Journal of Applied Microbiology, 2023, 134, 1–13

https://doi.org/10.1093/jambio/lxad080
Advance access publication date: 20 April 2023
Review Article

A systematic literature review of milk consumption and

associated bacterial zoonoses in East Africa
1,2,*
Jean Pierre Mpatswenumugabo , Marie Anne Mukasafari1,3 , Jean Baptiste Ndahetuye1 ,
Ewa Wredle3 , Renée Båge2
1
Department of Veterinary Medicine, College of Agriculture, Animal Science and Veterinary Medicine, University of Rwanda, Nyagatare,

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Rwanda
2
Department of Clinical Sciences, Swedish University of Agricultural Sciences, Uppsala SE-750 07, Sweden
3
Department of Animal Nutrition and Management, Swedish University of Agricultural Sciences, Uppsala SE-750 07, Sweden
∗
Corresponding author. Department of Clinical Sciences, Swedish University of Agricultural Sciences, Uppsala SE-750 07, Sweden.
E-mail: [email protected]

Abstract
Consumption of unsafe animal-source foods is the major cause of foodborne disease outbreaks in low-income countries. Despite current knowl-
edge of the threat posed by raw milk consumption to human health, people in many countries in East Africa still consume unboiled milk. This
literature review explored the association between milk consumption and the occurrence of five milk-borne bacterial zoonoses: brucellosis,
salmonellosis, campylobacteriosis, Escherichia coli infections, and tuberculosis. A search for literature published up to 1 October 2021 was
conducted through the Web of Science, PubMed, and Scopus databases, using Preferred Reporting Items for Systematic reviews and Meta-
Analyses guidelines. The selection process yielded 65 articles describing studies conducted in East Africa 2010–2021, which were carefully
scrutinized. The most investigated pathogen was Brucella spp. (54.5%), followed by E. coli (18.2%), Salmonella spp. (12.1%), Mycobacterium
spp. (6.1%), and E. coli O157: H7 (6.1%). The most common predisposing factors for potential milk-borne disease outbreaks were consumption
of contaminated raw milk, inadequate cold storage along the milk value chain, poor milk handling practices, and lack of awareness of the health
risks of consuming unpasteurized milk. Thus, a tailor-made training program is needed for all milk value chain actors to enhance the safety of
milk sold in informal markets, and a One Health approach should be applied. Future studies should employ more advanced diagnostic techniques
and countries in East Africa should invest in modern diagnostic tools and equipment, both in hospitals and in local rural settings where most
cases occur.
Keywords: dairy, East Africa, raw milk, foodborne disease, risk factors, food safety

Introduction milk production, pasteurization, low consumption of unpro-

Zoonoses are infectious diseases caused by pathogens that cessed milk, and hygienic food preparation (Nyokabi et al.
spread between humans and animals, with transmission 2021b).
through either direct or indirect contact. The main routes The past decade has seen rapid development of dairy farm-
by which humans are infected include animal handling and ing in East African countries. The top six milk-producing
husbandry, close habitation with livestock or animals, and countries in Africa now include two from East Africa,
consumption of contaminated animal products. Consuming namely Kenya, and Ethiopia, with annual milk produc-
undercooked animal-source foods such as meat, milk, and tion of 5 528 900 and 3 644 000 metric tonnes, respectively
dairy products are a major risk factor for foodborne dis- (FAO 2021). However, this increase in milk production has
eases. Additionally, consuming unboiled milk increases the not been accompanied by changes in cultural behaviors
risk of spread of multidrug-resistant pathogens to humans and traditions relating to milk consumption (Prakashbabu
(Caudell et al. 2018), thus posing a public health concern. et al. 2020), which remain strongly anchored in African
Unboiled milk is preferred by certain pastoral communities communities. Milk is regarded as having important so-
in East Africa and, this preference is positively linked to in- cial, cultural, and economic value in many African coun-
creased human infections (Nato et al. 2019, Makala et al. tries, and its consumption is often governed by traditions
2020). Raw milk consumption is reported to be the lead- and cultures (Ndambi et al. 2008). Some communities are
ing factor in transmission of foodborne pathogens through still engaging in risky practices in terms of zoonotic dis-
milk and milk products. For example, of 16 reported cases eases, such as drinking unboiled milk, assisting animal births
of human campylobacteriosis screened in the USA, 15 were with bare hands, and living near livestock (Amenu et al.
found to have consumed raw milk (Oliver et al. 2009). 2019a). Milk processing rates are very low in East Africa,
This high incidence was local, however, as it occurred in e.g. in Kenya only 15% of milk is processed and the re-
one of the few federal states that permit sale of raw milk maining 85% is consumed raw, of which 40% is con-
(Oliver et al. 2009). Otherwise, milk-borne diseases are sumed by farmers and their families (Dolecheck and Bewley
rarely observed in high-income countries, due to hygienic 2018).

Received: February 7, 2023. Revised: March 30, 2023. Accepted: April 18, 2023

C The Author(s) 2023. Published by Oxford University Press on behalf of Applied Microbiology International. This is an Open Access article distributed

under the terms of the Creative Commons Attribution-NonCommercial License (https://creativecommons.org/licenses/by-nc/4.0/), which permits
non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact
e-mail: [email protected]
2 Mpatswenumugabo et al.

