T. saginata causes few symptoms. In humans, infection is usually characterized by anal pruritus due the active migration of T. saginata proglottids and some mild abdominal pain [7]. Nevertheless, the (potential) presence of a tapeworm in the body can cause distress [8], and some people even suffer from a pathological fear of tapeworms, often encouraged by horror stories circulating in popular media or books [9, 10]. Moreover, although rare, complications due to taeniosis, such as appendicitis, have been reported [11]. In cattle, the infection is generally asymptomatic but nevertheless may incur great economic losses for the meat sector due to carcass condemnation or treatment upon detection of cysticerci during meat inspection, as well as related insurance costs [12, 13].

Taenia saginata is distributed globally, with the parasite occurring in both developed and developing countries, although less frequently in countries where cultural preferences limit consumption of bovids or where adequate sanitary infrastructure reduces the likelihood of bovids ingesting human faecal matter. Thus, the prevalence of human taeniosis and bovine cysticercosis are considered particularly high in Africa, Latin America and some parts of Asia [4].

In eastern and southern Africa, the cattle population was estimated at a massive 20.6 million in 2016 [14], so the parasite is thought to be of particular relevance here. In the area, bovines are essential for the livelihoods of smallholders, serving as a source of food, draft power and manure, as well as acting as a financial buffer for challenging times. Although there are indications of the widespread presence of the parasite in at least some countries in this region (e.g. Ethiopia: [1517]), an extensive overview of its distribution in this region, along with epidemiological considerations regarding its presence, is still lacking. Our aim was therefore to gather recent information on the presence of T. saginata in eastern and southern Africa.

Methods

Search strategy

A systematic review of published literature was conducted to collect data on the occurrence, prevalence, and geographical distribution of bovine cysticercosis and human taeniosis in eastern and southern Africa, published between January 1st, 1990 and December 31st, 2017. For the purpose of this study, eastern and southern Africa was defined as the area covered by the following countries/territories: Angola, Botswana, Burundi, Comoros, Djibouti, Eritrea, Ethiopia, Kenya, Lesotho, Madagascar, Malawi, Mauritius, Mayotte (French), Mozambique, Namibia, Réunion (French), Rwanda, Seychelles, Socotra (Yemini), Somalia (including the autonomous regions Puntland and Somaliland), South Africa, Swaziland, Tanzania (including the semi-autonomous region of Zanzibar), Uganda, Zambia and Zimbabwe. The PRISMA guidelines were followed whilst conducting the review [18] (Additional file 1). The search protocol can be found in Additional file 2.

The international bibliographic databases PubMed (http://www.ncbi.nlm.nih.gov/pubmed) and Web of Science (http://ipscience.thomsonreuters.com/product/web-of-science/) were searched using the following search phrase: (cysticerc* OR cisticerc* OR “C. bovis” OR taenia* OR tenia* OR saginata OR taeniosis OR teniosis OR taeniasis OR ténia OR taeniid OR cysticerque) AND (Angola OR Botswana OR Burundi OR Comoros OR Djibouti OR Eritrea OR Ethiopia OR Kenya OR Lesotho OR Madagascar OR Malawi OR Mauritius OR Mayotte OR Mozambique OR Namibia OR Réunion OR Rwanda OR Seychelles OR Socotra OR Somalia OR South Africa OR Swaziland OR Tanzania OR Uganda OR Zanzibar OR Zambia OR Zimbabwe OR “East Africa” OR “Horn of Africa” OR “Southern Africa” OR Puntland OR Somaliland).

Furthermore, a range of databases for grey literature and MSc/PhD thesis documents were searched using keywords from the above search phrase (the full list of databases is presented in Additional file 3). Data on bovine cysticercosis from the different scientific databases were complemented with data from OIE databases “Handistatius” (1996–2004) and “WAHIS” (2005) [19, 20]. Finally, reference lists of reviews on the topic were screened and additional relevant records were added to the database.

Selection criteria

Upon compilation of search results from the different databases, duplicate records were removed. Thereafter, titles and abstracts were screened for relevance, applying the following exclusion criteria: (i) studies concerning a parasite other than T. saginata; (ii) studies conducted outside the study area; (iii) studies published outside the study period; (iv) studies reporting results outside the scope of the review question (e.g. review, experiment, intervention trial); and (v) duplicated data. After the screening process, full text articles were evaluated using the same criteria listed above (Additional file 4).

