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Q Fever
Seroprevalence and risk factors for Q fever and Rift Valley fever in pastoralists and their livestock in Afar, Ethiopia: A One Health approach
Q fever and Rift Valley fever in Afar, Ethiopia
https://orcid.org/0000-0002-4085-8090
Oakley Regina Bina Conceptualization Data curation Formal analysis Investigation Methodology Project administration Validation Visualization Writing – original draft 1 2 *
Gemechu Gizachew Investigation Project administration Writing – review & editing 3
Gebregiorgis Ashenafi Data curation Writing – review & editing 3
Alemu Ayinalem Investigation Writing – review & editing 3
Zinsstag Jakob Supervision Writing – review & editing 2 4
Paris Daniel Henry Funding acquisition Supervision Writing – review & editing 1 2
Tschopp Rea Conceptualization Formal analysis Funding acquisition Project administration Supervision Writing – review & editing 2 3 4
1 Department of Medicine, Swiss Tropical and Public Health Institute, Allschwil, Switzerland
2 University of Basel, Basel, Switzerland
3 One Health Division, Armauer Hansen Research Institute, Addis Ababa, Ethiopia
4 Department of Epidemiology and Public Health, Swiss Tropical and Public Health Institute, Allschwil, Switzerland
Rayner Simon Editor
Universitetet i Oslo, NORWAY
The authors have declared that no competing interests exist.

* E-mail: regina.oakley@swisstph.ch
23 8 2024
8 2024
18 8 e00123921 12 2023
22 7 2024
© 2024 Oakley et al
2024
Oakley et al
https://creativecommons.org/licenses/by/4.0/ 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.

Background

Coxiella burnetii, the causative agent of Q fever, and Rift Valley fever virus are two under-researched zoonotic pathogens in Ethiopia. Potential outbreaks of these diseases, in light of the high dependency of nomadic pastoralists on their livestock, poses a risk to both human and animal health in addition to risking the pastoralists livelihoods. Our study aimed to determine the seroprevalence and associated risk factors for Q fever and Rift Valley fever in pastoral communities in the Afar region of north-eastern Ethiopia.

Methodology/Principal findings

This cross-sectional study screened pastoralists (n = 323) and their livestock (n = 1377) for IgG antibodies to Coxiella burnetii and Rift Valley fever virus. A seroprevalence for Q fever of 25.0% (95%CI 18.6–32.6) was found in pastoralists and 34.3% (95%CI 27.9–41.3) in livestock overall; with 51.9% in goats (95%CI 44.9–58.8), 39.9% in sheep (95%CI 24.6–51.2), 16.3% in camels (95%CI 10.4–24.6) and 8.8% in cattle (95%CI 5.0–15.0). For Rift Valley fever the seroprevalence in pastoralists was 6.1% (95%CI 3.3–11.0) and 3.9% (95%CI 2.6–5.7) in livestock overall; cattle had the highest seroprevalence (8.3%, 95%CI 3.3–19.2), followed by goats (2.7%; 95%CI 1.4–5.1), sheep (2.5%; 95%CI 1.0–5.9) and camels (1.8%; 95%CI 0.4–6.9). Human Q fever seropositivity was found to be associated with goat abortions (OR = 2.11, 95%CI 1.18–3.78, p = 0.011), while Rift Valley fever seropositivity in livestock was found to be associated with cattle abortions (OR = 2.52, 95%CI 1.05–6.08, p = 0.039).

Conclusions/Significance

This study provides evidence for a notable exposure to both Q fever and Rift Valley fever in pastoralists and livestock in Afar. The outbreak potential of these pathogens warrants ongoing integrated human and animal surveillance requiring close collaboration of the human and animal health sectors with community representatives following a One Health approach.

Author summary

Q fever and Rift Valley fever are two diseases that can affect both humans and animals, causing illness and death. These two diseases can cause large-scale outbreaks, not only affecting the health of individuals and communities but also resulting in a substantial economic loss at the individual, community, regional and national levels through losses in livestock products. We conducted a sero-epidemiological study in the Afar region of north-eastern Ethiopia to determine the presence of these two diseases in nomadic pastoralists and their livestock. Our results indicate that 25.0% of the pastoralists and 34.3% of their animals have had previous exposure to Q fever and 6.1% of the pastoralists and 3.9% of their animals have been exposed to Rift Valley fever. Goats appear to be the most common livestock species associated with Q fever in this region, while cattle are the most common species associated with Rift Valley fever. Our findings highlight the importance of continuous surveillance; additionally, we would recommend the development of rapid response plans for potential outbreaks that integrate the human and animal health sectors.

http://dx.doi.org/10.13039/501100004339 Stanley Thomas Johnson Stiftung 1053-KF Paris Daniel Henry U.S Centers for Disease Control and Prevention Tschopp Rea This study was funded by the Stanley Thomas Johnson Foundation (1053-KF, received by DHP; https://www.johnsonstiftung.ch/), and the U.S. Centers for Disease Control (CDC) who funded the original brucellosis study (received by RT; https://www.cdc.gov/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. PLOS Publication Stagevor-update-to-uncorrected-proof
Publication Update2024-09-05
Data AvailabilityThe authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files.
Data Availability

The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files.
==== Body
pmcIntroduction

Zoonotic diseases can directly affect the health of humans, animals and their environment, as well as creating a substantial economic burden at the individual, community, regional, and national levels. Ethiopia is among the top five countries in the world for zoonotic disease burden [1]. However, Q fever and Rift Valley fever (RVF) are two zoonotic diseases that are often under-diagnosed and under-reported due to their non-specific flu-like symptoms, diagnostic difficulties, poor infrastructure, poor public education and engagement, contributing to the burden of undiagnosed febrile illness in this region of Africa [2–4].

Q fever is caused by Coxiella burnetii, a zoonotic bacterium found globally with the primary reservoirs for human infection in cattle, sheep and goats [5]. Transmission to humans is predominantly through inhalation of aerosolized bacteria from birth products of infected animals, and direct contact with infected animals or their secretions, raw milk consumption as well as tick-borne transmission [5–7]. Acute Q fever can cause flu-like symptoms, including pneumonia and acute hepatitis [8–10]. Approximately 20% of patients develop Q fever fatigue syndrome (QFS), lasting from six months to many years, with patients suffering prolonged periods of fatigue among other symptoms [11]. Chronic Q fever in humans evolves from 1–5% of acute infections to complications such as: endocarditis, chronic vascular infections, osteomyelitis, osteoarthritis, chronic pulmonary infections, and chronic hepatitis [10]. C. burnetii infection is often associated with occupations that have close contact with animals, such as livestock farmers, slaughterhouse workers, butchers, veterinarians, and laboratory workers [8]. Animal infection, while mostly asymptomatic, can cause reproductive disorders in ruminants, including abortion, stillbirth, infertility, mastitis, and endometritis–with significant economic consequence for the livestock industry [8,12].

The RVF virus (RVFV) primarily affects animals (livestock and wildlife) but can infect humans as well. Transmission to humans can occur through mosquitoes and other hematophagous arthropods (vector-borne disease) or direct contact with infected animal tissues and fluids [13,14]. RVFV infection usually causes a mild non-specific febrile illness in humans, with the potential to progress to a haemorrhagic fever-like syndrome, meningo-encephalitis, or ocular disease. In animals, RVF is more severe with high fatalities. Vertical transmission from mother to fetus occurs in both humans and animals, commonly causing abortion in livestock [13]. A study in Sudan also reported an association between RVFV infection and miscarriage in pregnant women [15].

A scoping review on zoonotic diseases in the Horn of Africa that included 2,055 studies found Q fever to be comparatively understudied across the region, and both Q fever and RVF to be understudied in Ethiopia with each investigated in only 1% of publications [16]. C. burnetii and RVFV exposure has previously been reported in livestock in the southern and eastern regions of Ethiopia [17–21]. Information on the prevalence of these two pathogens in humans in Ethiopia is limited, although one study on pastoralists from the Somali region reported a seroprevalence of 27% and 13% for C. burnetii and RVFV antibodies, respectively [18].

The Afar region in north-eastern Ethiopia presents an important study region for zoonotic pathogens, with a large pastoralist population and mixture of livestock species. It is a major pastoral region in consideration of livestock numbers and importance to the regional economy in addition to cross-border movements of both humans and livestock to neighbouring countries within the Horn of Africa [22]. Following the recent conflict in the Tigray region of Ethiopia, Afar has also seen an influx of internally displaced people migrating to the region. Pastoralists in this region depend heavily on their livestock for meat and milk, either for their own consumption or to sell. Milk is the primary source of vitamin A for pastoral communities who traditionally have not had access to fruits and vegetables [23]. Animal losses directly affect the health of pastoralists, causing malnutrition and vitamin deficiencies [23]. This makes them particularly vulnerable to environmental changes, such as drought and zoonotic disease [24]. During the dry season people are migrating in search for grazing areas and water with their livestock [25]. This high rate of animal mobility is a potentially important factor in disease transmission. Additionally, the nomadic lifestyle of pastoralists creates a challenge for delivery of health services and disease surveillance [26]. In recent years, a substantial increase of migrants in the Afar region was due to conflicts in Eritrea and the northern Ethiopia region of Tigray. The nomadic pastoralists and increasingly mobile and vulnerable refugee populations, living in low-resource and poor hygienic conditions with high exposure to animals provide a rationale for improved awareness and evidence-based research to support the development of sustainable disease surveillance and control programs to reduce the burden of zoonotic diseases in Ethiopia.

