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A sero-epidemiological analysis of Coxiella burnetii infection and its risk factors in livestock from Addis Ababa, Adama, and Modjo abattoirs and pastoral areas of Oromia, Ethiopia

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Background Coxiella burnetii is causing infections in both humans and animals, resulting in Q fever and Coxiellosis, respectively. Information on the occurrence of C. burnetii infection is scarce in Ethiopia. This study estimated the sero-prevalence of C. burnetii infection and associated risk factors in four common livestock species from Addis Ababa, Adama, and Modjo abattoirs and pastoral areas of Oromia, Ethiopia. Results/principal findings Sera samples were analyzed for the presence of anti-C. burnetii antibodies using an indirect Enzyme Linked Immunosorbent Assay kit. Out of the 4140 serum samples tested, 777 (18.77%; 95% CI: 17.59, 19.99) were found positive for C. burnetii. The sero-prevalence estimate was 27.17% at Addis Ababa abattoir, 19.41% at Adama abattoir, 19.13% at Modjo abattoir and 12.1% in animals tested from pastoral areas. Sera analysis at the animal species level showed that cattle exhibited the lowest sero-prevalence estimate (11.83%; 95% CI, 10.27–13.53%), while the highest was observed in camels (28.39%; 95% CI, 25.16–31.80%). The sero-prevalence estimate was 21.34% (95% CI, 18.86–23.99%) in goats and 20.17% (95% CI, 17.49–23.07%) in sheep. The results of multivariable logistic regression analysis showed that species, age, sex of animals and tick infestation were important risk factors for C. burnetii infection. The odds of infection were 3.22 times higher in camels and almost twice as high in goats and sheep compared to cattle. Adult animals were infected more likely (OR = 3.23) than young ones. Interestingly, a significant difference was observed in the sero-prevalence of infection between animals that were infested with ticks (OR = 16.32) and those which were tick-free. Conclusion This study provides valuable insights into the sero-epidemiology of C. burnetii infection in four common livestock species at major abattoirs and pastoral areas of Ethiopia. The findings highlight the need for further studies and implementing surveillance and biosecurity measures to prevent the spread of the disease in both humans and livestock to safeguard the economical and public health aspects.
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RESEARCH ARTICLE
A sero-epidemiological analysis of Coxiella
burnetii infection and its risk factors in
livestock from Addis Ababa, Adama, and
Modjo abattoirs and pastoral areas of
Oromia, Ethiopia
Ashenafi Milkesa
1
, Tesfaye Rufael
2
, Getachew Kinfe
2
, Redeat Belaineh
2
, Abdella Bulbula
2
,
Donghee Cho
1
, Mohammed Naimuddin
1
, Teshale Sori
3
, Hunduma DinkaID
1
*
1Department of Applied Biology, School of Applied Natural Science, Adama Science and Technology
University, Adama, Ethiopia, 2Animal Health Institute (AHI), Sebeta, Ethiopia, 3Department of Clinical
Studies, College of Veterinary Medicine and Agriculture, Addis Ababa University, Bishoftu, Ethiopia
*dinkahu@gmail.com
Abstract
Background
Coxiella burnetii is causing infections in both humans and animals, resulting in Q fever and
Coxiellosis, respectively. Information on the occurrence of C.burnetii infection is scarce in
Ethiopia. This study estimated the sero-prevalence of C.burnetii infection and associated
risk factors in four common livestock species from Addis Ababa, Adama, and Modjo abat-
toirs and pastoral areas of Oromia, Ethiopia.
Results/principal findings
Sera samples were analyzed for the presence of anti-C.burnetii antibodies using an indirect
Enzyme Linked Immunosorbent Assay kit. Out of the 4140 serum samples tested, 777
(18.77%; 95% CI: 17.59, 19.99) were found positive for C.burnetii. The sero-prevalence
estimate was 27.17% at Addis Ababa abattoir, 19.41% at Adama abattoir, 19.13% at Modjo
abattoir and 12.1% in animals tested from pastoral areas. Sera analysis at the animal spe-
cies level showed that cattle exhibited the lowest sero-prevalence estimate (11.83%; 95%
CI, 10.27–13.53%), while the highest was observed in camels (28.39%; 95% CI, 25.16–
31.80%). The sero-prevalence estimate was 21.34% (95% CI, 18.86–23.99%) in goats and
20.17% (95% CI, 17.49–23.07%) in sheep. The results of multivariable logistic regression
analysis showed that species, age, sex of animals and tick infestation were important risk
factors for C.burnetii infection. The odds of infection were 3.22 times higher in camels and
almost twice as high in goats and sheep compared to cattle. Adult animals were infected
more likely (OR = 3.23) than young ones. Interestingly, a significant difference was observed
in the sero-prevalence of infection between animals that were infested with ticks (OR =
16.32) and those which were tick-free.