Data extraction and generation

Data from included records were extracted. In reports where the numerator and denominator of the study sample were available, prevalence data were calculated, if not already provided. When not presented in the manuscript, the 95% exact confidence intervals (CI) were calculated, using the “binom.test” function (“stats” package) in R 3.5.1 [21].

Results

Search results

A total of 1228 records were obtained from the database search, and four additional records were added through screening of the reference lists of relevant reviews (Additional file 4). After removal of duplicate records (n = 71), 1161 records were screened based on title and, thereafter, abstract. During title screening, 987 records were excluded, and a further 85 records were removed upon abstract screening; three of these were remaining duplicate records, whereas the other removed records focussed on a different parasite (n = 32) or study area (n = 18), were published outside the study period (n = 1), or had a different scope (e.g. laboratory experiments, review) (n = 31). Thus, 89 full text articles (n = 89) fulfilled the eligibility criteria for evaluation, but three of these were unavailable. During the evaluation of the remaining 86 records, eight were excluded due to having a different scope.

Thus, 78 records were included in the qualitative synthesis (journal articles: 73, online data repositories: 2, MSc thesis: 2, PhD thesis: 1). Apart from the two OIE sources describing the occurrence of bovine cysticercosis throughout the study area, the majority of records presented data from Ethiopia (n = 37). The others included data from Kenya (n = 11), Tanzania (n = 7), South Africa (n = 7), Zambia (n = 4), Zimbabwe (n = 2), Angola (n = 2), Uganda (n = 1), Swaziland (n = 1), Namibia (n = 1), Malawi (n = 1), Madagascar (n = 1) or Botswana (n = 1).

Human taeniosis occurrence

A total of 48 records reported the presence of human taeniosis cases (excluding those with confirmed T. solium taeniosis). Unspecified taeniosis cases were reported from Angola, Ethiopia, Kenya, Madagascar, Malawi, South Africa, Tanzania, Uganda and Zambia, whereas known T. saginata taeniosis cases were reported from Ethiopia, Kenya, South Africa, Tanzania, Zambia and Zimbabwe (Fig. 1). Microscopy results were included in 32 reports, most of which presented data from Ethiopia (18) (Table 1). Taeniosis prevalence based on microscopy alone ranged between 0.2–8.1% (villagers in Kenya [22] and Ethiopia [23], respectively), and one study reported the absence of taeniosis (in geophagous pregnant women in Kenya [24]). Four records presented data from coproAg-ELISA studies conducted in Kenya and/or Zambia, with a prevalence ranging between 0.12–19.7% (villagers in Zambia [25] and Kenya [26], respectively) (Table 2), two of which involved confirmed T. saginata cases. Overall, common study groups were school-children, patients suffering from other diseases [e.g. HIV infection, sleeping sickness and active pulmonary tuberculosis (TB)], as well as occupational groups (e.g. tobacco farm workers, food handlers). Furthermore, eight studies reported taeniosis prevalence in communities based on self-reporting by questionnaire respondents (prevalence range: 45.5–64.2%) (Table 3), and five records presented data on anthelmintic sales in towns (Table 4), both in Ethiopia. Another two records contained data on household latrine sampling, thus presenting prevalence at the household level (Malawi: 40.4% [27]; South Africa: 18.0% [28]). Finally, one report discussed a case of intestinal obstruction due to impaction of a T. saginata tapeworm in Zimbabwe, requiring enterotomy with bolus removal as well as appendectomy [29].
Fig. 1
Fig. 1

Human taeniosis in southern and eastern Africa

Table 1

Reported occurrence of taeniosis in southern and eastern Africa: microscopy studies

Country

Period

People tested

People positive

Prevalence (%)

(95% CI)

Species identification

Group studied

Reference

Angola

9/2012-12/2013

344

2

0.58 (0.07–2.1)

N

Children below 5 with diarrhea

[50]

Angola

1/2015-5/2015

230

2

0.87 (0.10–3.1)

N

School children in 16 schools

[51]

Ethiopia

11/1995-4/1996; 6-9/1996

1750

79

4.5 (3.6–5.6)

Ya

Sugar-estate residents

[52]