Studies on zoonotic diseases in the Horn of Africa often have not followed a One Health approach, but rather consider human and animal health individually [16]. However, to adequately control zoonotic diseases in these pastoral regions, a transdisciplinary approach is needed, involving the pastoral communities, the animal and public health authorities along with the research community [23].

This study aimed to determine the seroprevalence of C. burnetii and RVFV antibodies in humans and their livestock using a One Health approach and to identify associated risk factors in the Afar region of north-eastern Ethiopia. We hypothesized that pastoralists and livestock residing in the Afar region would have high rates of exposure to these pathogens due to the close contact between humans and animals, high rates of animal mobility, and limited medical and veterinary services in this area. The results of this study will be provided to the local health and veterinary authorities to guide in their priorities and practices for controlling zoonoses in Afar.

Methods

Ethics statement

The studies were performed in accordance with the principles of the Declaration of Helsinki and were approved by the Armauer Hansen Research Institute and Alert Hospital (AHRI/ALERT) Ethics Review Committee (PO-53-22) and “Ethikkommission Nordwest- und Zentralschweiz” (EKNZ) (AO_2022–0052).

Study design and sample collection

This cross-sectional study examined serum samples and epidemiological data (household questionnaire) collected from a recent One Health study on brucellosis [22,25]. Sample and data collection methodology of the brucellosis study are available in Tschopp et al (2022) [22]. In addition to informed written consent for the brucellosis study, a general written consent was obtained for further investigation of collected samples for zoonotic diseases, including Q fever and RVF. Serum samples and epidemiological data were collected between 2017 and 2022 from pastoralists and their livestock (sheep, goats, cattle and camels) in seven districts (woredas) within the Afar region of Ethiopia. A subset of serum samples was randomly selected from the recent One Health brucellosis study, representing five of the seven districts: Amibara, Awash, Asayta, Mille and Dubti.

Sample size calculation

A sample size of 323 and 87 pastoralists was calculated for C. burnetii and RVFV, respectively, using epitools from https://epitools.ausvet.com.au [27]. The sample size was calculated for a precision of 0.05, a confidence of 95% and estimated seroprevalences of 30% (C. burnetii) and 6% (RVFV) in the pastoralists [18]. A total of 335 pastoralists were included in the study.

Sample size for animals was similarly calculated with an estimated seroprevalence between 30% and 60% for C. burnetii and 6% and 45% for RVFV [18,19,28,29]. The highest sample size required for each species was: 323 sheep, 385 goats, 340 cattle and 369 camels. To determine the presence of correlations in the seroprevalences of Q fever and RVF for pastoralists and livestock, the livestock were selected to match the same households as the pastoralists. As samples were selected from the previous brucellosis study and there were only limited samples of sufficient volume for inclusion in the present study; consequently we included 684 goats, 199 sheep, 236 cattle and 258 camels.

Serological testing

Laboratory investigations were performed at the Armauer Hansen Research Institute (AHRI) in Addis Ababa, Ethiopia. For Q fever, serum from pastoralists (n = 335) was tested with the commercially available CE-labeled Fuller Laboratories Coxiella burnetii IFA IgG Phase I/II kit (Fuller Laboratories, Fullerton, CA, USA). Serum was screened at a titre of 1:32, with a positivity cut-off titre set at ≥1:32 [30,31]. A total of 1,377 sera from livestock were screened using the ID Screen Q fever indirect multi-species ELISA (ID.vet, Innovative Diagnostics, Grabes, France). The Sample/Positive% was calculated for each sample [S/P% = (ODsample−mean ODnegative control)/(mean ODpositive control−mean ODnegative control)]. The results were interpreted as negative (S/P% ≤ 50%) or positive (S/P% > 50%).

For RVF, serum from pastoralists (n = 335) and their livestock (n = 1,377) were tested with the ID Screen Rift Valley fever competition multi-species ELISA (ID.vet, Innovative Diagnostics, Grabes, France). The S/P% was calculated as above. The results were interpreted as positive (S/P% ≤ 40%) or negative (S/P% > 40%).

An independent evaluation of the ID.Screen Rift Valley fever multi-species ELISA determined a diagnostic sensitivity of 85.4% and specificity of 98.6% with the manufacture’s cut-off as described above [32]. The sensitivity and specificity of the ID.Screen Q fever multi-species ELISA could not be found in the literature in an independent evaluation, however, the manufacturer reported 100% for both sensitivity and specificity.

Statistical analysis

Statistical analysis was performed using Stata/IC 16.1. Descriptive statistics and seroprevalence of C. burnetii and RVFV antibodies were calculated for the pastoralists, total livestock, and for each species. For C. burnetii in humans, seroprevalence was calculated based on composite results of IgG Phase I and/or Phase II positivity.

Uni- and multi-variable logistic regression models with a random effect on village level to account for clustering were performed to identify factors associated with individual level seropositivity. Regression analysis was performed for pastoralists and total livestock. Variables from the household questionnaire relating to contact between pastoralists and livestock, movement of livestock, and symptoms of Q fever and RVF in livestock were included in the regression analysis (Table 1). Variables with a p-value ≤ 0.2 in the univariable analysis were selected for inclusion in the multivariable analysis with the model of best fit determined by the likelihood ratio test. Collinearity between included variables were checked for using the Pearson correlation coefficient. A p-value < 0.05 was considered significant.

10.1371/journal.pntd.0012392.t001 Table 1 Variables included logistic regression analysis.

	Description for pastoralists	Description for livestock	
Individual level variables	
Sex	Female	
Male	
Age	≤15 years	Breeder (camels ≥ 4 years; cattle: ≥ 3 years; sheep/goats ≥ 6 months)	
16–31 years	Young (camels < 4 years; cattle: < years; sheep/goats < 6 months)	
32–48 years		
≥49 years		
District	Amibara	
Awash	
Asayta	
Mille	
Dubti	
Species	Not applicable	Camel	
	Cattle	
	Sheep	
	Goat	
Household level variables	
Livestock ownership	Camel	Not applicable	
Cattle		
Sheep		
Goat		
Camel abortion event in the household in the past 12 months	No abortion events in the herds	
Abortion events in the herds	
No camels owned	
Cattle abortion event in the household in the past 12 months	No abortion events in the herds	
Abortion events in the herds	
No cattle owned	
Sheep abortion event in the household in the past 12 months	No abortion events in the herds	
Abortion events in the herds	
No sheep owned	
Goat abortion event in the household in the past 12 months	No abortion events in the herds	
Abortion events in the herds	
No goats owned	
Abortion period	No abortion events in the herds	
Early (first semester for small ruminants; first trimester for large ruminants)	
Late (second semester for small ruminants; second and third trimester for large ruminants)	
Mix of both early and late abortions	
Livestock stillborn in the past 12 months	No	
Yes	
Migration in the past 12 months	No	
Yes	
Livestock purchased in the past 12 months	No	
Yes	
Livestock sold in the past 12 months	No	
Yes	
Men involved in shepherding of livestock	No	
Yes	
Women involved in shepherding of livestock	No	
Yes	
Children* involved in shepherding of livestock	No	
Yes	
*As identified by the respondent.

Results

This cross-sectional study included 335 pastoralists from 249 households in 32 villages. Pastoralists were aged between 7 and 80 years with a median age of 35 years (IQR 25–45). Men accounted for 55.2% of included pastoralists. Pastoralists came from five districts: Amibara (n = 109), Awash (n = 60), Asayta (n = 70), Mille (n = 80) and Dubti (n = 16) (Fig 1). Additionally, 1,377 livestock were tested to determine seroprevalence, including: goats (n = 684), sheep (n = 199), cattle (n = 236) and camels (n = 258). The majority of the livestock were female (92.4%) and of breeding age (95.5%). Household questionnaire data matched to both pastoralist and livestock seroprevalence data were available for 239 households in 32 villages. Livestock abortions were reported by 32.6% (78/239) of households spread throughout 32 villages, with 44.9% of these occurring in the late stage of pregnancy (towards the end of gestation) with a further 42.3% reported as mixed, including early (first trimester for large ruminants or first semester for small ruminants) to late stage abortions. Additionally, 35.1% (84/239) of households reported stillbirths among their livestock. All households interviewed in this study reported the practice of animal afterbirth disposal by discarding it in the bush. Selling livestock in the past 12 months was reported by 67.8% of households, while only 22.2% reported purchasing of new animals. The majority of households (72.4%) reported migration with their livestock.