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OPEN ACCESS
Citation: Milkesa A, Rufael T, Kinfe G, Belaineh R,
Bulbula A, Cho D, et al. (2024) A sero-
epidemiological analysis of Coxiella burnetii
infection and its risk factors in livestock from Addis
Ababa, Adama, and Modjo abattoirs and pastoral
areas of Oromia, Ethiopia. PLoS Negl Trop Dis
18(7): e0012287. https://doi.org/10.1371/journal.
pntd.0012287
Editor: Wen-Ping Guo, Chengde Medical
University, CHINA
Received: August 9, 2023
Accepted: June 11, 2024
Published: July 16, 2024
Peer Review History: PLOS recognizes the
benefits of transparency in the peer review
process; therefore, we enable the publication of
all of the content of peer review and author
responses alongside final, published articles. The
editorial history of this article is available here:
https://doi.org/10.1371/journal.pntd.0012287
Copyright: ©2024 Milkesa et al. This is an open
access article distributed under the terms of the
Creative Commons Attribution License, which
permits unrestricted use, distribution, and
reproduction in any medium, provided the original
author and source are credited.
Data Availability Statement: All relevant data are
within the manuscript.
Conclusion
This study provides valuable insights into the sero-epidemiology of C.burnetii infection in
four common livestock species at major abattoirs and pastoral areas of Ethiopia. The find-
ings highlight the need for further studies and implementing surveillance and biosecurity
measures to prevent the spread of the disease in both humans and livestock to safeguard
the economical and public health aspects.
Author summary
Coxiella burnetii causes infections in both humans and animals, resulting in Q fever and
Coxiellosis, respectively. This bacterium poses significant public health, veterinary, and
economic risks worldwide due to its potential to cause severe illness and low infectious
dose. Therefore, it is important to estimate the sero-prevalence of C.burnetii infection
and associated risk factors in cattle, sheep, goats, and camels, respectively. The serum sam-
ples were analyzed for the presence of anti-C.burnetii antibodies using an indirect
Enzyme Linked Immunosorbent Assay (iELISA) kit. A prevalence estimate of 18.77% was
observed for C.burnetii. The sero-prevalence estimate at abbatoirs and pastoral areas was
found in the order of Addis Ababa (27.17%)>Adama (19.41%)>Modjo (19.13)>pastoral
areas (12.1%). The risk factors were identified as animal species, age, sex, and tick infesta-
tion. Camels were more vulnerable than sheep, goats and cattle. The adults were infected
more than young. The ticks may be a potential vector for the transmission of the
pathogen.
Introduction
Coxiella burnetii is a bacterium that causes Q fever in humans [1,2] and coxiellosis in animals
[3,4]. Transmission is primarily through inhalation of dry aerosol particles from infected ani-
mals although tick associated transmission has also been reported in animals [5]. Coxiellosis is
known to cause reproductive losses in livestock and debilitating illness in humans [2]. For
instance, the outbreak that occurred in the Netherlands between 2007 and 2010 resulted in the
culling of over 58,000 (~21%) livestock and illness in more than 4,000 people [6].
Despite its significant impact on both animal and human health, C.burnetii is often over-
looked in developing countries including Ethiopia. Since its identification in southern Moroc-
can ticks in 1947, only limited investigations have been conducted in Africa, primarily due to
challenges in the diagnosis of infection, insufficient resources and/or expertise, and prioritiza-
tion of other infectious diseases [7,8]. The seroprevalence of C.burnetii infection has been
noted to vary considerably in African countries; higher seroprevalence observed in countries
with greater pastoral land use, such as Chad, Egypt, Tanzania, Niger, and Kenya [810].
The first detection of C.burnetii in Ethiopia dated back to 1966 [11]. Subsequently, it was
reported in 6.5% of abattoir workers in Addis Ababa in 1990 [12] and in cases of infectious
endocarditis [7]. Gumi and his colleagues also reported evidence of infection in ruminants
and camels in pastoral areas, with seroprevalence of 31.6% in cattle, 90% in camels, and 54.2%
in goats [13]. A single study pointed out the association of C.burnetii infection with abortion
in animals [7].
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Coxiella burnetii infection and its risk factors in livestock of Ethiopia
PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0012287 July 16, 2024 2 / 15
Funding: The author(s) received no specific
funding for this work.
Competing interests: The authors have declared
that no competing interests exist.
Many countries which have conducted serological surveys had determine the prevalence of
C.burnetii in domestic ruminants using various serological techniques such as complement
fixation test, immunofluorescence assays, and enzyme-linked immunosorbent assays. For
example, serological investigations on coxiellosis were conducted in Europe, Latin America
and several African countries. The presence of C.burnetii in several animal species linked to
its zoonotic importance has been justified. The reservoirs of C.burnetii have been largely
investigated in many countries, especially in Europe. The occurrence of C.burnetii in wildlife
has also been evident [2,3,14]. In Ethiopia few serological studies were conducted in few loca-
tions focusing on a small number of animals and using various sampling procedures [12,13].
Therefore, this study aimed to estimate the seropevalence of coxiellosis in four common live-
stock species originated from various areas of Ethiopia and determine the associated risk factor
for C.burnetii infection.