Ethiopia

3-4/1999; 2/2002

3167

na

< 4 (na)

N

Schoolchildren, peasants and teachers

[53]

Ethiopia

1/2002-2/2002

104

1

0.96 (0.02–5.2)

Ya

HIV/AIDS and HIV-seronegative individuals in a teaching hospital

[54]

Ethiopia

2007–2012

32191

322

1.0 (0.9–1.1)

N

Rural hospital visiters

[55]

Ethiopia

5/2007-6/2007

419

na

1.4 (na)

N

na

[56]

Ethiopia

12/2007-2/2008

7171

23

0.32 (0.20–0.48)

N

Visitors of health centers

[57]

Ethiopia

8/2008-12/2008

343

14

4.1 (2.2–6.8)

N

HIV patients recruited at hospital

[58]

Ethiopia

11/2008

121

5

4.1 (1.4–9.4)

N

Prison inmates

[59]

Ethiopia

11/2008

115

1

0.87 (0.02–4.7)

N

Tobacco farm workers

[59]

Ethiopia

4/2009

384

5

1.3 (0.4–3.0)

N

Food handlers

[60]

Ethiopia

9/2010-7/2011

858

18

2.1 (1.2–3.3)

N

Highland and lowland dwellers

[61]

Ethiopia

1/2011-6/2011

200

1

0.5 (0.01–2.8)

N

Food handlers

[62]

Ethiopia

3/2012-11/2012

260

1

0.38 (0.01–2.12)

N

Children recruited in Health Center

[63]

Ethiopia

1/2013-5/2013

172

5

2.9 (1.0–6.7)

N

Asymptomatic food handlers

[64]

Ethiopia

8/2013-11/2013

180

2

1.1 (0.13–4.0)

N

HAART initiated and naive paediatric HIV patients

[65]

Ethiopia

1/2015-2/2015

503

13

2.6 (1.4–4.4)

N

School children from 5 schools

[66]

Ethiopia

1/2016-8/2016

213

5

2.3 (0.8–5.4)

N

Active pulmonary TB patients

[67]

Ethiopia

na

1537

na

8.1 (na)

Ya

Participants from 19 communities, includes children and adults

[23]

Ethiopia

na

491

12

2.4 (1.3–4.2)

N

Villagers

[68]

Kenya

2000–2009

31

1

3.2 (0.08–16.7)

N

Sleeping sickness patients

[69]

Kenya

7/2010-7/2012

2057

na

0.20 (na)

N

na

[22]

Kenya

8/2010-7/2012

2113

na

0.30 (0–0.5)

N

Mixed-farming community

[26]

Kenya

na

285

na

5.3 (na)

N

HIV-positive patients

[70]

Kenya

na

151

0

0 (0–2.4)

N

Geophagous pregnant women

[24]

Madagascar

11/1996-1/1997

401

3

0.75 (0.15–2.2)

N

Patients referred for parasitological examination

[71]

South Africa

2009

na

2

na

N

Laboratory results

[72]

South Africa

2009

na

4

na

Y

Laboratory results

[72]

South Africa

4/2009-9/2009

162

3

1.9 (0.4–5.3)

N

School children

[73]

South Africa

2010

na

11

na

Y

Laboratory results

[72]

South Africa

2010

na

1

na

N

Laboratory results

[72]

South Africa

na

183

3

1.6 (0.3–4.7)

N

Rural black preschool children

[74]

Tanzania

2008–2009

1057

3

0.30 (0.06–0.8)

Yb

Villagers, after treatment with niclosamide/praziquantel and purgation

[75]

Uganda

na

5313

36

0.70 (0.5–0.9)

N

Primary school children

[76]

Zambia

6/2007-8/2007

403

na

0.90 (na)

N

School children

[77]

aReported as T. saginata, yet unclear from methodology

bConfirmed by PCR

Abbreviations: CI, confidence interval; na, not available; HAART, highly active antiretroviral therapy

Table 2

Reported occurrence of taeniosis in southern and eastern Africa: coproAg-ELISA studies

Country

Study period

People tested

People positive

Prevalence (%)

95% CI

Species identification

Group studied

Reference

Kenya

1/2007-4/2007

204

12

5.9 (3.1–10.0)

Ya

District inhabitants

[78]