Scientific evidence has shown that pasteurization of raw and what is the relationship between milk consumption
milk kills pathogenic bacteria but does not affect its and occurrence of these bacterial zoonoses in East African
nutritional values (Macdonald et al. 2011). Pasteurization in- countries?”
volves heating food to a specific temperature for a set period
of time to inactivate non-spore-forming pathogenic bacteria,
to destroy most heat-sensitive bacteria, and extend the shelf
life of foods (LeJeune and Rajala-Schultz 2009). The most Materials and methods
common method of pasteurization in developing countries is Study design
cooking or boiling in the household, which lacks standardiza- A systematic review was performed according to the Preferred
tion (Murchie 2016). It is thus difficult to effectively eliminate Reporting Items for Systematic reviews and Meta-Analyses
pathogenic bacteria from pasteurized foods, while in devel- (PRISMA) guidelines (Fig. 1).
oped countries like the USA, high-temperature short-time pas-
teurization is the most commonly used method (Ahmed and Search strategy

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Ramaswamy 2007).
An initial review of the literature was conducted through
Some factors associated with zoonosis outbreaks have been
a search in databases such as Web of Science, PubMed,
identified. For example, in Tanzania, assisting an aborting ani-
and Scopus for all relevant and recent articles published
mal, proximity of cattle to residential neighborhoods, and reli-
from 2010 to 2021 on milk quality and bacterial zoonoses
gious beliefs have been found to be associated with brucellosis
(brucellosis, campylobacteriosis, E. coli, Q fever, salmonel-
infection in humans (John et al. 2010). These contributing fac-
losis, and tuberculosis) in seven East African countries (Bu-
tors vary from country to country, but most are very common
rundi, Ethiopia, Kenya, Rwanda, South Sudan, Tanzania, and
in East Africa. Moreover, several studies have demonstrated
Uganda). Since the search strategies involved complex com-
that knowledge of some zoonotic diseases is low among com-
binations, milk-related terms (e.g. cow milk, milk quality, and
munities in low-income countries (Morse et al. 2012, Worsley-
milk contamination), disease-specific names, and finally coun-
Tonks et al. 2022). Additionally, some zoonotic diseases are
try, search strings were systematically constructed. Disease-
neglected or confused with febrile illnesses, most of which are
specific search strings were formed using a combination of sci-
confused with endemic malaria, hindering effective diagno-
entific disease name (e.g. tuberculosis), and agent name (e.g.
sis and treatment, and also prevention (Chipwaza et al. 2014,
Mycobacterium), combined using the Boolean operator, ‘OR’.
Carugati et al. 2019). Q fever; an infectious disease caused by
Additionally, the Boolean operator ‘AND’ was used to com-
Coxiella burnetii, remains a neglected zoonosis in many devel-
bine milk-related terms to zoonotic diseases and specific coun-
oping countries and this has implications for its management
tries. The following search terms, combined with Boolean op-
and resurgence (Njeru et al. 2016). Although evidence sug-
erators, were used to conduct the literature review: cow milk,
gests that Q fever prevalence is relatively low in some African
milk product, milk consumption, milk contamination, milk
countries, its endemicity requires good human awareness for
quality, bacterial zoonosis, zoonos∗, tuberculosis, Mycobac-
appropriate control measures (Wardrop et al. 2016). There-
terium, Brucell∗, Salmonell∗, Campylobact∗, E. coli, E. coli,
fore, it is very important to raise awareness among communi-
and Country. When a relevant publication was identified, the
ties and health service providers about the burden and man-
reference list was examined to identify additional relevant
agement of zoonotic diseases (Zhang et al. 2016).
publications. Search hits were exported to Endnote, combined
Studies conducted specifically in East Africa have shown
into one library, and scanned for duplicates using methods
a trend for brucellosis, tuberculosis, and Q fever out-
described previously (Bramer et al. 2016). A manual check
breaks in pastoralist communities (Cavalerie et al. 2021).
was performed to confirm the relevance of the final set of
In knowledge, attitude, and practices (KAP) studies on
papers.
dairy farmers regarding zoonotic diseases, a correlation has
been found between farmers’ behavior and an increase in
zoonotic disease incidence (Amenu et al. 2019b, Prakash- Selection of studies and data extraction
babu et al. 2020, Nyokabi et al. 2021b). Several recom- For this review, only papers published in English were consid-
mendations for control programs for major zoonotic dis- ered. Apart from that, cross-sectional, longitudinal, and co-
eases in East Africa have been formulated (Cavalerie et al. hort studies were considered eligible. Articles involving milk
2021), including enhancing national research agendas and consumption and prevalence of zoonotic infections in humans
promoting the One Health approach. Prevention of bac- were considered eligible. Additionally, KAP studies were in-
terial zoonoses is a key component of future agricultural cluded to obtain relevant information on risk factors associ-
policies that could be implemented to reduce the health ated with zoonotic disease outbreaks in the study area, but
and economic burden of these diseases on the local com- meta-analysis papers were not included (Fig. 1). Papers with
munity members in East Africa. Therefore, this review fo- titles and/or abstracts that were not pertinent to the current
cused on the relationship between milk consumption and oc- research interest were excluded. The last search was made
currence of bacterial zoonoses in East Africa and particu- on 1 October 2021. All searches were conducted indepen-
larly on risk factors associated with the occurrence of im- dently by two authors (J.P.M. and M.A.M.), and disagree-
portant milk-borne bacterial zoonoses [brucellosis, salmonel- ments were resolved by consensus or by consultation with a
losis, campylobacteriosis, Escherichia coli infections, tuber- third author (J.B.N.). The following data were extracted from
culosis, and some neglected zoonoses (Q fever)] in hu- the original articles: (1) country of publication; (2) year of
mans consuming unsafe raw cow milk and other predis- publication; (3) zoonose occurrence; (4) type of study (cross-
posing factors. The analysis addressed the following re- sectional, KAP); (5) source of pathogens/data; and (6) name of
search question: “What are the most prevalent zoonoses, authors.
Bacterial zoonoses in East Africa 3

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Figure 1. PRISMA flow diagram showing the number of papers retained in different stages of the literature search. The final selection of papers to be
included in the review was done by considering both country and type of databases.