Materials and methods
Ethics statement
Sampling of animals followed the approved experimental procedures and standards estab-
lished by Animal Research Scientific and Ethics Review Committee (ARSERC) at the Animal
Health Institute (AHI), the Institutional Animal Care and Use Committee (IACUC), and
Adama Science and Technology University (ASTU) with certificate Ref. No. RECSoANS/BIO/
11/2022.
Description of the study area
The research was carried out with animals destined for slaughter at Addis Ababa, Adama, and
Modjo abattoirs, as well as from the Borana pastoral area of Oromia, which are depicted in
Fig 1. The Borana pastoral area is located in the southern part of Ethiopia’s Oromia Regional
State. The capital of Borana Zone, Yabello, is situated 575 kilometers south of Addis Ababa.
The Borana Zone has thirteen districts and share borders with Kenya in the southern part at
Moyale, Miyo, Dirre, and Teltelle districts. For this study, three districts were chosen ran-
domly, that included Yabelo, Dubuluk, and Mega. The Borana Zone has a semi-arid to arid cli-
mate and is geographically located between to N latitude and 36˚ to 42˚ E longitude,
featured with isolated mountains and valleys. The altitude of the Borana Zone ranges from
1,000 to 1,700 meters above sea level, and the mean annual rainfall in the area ranges from 250
to 700 mm. The average annual temperature in the area ranges from 19 to over 25˚C. The Bor-
ana people rely mainly on extensive pastoralism, or nomadic herding, as their primary means
of livelihood. The main livestock species raised in the region comprises cattle, goats, sheep,
and camels. The Borana Zone Pastoral Development Office [15] reports that the zone has live-
stock population of 1,416,180 cattle, 1,262,782 goats, 776,870 sheep, 237,205 camels, 306,057
poultry, 102,767 donkeys, 1,841 horses, and 4,433 mules. As of 2015, the human population
was reported to be 1,283,925 [16].
The Addis Ababa abattoir Enterprise in Addis Ababa is situated in the central highlands of
Ethiopia at an altitude of 2500 meters above sea level. The average annual temperature and
rainfall in the city are 21˚C and 1800 mm, respectively. During the rainy season, the relative
humidity ranges from 70 to 80%, while during the dry season, it ranges from 40 to 50%.
According to the CSA [17] of Addis Ababa City Administration Agricultural Report, an aver-
age of 183,000 cattle, 42,200 sheep, 4,700 goats, and 830 pigs are slaughtered at the abattoir
each year. Generally, the cattle, sheep, and goats that are slaughtered in the abattoir come from
different regions and agro-ecological zones across the country.
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Adama town is a significant town located in the East Shoa Zone of Ethiopia’s Oromia
region, situated at 8.54˚N and 39.27˚E, with an elevation of 1712 meters and approximately 99
kilometers southeast of Addis Ababa. It is one of the largest metropolitan cities in Ethiopia,
with an estimated population of 450,000 humans and many resorts that make it suitable for
conferences and tourism. Adama abattoir has the capacity to slaughter approximately 150 cat-
tle and 500 sheep and goats per day [17].
Modjo is the administrative center of Lume district, which is located in the East Shoa Zone
of Ethiopia’s Oromia Region. It is located 66 kilometers southeast of Addis Ababa, at latitude
8˚35’N and longitude 39˚7’E, at an elevation of 1790 meters above sea level. The area receives
rainfall twice a year, during the long and short rainy seasons. The rainy season lasts from June
to September. The average annual rainfall, temperature, and mean relative humidity are 776
mm, 19.4˚C, and 59.9%, respectively [17]. The livestock used in this study were all local breeds
and mostly came from different agro-ecological zones, including Arsi, Borana, Jimma, Somali,
and South Wello, respectively. These animals were raised under extensive production systems,
either as part of a mixed crop-livestock production system or within a pastoral system of pro-
duction. They were acquired from various local markets and transported to the abattoirs,
where they were given food, water, and rest for a period ranging from 24 to 72 hours before
being slaughtered [18].
Study population and design
A cross-sectional study was conducted from January 2021 to May, 2022. The study population
comprise cattle, sheep, goat and camel population raised in the catchment areas of the abattoirs
(Addis Ababa, Adama, and Modjo) and Borana pastoral area. Animals of both sexes aged
more than 6 months and clinically healthy animals from selected abattoirs and three selected
Fig 1. Map of Ethiopia depicting the locations of the study areas (http://www.usgs.gov).
https://doi.org/10.1371/journal.pntd.0012287.g001
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pastoral areas, under the observation of veterinary workers, were the study population. The
age of the study animals was estimated as previously described by Schelling and his colleagues
[19].
After having a list of pastoralist households in Borana, clustered households and their live-
stock were chosen randomly for sampling from households and their herds. In the Borana pas-
toral area, the majority of animals included in the study were females as they were used for
milk production purpose. In contrast, the majority of animals sampled at abattoirs were male
livestock. All the study animals were not vaccinated against C.burnetii.