10.1371/journal.pntd.0012392.g001 Fig 1 Map of Afar, north–eastern Ethiopia.

Study sites shown in grey. Insert shows a map of Ethiopia with the Afar region in grey. Adapted from [33].

Seroprevalence of C. burnetii and RVFV in pastoralists and livestock

The C. burnetii and RVFV seroprevalences in pastoralists were 25.0% (95% CI 18.6–32.6) and 6.1% (95% CI 3.3–11.0), respectively (Table 2). The overall seroprevalence of C. burnetii in livestock was 34.3% (95% CI 27.9–41.3) and 3.9% (95% CI 2.6–5.7) for RVFV. Goats had the highest seroprevalence for C. burnetii (51.9%, 95% CI 44.9–58.8), while cattle had the highest for RVFV (8.3%, 95% CI 3.3–19.2) (Table 2).

10.1371/journal.pntd.0012392.t002 Table 2 Seroprevalence of Coxiella burnetii and Rift Valley fever virus in pastoralists and livestock in Afar, Ethiopia.

	C. burnetii positive	RVFV positive	
	Positive, n	%	95% CI	Positive, n	%	95% CI	
Pastoralists	91	25.0	18.6–32.6	25	6.1	3.3–11.0	
Livestock	510	34.3	27.9–41.3	63	3.9	2.6–5.7	
 Camels	42	16.3	10.4–21.6	6	1.8	0.4–6.9	
 Cattle	23	8.8	5.0–15.0	32	8.3	3.3–19.2	
 Sheep	85	39.9	24.6–51.2	5	2.5	1.0–5.9	
 Goats	360	51.9	44.9–58.8	20	2.7	1.4–5.1	

No correlation in seroprevalence of C. burnetii or RVFV was observed between humans and livestock within the same household.

Risk factors associated with Coxiella burnetii seropositivity in pastoralists

Univariable analysis was performed to identify risk factors associated with C. burnetii seropositivity in pastoralists (Table 3). Pastoralists from Asayta (OR = 0.36, 95% CI 0.15–0.87, p = 0.022) and Mille (OR = 0.42, 95% CI 0.18–0.98, p = 0.045) had a lower odds ratio (OR) of C. burnetii seropositivity than those from Amibara. Pastoralists ≥ 49 years old (OR = 2.82, 95% CI 1.34–5.93, p = 0.006) and children ≤ 15 years old (OR = 3.83, 95% CI 1.35–10.81, p = 0.011) had an increase in OR for being seropositive for C. burnetii (OR = 2.82, 95% CI 1.34–5.93, p = 0.006) than adults aged between 16 and 31 years of age. Further, pastoralists from households where children were involved in shepherding of livestock had an increased OR of being seropositive for C. burnetii (OR = 2.24 95% CI 1.16–4.35, p = 0.017). Pastoralists from households reporting livestock abortions, across both early and late pregnancy periods, had an increased OR of C. burnetii seropositivity, compared to no abortions in livestock (OR = 3.16, 95% CI 1.43–7.00, p = 0.004). Pastoralists from households that reported abortion events in goats had a 2.1-fold (95% CI 1.18–3.78, p = 0.011) increase in OR of C. burnetii infection compared to households that reported no goat abortions.

10.1371/journal.pntd.0012392.t003 Table 3 Univariable and multivariable analysis of predictors for Coxiella burnetii seropositivity in pastoralists.

	Positive (%)	Univariable	Multivariable	
		OR	95% CI	P-value	AOR	95% CI	P-value	
Individual variables	
Sex	
 Male	47/185 (25.4)	1.00						
 Female	45/150 (30.0)	1.22	0.73–2.05	0.441				
Age	
 ≤15	10/22 (45.5)	3.83	1.35–10.81	0.011	4.29	1.47–12.54	0.008	
 16–31	27/129 (20.9)	1.00			1.00			
 32–48	32/126 (25.4)	1.36	0.73–2.55	0.337	1.24	0.65–2.38	0.512	
 ≥49	23/58 (39.7)	2.82	1.34–5.93	0.006	2.31	1.06–5.05	0.036	
District	
 Amibara	41/109 (37.6)	1.00						
 Awash	17/60 (28.3)	0.64	0.23–1.58	0.330				
 Asayta	13/70 (18.6)	0.36	0.15–0.87	0.022				
 Mille	16/80 (20.0)	0.42	0.18–0.98	0.045				
 Dubti	5/16 (31.3)	0.78	0.20–3.07	0.727				
Household variables	
Livestock ownership	
 Camel	66/246 (26.8)	0.83	0.39–1.75	0.621				
 Cattle	68/255 (26.7)	0.81	0.37–1.75	0.585				
 Sheep	59/214 (27.6)	1.03	0.57–1.89	0.914				
 Goat	87/310 (28.1)	5.15	0.61–43.77	0.133				
Camel abortion event in the household in the past 12 months	
 No abortion	61/231 (26.4)	1.00						
 Abortion	5/15 (33.3)	1.93	0.56–6.57	0.295				
 No camels	22/78 (28.2)	1.27	0.59–2.73	0.545				
Cattle abortion event in the household in the past 12 months	
 No abortion	63/236 (26.7)	1.00						
 Abortion	5/19 (26.3)	1.69	0.46–6.24	0.431				
 No cattle	20/69 (29.0)	1.31	0.59–2.95	0.506				
Sheep abortion event in the household in the past 12 months	
 No abortion	59/211 (28.0)	1.00						
 Abortion	0/4 (0.0)	Omitted						
 No sheep	29/109 (26.6)	0.93	0.50–1.70	0.804				
Goat abortion event in the household in the past 12 months	
 No abortion	53/222 (23.9)	1.00						
 Abortion	34/88 (28.6)	2.11	1.18–3.78	0.011	2.13	1.17–3.86	0.013	
 No goats	1/14 (7.1)	0.23	0.03–0.42	0.186	0.21	0.02–1.93	0.169	
Abortion period	
 No abortion	53/226 (23.5)	1.00						
 Early	1/4 (25.0)	1.94	0.14–26.54	0.617				
 Late	14/44 (31.8)	1.56	0.73–3.37	0.254				
 Mix	18/41 (43.9)	3.16	1.43–7.00	0.004				
 Not answered	2/9 (22.2)	0.85	0.15–4.81	0.854				
Livestock stillborn in the past 12 months	35/120 (29.2)	1.10	0.63–1.92	0.726				
Migration in the past 12 months	62/231 (26.8)	0.82	0.41–1.66	0.575				
Livestock purchased in the past 12 months	17/67 (25.4)	0.84	0.43–1.63	0.601				
Livestock sold in the past 12 months	61/221 (27.6)	1.17	0.62–2.21	0.635				
Men involved in shepherding of livestock	23/105 (21.9)	0.63	0.34–1.16	0.137				
Women involved in shepherding of livestock	65/212 (30.7)	1.73	0.91–3.27	0.094				
Children involved in shepherding of livestock	70/224 (31.3)	2.24	1.16–4.35	0.017				
Statistically significant (p–value ≤ 0.05) variables are highlighted in bold italics. OR = Odds ratio. AOR = Adjusted odds ratio.

The multivariable model of best fit for C. burnetii seropositivity in pastoralists included age and a history of goat abortions in the household. Pastoralists aged ≤ 15 years (OR = 4.29, 95% CI 1.47–12.54, p = 0.008) and those aged ≥ 49 (OR = 2.31, 95% CI 1.06–5.05, p = 0.036) had an increased OR for seropositivity to C. burnetii. Pastoralists from households spread throughout 32 villages, that reported abortion events in goats had an increased OR of C. burnetii seropositivity (OR = 2.13, 95% CI 1.17–3.86, p = 0.013).

Risk factors associated with Rift Valley fever virus seropositivity in pastoralists

Univariable analysis was performed to identify risk factors associated with RVFV seropositivity in pastoralists (Table 4). Pastoralists ≥ 49 years old had an increase in OR for being seropositive for RVFV (OR = 3.29, 95% CI 1.02–10.61, p = 0.036) than adults aged between 16 and 31 years of age.

No other factors were associated with RVF seropositivity, thus multivariable analysis was not done.

10.1371/journal.pntd.0012392.t004 Table 4 Univariable analysis of predictors for Rift Valley fever virus seropositivity in pastoralists.