Figure 2. Distribution of different pathogens studied in published papers for countries in East Africa (2010–2021).

Results Studies on both pathogenic and commensal E. coli were

A review of the selected papers revealed that the most inves- included in the dataset (Table 3). Out of 15 articles re-
tigated pathogen was Brucella spp. (54.5%), followed by E. trieved, 26.6% (4/15) described pathogenic E. coli O157:
coli (18.2%), Salmonella spp. (12.1%), Mycobacterium spp. H7 serotype, while 66.6% (10/15) reported on other E. coli
(6.1%), and E. coli O157: H7 (6.1%) (Fig. 2). The least stud- strains in general. Most of the studies on E. coli O157: H7
ied pathogens were C. burnetii and Campylobacter spp. (both were carried out in Ethiopia (3/4), with only one in Tanza-
1.5%). Regardless of the country, brucellosis was the most nia. All these studies were cross-sectional (100%) in nature,
studied disease in East Africa. Among the selected countries, and the majority of bacteria were isolated from raw cow milk
Uganda and Tanzania had the highest number of publica- (80%). Irrespective of the E. coli serotype studied, Ethiopia ac-
tions on brucellosis [27.8% and 25.0% (n = 36), respectively], counted for the majority (46.6%) of the papers retrieved, fol-
while Burundi had the lowest number (2.8%) (Table 1). lowed by Kenya (26.6%), Tanzania (13.3%), Rwanda (6.6%),
In terms of study type, cross-sectional studies were predom- and Uganda (6.6%), while no articles were found for Burundi
inant (72.2%), while KAP studies only represented 11% of all and South Sudan.
studies included in the review. Only five case controls and one In total, seven articles on Salmonella spp. were included in
cohort study were considered eligible due to their target pop- the dataset, all from four countries (Table 4). The majority of
ulation and descriptive findings. Overall, studies on humans, these studies were cross-sectional (85.7%), with only one lon-
raw milk, livestock-humans, and livestock represented 41.6%, gitudinal study (14.3%). Most were carried out in Ethiopia
19.4%, 19.4%, and 16.7% of the total, respectively (Table 2). (42.8%), followed by Rwanda (28.6%), while only one
4 Mpatswenumugabo et al.

Table 1. Number of publications per pathogen and country.

E. coli
Country Brucella spp. Salm. spp. E. coli 0157:H7 Mycob. spp. Camp. spp. C. burnetii Total

Burundi 1 0 0 0 0 0 0 1
Ethiopia 5 4 4 3 1 0 0 17
Kenya 5 0 4 0 0 0 1 10
Rwanda 2 2 1 0 0 0 0 5
South. Sudan 4 0 0 0 1 0 0 5
Tanzania 9 1 2 1 0 1 0 14
Uganda 10 1 1 0 2 0 0 14
Total 36 8 12 4 4 1 1 66

Salm., Salmonella; E. coli, Escherichia coli; Mycob., Mycobacterium; Camp., Campylobacter.