Kenya

8/2010-7/2012

2113

na

19.7 (16.7–22.7)

N

Mixed-farming community

[26]

Kenya

na

691

na

1.9 (na)

N

Slaughterhouse workers

[79]

Zambia

2006

190

5

2.6 (0.9–6.0)

Ya

Pupils primary schools

[78]

Zambia

8/2009;10/2010

817

1

0.12 (0.003–0.68)

Yb

Consenting villagers

[25]

aResults based on coproAg-ELISA, specific for T. saginata

bResults based on coproAg-ELISA with coproPCR (T. saginata specific) confirmation

Abbreviations: CI, confidence interval; na, not available

Table 3

Reported occurrence of taeniosis: questionnaire studies in Ethiopia

Town

Study period

People interviewed

People reporting infection

Prevalence (%)

95% CI

Reference

Awassa

10/2005-4/2006

120

77

64.2 (54.9–72.7)

[44]

Soddo

11/2007-4/2008

79

40

50.6 (39.1–62.1)

[45]

Jimma

11/2008-3/2009

60

34

56.7 (43.2–69.4)

[46]

Yirgalem

11/2009-3/2011

170

119

70.0 (62.5–76.8)

[47]

Sebeta, Tulu Bolo, Weliso

na

392

na

55.1 (na)

[48]

Harar

na

300

182

60.7 (54.9–66.2)

[16]

Adama

11/2013-4/2014

200

91

45.5 (38.5–52.7)

[15]

Batu

12/2014-4/2015

100

59

59.0 (48.7–68.7)

[49]

Abbreviations: CI, confidence interval; na, not available

Table 4

Reported town level taeniicidal sales in Ethiopia

Town

Year

Number

Value (ETB)

Value (EUR)a

Reference

Awassa

2002

1,582,254

1,880,330

58,290

[44]

Awassa

2003

1,221,004

1,746,585

54,144

[44]

Awassa

2004

946,330

1,803,300

55,902

[44]

Awassa

2005

889,759

1,788,776

55,452

[44]

Soddo

2004

74,747

192,979

5982

[45]

Soddo

2005

77,705

203,675

6342

[45]

Soddo

2006

79,230

210,133

6314

[45]

Soddo

2007

105,090

279,660

8669

[45]

Jimma

2007

51,462

na

na

[46]

Jimma

2008

52,134

na

na

[46]

Yirgalem

2005

95,712

na

na

[47]

Yirgalem

2006

93,059

na

na

[47]

Yirgalem

2007

95,093

na

na

[47]

Yirgalem

2008

95,121

na

na

[47]

Yirgalem

2009

93,028

na

na

[47]

Batu

2013

42,557

148,100

4591

[49]

Batu

2014

29,049

97,492

3022

[49]

aBased on July 2018 exchange rates (1 ETB = 0.0310 EUR)

Abbreviation: na, not available

Bovine cysticercosis

Based on the retrieved data sources (both OIE databases and manuscripts/reports), the presence of bovine cysticercosis was reported in all of the 27 countries/territories studied, except for Comoros, Madagascar, Mauritius, Mayotte and Seychelles. In addition, no information was available for Rwanda, Somalia, Mayotte and Socotra (Fig. 2). Data from the two OIE data sources indicating the occurrence and/or number of cases are presented in Table 5. Apart from the OIE data sources, a total of 39 records were found to document results on bovine cysticercosis in the study region. Meat inspection results were included in 35 records (Table 6), with prevalence estimates ranging between 0.02–26.3%, while two records reported the absence of positive animals (Tanzania: 2011 [30], Zambia: 2001 [31]). Seven records provided serological data, mostly based on Ag-ELISA results (prevalence range: 6.1–53.5%), while one presented Ab-ELISA data (prevalence: 10.0%) [32] and another IHAT results (prevalence: 25.7%) [33] (Table 7). One study estimated the town level costs due to condemnation caused by bovine cysticercosis [Mekelle, abattoir level: 31,952 ETB/6 months (991 EUR, according to July 2018 exchange rates; 1 ETB = 0.0310 EUR) [34]], and another five studies provided data on total economic losses due to condemnation for a wide variety of conditions [17, 30, 3537]. Overall, the majority of records presented data from Ethiopia (21/41), followed by Tanzania (8/41) and Kenya (7/41).
Fig. 2
Fig. 2