Sample size determination
To determine the minimum number of animals needed for this study, a formula developed by
Thrusfield [20] was employed. In this formula, n represents the required sample size, P
exp
is
the expected prevalence, and d is the absolute precision as indicated in Eq (1).
n¼ð1:96Þ2X Peepð1Pexp Þ
d2ð1Þ
where, nis the total sample size, P
exp
is expected prevalence (50%), dis absolute precision
(0.05) at 95% CI.
n¼ð1:96Þ2X0:5ð10:5Þ
ð0:5Þ2¼384
The study required a total of 1536 animals, with 384 animals needed for each of the four
animal species. In order to increase precision and decrease the standard error, a total of 4,140
animals (1,564 cattle, 736 camels, 1,012 goats, and 828 sheep) were utilized in this study. Of
these, 1,012 samples were obtained from Addis Ababa abattoir, 1,511 from Modjo abattoir,
and 237 from Adama abattoir, while 1,380 animals were sampled from pastoral areas.
Blood sample collection and serum separation
To make the sample collection process easier, it was preferred to collect the samples early in
the morning before the animals were taken out for grazing or slaughter, depending on whether
they were from pastoral areas or abattoirs. During the blood sample collection process, the ani-
mals were held in a crush to limit their mobility. Aseptic blood samples, approximately 6–8
mL, were collected from each animal’s jugular vein by using sterile plain vacutainer tubes and
needles. Each sample was given a code to identify the specific animal, and protected from
direct sunlight.
The samples were placed in a slant position overnight at room temperature to allow clot-
ting. The next morning tubes containing samples were centrifuged at 2000×g for 10 min at
room temperature by taking them to the nearby veterinary clinics, and serums were separated
from the blood and stored in 1.8 mL disposable screw-capped cryovials (Cryo.STM; Greiner
Bio-one, GmbH Frickenhausen, Germany). Then the samples were transported to Animal
Health Institute (AHI) laboratory in Sebeta, Ethiopia, at a temperature of 4˚C using a portable
refrigerator that was plugged into a car and subsequently stored at -20˚C until they were
analysed.
Information about the individual animal such as its area, sex, age, species, and tick infesta-
tion, was recorded during the sample collection process by using sample information collec-
tion sheet prepared for this purpose.
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Serological examination
The commercial indirect enzyme-linked immunosorbent assay (iELISA) kit (Switzerland AG,
CH3097, Liebefeld-Bern, Switzerland) was used to detect antibodies to phase I antigens of C.
burnetii. The antigen coated wells of the ELISA plates were incubated with the diluted serum
samples according to the manufacturer’s instructions. The negative and positive controls were
diluted at 1:400 using wash solution and dispensed into duplicate wells, while the serum sam-
ples were added to the remaining wells. The plate was covered and gently shaken and incu-
bated for 60 min at 37˚C in a humid chamber. After incubation, the wells were emptied and
washed three times with 300 μL of wash solution, and then 100 μL of secondary antibody con-
jugate was added and incubated as described above. The plate contents were discarded, and
the plate was washed three times using 300 μL of wash solution. Subsequently, 100 μL of sub-
strate was added, and the plate was incubated at room temperature for 15 min. Finally, 100 μL
of stop solution was added, and the absorbance was read at 450 nm.
The Agilent BioTek ELx800 absorbance microplate Reader was employed to measure the
absorbance values as Optical density (OD). The S/P-ratio, which represents the percentage of
the ratio between the sample OD and the positive control OD, was calculated as follows: Sam-
ples with an S/P percent 40% were considered seropositive for C.burnetii, while those with
values between 30–40% were considered dubious, and those 30% were considered negative.
Based on the sensitivity (99%) and specificity (98%) of the commercial ELISA kit we used, the
true prevalence of C.brnetii infection was also calculated using the formula previously
described by Farrokh et al. [21].
Geo-referencing
The animals that were tested were distributed across the areas/districts from where they origi-
nated. During the study period, they were sampled and analyzed using thematic density maps
created using QGIS 10.0 [22]. The thematic density maps were used to show the distribution
of the animal samples collected during the study period, as well as the distribution of the ani-
mals that tested positive for C.burnetii. Two thematic maps were created to show the distribu-
tion of the samples: one indicating the total number of samples, and another indicating the
number of serologically-positive samples identified by using iELISA.
Data management and analyses
The STATA software version 16.0 (Stata Corp, 4905 Lake way Drive, College Station, Texas
77845 USA) was used to analyse the data and determine the effects of risk factors on the preva-
lence of C.burnetii infection. Test statistics such as chi-squared test was to analyse the effect of
individual factors on the prevalence of C.burnetii infection. Multivariable logistic regression
was employed to compute the associations between the risk factors and prevalence. The vari-
ables were manually fitted to the model to check for confounding. To evaluate the fitness of
the logistic regression model, the Hosmer-Lemeshow and Pearson methods were used. A P
value of 0.05 and a 95% confidence interval were considered to be significant in this study.