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article was retrieved for Tanzania (14.3%) and one for prevalence was higher among people consuming locally pro-
Uganda (14.3%). cessed milk products (OR 2.54, 95% CI 1.12–5.78) (Tumwine
Analysis of the dataset revealed that KAP studies accounted et al. 2015).
for 58.8% (10/17) and studies on risk factors 35.2% (6/17)
(Table 5). Regardless of the type of zoonotic disease investi-
gated, most studies were carried out in Kenya (35.2%), fol- Brucellosis
lowed by Uganda (23.5%), while Ethiopia and Tanzania each Although both animals and humans are at high risk of con-
accounted for 17.6%, and only one study was carried out tracting brucellosis, a comparative study of humans and live-
in South Sudan (5.8%). No studies were retrieved for the stock in Kenya revealed that the seroprevalence was two-fold
remaining two East African countries considered (Burundi higher in animals than in humans living in the same pastoral
and Rwanda). Different laboratory techniques were used to community (Osoro et al. 2015). Reported seroprevalence rates
isolate, identify, and characterize selected bacteria, ranging of Brucella spp. isolated from raw milk varied by country, with
from standard microbiological methods to molecular diagnos- the highest rate recorded in Tanzania (Swai and Schoonman
tic techniques (Table 6). 2011) and the lowest in Uganda (Makita et al. 2010). Inter-
estingly, similar findings on human brucellosis were reported
in studies on pastoral communities in Tanzania (Asakura et
al. 2018a) and on pregnant women living close to wildlife
Discussion and livestock areas who suffered abortions in association with
In the selected dataset, brucellosis was the most frequently some predisposing factors to brucellosis (Assenga et al. 2015,
investigated of prevalent zoonotic diseases in East Africa. Bodenham et al. 2020, Makala et al. 2020, Ntirandekura et
The analysis revealed some discrepancies between the diag- al. 2020). Other studies have found that consuming unboiled
nostic methods used, which suggests underestimation of the raw milk (Nasinyama et al. 2014) and living in proximity
true prevalence rates of the zoonotic pathogens investigated to livestock (Asiimwe et al. 2015, Tumwine et al. 2015) are
and their relationship to the milk consumption patterns. It strongly associated with occurrence of human brucellosis. A
also revealed that consumption of unpasteurized milk, lack study in Kenya concluded that consumption of unpasteurized
of knowledge about zoonotic diseases, and poor milk han- milk, handling infected aborted materials without protection,
dling were associated with the occurrence of zoonotic bacte- and consuming raw meat and raw blood were potential routes
rial infections. In low- and middle-income countries, the bur- of exposure to brucellosis and other zoonoses (Onono et al.
den of foodborne disease is disproportionately high and orig- 2019). Another study reported that 79.5% of nomadic pas-
inates from many food sources (Havelaar et al. 2022), and toralists participate in risky practices for human brucellosis,
their effects may be acute or chronic in nature. Evidence from e.g. drinking unboiled milk showed a positive correlation with
various studies indicated a positive association between milk Brucella spp. seroprevalence (68.2%) (Njenga et al. 2020).
consumption and the risk of contracting bacterial zoonoses Majalija et al. (2018) found that 14% of respondents reported
in Africa (Kazoora et al. 2016, Dadar et al. 2019, Nyokabi drinking raw milk, of which 46.4% were seropositive to Bru-
et al. 2021). Conventionally, raw milk is boiled before con- cella abortus, compared with 1.2% seropositive among those
sumption (Fusco et al. 2020), but some African communi- who did not drink raw milk. They also found a significant
ties do not boil milk owing to traditional and cultural beliefs, association between consuming raw milk and seroprevalence
including that “if you boil milk you will provoke udder in- of B. abortus (OR 2.162, 95% CI 0.021–1.379), while other
flammation in the cows that produced the milk” (Prakashbabu risk factors did not show any significant correlation (Majal-
et al. 2020). While boiling milk greatly reduces the presence ija et al. 2018). Other studies observed a similar pattern where
of most bacteria (Tremonte et al. 2014), it is possible for milk seroprevalence of human brucellosis was positively associated
to be re-contaminated due to poor storage and handling prac- with raw milk consumption (OR 406.15, 95% CI 47.67–
tices. In fact, one study found no statistically significant differ- 3461.69) (Migisha et al. 2018) or consumption of unpasteur-
ence between the levels of bacterial contamination in raw and ized milk (P = .023; OR 2.57; 95% CI 1.14–5.80) (Muloki et
boiled milk (Häsler et al. 2014). Locally processed milk and al. 2018).
milk products could potentially pose a risk to consumers, pos- Low education level coupled with lack of other sources of
sibly due to inadequate cooling chain, poor processing, and/or income were reported to leave the communities concerned
handling practices when serving customers. This risk was con- with no choice but to engage in risky milk consumption prac-
firmed by findings in a study where human brucellosis sero- tices (Njenga et al. 2020). Many studies showed that economic
Bacterial zoonoses in East Africa 5

Table 2. Studies on livestock and human brucellosis in East Africa (2010–2021).

Source of
Country Prevalence rate Type of study pathogens/data Reference(s)

Burundi
14.7% (95% CI 9.4%–20.8%) Cross-sectional Dairy cattle Musallam et al.
(2019)
Ethiopia
2.4% (95% CI 1.4%–3.7%) in cattle 2.6% Cross-sectional Ruminants and Edao et al. (2020)
(95% CI 1.2%–5%) in humans pastoralists
3.0% in cows and 2.4% in humans Cross-sectional Livestock and Lakew et al. (2019)
humans
31.5% (95% CI 27.4%–36.0%) Cross-sectional Humans Mehari et al. (2021)
NA KAP study Farmers Legesse et al. (2018)

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3.5% (95% CI 2.4%–4.5%) Cross-sectional Cattle Megersa et al. (2011)
Kenya
15.4% (95% CI 12.0%–19.5%) Cross-sectional Humans Kiambi et al. (2020)
OR 7.7 (95% CI 1.5–40.1) Case-control Humans/unboiled Muturi et al. (2018)
milk
NA KAP Study Livestock and Njenga et al. (2020)
humans
NA Cross-sectional and Raw milk Onyango et al.
case-control (2021)
16% in animals and 8% in humans Cross-sectional Livestock and Osoro et al. (2015)
humans
Rwanda
19.7% (95% CI 15.5%–24.4%) Cross-sectional Raw milk Djangwani et al.
(2021)
25% Cross-sectional Humans Rujeni and
Mbanzamihigo
(2014)
South Sudan
NA Case-control Humans Lado et al. (2012)
31% (95% CI 28.0%–34.2%) in cattle Cross-sectional Cattle and herders Madut et al. (2018a)
and 33.3% (23.9%–44.3%) in herders
23.3% (97/416) Cross-sectional Humans Madut et al. (2018b)
27.2% (95% CI 23.9%–30.6%) Cross-sectional Humans Madut et al. (2019)
Tanzania
44.4% (55/124, 95% CI 35.5%–53.5%) Cross-sectional Cattle Asakura et al.
(2018a)
7.0% (28/673, 95% CI 5.7%–8.4%) Cross-sectional Cattle Asakura et al.
(2018b)
0.6% (95% CI 0.1–2.1%) in humans and Cross-sectional Livestock, wildlife, Assenga et al. (2015)
6.8% (95%CI: 5.4%–8.5%) in cattle and humans
NA Case-control Livestock Assenga et al. (2016)
6.10% Cross-sectional Humans Bodenham et al.
(2020)
10.9% (34/313) Cross-sectional Humans Makala et al. (2020)
NA KAP study Local community Mburu et al. (2021)
21% (95% CI 12.5%–32%) in women Cohort Livestock and Ntirandekura et al.
and 5% (95% CI 3.1%–8%) in ruminants humans (2020)
56% Cross-sectional Raw cow milk Swai and Schoonman
(2011)
Uganda
NA Case-control Pastoralists Asiimwe et al. (2015)
26.5% (49/185) Cross-sectional Raw cow milk Asiimwe et al. (2015)
NA KAP study Pastoralists Kansiime et al.
(2014)
7.5% (n = 200) Cross-sectional Humans Majalija et al. (2018)
12.6% (90% CI 6.8%–18.9%) Risk assessment Raw cow milk Makita et al. (2011)
14.9% (95% CI 10.6%–20.1%) Cross-sectional Humans Migisha et al. (2018)
18.70% Cross-sectional Humans Muloki et al. (2018)
5.8% (95% CI 3.3%–8.3%) in farmers Cross-sectional Cattle farmers and Nasinyama et al.
and 9% (95% CI 13.3%, 4.7%) in milk consumers (2014)
consumers
25.50% Cross-sectional Raw cow milk Rock et al. (2016)
17.0% (n = 235) Cross-sectional Humans Tumwine et al.
(2015)