	Positive (%)	OR	95% CI	P-value	
Individual variables	
Sex	
 Male	16/185 (8.6)	1.00			
 Female	9/150 (6.0)	0.69	0.28–1.68	0.411	
Age	
 ≤15	0/22 (0.0)	Omitted			
 16–31	6/129 (4.7)	1.00			
 32–48	11/126 (8.7)	1.86	0.64–5.42	0.253	
 ≥49	8/58 (13.8)	3.29	1.02–10.61	0.046	
District	
 Amibara	5/109 (4.7)	1.00			
 Awash	5/60 (8.3)	2.03	0.43–9.54	0.368	
 Asayta	10/70 (14.3)	3.69	0.99–13.80	0.052	
 Mille	5/80 (6.3)	1.59	0.36–7.05	0.539	
 Dubti	0/16 (0.0)	Omitted			
Household variables	
Livestock ownership	
 Camel	16/246 (6.5)	0.94	0.27–3.26	0.919	
 Cattle	17/255 (6.7)	0.97	0.27–3.51	0.966	
 Sheep	17/214 (7.9)	2.10	0.69–6.43	0.193	
 Goat	23/310 (7.4)	Omitted			
Camel abortion event in the household in the past 12 months	
 No abortion	15/231 (6.5)	1.00			
 Abortion	1/14 (7.1)	0.86	0.09–8.05	0.893	
 No camels	7/78 (9.0)	1.05	0.30–3.73	0.935	
Cattle abortion event in the household in the past 12 months	
 No abortion	15/236 (6.4)	1.00			
 Abortion	2/19 (10.5)	1.31	0.22–7.77	0.765	
 No cattle	6/69 (8.7)	1.07	0.29–3.92	0.921	
Sheep abortion event in the household in the past 12 months	
 No abortion	17/211 (8.1)	1.00			
 Abortion	0/4 (0.0)	Omitted			
 No sheep	6/109 (5.5)	0.49	0.16–1.49	0.208	
Goat abortion event in the household in the past 12 months	
 No abortion	19/222 (8.6)	1.00			
 Abortion	4/88 (4.5)	0.53			
 No goats	0/14 (0.0)	Omitted	0.16–1.72	0.292	
Abortion period	
 No abortion	18/226 (6.8)	1.00			
 Early	0/4 (0.0)	Omitted			
 Late	2/44 (4.5)	0.61	0.12–2.95	0.534	
 Mix	3/41 (7.3)	0.88	0.22–3.46	0.852	
 Not answered	0/9 (0.0)	Omitted			
Livestock stillborn in the past 12 months	7/120 (5.8)	0.73	0.27–1.96	0.536	
Migration in the past 12 months	15/231 (6.5)	0.88	0.29–2.71	0.824	
Livestock purchased in the past 12 months	5/67 (7.5)	0.99	0.33–3.02	0.990	
Livestock sold in the past 12 months	19/221 (8.6)	2.66	0.79–9.00	0.116	
Men involved in shepherding of livestock	9/105 (5.6)	1.19	0.45–3.16	0.723	
Women involved in shepherding of livestock	11/212 (5.2)	0.52	0.19–1.41	0.199	
Children involved in shepherding of livestock	13/224 (5.8)	0.85	0.47–2.64	0.781	
Statistically significant (p–value ≤ 0.05) variables are highlighted in bold italics. OR = Odds ratio.

Risk factors associated with Coxiella burnetii seropositivity in livestock

Univariable analysis was performed to identify risk factors associated with C. burnetii seroprevalence in livestock (Table 5). Sheep (OR = 0.56, 95% CI 0.40–0.80, p = 0.001), cattle (OR = 0.09, 95% CI 0.05–0.14, p < 0.001) and camels (OR = 0.16, 95% CI 0.10–0.24, p < 0.001) had a significantly lower OR of being seropositive for C. burnetii compared to goats. Young animals also had a lower OR (OR = 0.07, 95% CI 0.02–0.30, p < 0.001) of being C. burnetii seropositive compared to those of breeding age. Livestock in Mille had decreased OR (OR = 0.42, 95% CI 0.21–0.84, p = 0.014) of being seropositive for C. burnetii compared to those in Amibara. Livestock from households that did not have goats had a lower OR of C. burnetii seropositivity than those from households that had goats, even without abortion events.

10.1371/journal.pntd.0012392.t005 Table 5 Univariable and multivariable analysis of predictors for Coxiella burnetii seropositivity in livestock.

	Univariable	Multivariable	
	Positive (%)	OR	95% CI	P-value	AOR	95% CI	P-value	
Individual variables	
Sex								
 Female	479/1272 (37.7)	1.00			1.00			
 Male	31/105 (29.5)	0.60	0.38–0.96		0.71	0.41–1.20	0.197	
Age	
 Breeder	508/1315 (38.6)	1.00			1.00			
 Young	2/60 (3.3)	0.07	0.02–0.30	<0.001	0.23	0.05–1.02	0.053	
 Unknown	0/2 (0.0)	Omitted						
Species	
 Goat	360/684 (52.6)	1.00			1.00			
 Sheep	85/199 (42.7)	0.56	0.40–0.80	0.001	0.60	0.42–0.86	0.005	
 Cattle	23/236 (10.6)	0.09	0.05–0.14	<0.001	0.08	0.05–0.14	<0.001	
 Camel	42/258 (16.3)	0.16	0.10–0.24	<0.001	0.18	0.11–0.27	<0.001	
District	
 Amibara	199/560 (35.5)	1.00			1.00			
 Awash	119/224 (53.1)	1.46	0.65–3.30	0.361	0.71	0.40–1.27	0.250	
 Asayta	93/214 (43.5)	1.36	0.71–2.60	0.351	0.48	0.29–0.80	0.005	
 Mille	71/310 (22.9)	0.42	0.21–0.84	0.014	0.31	0.18–0.52	<0.001	
 Dubti	28/69 (40.6)	1.14	0.40–3.24	0.806	1.12	0.53–2.38	0.765	
Household variables	
Camel abortion event in the household in the past 12 months	
 No abortion	334/978 (34.2)	1.00						
 Abortion	34/67 (50.7)	1.17	0.66–2.07	0.591				
 No camels	127/281 (45.2)	0.95	0.61–1.46	0.798				
Cattle abortion event in the household in the past 12 months	
 No abortion	349/1006 (34.7)	1.00						
 Abortion	22/77 (28.6)	0.84	0.44–1.58	0.584				
 No cattle	124/243 (51.0)	1.20	0.76–1.89	0.443				
Sheep abortion event in the household in the past 12 months	
 No abortion	353/990 (35.7)	1.00						
 Abortion	2/7 (28.6)	0.49	0.09–2.83	0.427				
 No sheep	140/329 (42.6)	1.24	0.89–1.72	0.199				
Goat abortion event in the household in the past 12 months	
 No abortion	323/877 (36.8)	1.00			1.00			
 Abortion	165/394 (41.9)	1.11	0.85–1.46	0.448	1.22	0.84–1.49	0.453	
 No goats	7/55 (12.7)	0.37	0.15–0.93	0.034	0.45	0.18–1.10	0.080	
Abortion period	
 No abortion	194/483 (40.2)	1.00						
 Early	0/14 (0.0)	Omitted						
 Late	78/199 (39.2)	0.83	0.56–1.23	0.357				
 Mix	80/181 (44.2)	1.11	0.74–1.65	0.611				
 Not answered	13/39 (33.3)	0.91	0.42–1.96	0.813				
Livestock stillborn in the past 12 months	180/438 (41.1)	1.07	0.81–1.38	0.690				
Migration in the past 12 months	341/988 (34.5)	0.97	0.65–1.44	0.883				
Livestock purchased in the past 12 months	124/315 (39.4)	1.04	0.77–1.39	0.812				
Livestock sold in the past 12 months	362/583 (62.19	1.32	0.94–1.84	0.108				
Men involved in shepherding of livestock	150/384 (39.1)	1.33	0.99–1.80	0.059				
Women involved in shepherding of livestock	321/922 (34.8)	0.74	0.53–1.04	0.084	0.67	0.47–0.94	0.020	
Children involved in shepherding of livestock	361/970 (37.2)	1.06	0.77–1.46	0.734				
Statistically significant (p–value ≤ 0.05) variables are highlighted in bold italics. OR = Odds ratio. AOR = Adjusted odds ratio.

In the multivariable analysis the model of best fit for C. burnetii seropositivity in livestock included district, sex, age, species, abortion in goats and shepherding by women. Sheep (OR = 0.60, 95% CI 0.42–0.86, p = 0.005), cattle (OR = 0.08, 95% CI 0.05–0.14, p < 0.001) and camels (OR = 0.18, 95% CI 0.11–0.27, p < 0.001) still showed a reduced OR for C. burnetii seropositivity compared with goats. In the multivariable analysis, Asayta (OR = 0.48, 95% CI 0.29–0.80, p = 0.005) also showed reduced odds of C. burnetii seropositivity in individual animals, along with Mille (OR = 0.31, 95% CI 0.18–0.52, p < 0.001). Livestock in households where women were involved in shepherding also had a lower OR of C. burnetii seropositivity (OR = 0.67, 95% CI 0.47–0.94, p = 0.020).