Bovine cysticercosis in southern and eastern Africa

Table 5

OIE data on occurrence of bovine cysticercosis in the southern and eastern Africa (1996–2005) [19, 20]

Country

Year

1996

1997

1998

1999

2000

2001

2002

2003

2004

2005

Angola

6

11

na

na

na

na

na

na

4

+

Botswana

na

53

4356

12,863

14,000

14,000

10,181

15,363

na

+

Burundi

na

na

na

na

na

+

na

na

na

na

Comoros

na

na

-

na

na

na

na

na

na

na

Djibouti

na

na

na

na

na

na

+

+

+

+

Eritrea

+

+

+

2

+

+

na

+

370

-

Ethiopia

+

na

na

na

na

+

+

+

+

+

Kenya

+

+

+

+

+

+

+

+

3999

na

Lesotho

56

38

139

na

na

na

68

na

na

-

Madagascar

na

na

na

na

na

na

-

na

na

-

Malawi

+

+

+

+

+

+

+

+

6

+

Mauritius

na

na

na

na

na

-

-

-

-

na

Mozambique

+

+

+

na

na

na

na

na

na

-

Namibia

+

3833

3118

+

2852

2226

2399

54

1616

+

Réunion

+

na

na

-

-

-

-

-

na

-

Rwanda

na

na

na

na

na

na

na

na

na

na

Seychelles

-

-

-

na

-

na

-

na

-

na

Somalia

na

na

na

na

na

na

na

na

na

na

South Africa

+

+

+

+

+

+

+

+

+

+

Swaziland

969

+

+

+

1419

530

245

1909

561

+

Tanzania

+

+

+

+

na

na

+

6

na

+

Uganda

+

24

152

+

+

+

+

na

na

+

Zambia

na

na

na

na

+

na

2

248

na

na

Zimbabwe

244

1744

2062

1988

160

1447

+

na

na

na

Abbreviations: na, not available; +, occurrence of the disease; -, absence of the disease

Table 6

Reported occurrence of bovine cysticercosis in southern and eastern Africa: meat inspection studies

Country

Period

Animals tested

Animals positive

Prevalence (%)

(95% CI)

Reference

Botswana

1995

na

na

na (9.1–12.6)

[80]

Ethiopia

9/2004-8/2005

11,227

842

7.5 (7.0–8.0)

[81]

Ethiopia

9/2005-2/2007

4456

824

18.5 (17.4–19.7)

[82]

Ethiopia

10/2005-4/2006

400

105

26.3 (22.0–30.9)

[83]

Ethiopia

12/2006-7/2007

3711

308

8.3 (7.4–9.2)

[34]

Ethiopia

10/2007-3/2008

512

15

2.9 (1.6–4.8)

[84]

Ethiopia

11/2007-4/2008

415

47

11.3 (8.4–14.8)

[45]

Ethiopia

12/2007-2/2008

1023

74

7.2 (5.7–9.0)

[57]

Ethiopia

11/2008-3/2009

500

22

4.4 (2.8–6.6)

[46]

Ethiopia

10/2009-9/2010

898

177

19.7 (17.2–22.5)

[16]

Ethiopia

11/2009-3/2011

400

48

12 (9.0–15.6)

[47]

Ethiopia

2010

12,708

669

5.3 (4.9–5.7)

[37]

Ethiopia

9/2010-9/2012

3055

126 organs

na

[35]

Ethiopia

2011

34,674

3259

9.4 (9.1–9.7)

[37]

Ethiopia

2012

10,363

803

7.7 (7.2–8.3)

[37]

Ethiopia

10/2012-4/2013

745

21 organs

na

[35]

Ethiopia

2013

5172

247

4.8 (4.2–5.4)

[37]

Ethiopia

11/2013-4/2014

384

10

2.6 (1.3–4.7)

[15]

Ethiopia

11/2013-5/2014

3675

40 organs

na

[36]

Ethiopia

05/2014-6/2014

439

23

5.2 (3.3–7.8)

[85]

Ethiopia

12/2014-4/2015

384

10

2.6 (1.3–4.7)

[49]

Ethiopia

na

522

39

7.4 (5.4–10.1)

[33]

Ethiopia

na

1022

64

6.3 (4.9–7.9)