NA, not available/applicable.

6 Mpatswenumugabo et al.

Table 3. Studies on E. coli spp., including E. coli O157: H7, in East Africa (2010–2021).

Source of
Country Prevalence rate (%) Type of study pathogens/data Reference(s)

Ethiopia
5.2% (E. coli O157:H7) Cross-sectional Raw cow milk Ababu et al. (2020)
2.5% (E. coli O157:H7) 51.7% (E. coli) Cross-sectional Ready to consume Amenu et al. (2019a)
milk
2.9% (E. coli O157:H7) Cross-sectional Raw cow milk Disassa et al. (2017)
33.9% (E. coli) Cross-sectional Raw cow milk
58% (E. coli) Cross-sectional Raw cow milk Reta et al. (2016)
29.6% (E. coli) Cross-sectional Raw and pasteurized Garedew et al. (2012)
cow milk
NA (E. coli) Cross-sectional Raw cow milk Berhe et al. (2020)

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Kenya
66.7% (E. coli) Cross-sectional Unpasteurized milk Brown et al. (2020)
25% in cow milk and 32% in camel milk Cross-sectional Cow milk and camel Nato et al. (2019)
(E. coli) milk
13.8% (E. coli) Cross-sectional Raw cow milk Ngaywa et al. (2019)
42.4% (E. coli) Cross-sectional Raw cow milk Nyokabi et al. (2021a)
Rwanda
8.5% (E. coli) at farm level 62.5% (E. coli) Cross-sectional Raw cow milk Ndahetuye et al.
at MCC level (2020)
Tanzania
66% (E. coli) Cross-sectional Raw cow milk Ngasala et al. (2015)
10.1% (E. coli O157:H7) Cross-sectional Raw cow milk and Schoder et al. (2013)
milk products
Uganda
12% (E. coli) Cross-sectional Raw cow milk Majalija et al. (2020)

NA, not available/applicable.

Table 4. Studies on Salmonella spp. in East Africa (2010–2021).

Source of
Country Prevalence rate (%) Type of study pathogens/data Reference(s)

Ethiopia
6% Cross-sectional Raw milk Ejo et al. (2016)
6.3% Longitudinal Raw milk Geresu et al. (2021)
3.3% Cross-sectional Raw milk Reta et al. (2016)
Rwanda
5.2% Cross-sectional Raw milk Kamana et al. (2014)
14% Cross-sectional Raw milk Ndahetuye et al.
(2020)
Tanzania
10.1% Cross-sectional Raw milk and milk Schoder et al. (2013)
products
Uganda
5% Cross-sectional Raw cow milk Majalija et al. (2020)

insecurity and culture are positively associated with engage- with bare hands (P = .03) than other tribes (Asakura et al.
ment in risky food practices (James et al. 2014, Kopetz et 2018a). Other studies suggested that community knowledge
al. 2014, Cheng et al. 2016). Education is important to pre- about the zoonotic nature of brucellosis is not positively as-
vent the spread of disease in such communities, e.g. 33.3% sociated with a decrease in use of risky practices by commu-
seroprevalence to B. abortus was found among those with no nity members. Legesse et al. (2018) conducted a KAP study on
formal education in Uganda (Majalija et al. 2018) and poor human brucellosis and found that the majority (89.3%) of in-
community knowledge of brucellosis was shown to be signif- terviewed farmers had good knowledge of brucellosis but still
icantly associated with human brucellosis seroprevalence and consumed unpasteurized milk. Lack of knowledge about bru-
risky practices such as drinking raw milk (17.6%, P < .01) cellosis among community members is a predisposing factor
and blood (35.3%, P < .01) (Asakura et al. 2018b). In some to human brucellosis (Mburu et al. 2021). It is possible that
low-income settings, cultural beliefs are a constraint to edu- there may be perpetual transmission of brucellosis to humans
cation. For example, Maasai communities in Tanzania were from raw milk consumption in these communities, due to in-
found to rate education less highly than other communities in creased malpractices. These findings emphasize the need for
that country, and are thus more likely to employ more risky awareness campaigns and training programs for smallholder
practices for human brucellosis infection, such as drinking raw dairy farmers in order to foster behavioral change and im-
milk (P = .06) or blood (P < .01) and helping calf delivery prove milk quality along the whole value chain.
Bacterial zoonoses in East Africa 7

Table 5. KAP studies and risk factors associated with milk-borne bacterial zoonoses identified in East Africa (2010–2021).