Risk factors associated with Rift Valley fever virus seropositivity in livestock

Univariable analysis was performed to identify risk factors associated with RVFV seroprevalence in livestock (Table 6). Livestock in Dubti had a 7.0-fold (95% CI 2.58–18.75, p < 0.001) increase in OR of being seropositive for RVFV compared to those in Amibara. Cattle had a 6.6-fold (95% CI 3.29–13.31, p < 0.001) increase in OR of being seropositive to RVFV compared to goats, with livestock from households that reported abortion events in cattle having a 2.5-fold (95% CI 10.5–6.08, p = 0.039) increase in odds. Livestock from households reporting early-term (OR = 7.97, 95% CI 1.49–42.62, p = 0.015) abortions in livestock had an increased OR of RVFV seropositivity compared to those that did not report abortion events in livestock.

10.1371/journal.pntd.0012392.t006 Table 6 Univariable and multivariable analysis of predictors for Rift Valley fever virus seropositivity in livestock.

	Univariable	Multivariable	
	Positive (%)	OR	95% CI	P-value	AOR	95% CI	P-value	
Individual variables	
Sex	
 Female	7/105	1.00						
 Male	56/1272	1.58	0.68–3.66	0.285				
Age	
 Breeder	59/1315 (4.5)	1.00						
 Young	4/60 (6.7)	1.61	0.54–4.83	0.393				
 Unknown	0/2 (0.0)	Omitted						
Species	
 Goat	20/684 (2.9)	1.00			1.00			
 Sheep	5/199 (2.5)	0.96	0.35–2.65	0.935	1.26	0.43–3.71	0.678	
 Cattle	32/236 (13.6)	6.62	3.29–13.31	<0.001	4.35	1.82–10.36	0.001	
 Camel	6/258 (2.3)	0.96	0.35–2.60	0.930	0.51	0.13–1.98	0.329	
District								
 Amibara	21/560 (3.8)	1.00			1.00			
 Awash	8/224 (3.6)	0.92	0.34–2.48	0.862	0.91	0.23–3.57	0.887	
 Asayta	8/214 (3.7)	1.02	0.40–2.57	0.969	0.52	0.12–2.24	0.378	
 Mille	12/310 (3.9)	1.12	0.48–2.64	0.792	0.56	0.12–2.71	0.471	
 Dubti	14/69 (20.3)	6.95	2.58–18.75	<0.001	10.62	3.16–35.72	<0.001	
Household variables	
Camel abortion event in the household in the past 12 months	
 No abortion	44/978 (4.5)	1.00						
 Abortion	6/67 (9.0)	2.15	0.77–6.01	0.144				
 No camels	11/281 (3.9)	1.02	0.44–2.39	0.963				
Cattle abortion event in the household in the past 12 months	
 No abortion	45/1006 (58.4)	1.00			1.00			
 Abortion	9/77 (11.7)	2.52	1.05–6.08	0.039	2.70	0.75–9.73	0.129	
 No cattle	7/243 (2.9)	0.67	0.26–1.75	0.416	1.17	0.34–4.03	0.805	
Sheep abortion event in the household in the past 12 months	
 No abortion	42/990 (4.2)	1.00						
 Abortion	0/7 (0.0)	Omitted						
 No sheep	19/329 (5.8)	1.69	0.87–3.28	0.118				
Goat abortion event in the household in the past 12 months	
 No abortion	36/877 (4.1)	1.00						
 Abortion	22/394 (5.6)	1.19	0.67–2.14	0.553				
 No goats	3/55 (5.5)	1.37	0.36–5.24	0.645				
Abortion period	
 No abortion	14/483 (2.9)	1.00			1.00			
 Early	3/14 (2.1)	7.97	1.49–42.62	0.015	2.29	0.29–17.98	0.430	
 Late	11/199 (5.5)	1.71	0.71–4.11	0.230	1.37	0.52–3.62	0.528	
 Mix	12/169 (7.1)	2.13	0.88–5.16	0.093	1.25	0.45–3.47	0.671	
 Not answered	0/39 (0.0)	Omitted			Omitted			
Livestock stillborn in the past 12 months	24/438 (5.5)	1.10	0.62–1.95	0.756				
Migration in the past 12 months	38/988 (3.8)	0.75	0.36–1.57	0.444				
Livestock purchased in the past 12 months	12/315 (3.8)	0.97	0.49–1.93	0.935				
Livestock sold in the past 12 months	40/583 (6.9)	1.00	0.51–1.95	0.997				
Men involved in shepherding of livestock	16/384 (4.2)	0.78	0.41–1.49	0.455				
Women involved in shepherding of livestock	38/922 (4.1)	0.58	0.29–1.14	0.115	0.43	0.01–0.15	0.104	
Children involved in shepherding of livestock	48/970 (4.9)	1.40	0.69–2.84	0.347				
Statistically significant (p–value ≤ 0.05) variables are highlighted in bold italics. OR = Odds ratio. AOR = Adjusted odds ratio.

In the multivariable analysis, the model of best fit for RVFV seropositivity in livestock included district, species, abortion events in cattle, abortion periods and shepherding by women. The increase in OR of seropositivity was similar to that of the univariable analysis with cattle having a higher OR (OR = 4.35, 95% CI 1.82–10.36, p = 0.001) compared with goats and animals in Dubti having a higher OR (OR = 10.62, 95% CI 3.16–35.72, p < 0.001) compared with those in Amibara.

Discussion

In our study we employed a One Health approach to investigate the relationship between seropositivity of Q fever and RVFV in pastoralists and their livestock in Afar, north-eastern Ethiopia. We found a quarter (25.0%) of the pastoralists were seropositive for Q fever, matching a similar study by Ibrahim et al. from the Somali region of Ethiopia that found 27% seroprevalence to C. burnetii in pastoralists [18]. These results, however, are in contrast to the only other study to date in humans in Ethiopia, in which Addis Ababa abattoir workers had a 6.5% prevalence for Q fever [34]. While abattoir workers are considered a high-risk group [8], these results may indicate that pastoralists are at even higher risk, possibly due to life-long close contact with their livestock representative of a cumulative risk. A recent study in Chad that looked at 960 mobile agro-pastoralists found an even higher prevalence of 49.7% for C. burnetii antibodies [35].

A third of the livestock (34.3%) were seropositive for C. burnetii, with goats having the highest AP (51.9%), followed by sheep (36.9%), camels (16.3%) and cattle (8.8%). The differences in seroprevalence between species was suggested by a study by Tschopp et al. to be the result of pastoralists in Afar often keeping herds separated by species [25]. Goats are the most commonly sold species, potentially exposing them to other infected animals at markets [25]. Regular market exposure highlights the potential risk of infected goats transmitting the disease to new (uninfected/unexposed) herds or unsold animals returning to their original herds with newly acquired pathogens.

In our study, we found an association between children ≤ 15 years and C. burnetii seropositivity. Children in the Afar region often assist in caring for goats in addition to regularly being fed raw milk [25]. A study on risk factors of zoonoses among pastoralists in Afar found all participants drank raw milk with goat milk being the most commonly consumed and 20% of participants also reported consuming soured milk [25]. Further, pastoralists from households that reported abortion events in goats had a 2.1-fold increase in OR of being seropositive compared to pastoralists from households without goat abortions. These findings suggest goats may be a primary cause of C. burnetii transmission to humans in this region.

The study in the Somali region of Ethiopia reported similar seroprevalence results for goats (48.8%), sheep (28.9%) and cattle (9.6%), however, reported a much higher seroprevalence in camels (55.7%) [18]. A study in livestock from pastoral regions in south-eastern Ethiopia also found a similar seroprevalence in goats (54.2%), but higher in camels (90.0%) and cattle (31.6%) [17]. While a study in small ruminants from the Borana pastoral area in southern Ethiopia found lower seroprevalences with 35.7% in goats and 18.3% in sheep [19]. The study in Chad also found lower seroprevalences of 7.1% in cattle, 17.1% in goats and 19.1% in sheep [35]. Although direct comparisons cannot be made due to differences in testing methods, the variation in reported seroprevalences could be attributed to differences in animal husbandry methods or environmental conditions including the presence of ticks. Pastoralists from Asayta and Mille in central Afar had significantly lower OR of being C. burnetii seropositive than those from Amibara in southern Afar, bordering the Somali and Oromia regions of Ethiopia. Similarly, in the multivariable analysis livestock from Asayta and Mille had a significantly decreased OR of C. burnetii compared to livestock in Amibara.