[17]

Ethiopia

na

1216

na

4.6 (na)

[48]

Kenya

1974

77,810

6784

8.8 (8.5–8.9)

[86]

Kenya

1975–1978

na

na

< 6.0 (na)

[86]

Kenya

1979–1983

na

na

< 4.0 (na)

[86]

Kenya

1984

na

na

1.8 (na)

[86]

Kenya

1985–1990

na

na

< 2.0 (na)

[86]

Kenya

1991

315,801

3457

1.1 (1.06–1.13)

[86]

Kenya

9/2006-1/2007

188

6

3.2 (1.2–6.8)

[87]

Kenya

na

511

39

7.6 (5.5–10.3)

[88]

Kenya

na

1184

189

16.0 (13.9–18.2)

[32]

Namibia

2000

12,204

973

8.0 (7.5–8.5)

[89]

Namibia

2001

7888

713

9.0 (8.4–9.7)

[89]

Namibia

2002

10,561

798

7.6 (7.1–8.1)

[89]

Namibia

2003

4411

347

7.9 (7.1–8.7)

[89]

Namibia

2004

5309

401

7.6 (6.9–8.3)

[89]

Namibia

2006

7085

435

6.1 (5.6–6.7)

[89]

Namibia

2006

71,388

243

0.34 (0.30–0.39)

[89]

South Africa

2009–2011

1,022,556

24,443

2.39 (2.36–2.42)

[90]

South Africa

2010

356,006

2169

0.61 (0.58–0.64)

[91]

South Africa

2011

349,458

2389

0.68 (0.66–071)

[91]

South Africa

2012

348,309

1980

0.57 (0.54–0.59)

[91]

South Africa

2013

361,232

3382

0.94 (0.91–0.97)

[91]

Tanzania

1987–1989

42,434

na

16.4 (na)

[92]

Tanzania

1/2002-4/2004

12,444

185

1.5 (1.3–1.7)

[93]

Tanzania

2005

na

19

0.06 (na)

[94]

Tanzania

2006

na

24

0.06 (na)

[94]

Tanzania

2007

na

16

0.04 (na)

[94]

Tanzania

2010

27,444

20 organs

na

[30]

Tanzania

2/2010-1/2011

30,713

18 organs

na

[95]

Tanzania

2011

30,671

0 organs

na

[30]

Tanzania

2012

27,865

6 organs

na

[30]

Tanzania

12/2013

2438

1 and 0.1% organs

na

[30]

Tanzania

na

na

21

na

[96]

Zambia

2000

4629

1

0.02 (0.0005–0.12)

[31]

Zambia

2001

9422

0

0 (0–0.04)

[31]

Zambia

2002

10,147

2

0.02 (0.002–0.07)

[31]

Zambia

2003

11,519

2

0.02 (0.002–0.06)

[31]

Zimbabwe

1/2006-12/2007

86,080

1364

1.6 (1.5–1.7)

[97]

Abbreviations: CI, confidence interval; na, not available

Table 7

Reported occurrence of bovine cysticercosis in southern and eastern Africa: serological studies

Country

Period

Diagnostic tool

Animals tested

Animals positive

Prevalence (%)

95% CI

Reference

Ethiopia

na

IHAT

743

190

25.6 (22.4–28.9)

[33]

Kenya

9/2006-1/2007

Ag-ELISA

188

44

23.4 (17.8–30.1)

[87]

Kenya

10/2006-11/2006

Ag-ELISA

792

143

18.1 (15.4–20.9)

[87]

Kenya

8/2010-7/2012

Ag-ELISA

983

na

53.5 (48.7–58.3)

[26]

Kenya

na

Ag-ELISA

511

117

22.9 (19.3–26.8)

[88]

Kenya

na

Ag-ELISA

1184

413

34.9 (32.2–37.7)

[32]

Kenya

na

Ab-ELISA

1184

118

10.0 (8.3–11.8)

[32]

South Africa

na

Ag-ELISA

1315

300

22.8 (20.6–25.2)

[98]

South Africa

na

Ag-ELISA

1159

174

15.0 (13.0–17.2)

[98]

Swaziland

na

Ag-ELISA

600

na

28.0 (na)

[99]

Zambia

12/1999-9/2000

Ag-ELISA

628

38

6.1 (4.3–8.2)

[100]

Abbreviations: CI, confidence interval; na, not available; IHAT, indirect hemagglutination test

Taeniosis and bovine cysticercosis occurrence

The co-occurrence of both bovine cysticercosis and taeniosis during the study period was reported in Angola, Ethiopia, Malawi, South Africa, Tanzania, Uganda, Zambia and Zimbabwe, but this was not the case for the other countries/territories studied. The occurrence of bovine cysticercosis or taeniosis was reported for all the countries/territories studied, except for Somalia, Rwanda and the Comoros, Mauritius, Mayotte, Seychelles, Mayotte and Socotra islands.