Results
Seroprevalence of C.burnetii infection
The present study analysed a total of 4140 sera samples to estimate the prevalence of antibodies
against C.burnetii. The overall seroprevalence of C.burnetii infection was 18.77% (95% CI,
17.55–19.99%) (Table 1). Hence, based on the sensitivity (99%) and specificity (98%) of the
commercial ELISA kit we used, the calculated true prevalence of C.brnetii infection was
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17.29%. The lowest seroprevalence was recorded in animals from pastoral areas (12.1%; 95%
CI, 10.43–13.94%) while the highest prevalence observed in animals from Addis Ababa abat-
toir (27.17%; 95% CI, 24.45–30.03%). Sera analysis at the animal species level showed that cat-
tle exhibited the lowest seroprevalence (11.83%; 95% CI, 10.27–13.53%), while the highest was
observed in camels (28.39%; 95% CI, 25.16–31.80%). The seroprevalence was 21.34% (95% CI,
18.86–23.99%) in goats and 20.17% (95% CI, 17.49–23.07%) in sheep.
Female animals were observed to have a higher seroprevalence (26.65%; 95% CI, 23.37
30.13%) than male animals (17.21%; 95% CI, 15.97–18.51%). The prevalence was also higher
in adult animals (25.02%; 95% CI, 23.26–26.85%) than their younger counterparts (11.03%;
95% CI, 9.64–12.54%). Higher seroprevalence of C.burnetii infection was also observed in ani-
mals infested with ticks (carry ticks on several body parts) (80.99%; 95% CI, 73.55–87.08%)
than those animals which were not infested by ticks at all (7.05%; 95% CI, 6.52–7.59%).
Geo-referencing the seroprevalence of C.burnetii from Abattoirs
Abattoirs serve as a valuable source of information on the prevalence of C.burnetii infection in
different regions of the country, as the animals that are slaughtered there come from various
parts of the country. In order to provide insight into the distribution of seroprevalence results
across the country, the data obtained from the animals slaughtered at different Abattoirs were
geo-referenced by thematic density maps created by using QGIS 10.0 and presented in Fig 2.
This spatial information is critical in identifying areas with a higher risk of C.burnetii infec-
tion, which may serve to inform targeted interventions to mitigate the spread of the bacterium
and reduce the risk of transmission to humans. Consequently, this data may play a pivotal role
in enhancing public health outcomes and reducing the burden of zoonotic diseases.
In the context of Addis Ababa Abattoir (AAA), animals (sample size, 1012) were predomi-
nantly sourced from three distinct regions, which are Amhara (East and West Gojam; North
and South Gondar), Oromia (Bale and Borana), and Southern Nations Nationalities and Peo-
ple Region (SNNPR) (Wolayita). These regions were identified and are graphically represented
in Fig 2A. For Adama Abattoir (AA), animals (sample size, 237) were procured from a diverse
range of regions from Somali, Oromia, Afar, Babile, and Jinka, as illustrated in Fig 2B. These
Table 1. The seroprevalence of Coxiella burnetii infection determined in livestock sampled from diverse geographic localities.
Variable Category No. tested No. positive Prevalence (%) X
2
95% CI
Lower Upper
Area Addis Ababa Abattoir 1012 275 27.17 87.32 24.45 30.03
Modjo Abattoir 1511 289 19.13 17.17 21.2
Adama Abattoir 237 46 19.41 14.57 25.03
Borana pastoral areas 1380 167 12.1 10.43 13.94
Species Cattle 1564 185 11.83 99.63 10.27 13.53
Camel 736 209 28.39 25.16 31.8
Goat 1012 216 21.34 18.86 23.99
Sheep 828 167 20.17 17.49 23.07
Sex Female 683 182 26.65 33.31 23.37 30.13
Male 3457 595 17.21 15.97 18.51
Age Young 1850 204 11.03 131.46 9.64 12.54
Adult 2290 573 25.02 23.26 26.85
Tick infestation Yes 142 115 80.99 378.48 73.55 87.08
No 3998 621 7.05 6.52 7.59
Total 4140 777 18.77 17.59 19.99
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regions were identified and mapped to provide a comprehensive understanding of the geo-
graphical origins of the animals. For Modjo Abattoir (MA), animals (sample size, 1511) were
primarily sourced from regions similar to Adama Abattoir (AA), with an additional procure-
ment from Bale, East Harerge in Oromia, and the Southern Nations Nationalities and People
Region (SNNPR), as depicted in Fig 2C. In the Borana Pastoral region of Oromia, animals
(sample size, 1038) were sourced from Dubuluk, Mega, and Yabelo, as depicted in Fig 2D.
This geographical information is crucial in determining the epidemiology of infectious dis-
eases that may affect the animals and subsequently pose a risk to human health. By utilizing
this data, targeted interventions may be designed to mitigate the risk of zoonotic disease trans-
mission, thereby improving public health outcomes.
The geographical distribution of C.burnetii infection was analysed and is presented in
Fig 3. The prevalence was found to be higher in animals at the Addis Ababa Abattoirs than
those at the other two Abattoirs and pastoral region. The tested sample size and prevalence in
case of Addis Ababa Abattoir were 1012 and 27.12%, Adama Abattoir were 237 and 19.41%,
Fig 2. The serum samples collected from animals were systematically categorized according to their respective
sampling areas and sources. The four sampling areas were as follows: (a) Addis Ababa Abattoir (AAA), which is
located in the capital city of Ethiopia, (b) Adama Abattoir (AA), which is situated in the city of Adama, (c) Modjo
Abattoir (MA), located in the town of Modjo, and (d) Borana Pastoral Oromia (PO), which is a pastoral region in
Ethiopia. https://www.ethiogis-mapserver.org/.