While no association was seen with sex for either humans or their livestock, the majority of animals included were female due to pastoralists primarily keeping animals for milk production and reproduction purposes [18]. A positive association was observed for pastoralists aged ≥ 49 years with C. burnetii seropositivity, this is often observed due to an individual having more cumulative time to become exposed to the pathogen [18]. Similarly, in livestock, young animals also had a significantly lower OR of being C. burnetii seropositive compared with animals of breeding age.

In our study we found a prevalence of 6.1% for RVFV in pastoralists and as with C. burnetii those aged ≥ 49 years had an increased OR of seropositivity. The study by Ibrahim et al. was the only study identified that reported on RVFV seroprevalence in humans in Ethiopia, this study from the Somali region found a higher prevalence of 13.2% [18]. Further, the study in Chad found a much higher seroprevalence of 28.1% for RVFV among mobile agro-pastoralists [35]. In our study, we found an overall prevalence of RVFV in livestock of 3.9%. Cattle had the highest seroprevalence (8.3%), with the other livestock species being significantly lower: goats (2.7%), sheep (2.5%) and camels (1.8%).

Asebe et al. reported a significant association between RVFV infection in cattle and a history of abortion [18]. We saw a similar significant association in the univariable analysis with livestock from households that had a history of abortions in cattle having a 2.5-fold increase in OR of being seropositive for RVFV antibodies. This association, while no longer significant in the multivariable analysis, may be worth further exploration. Moreover, the study investigating brucellosis in Afar found that while there was an association between abortion history and Brucella seropositivity in camels, goats and sheep, this association was not present for cattle and postulated there should be a different cause for abortion in cattle [22]. Our study indicates that RVFV could be a contributing agent of abortion in this species.

In contrast to our study, the study in the Somali region reported camels having the highest apparent seroprevalence for RVFV of 42.6%, followed by cattle (17.9%), sheep (7.4%) and goats (6.3%) [18]. Two further studies on RVFV in Ethiopian livestock, which only investigated cattle, reported lower seroprevalences of 5.0% in the south Omo area of southern Ethiopia and 7.6% in south-western Ethiopia, bordering South Sudan [20,21]. While the study in Chad found 9.5% of cattle, 3.9% of goats, and 15.5% of sheep to be seropositive for RVFV [35].

In our study, livestock in Dubti had a 10.6-fold increase in OR of RVFV seropositivity compared to their counterparts in Amibara. The variation in prevalence of RVFV seen in different pastoral areas of Ethiopia and other pastoral communities in Africa may be related to environmental conditions including water sources that directly affect the presence of the mosquito vectors. Dubti neighbours the district of Afambo, in which lie a series of lakes marking the end of the Awash River. These lakes may offer areas of stagnant water, providing breeding grounds for mosquitos, and may be the source of the high seroprevalences of RVFV found in central Afar. A study in southern Ethiopia found Aedes mosquitos accounted for 25% of those collected, however further entomological studies would be required to map the density of RVFV vectors in other regions of Ethiopia including Afar [36]. Environmental monitoring of heavy rainfall, flooding, and mosquito swarms have been suggested to identify high risk areas for RVFV control in the Horn of Africa, allowing for targeted livestock vaccination campaigns [37]. This monitoring would provide early warnings for outbreak preparedness programs that may include expanding vaccination coverage to surrounding areas, restrictions on livestock movements or vector control, for example: applying insecticides to livestock [37].

Additional factors influencing RVF prevalence may involve the movement of animals, potentially exposing them to vectors or infected animals from other regions. Large animals, cattle and camels, are generally taken during seasonal migrations, while small ruminants often remain at the settlement, which may account for the higher RVFV antibody prevalence seen in cattle in our study [25]. Pastoralists in different districts use distinct migration pathways, potentially also explaining why RVFV appears to be circulating predominantly in Central Afar while C. burnetii was more common in the southern part [26].

No correlation was observed for either C. burnetii or RVFV seropositivity between pastoralists and livestock from the same household. It is possible that pastoralists became infected from livestock no longer in their herds, either from selling or death, considering the shorter lifespan of livestock in comparison to humans [22]. Alternatively, pastoralists may have become infected from contact with other animals or their excretions into the environment [22]. C. burnetii has been shown to survive in the environment for at least a year [38]. While RVFV could be transmitted by mosquitos from neighbouring herds. A similar study on the seroprevalence of brucellosis in Kyrgyzstan demonstrated clear dependence of human seropositivity from sheep seroprevalence and not from goats or cattle [39]. The study sites included in the Kyrgyzstan study, however, were located at a greater distance from each other than the study sites included in our study in Afar, indicating that correlation of human-animal exposure to zoonoses may be dependent on the scale of comparison. It seems that comparisons over more than a hundred kilometres can be more easily demonstrated because of the higher variability of human-animal contacts at shorter distances [39].

Pastoral regions present a challenge for disease surveillance as well as providing human and veterinary health services, generally being in remote, harsh areas that lack infrastructure including diagnostic facilities. Maintaining the cold chain to these regions for test kits or alternatively to bring samples to a central reference laboratory is often logistically difficult [22]. Correctly diagnosing both humans and animals is essential to ensure appropriate treatment is utilized and prevent antimicrobial resistance increasing in these regions. Current recommended diagnostic tests for Q fever are IFA and for RVF either PCR, virus isolation, or antigen-detection ELISA, all of which are technically demanding and require sophisticated laboratories, which are often found only in urban centres [5,40]. The development of highly sensitive and specific rapid diagnostic tests (RDTs), that are stable at room temperature, would prove particularly beneficial in these pastoral settings, providing immediate results. Additionally, RDTs have been found to be well received by participants who refused venous blood draws [22]. Appropriate diagnostics are also essential for surveillance of these diseases for early detection of potential outbreaks. Large outbreaks in livestock can also see large-scale transmission to humans, as was the case of the Q fever outbreak in the Netherlands from 2007–2010, with more than 4,000 human cases reported and more than 40,000 cases estimated in total [5,41]. The Netherlands outbreak was attributed primarily to dairy goat farming [42]. Furthermore, large outbreaks of zoonotic diseases can cause economic loss at the individual, community and national level. Estimated economic impacts of RVF outbreaks between 1930 and 2009 have ranged from 5–470 million USD at national levels [24]. Ethiopia is particularly vulnerable to large outbreaks of zoonotic disease, having the largest livestock population in Africa [43]. Livestock accounts for 16.5% and 35.6% of the national Gross Domestic Product (GDP) and the agricultural GDP, respectively, supporting 80% of rural inhabitants [43–45]. Since both Q fever and RVF commonly affect domestic ruminants, pastoral livelihoods can be expected to be significantly adversely affected by disease outbreaks.

A limitation of this study is that we made use of samples collected for a previous study and not all samples had enough volume remaining for the Q fever and RVF serological testing. This is evident in only five of the seven districts included in the brucellosis study being included in the present study and also the lower sample numbers for Dubti. Further, only limited samples from sheep, cattle and camels were available and did not meet the required sample size, subsequently regression analysis for individual species seropositivity was not performed. The sample size calculation was done for each pathogen as a single proportion, however, a sample size calculation adjusting for clustering would have been more appropriate. This may have played a role in the broad confidence intervals observed, however, this does not impact our conclusions. An additional limitation of the study was that there was no availability of an independent evaluation of the Q fever ELISA to provide robust diagnostic accuracy data. Serological assays should be evaluated in the population of interest to determine the diagnostic accuracy and most appropriate cut off for use in that specific setting. These evaluations, however, rely on well-characterized reference sample that are often not available in resource-limited settings [46].

Conclusions

Our study showed that both zoonotic diseases; Q fever and RVF are circulating among pastoralists and their livestock in Afar. Goats appeared to be the main species affected by Q fever and may be leading cause of transmission to humans. Cattle, on the other hand, appeared to be the main species affected by RVF with abortion events in this species possibly attributed to this viral infection.

To reduce the potential impact of large-scale outbreaks of both these pathogens in vulnerable pastoral regions, early detection and rapid response programs tailored to the mobility of pastoral communities are needed. This requires strengthening of integrated animal-human surveillance systems, including establishing suitable diagnostics, and improved communication between the human and animal health sectors.

We thank AHRI for the logistical support and especially the AHRI laboratory team for their support of this project. We would also like to thank Silvia Cicconi from the Clinical Statistics and Data Management group and Jan Hattendorf from the One Health group, Swiss TPH for all their advice and support for the statistical analysis. A great thank you also goes to all participating pastoralists.

10.1371/journal.pntd.0012392.r001
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Remais Justin V. Section Editor
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2024
Remais, Rayner
https://creativecommons.org/licenses/by/4.0/ 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.
Submission Version0
5 Mar 2024

Dear Dr Oakley,

Thank you very much for submitting your manuscript "Seroprevalence and risk factors for Q Fever and Rift Valley Fever in pastoralists and their livestock in Afar, Ethiopia: A One Health approach" for consideration at PLOS Neglected Tropical Diseases. As with all papers reviewed by the journal, your manuscript was reviewed by members of the editorial board and by several independent reviewers. In light of the reviews (below this email), we would like to invite the resubmission of a significantly-revised version that takes into account the reviewers' comments.