Discussion

The present study aimed at describing the epidemiology of T. saginata taeniosis/cysticercosis in eastern and southern Africa (1990–2017). Based on our findings, both human taeniosis and bovine cysticercosis were widespread in the 27 countries/territories studied, except for Somalia, Rwanda and six island states/territories, indicating that T. saginata is present in most countries of the study area. However, lack of diagnosis and reporting, particularly in rural areas, mean that the data accrued are likely to underestimate occurrence. The absence of data for some countries does not exclude the possibility that this parasite is present there as well. For example, given that of the three countries bordering Rwanda that are included in this review (Burundi, Tanzania and Uganda) all report the presence of this parasite, it seems unlikely that Rwanda is free from T. saginata. On the other hand, one potential hypothesis for the lack of reported T. saginata in Rwanda is the remarkably higher rate of access to improved sanitation services, at 60.8% in comparison to neighbouring Burundi at 35.5% [38]. The Rwandan civil war, during 1990–1994, culminating in the genocide of 1994, may have impacted reporting during that period, but does not explain the more recent lack of reporting. For Somalia, the ongoing civil war might explain the lack of reported data for the country, whereas for the six island states and territories, governmental or scientific interest in reporting cases may be lacking.

Cases of taeniosis were reported for Angola, Ethiopia, Kenya, Madagascar, Malawi, South Africa, Tanzania, Uganda, Zambia and Zimbabwe, yet the majority of reports on human taeniosis cases did not, unfortunately, provide species determination. Thus, cases of T. saginata taeniosis were not differentiated from infections caused by other Taenia spp. The pork tapeworm, T. solium, for instance, is presumed to also be widely distributed throughout eastern and southern Africa [39] and therefore we cannot conclude that all reported, unspecified taeniosis cases are due to T. saginata. Taenia solium is known to be the causative agent of the severe condition neurocysticercosis, associated with epilepsy, severe headaches, cognitive deficits [40] and a major cause of deaths among the food-borne diseases [41]. The presence of a single T. solium tapeworm carrier poses a major risk for his/her surroundings, as humans acquire neurocysticercosis through the ingestion of T. solium eggs transmitted through poor hygiene practices resulting in faecal-oral transmission [42]. Although tapeworm infections usually have an asymptomatic course [7] apart from some sporadic complications (e.g. intestinal obstruction in the Zimbabwean patient [29]), it is thus paramount to register cases as well as to differentiate case species, to allow precise prevalence estimates, and to guide appropriate control measures. Species determination, however, is hampered by the fact that Taenia spp. eggs cannot be differentiated upon coprological examination. Expelled proglottids of T. solium and T. saginata can be distinguished on the basis of the number of uterine branches, but such material is not always available. Moreover, more advanced diagnostic tools (e.g. copro-PCR) to differentiate species are often lacking in resource poor settings [43], and even in developed countries are not often performed due to lack of awareness about neurocysticercosis [12].

In certain countries in the study area, specific culinary habits put the consumers at great risk of contracting T. saginata taeniosis. For instance, in Ethiopia, “kitfo” is a very popular beef dish, in which the meat is usually consumed raw or lightly cooked, while “tibs” is another dish often containing undercooked beef. Furthermore, “kurt” refers to the habit of eating cubes of raw beef, finished off with local spices. Unsurprisingly, a high proportion of the Ethiopian population reports having had a tapeworm, and sales of taeniicidal drugs in Ethiopia are high [15, 16, 4449].