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Modjo Abattoir were 1511 and 19.13% and Borana Pastoral Oromia were 1380 and 12.1%,
respectively (Fig 3 and Table 1).
Analysis of risk factors of C.burnetii infection
Statistically significant association (p <0.001) was found between animal species and the sero-
prevalence of C.burnetii (Table 2). The odds of infection in camels was 3.22 (95% CI, 2.57–
4.05%) times that of cattle. Sheep and goats were twice more likely to be infected with C.burne-
tii than cattle (for sheep, OR = 2.15; 95% CI, 1.63–2.82%; for Goats, OR = 1.99; 95% CI, 1.53–
2.6%). The adult animals had higher odd of infection than younger animals (OR = 3.23; 95%
CI, 2.63–3.96%; and p <0.001). Those animals infested with ticks were more likely to be sero-
positive to C.burnetii than animals which were free of ticks. The odds of infection in animals
carrying one or more ticks was 16.32 times (95% CI, 10.17–26.18%) the odds of infection in
animals that were not infested by ticks. Additionally, a higher prevalence was observed in the
female animals compared with male animals, however, the difference in prevalence between
Fig 3. The seropositivity of animals infected with Coxiella burnetii was evaluated using the Indirect Enzyme-
linked Immunosorbent assay (iELISA) method in four distinct sampling regions: Addis Ababa Abattoir (AAA),
Adama Abattoir (AA), Modjo Abattoir (MA), and Pastoral Oromia (PO). The study presented the distribution of
samples tested, positive, and prevalence percentage, which were represented using different colors. https://open.africa/
dataset/ethiopia-shapefiles.
https://doi.org/10.1371/journal.pntd.0012287.g003
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Coxiella burnetii infection and its risk factors in livestock of Ethiopia
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the two sexes was not statistically significant (OR = 0.78; 95% CI, 0.59–1.02). The results of the
multivariable logistic regression analysis are presented in Table 2.
Discussion
Currently, there is insufficient information on the epidemiology of C.burnetii in livestock spe-
cies in Ethiopia. The present study estimated the seroprevalence of coxiellosis and determined
its risk factors in four livestock species originating from major abattoirs and pastoral areas of
Ethiopia. Notably, the abattoir study was conducted 56 years after the first evidence of the dis-
ease was reported in goats and sheep slaughtered at the Addis Ababa abattoir [11]. The find-
ings of present study revealed that coxiellosis is prevalent in all the livestock species tested
across a wider geographical area, indicating a significant public health risk.
The current study reports an overall seroprevalence of 18.77% (95% CI, 17.59–19.99%) with
varying levels from the tested livestock species of various locations in Ethiopia. Our finding is
in a close similarity with the 20% prevalence reported from south-western Ethiopia using simi-
lar serological methods [23]. However, it is lower than those reported by Gumi et al. [13] and
Tesfaye et al. [24] who estimated a prevalence of 31.6% and 28.46%, respectively, in other parts
of Ethiopia. Some studies from other countries by Cekani et al. [14] in Albania (9.1%), Mwo-
lolo et al. [25] in Kenya (12.80%), and Gummow et al. [26] in South Africa (7.78%), also
reported a lower seroprevalence than our observation. The variation in seroprevalence
observed between our study and the previous ones could be attributed to differences in sample
size, sampling methodology, and diagnostic tests utilized. Although some of the previous stud-
ies used similar serological tests, they had smaller sample sizes [25,27]. Other possible reason
for the variation could be differences in geographical locations and management practices
[28]. It is, therefore, crucial to consider these factors when interpreting the results of serologi-
cal studies on the prevalence of C.burnetii infection in animal populations.
In this study significantly higher prevalence of C.burnetii infection was observed in camels’
goats, and sheep than cattle. In consent to our finding, previous studies have demonstrated sig-
nificantly higher seroprevalence of C.burnetii infection in camels than in other livestock spe-
cies in Kenya [29], the Sahel region [19], and Ethiopia [13]. This variation in seroprevalence
among different animal species could be attributed to differences in susceptibility to C.burnetii
Table 2. Results of a multivariable logistic regression analysis examining the association between various variables for the seroprevalence of Coxiella burnetii infec-
tion in livestock.