We cannot make any decision about publication until we have seen the revised manuscript and your response to the reviewers' comments. Your revised manuscript is also likely to be sent to reviewers for further evaluation.

When you are ready to resubmit, please upload the following:

[1] A letter containing a detailed list of your responses to the review comments and a description of the changes you have made in the manuscript. Please note while forming your response, if your article is accepted, you may have the opportunity to make the peer review history publicly available. The record will include editor decision letters (with reviews) and your responses to reviewer comments. If eligible, we will contact you to opt in or out.

[2] Two versions of the revised manuscript: one with either highlights or tracked changes denoting where the text has been changed; the other a clean version (uploaded as the manuscript file).

Important additional instructions are given below your reviewer comments.

Please prepare and submit your revised manuscript within 60 days. If you anticipate any delay, please let us know the expected resubmission date by replying to this email. Please note that revised manuscripts received after the 60-day due date may require evaluation and peer review similar to newly submitted manuscripts.

Thank you again for your submission. We hope that our editorial process has been constructive so far, and we welcome your feedback at any time. Please don't hesitate to contact us if you have any questions or comments.

Sincerely,

Simon Rayner

Academic Editor

PLOS Neglected Tropical Diseases

Justin Remais

Section Editor

PLOS Neglected Tropical Diseases

***********************

Reviewer's Responses to Questions

Key Review Criteria Required for Acceptance?

As you describe the new analyses required for acceptance, please consider the following:

Methods

-Are the objectives of the study clearly articulated with a clear testable hypothesis stated?

-Is the study design appropriate to address the stated objectives?

-Is the population clearly described and appropriate for the hypothesis being tested?

-Is the sample size sufficient to ensure adequate power to address the hypothesis being tested?

-Were correct statistical analysis used to support conclusions?

-Are there concerns about ethical or regulatory requirements being met?

Reviewer #1: (No Response)

Reviewer #2: (No Response)

Reviewer #3: Methods

-Are the objectives of the study clearly articulated with a clear testable hypothesis stated?

-> objectives yes, hypothesis no.

-Is the study design appropriate to address the stated objectives?

-> no. Study design, in pariclar sampling design could use some improvement.

-Is the population clearly described and appropriate for the hypothesis being tested?

-> What is not comptelety clear is why a different number of household from each study site (the 5 sites) were sampled. Further comments within the point by point revisions document (attached word file).

-Is the sample size sufficient to ensure adequate power to address the hypothesis being tested?

-> sample size was calculated suing appripriate tools, however clustering of the data (region-study site-hoseholds- humans/livestock) should have been considered. (More on this in the attached point by point revision.)

-Were correct statistical analysis used to support conclusions?

-> Yes

-Are there concerns about ethical or regulatory requirements being met?

-> Yes

--------------------

Results

-Does the analysis presented match the analysis plan?

-Are the results clearly and completely presented?

-Are the figures (Tables, Images) of sufficient quality for clarity?

Reviewer #1: (No Response)

Reviewer #2: (No Response)

Reviewer #3: Results

-Does the analysis presented match the analysis plan?

-> in the analysis plan more detailed info on the so called risk factors should have been provided.

-Are the results clearly and completely presented? (More on this in the attached point by point revision.)

-Are the figures (Tables, Images) of sufficient quality for clarity?

-> yes

--------------------

Conclusions

-Are the conclusions supported by the data presented?

-Are the limitations of analysis clearly described?

-Do the authors discuss how these data can be helpful to advance our understanding of the topic under study?

-Is public health relevance addressed?

Reviewer #1: (No Response)

Reviewer #2: (No Response)

Reviewer #3: Conclusions

-Are the conclusions supported by the data presented?

-> mostly yes. There are conclusion on the stronger collaboration of human and animal sectors and while these are generell recommendations, the study it self and the data do not suggest anything on One Health governence level.

-Are the limitations of analysis clearly described?

-> No, this is missing and should be added.

-Do the authors discuss how these data can be helpful to advance our understanding of the topic under study?

-> Yes.

-Is public health relevance addressed?

-> Yes.

--------------------

Editorial and Data Presentation Modifications?

Use this section for editorial suggestions as well as relatively minor modifications of existing data that would enhance clarity. If the only modifications needed are minor and/or editorial, you may wish to recommend “Minor Revision” or “Accept”.

Reviewer #1: (No Response)

Reviewer #2: (No Response)

Reviewer #3: (No Response)

--------------------

Summary and General Comments

Use this section to provide overall comments, discuss strengths/weaknesses of the study, novelty, significance, general execution and scholarship. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. If requesting major revision, please articulate the new experiments that are needed.

Reviewer #1: Well written and timely manuscript.

Good use of One Health approach.

Good evidence and argument for tailoring epidemiological services to nomadic people.

Fills in some gaps in understudied RVFV-endemic region.

Some minor corrections suggested here:

Line 69 & throughout - use serial commas (i.e., should be “… humans, animals, and their environment …”)

Line 71 & throughout - Q fever (not Q fever)

Line 72 & throughout - Rift Valley fever (not Fever)

Line 73 - RVFV is also under-reported due to poor infrastructure, poor public education/engagement, and severe economic impact from OIE/WOAH trade bans.

Line 89 - clarify “animals”; redundant given rest of sentence?

Line 90 - through mosquitoes and other hematophagous arthropods

Line 91 - “RVF” should be “RVFV” — check throughout for appropriate use of RVF vs RVFV.

Line 93 - establish the use of RVFV throughout instead of “RVF virus”

Line 103 - should be “… migrating and searching for …”

Line 104 & throughout - suggest use either mobile or nomadic, not both; or clarify the terms

Line 101 & throughout - no need to capitalize compass directions

Line 107-111 — very good; should link anticipated results from statement in line 112-113 with suggested action to accomplish statement in line 107-111.

Line 122 - were should be was

Line 123 - should be “… representing five of the seven woredas, I.e., Amibara, Awash, …”

Line 127 - remove comma

Line 161 - should be “manufacturer’s”

Line 163 - should be “reported”

Line 182 - “was” should be “were”

Line 303 - separated by … what?

Line 324 - should be “… aged ≥49 years with C. burnetii seropositivity.”

Line 355 - Aedes should be italicized

Line 366 & throughout - be consistent with capitalization of Woredas

Line 377 - change “is” to “could be”

Line 392 - change “lower” to “shorter”

Line 399 - no comma after “drought”

Line 553 - missing authors on Ref #32

Reviewer #2: (No Response)

Reviewer #3: Please refere to the line by line revision document (word file) sugegstion improvement of the manuscript.

--------------------

PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

Reviewer #3: No

Figure Files:

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email us at figures@plos.org.

Data Requirements:

Please note that, as a condition of publication, PLOS' data policy requires that you make available all data used to draw the conclusions outlined in your manuscript. Data must be deposited in an appropriate repository, included within the body of the manuscript, or uploaded as supporting information. This includes all numerical values that were used to generate graphs, histograms etc.. For an example see here: http://www.plosbiology.org/article/info%3Adoi%2F10.1371%2Fjournal.pbio.1001908#s5.

Reproducibility:

To enhance the reproducibility of your results, we recommend that you deposit your laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. Additionally, PLOS ONE offers an option to publish peer-reviewed clinical study protocols. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols

Attachment Submitted filename: Seroprevalence of C burnetii and RVF in Ethiopia.docx

Attachment Submitted filename: Line by line revisions.docx

10.1371/journal.pntd.0012392.r002
Author response to Decision Letter 0
Submission Version1
7 May 2024

Attachment Submitted filename: Response to reviewers comments_v2.1.docx

10.1371/journal.pntd.0012392.r003
Decision Letter 1
Remais Justin V. Section Editor
Rayner Simon Academic Editor
© 2024 Remais, Rayner
2024
Remais, Rayner
https://creativecommons.org/licenses/by/4.0/ 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.
Submission Version1
24 Jun 2024

Dear Dr Oakley,

Thank you very much for submitting your manuscript "Seroprevalence and risk factors for Q fever and Rift Valley fever in pastoralists and their livestock in Afar, Ethiopia: A One Health approach" for consideration at PLOS Neglected Tropical Diseases. As with all papers reviewed by the journal, your manuscript was reviewed by members of the editorial board and by several independent reviewers. The reviewers appreciated the attention to an important topic. Based on the reviews, we are likely to accept this manuscript for publication, providing that you modify the manuscript according to the review recommendations.

Please prepare and submit your revised manuscript within 30 days. If you anticipate any delay, please let us know the expected resubmission date by replying to this email.