Milk-borne diseases of
Country interest/pathogen Type of study Target population Reference(s)

Ethiopia
Brucellosis KAP study Farmers Legesse et al. (2018)
Salmonella spp. Quantitative risk assessment Raw milk Weldeabezgi et al. (2020)
Bovine tuberculosis Cross-sectional Cattle Kemal et al. (2019)
Kenya
C. burnetii (Q fever) KAP study Residents Ndeereh et al. (2016)
Brucella spp. KAP study Nomadic pastoralists and Njenga et al. (2020)
non-pastoralists
Zoonotic diseases KAP study Informal value chain actors Nyokabi et al. (2018)
N/A KAP study Farmers Nyokabi et al. (2021b)

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Brucellosis KAP study Farmers Onono et al. (2019)
Brucellosis Cross-sectional and Pastoral communities Onyango et al. (2021)
case-control
South Sudan
Brucellosis Case-control Humans Lado et al. (2012)
Tanzania
E. coli Cross-sectional Humans Caudell et al. (2018)
Brucellosis KAP study Local community Mburu et al. (2021)
Zoonoses KAP study Local community Swai et al. (2010)
Uganda
Brucellosis Case-control Pastoralists Asiimwe et al. (2015)
Human brucellosis KAP study Local community Majalija et al. (2018)
Brucellosis KAP study Pastoralists Kansiime et al. (2014)
Human tuberculosis Cross-sectional Livestock and humans Meisner et al. (2019)
Mycobacterium spp. KAP study Cattle farmers Kazoora et al. (2016)

Campylobacter spp. 1% and 50% of healthy cattle carry and shed E. coli O157:
Isolation and identification of Campylobacter spp. are difficult H7 in their feces (Cho et al. 2006), raw milk contamination
due to its long incubation period and special culture require- can occur during milk handling. Some of the studies reviewed
ments, such as microaerobic conditions (Brandl et al. 2004), suggested that the presence of E. coli bacteria in raw and pas-
which makes it difficult to study. Only one study on Campy- teurized milk is associated with poor and unhygienic milk
lobacter spp., in raw milk from East Africa (Kashoma et al. handling practices, fecal contamination, higher environmen-
2016), was included in this review. That study found that 13% tal contamination, and poor storage conditions (Ngasala et
of the sampled raw milk contained different Campylobacter al. 2015; Reta et al. 2016). Other studies reported that E.
species. In contrast, studies in developed countries show that coli is frequently detected at milk collection center (MCC)
Campylobacter species are highly frequently isolated from level, possibly due to bacterial contamination by workers and
raw milk and are associated with campylobacteriosis in hu- equipment used in milk storage (Ndahetuye et al. 2020). The
mans. For example, Del Collo et al. (2017) detected Campy- presence of E. coli O157: H7 bacteria in raw milk is a global
lobacter spp. at 46% of bulk tank milk samples from US public health concern. In Africa, the risk of E. coli O157:
dairies, while a follow-up study of a milk-borne campylobac- H7 outbreaks is highly associated with raw milk consump-
teriosis outbreak in Finland revealed persistent C. jejuni con- tion. Moreover, a study in Tanzania found that consumption
tamination of bulk tank milk for several months (Jaakkonen of raw milk was associated with an increased probability of
et al. 2020). Further, a retrospective cohort study conducted in carrying multidrug-resistant E. coli strains, which was most
England revealed a positive correlation between campylobac- likely connected to scarcity of potable water and to the in-
teriosis outbreaks in humans and consumption of unpasteur- formal sales channels for raw milk that prevail in low-income
ized milk (Kenyon et al. 2020). These findings suggest that countries operating outside national quality control standards
raw milk is likely to be contaminated with pathogenic Campy- and regulations (Caudell et al. 2018). In the USA, researchers
lobacter spp. and, if consumed, could pose a potential human have found a positive correlation between E. coli O157: H7
health risk. outbreaks and consumption of raw cow milk (Denny et al.
2008). Similar findings have been reported in Brazil (Cerva et
al. 2014).
Escherichia coli
Escherichia coli is a gram-negative, rod-shaped, facultative Salmonella spp.
anaerobic bacterium. Most E. coli strains are non-pathogenic In the set of papers reviewed, presence of Salmonella spp.
and colonize the gastrointestinal tract of both animals and hu- in raw milk was significantly associated with poor hygiene
mans, but some strains have become very pathogenic through practices at farm level (Ndahetuye et al. 2020) or poor milk
genetic evolution (Kaper et al. 2004). The most frequently handling practices by traders due to lack of adequate train-
isolated pathogenic E. coli is the enterohemorrhagic E. coli ing (Schoder et al. 2013). Similarly, findings in Uganda sug-
(EHEC) serotype O157: H7 (Shridhar et al. 2017). Since cat- gest that the main sources of Salmonella spp. in raw milk
tle are the natural reservoir of E. coli O157: H7 and between can be grouped into poor hygiene, handling, and transporta-
8 Mpatswenumugabo et al.

Table 6. Diagnostic techniques used in isolating and identifying zoonotic pathogens.