Variables Category OR SE Z p-value 95% CI
Lower Upper
Species Cattle Ref
Camel 3.22 0.374 10.09 0.000 2.56835 4.04817
Goat 1.99 0.27 5.11 0.000 1.5315 2.60322
Sheep 2.15 0.299 5.5 0.000 1.63525 2.82048
Sex Female Ref
Male 0.78 0.108 -1.81 0.071 0.59126 1.02174
Age Young Ref
Adult 3.23 0.337 11.24 0.000 2.63228 3.96245
Tick infestation Yes 16.32 3.935 11.58 0.000 10.1726 26.1781
No Ref
Constant 0.07 0.012 -15 0.000 0.04674 0.09504
OR, Odds Ratio; CI, Confidence Interval; Ref., Reference; SE, Standard Error; Z, z-score.
https://doi.org/10.1371/journal.pntd.0012287.t002
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Coxiella burnetii infection and its risk factors in livestock of Ethiopia
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infection, can vary based on several factors, including the immune system, age, sex, and man-
agement practices [7]. Previous studies have revealed variations in seroprevalence among dif-
ferent animal species [30], where transmission dynamics and environmental factors differ.
The higher seroprevalence in camels may be attributed to several factors. Camels are known to
have longer lifespans (~40 yrs) than other livestock species [31], and therefore, they may have
greater exposure to C.burnetii. The prevalence recorded in sheep and goats is consistent with
the results of previous studies conducted in Ethiopia and elsewhere in the world [3,13,3234].
The lower seroprevalence in cattle observed in the present study is also in agreement with the
reports of previous studies [35,36]. Similarly, lower prevalence was reported from few African
countries such as Togo [37] and Chad [19]. However, higher seroprevalence is reported from
other countries by Adesiyun et al. [38] who reported prevalence of 59.8% in dairy cows from
Nigeria, Kelly et al. [39] who recorded 39% in cattle and 10% in goats from Zimbabwe and
Hussien et al. [40] who reported prevalence of 64.5% in camels and 29.9% in cattle from
Sudan.
In our study, we observed a significantly higher seroprevalence of C.burnetii infection in
adult animals (OR = 3.23; P <0.001) than in younger animals. This finding is in agreement
with the results of several previous studies [25,13,35]. The higher seroprevalence of C.burnetii
infection in older animals may be attributed to the cumulative exposure to the pathogen over
time. Older animals have a higher likelihood of being exposed to the pathogen through contact
with infected animals or the environment, and repeated exposure may increase the likelihood
of infection and development of antibodies. This is supported by previous studies demonstrat-
ing a higher prevalence of C.burnetii infection in animals with a longer exposure history [3]. It
could also be attributed to the pathogen’s ability to infect the reproductive tissues of animals,
leading to a higher dissemination and impact in older animals, which have a longer reproduc-
tive history [41].
Our study demonstrated a significant difference in the seroprevalence of C.burnetii infec-
tion between animals infested with ticks and those which were tick free. This observation is
consistent with the reports of previous studies suggesting the possible role of ticks in the trans-
mission and spread of the bacterium [41,5]. It has been elucidated that ticks infesting both
wild and domestic animals can transmit C.burnetii to both animals and humans [41,42]
although only two experimental studies evaluated the vector competence of ticks for C.
burnetii.
Our study revealed a higher seroprevalence of C.burnetii infection in animals slaughtered
at Addis Ababa abattoir. This could be attributed to the fact that Addis Ababa abattoir receives
animals from all corners of the country mainly from the three largest regions where over 70%
of the national livestock are located. This observation implies that Addis Ababa abattoir is a
high-risk area for the transmission of C.burnetii to abattoir workers and the community.
Implementation of biosecurity measures such as personal protective equipment is needed.
Moreover, there should be screening of animals before slaughter for zoonotic diseases includ-
ing C.burnetii infection in order to protect the public health.
The geo-referencing maps done in the present study can provide useful insights into the
spatial distribution of the phenomenon being studied, in this case, the prevalence of coxiellosis
in indigenous Ethiopian cattle, sheep, goats, and camels. The maps can also help researchers to
identify areas where the infection is more prevalent, which can assist with disease control and
prevention efforts.
Our study has some limitations. We used an indirect ELISA to test the presence of antibod-
ies against C.burnetti and could not distinguish between historical exposure and active infec-
tions. Additionally, the tests used had less than 100% sensitivity and specificity which could
pose a risk of misclassification. Our study did not include environmental factors as covariates
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Coxiella burnetii infection and its risk factors in livestock of Ethiopia
PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0012287 July 16, 2024 11 / 15
when investigating factors associated with coxiellosis antibody seropositivity, which may have
accounted for some of the observed variations across different study sites. Furthermore, sero-
logical cross-reactions might have occurred between C.burnetii and other bacteria.
In conclusion, the current study reported the seroprevalence of C.burnetii in four common
livestock species which is significantly higher in camels, sheep and goats than in cattle. It was
also significantly higher in females than males, in adults than younger animals and in tick
infested animals than tick free animals. Our findings highlight the importance of C.burnetii in
livestock, which can pose serious public health risks. Further investigation into the economic
impacts of C.burnetii and establishment of molecular diagnosis and surveillance of the disease
both in animals and human is warranted for the design of effective control strategies.