Access to adequate clean water and sanitation services (WASH) is notoriously poor across the whole of sub-Saharan Africa, including the region of interest to this paper. There are large between and within-country disparities, but overall sub-Saharan Africa lags far behind the goals set out by the international community in both the millennium development and the sustainable development goals with only 25.7% (23.1–28.6%) of the population having access to improved sanitation [38]. This lack of WASH capacity is strongly reflected by the presence of parasites such as T. saginata which requires ingestion of eggs passed in faecal material for the propagation of its life-cycle.

In eastern and southern Africa the cattle population is large, and bovine products, including meat, are an important protein source for humans, as well as a source of draft power and form of investment. Beef cattle are typically kept in an extensive manner; animals are basically free-ranging. The presence of human T. saginata carriers shedding eggs into the environment puts these cattle at risk of bovine cysticercosis, and this presumably occurs widely in the study area. In developed countries, the condition is known to cause economic losses due to freezing or condemnation of the carcass as well as related insurance costs (e.g. Belgium: 3,408,455 EUR/year [13]). Studies investigating the magnitude of this economic loss in the study area are, however, limited, with data available from only one abattoir in Ethiopia [34]. Furthermore, reporting of bovine cysticercosis to OIE appeared to be inconsistent, with large variations in number of cases reported even within the same country, and gaps in the annual reporting (e.g. no data available after 2005).

Conclusions

Taenia saginata taeniosis/cysticercosis is a widespread, yet largely ignored, condition in southern and eastern Africa. This is probably due to the lack of symptoms in cattle, the lack of good data on its economic impact, and because human taeniosis is considered a minor health problem. Nevertheless, the presence of bovine cysticercosis is a clear sign of inadequate sanitation, insufficient meat inspection, and culinary habits that may favour transmission. Measures to reduce transmission of T. saginata are therefore warranted, and the infection should be properly monitored, in both humans and cattle. It should also be noted that as cattle are an important source of human protein and livelihoods in the area, ensuring optimal health and productivity of cattle is of indirect importance to human health and welfare as well as any direct impact. Species identification in tapeworm carriers is paramount to gain detailed insights in the distribution of the different Taenia spp. in the area, as well to avoid the development of the severe condition neurocysticercosis within communities due to ingestion of eggs shed by a T. solium tapeworm carrier. We conclude that in order to ensure both the safety of beef consumed in the southern and eastern Africa, and to improve the underlying sanitary conditions perpetuating the parasitic life-cycle, concerted, co-ordinated efforts must be made by integrating public, animal and environmental health in a One Health approach.

Abbreviations

ETB: 

Ethiopian Birr

EUR: 

Euro

HAART: 

Highly active antiretroviral therapy

IHAT: 

Indirect hemagglutination test

OIE: 

World Organisation for Animal Health/Office International des Epizooties

Declarations

Acknowledgments

This work was performed within the framework of CYSTINET, the European network on taeniosis/cysticercosis, COST ACTION TD1302.

Funding

Not applicable.

Availability of data and materials

The data supporting the conclusions of this article are included within the article and its additional files.

Authors’ contributions

VD conducted the systematic review of literature, extracted and analysed the data and drafted the first version of the manuscript. All authors contributed to the design of the study, interpretation of the data and writing the paper. All authors read and approved the final manuscript.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Open AccessThis 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.

Authors’ Affiliations

(1)
Department of Biomedical Sciences, Institute of Tropical Medicine, Antwerp, Belgium
(2)
Department of Virology, Parasitology and Immunology, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium
(3)
One Health Center for Zoonoses and Tropical Veterinary Medicine, Ross University School of Veterinary Medicine, Basseterre, Saint Kitts, Trinidad and Tobago
(4)
Department of Epidemiology and Public Health, Sciensano, Brussels, Belgium
(5)
Department of Veterinary Public Health and Food Safety, Faculty of Veterinary Medicine, Ghent University, Merelbeke, Belgium
(6)
Parasitology, Department of Food Safety and Infection Biology, Faculty of Veterinary Medicine, Norwegian University of Life Sciences, Adamstuen Campus, Oslo, Norway
(7)
Laboratory of Parasitology, Veterinary Research Institute, Hellenic Agricultural Organization Demeter, Thermi, 57001 Thessaloniki, Greece
(8)
International Livestock Research Institute (ILRI), P.O. Box 30709, Nairobi, Kenya
(9)
Institute for Infection and Global Health, University of Liverpool, Neston, UK

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