Number of
Pathogens Laboratory method references Reference(s)

Brucella spp. Milk ring test (only) 1 Swai and Schoonman (2011)
Milk ring test and ELISA 1 Kamwine et al. (2017)
ELISA (only) 9 Makita et al. (2010), Muloki et al. (2018), Muturi et
al. (2018), Asakura et al. (2018a), Madut et al. (2019),
Musallam et al. (2019), Djangwani et al. (2021),
Osoro et al. (2015), and Rock et al. (2016)
Rose Bengal (only) 1 Rujeni and Mbanzamihigo (2014)
Rose Bengal and ELISA 5 Asakura et al. (2018b), Assenga et al. (2015), Edao et
al. (2020), Madut et al. (2018a), and Makala et al.
(2020)

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Rose Bengal and any other test 5 Megersa et al. (2011), Tumwine et al. (2015), Migisha
(complement fixation, culture, et al. (2018), Makala et al. (2020), and Ntirandekura
agglutination, fluorescence et al. (2020)
polarization)
Rose Bengal, agglutination, and 1 Madut et al. (2018b)
ELISA
Agglutination (Only) 2 Asiimwe et al. (2015) and Majalija et al. (2018)
Agglutination and ELISA 1 Nasinyama et al. (2014)
PCR (only) 1 Kiambi et al. (2020)
Culture and PCR 1 Bodenham et al. (2020)
Campylobacter spp. Multiplex PCR 1 Kashoma et al. (2016)
E. coli Standard microbiological 12 Caudell et al. (2018), Amenu et al. (2019b), Ababu et
techniques (culture, biochemical al. (2020), Berhe et al. (2020), Brown et al. (2020),
tests, and microscopic Garedew et al. (2012), Nato et al. (2019), Majalija et
examination) al. (2020), Ndahetuye et al. (2020), Nyokabi et al.
(2021b), Reta et al. (2016), and Gwandu et al. (2018)
Standard microbiological 1 Ngaywa et al. (2019)
techniques confirmed by PCR and
sequencing
Viable counts (TBC, TCC) 2 Schoder et al. (2013) and Ngasala et al. (2015)
Salmonella spp. Standard microbiological 6 Kamana et al. (2014), Ejo et al. (2016), Majalija et al.
techniques (culture, biochemical (2020), Ndahetuye et al. (2020), Geresu et al. (2021),
tests, and microscopic and Reta et al. (2016)
examination)
Viable counts (TBC, TCC) 1 Schoder et al. (2013)
Mycobacterium spp. Ziehl–Neelsen (ZN) and 1 Boyong et al. (2018)
fluorescence microscopy (FM)
Tuberculosis skin test (TST) 1 Meisner et al. (2019)

ELISA, enzyme-linked immunosorbent assay; PCR, polymerase chain reaction; TBC, total bacteria count; and TCC, total coliform count.

tion practices (Majalija et al. 2020). However, Reta et al. Tuberculosis

(2016) observed a more complex contamination process that Tuberculosis (TB) is a leading zoonotic infectious cause of
included all critical control points along the raw milk value human death worldwide, which is transmitted to humans
chain, resulting in an increase in total bacterial counts from through consumption of raw, unpasteurized or contaminated
the start (12% on-farm) to the end (42.9% at the point of milk, dairy products and other animal products (Kazoora et
sale) of the value chain. Similarly, a study in Rwanda found al. 2016). Two studies dealing with perceptions of the lo-
that Salmonella spp. isolation rate was much lower (5.2%) at cal communities and risk factors associated with the occur-
farm level than in milk shops (21.4%) (Kamana et al. 2014). rence of TB in humans were included in this review (Kazoora
In that study, the high isolation rate at milk shops was ten- et al. 2016, Meisner et al. 2019). The two studies revealed
tatively attributed to poor handling and unhygienic practices that local communities engage in predisposing risk practices
by the personnel (Kamana et al. 2014). However, contradic- such as consuming raw milk, consuming dairy products from
tory findings were made by Ndahetuye et al. (2020), who raw milk, living in proximity with livestock among others
recovered no Salmonella spp. in milk samples from MCC, (Kazoora et al. 2016, Meisner et al. 2019). It was also re-
whereas a significant proportion (14.0%) of milk samples ported that the majority of study respondents have very low
from farms showed presence of Salmonella spp. This differ- knowledge and poor practices regarding zoonotic aspect of
ence could have been due to the dilution effect resulting in TB (Meisner et al. 2019). It is important to note that de-
undetectable levels of Salmonella spp. in milk samples from spite the knowledge about TB, many people still consume
MCC (Ndahetuye et al. 2020). This is supported by the fact raw milk as a necessity due to lack of time or resources to
that MCCs have cold chain infrastructure that reduces growth properly pasteurize milk before consumption (Kazoora et al.
of microorganisms and improves milk quality (Demirbaş et al. 2016). This poor practice is also associated with low educa-
2009, O’Connell et al. 2017), in contrast to direct sales from tion level and living in low-resource settings (Njenga et al.
farms. 2020).
Bacterial zoonoses in East Africa 9

Q fever income countries, due to lack of adequate diagnostic capabil-

Q fever is an emerging zoonotic disease caused by an intra- ity (Ndeereh et al. 2016). Finally, access to improved diagnos-
cellular bacterium C. burnetii (Porter et al. 2011). Coxiella tic tools and equipment in low- and middle-income countries
burnetii is transmitted to humans through direct contact, in- is very difficult due to insufficient funding allocated to disease
halation of contaminated aerosols, or by consuming contam- diagnosis, lengthy procurement processes, to cite a few (Yadav
inated animal products, mainly unboiled milk (Celina and et al. 2021).
Cerný 2022). Only one article investigating the knowledge,
attitudes, and practices about Q fever and rickettsioses were
Conclusions
included in this review (Ndeereh et al. 2016). The study re-
vealed that the local communities have no knowledge about Overall, this review revealed potential health risks to raw
Q fever, while only 9.1% of health providers know about the milk consumers in East Africa. There is sufficient evidence
disease (Ndeereh et al. 2016). This low knowledge among to show that milk-borne bacterial infections in East African
health providers could be justified by the fact that Q fever is countries are associated with consumption of contaminated