Acknowledgments
We would like to express our gratitude to Addis Ababa, Adama, and Modjo Abattoirs, as well
as the Borana Zone Administration office for their collaboration and support during the data
collection process from livestock in various districts. We extend our appreciation to Defense
Threat Reduction Agency (DTRA), Adama Science and Technology University (ASTU), and
the Animal Health Institute (AHI) for technical and chemicals supports received. In addition,
we would like to acknowledge the contributions of the following scientists from the National
Animal Health Institute (AHI): Solomon Gebre, Asamenew Tesfaye, Fasil Aklilu, Hagos Asge-
dom, Getachew Tuli, Matios Lakew, and Delesa Damena. We are also grateful to the scientists
at Addis Ababa University (AAU), Naval Medical Research Center (NMRC), Viral and Rick-
ettsial Diseases Department, Silver Spring, including Christina M. Farris and MAJ Amanda
Christy.
Author Contributions
Conceptualization: Ashenafi Milkesa, Tesfaye Rufael, Redeat Belaineh, Donghee Cho, Hun-
duma Dinka.
Data curation: Ashenafi Milkesa, Mohammed Naimuddin, Teshale Sori, Hunduma Dinka.
Formal analysis: Ashenafi Milkesa, Teshale Sori.
Funding acquisition: Tesfaye Rufael, Redeat Belaineh, Hunduma Dinka.
Investigation: Ashenafi Milkesa, Getachew Kinfe, Abdella Bulbula.
Methodology: Ashenafi Milkesa, Getachew Kinfe, Abdella Bulbula, Hunduma Dinka.
Project administration: Tesfaye Rufael, Redeat Belaineh, Hunduma Dinka.
Resources: Ashenafi Milkesa, Tesfaye Rufael, Redeat Belaineh.
Software: Ashenafi Milkesa, Teshale Sori, Hunduma Dinka.
Supervision: Tesfaye Rufael, Redeat Belaineh, Donghee Cho, Hunduma Dinka.
Validation: Ashenafi Milkesa, Getachew Kinfe, Redeat Belaineh, Hunduma Dinka.
Visualization: Ashenafi Milkesa, Redeat Belaineh, Teshale Sori, Hunduma Dinka.
Writing original draft: Ashenafi Milkesa, Tesfaye Rufael, Redeat Belaineh, Teshale Sori,
Hunduma Dinka.
Writing review & editing: Ashenafi Milkesa, Donghee Cho, Mohammed Naimuddin,
Teshale Sori, Hunduma Dinka.
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Coxiella burnetii infection and its risk factors in livestock of Ethiopia
PLOS Neglected Tropical Diseases | https://doi.org/10.1371/journal.pntd.0012287 July 16, 2024 12 / 15
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Q fever remains a neglected zoonosis in many developing countries including Pakistan. The causing agent Coxiella (C.) burnetii is resistant to environmental factors (such as drying, heat and many disinfectants), resulting in a long-lasting infection risk for both human and animals. As the infection is usually asymptomatic, it mostly remains undiagnosed in animals until and unless adverse pregnancy outcomes occur in a herd. In humans, the infection leads to severe endocarditis and vascular infection in chronic cases. Limited data are available on molecular epidemiology and evolution of this pathogen, especially in ruminants. Genomic studies will help speculating outbreak relationships in this scenario. Likewise, pathogenesis of C. burnetii needs to be explored by molecular studies. Awareness programs and ensuring pasteurization of the dairy milk before human consumption would help preventing Q fever zoonosis.
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Q fever is a zoonosis occurring worldwide in livestock. Often neglected in differential diagnoses, Q fever can persist in herds causing financial losses. In ruminants, well-known manifestations of Q fever are metritis, infertility, abortion, stillbirth and delivery of a weak or premature calf. In cattle, Q fever is frequently asymptomatic and/or under-reported. Few studies are available on the diagnosis of Coxiella burnetii as a cause of abortion in cattle using polymerase chain reaction (PCR) for pathogen detection while enzyme-linked immunosorbent assay (ELISA) is used to assess exposure. Moreover, existing studies include a relatively small number of abortions. The aim of this study is to assess, in the southern part of Belgium, during a year, the performance of diagnosis of C. burnetii as a cause of abortion and the putative benefit of enhanced serology using anamnesis (animal patient data, and present, past and environmental history). A one-year random selection of 1212 abortions was analysed both with the PCR method (tissues from fetuses) and two commercialised ELISAs (sera from the mothers). Relative sensitivity and specificity of the ELISA tests were assessed using PCR as the reference test. The prevalence of C. burnetii PCR positive was 8.5% (95% CI: 6.99–10.21). The diagnostic value of the ELISA tests was assessed using the area under the receiver operating characteristic curve (AUC-ROC). The sensitivity, specificity and AUC-ROC were similar for both ELISA tests. The diagnostic capacity of the ELISA was confirmed and slightly enhanced if anamnestic information was integrated with a unique scoring index system. A high negative predictive value was demonstrated and a significant reverse association between Ct values and a percentage of the ratio of the optical density between the sample and the positive control (ELISA A or ELISA B) enabling the use of ELISA as an exclusion diagnostic. This study is original by integrating the serological result and the anamnesis in a single index. It opens a new window in enhanced veterinary clinical decision-making.
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