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poorly diagnosed in low and middle-income countries, and the raw milk, which is common practice in many East African
disease is worldwide considered a neglected and re-emerging counties. Inadequate cold chain conditions along the milk
zoonotic disease (Ullah et al. 2022). It is currently known that value chain, poor milking practices, and lack of awareness of
ingestion of contaminated raw milk poses a low risk of con- the health risks of consuming unpasteurized milk further pre-
tracting Q fever since the oral route is reported to be a less dispose milk consumers to the risk of contracting milk-borne
efficient way of transmission (Arricau-Bouvery and Rodolakis diseases, as do lack of infrastructure, inadequate boiling, and
2005). Despite this low probability of transmission, we recom- recontamination of boiled milk due to poor storage conditions
mend special attention to reducing exposure to raw milk for and handling practices. However, the findings should be in-
at risk people (young children, old people, pregnant women, terpreted with caution because most of the articles reviewed
patients with cardiac pathology, or immunosuppressed) and described cross-sectional studies that could not provide clear
promoting consumption of pasteurized milk and its products evidence on the persistent exposure of consumers to contami-
to decrease the prevalence of Q fever. nated raw milk. Therefore, further studies involving isolation
and identification of pathogenic bacteria in milk are needed
to identify zoonotic risk factors associated with raw milk con-
Investigation methods sumption.
Scrutiny of the investigation methods used in the articles in- Only papers published in English were included in the re-
cluded in this review revealed that cross-sectional study was view, which may explain why there were few articles from
the most common method used. This method has scientific Rwanda (a bilingual country) and Burundi (a French-speaking
limitations when assessing temporal variations and the causal country). In addition, Rwanda and Burundi are smaller than
effect of independent variables on the response variable (Wang other East African countries from which many publications
and Cheng 2020). However, the trends in the dataset revealed were retrieved. However, the findings are still generalizable to
a common pattern of prevalence of the investigated diseases those two countries. In fact, since similar findings were found
or pathogens in all selected countries, confirming the validity for different countries at different times, the conclusions on as-
of the results. Laboratory diagnostic methods used in the pa- sociations between risk factors and the occurrence of zoonotic
pers included rapid tests, conventional microbiological tech- infections are likely to be valid. Considering the limitations in
niques, and enzymatic techniques coupled with molecular di- diagnostic methods used in some of the studies reviewed, it is
agnosis. However, the laboratory methods employed in many obvious that the true prevalence rates of these zoonotic dis-
studies resulted in some data gaps. For example, Kamwine et eases might be higher than reported. Therefore, further live-
al. (2017) found that the milk ring test for brucellosis identi- stock and human studies using advanced investigation meth-
fication had lower sensitivity (85%) and specificity (95.5%) ods are needed. Additionally, East African countries need to
than the indirect enzyme-linked immunosorbent assay (sen- invest in modern diagnostic tools and equipment, in hospitals
sitivity 98.5%, specificity 99.5%). They concluded that the and especially in local rural settings. Greater access to these
presence of Brucella spp. antibodies in milk could not be as- tools should be supported to improve surveillance and con-
sociated with a current infection in lactating cows, and rec- trol programs for both humans and animals. Finally, a tailor-
ommended a field study to confirm the source of the antibod- made training program for all milk value chain actors should
ies in raw milk (Kamwine et al. 2017). Most ELISA methods be implemented to improve the safety of milk sold via infor-
do not report the current infection and sometimes detect some mal channels and a One Health approach should be applied.
immunoglobulins (Ig) and not others (Osoro et al. 2015). Sim-
ilarly, a study on patients presenting with febrile illnesses and
seeking healthcare services in Kenya found that the febrile bru- Conflict of interest
cella plate agglutination test, which is commonly used in hos- The authors declare that there are no commercial or financial
pitals, had low diagnostic performance compared with real- relationships that could be construed as a potential conflict of
time polymerase chain reaction, with estimated sensitivity of interest.
only 36.6% (95% CI 24.6%–50.1%) and specificity of 69.3%
(95% CI 64.0%–74.3%) (Kiambi et al. 2020). Additionally,
identification and differentiation of mycobacteria belonging Funding
to the Mycobacterium tuberculosis complex could have pro- This material is based on project work supported by the
vided evidence of their zoonotic nature and their transmis- Swedish International Development Cooperation Agency
sion in humans. These discrepancies in diagnostic methods (SIDA). Research Partnership 2019–2024, SIDA contribution
result in underreporting of many zoonotic diseases in low- No. 11277.
10 Mpatswenumugabo et al.

Author contributions Bramer WM, Giustini D, De Jong GB et al. De-duplication of database

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tiste Ndahetuye (Conceptualization, Supervision, Writing – re- Campylobacter jejuni in the phyllosphere with that in the rhi-
view & editing), Ewa Wredle (Conceptualization, Supervision, zosphere of spinach and radish plants. Appl Environ Micro-
Writing – review & editing), and Renée Båge (Conceptualiza- biol 2004;70:1182–9. https://doi.org/10.1128/AEM.70.2.1182-11
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resistant bacteria detected in milk marketed for human consumption
in Kibera, Nairobi. PLoS One 2020;15:1–8. https://doi.org/10.137
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Carugati M, Kilonzo KG, Crump JA. Fever, bacterial zoonoses, and One
The authors declare that all data supporting the findings of

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Health in sub-Saharan Africa. Clin Med 2019;19:375–80. https://do
this study are available within the article (Tables 1–6). i.org/10.7861/clinmed.2019-0180
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