When you are ready to resubmit, please upload the following:

[1] A letter containing a detailed list of your responses to all review comments, and a description of the changes you have made in the manuscript.

Please note while forming your response, if your article is accepted, you may have the opportunity to make the peer review history publicly available. The record will include editor decision letters (with reviews) and your responses to reviewer comments. If eligible, we will contact you to opt in or out

[2] Two versions of the revised manuscript: one with either highlights or tracked changes denoting where the text has been changed; the other a clean version (uploaded as the manuscript file).

Important additional instructions are given below your reviewer comments.

Thank you again for your submission to our journal. We hope that our editorial process has been constructive so far, and we welcome your feedback at any time. Please don't hesitate to contact us if you have any questions or comments.

Sincerely,

Simon Rayner

Academic Editor

PLOS Neglected Tropical Diseases

Justin Remais

Section Editor

PLOS Neglected Tropical Diseases

***********************

Reviewer's Responses to Questions

Key Review Criteria Required for Acceptance?

As you describe the new analyses required for acceptance, please consider the following:

Methods

-Are the objectives of the study clearly articulated with a clear testable hypothesis stated?

-Is the study design appropriate to address the stated objectives?

-Is the population clearly described and appropriate for the hypothesis being tested?

-Is the sample size sufficient to ensure adequate power to address the hypothesis being tested?

-Were correct statistical analysis used to support conclusions?

-Are there concerns about ethical or regulatory requirements being met?

Reviewer #2: (No Response)

Reviewer #3: Thank you to the authors for their accomplished efforts in revising their manuscript accoding to reviewer guidance givven. I blieve the mansucript has improved technically, scientifically and in readability. Thank you also fo providing detailed explanation on where amanemends weren´t possible authors hae agrumented otherwise. This helped to understand the justufucation for sthe study conducted.

--------------------

Results

-Does the analysis presented match the analysis plan?

-Are the results clearly and completely presented?

-Are the figures (Tables, Images) of sufficient quality for clarity?

Reviewer #2: (No Response)

Reviewer #3: (No Response)

--------------------

Conclusions

-Are the conclusions supported by the data presented?

-Are the limitations of analysis clearly described?

-Do the authors discuss how these data can be helpful to advance our understanding of the topic under study?

-Is public health relevance addressed?

Reviewer #2: (No Response)

Reviewer #3: (No Response)

--------------------

Editorial and Data Presentation Modifications?

Use this section for editorial suggestions as well as relatively minor modifications of existing data that would enhance clarity. If the only modifications needed are minor and/or editorial, you may wish to recommend “Minor Revision” or “Accept”.

Reviewer #2: (No Response)

Reviewer #3: (No Response)

--------------------

Summary and General Comments

Use this section to provide overall comments, discuss strengths/weaknesses of the study, novelty, significance, general execution and scholarship. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. If requesting major revision, please articulate the new experiments that are needed.

Reviewer #2: (No Response)

Reviewer #3: (No Response)

--------------------

PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #2: No

Reviewer #3: No

Figure Files:

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email us at figures@plos.org.

Data Requirements:

Please note that, as a condition of publication, PLOS' data policy requires that you make available all data used to draw the conclusions outlined in your manuscript. Data must be deposited in an appropriate repository, included within the body of the manuscript, or uploaded as supporting information. This includes all numerical values that were used to generate graphs, histograms etc.. For an example see here: http://www.plosbiology.org/article/info%3Adoi%2F10.1371%2Fjournal.pbio.1001908#s5.

Reproducibility:

To enhance the reproducibility of your results, we recommend that you deposit your laboratory protocols in protocols.io, where a protocol can be assigned its own identifier (DOI) such that it can be cited independently in the future. Additionally, PLOS ONE offers an option to publish peer-reviewed clinical study protocols. Read more information on sharing protocols at https://plos.org/protocols?utm_medium=editorial-email&utm_source=authorletters&utm_campaign=protocols

References

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article's retracted status in the References list and also include a citation and full reference for the retraction notice.

Attachment Submitted filename: Q fever and RVF seroprevalence in Ethiopia.docx

10.1371/journal.pntd.0012392.r004
Author response to Decision Letter 1
Submission Version2
18 Jul 2024

Attachment Submitted filename: Response to reviewers comments.docx

10.1371/journal.pntd.0012392.r005
Decision Letter 2
Remais Justin V. Section Editor
Rayner Simon Academic Editor
© 2024 Remais, Rayner
2024
Remais, Rayner
https://creativecommons.org/licenses/by/4.0/ 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.
Submission Version2
22 Jul 2024

Dear Dr Oakley,

We are pleased to inform you that your manuscript 'Seroprevalence and risk factors for Q fever and Rift Valley fever in pastoralists and their livestock in Afar, Ethiopia: A One Health approach' has been provisionally accepted for publication in PLOS Neglected Tropical Diseases.

Before your manuscript can be formally accepted you will need to complete some formatting changes, which you will receive in a follow up email. A member of our team will be in touch with a set of requests.

Please note that your manuscript will not be scheduled for publication until you have made the required changes, so a swift response is appreciated.

IMPORTANT: The editorial review process is now complete. PLOS will only permit corrections to spelling, formatting or significant scientific errors from this point onwards. Requests for major changes, or any which affect the scientific understanding of your work, will cause delays to the publication date of your manuscript.

Should you, your institution's press office or the journal office choose to press release your paper, you will automatically be opted out of early publication. We ask that you notify us now if you or your institution is planning to press release the article. All press must be co-ordinated with PLOS.

Thank you again for supporting Open Access publishing; we are looking forward to publishing your work in PLOS Neglected Tropical Diseases.

Best regards,

Simon Rayner

Academic Editor

PLOS Neglected Tropical Diseases

Justin Remais

Section Editor

PLOS Neglected Tropical Diseases

***********************************************************

10.1371/journal.pntd.0012392.r006
Acceptance letter
Remais Justin V. Section Editor
Rayner Simon Academic Editor
© 2024 Remais, Rayner
2024
Remais, Rayner
https://creativecommons.org/licenses/by/4.0/ 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.
2 Aug 2024

Dear Dr Oakley,

We are delighted to inform you that your manuscript, "Seroprevalence and risk factors for Q fever and Rift Valley fever in pastoralists and their livestock in Afar, Ethiopia: A One Health approach," has been formally accepted for publication in PLOS Neglected Tropical Diseases.

We have now passed your article onto the PLOS Production Department who will complete the rest of the publication process. All authors will receive a confirmation email upon publication.

The corresponding author will soon be receiving a typeset proof for review, to ensure errors have not been introduced during production. Please review the PDF proof of your manuscript carefully, as this is the last chance to correct any scientific or type-setting errors. Please note that major changes, or those which affect the scientific understanding of the work, will likely cause delays to the publication date of your manuscript. Note: Proofs for Front Matter articles (Editorial, Viewpoint, Symposium, Review, etc...) are generated on a different schedule and may not be made available as quickly.

Soon after your final files are uploaded, the early version of your manuscript will be published online unless you opted out of this process. The date of the early version will be your article's publication date. The final article will be published to the same URL, and all versions of the paper will be accessible to readers.

Thank you again for supporting open-access publishing; we are looking forward to publishing your work in PLOS Neglected Tropical Diseases.

Best regards,

Shaden Kamhawi

co-Editor-in-Chief

PLOS Neglected Tropical Diseases

Paul Brindley

co-Editor-in-Chief

PLOS Neglected Tropical Diseases
==== Refs
References

1 Grace D , Mutua F , Ochungo P , Kruska R , Jones K , Brierley L , et al . Mapping of poverty and likely zoonoses hotspots. Department for International Development; IKRI, Kenya. 2012:119 . Available from: https://www.gov.uk/research-for-development-outputs/mapping-of-poverty-and-likely-zoonoses-hotspots
2 Kanouté YB , Gragnon BG , Schindler C , Bonfoh B , Schelling E . Epidemiology of brucellosis, Q Fever and Rift Valley Fever at the human and livestock interface in northern Côte d’Ivoire. Acta Tropica. 2017;175 :121–9.28867393
3 Nooh F , Chernet A , Reither K , Okuma J , Brattig NW , Utzinger J , et al . Prevalence of fever of unidentified aetiology in East African adolescents and adults: a systematic review and meta-analysis. Infect Dis Poverty. 2023;12 (1 ):55. doi: 10.1186/s40249-023-01105-z 37231500
4 Tinto B , Quellec J , Cêtre-Sossah C , Dicko A , Salinas S , Simonin Y . Rift Valley fever in West Africa: A zoonotic disease with multiple socio-economic consequences. One Health. 2023;17 :100583. doi: 10.1016/j.onehlt.2023.100583 37664171
5 Eldin C , Mélenotte C , Mediannikov O , Ghigo E , Million M , Edouard S , et al . From Q Fever to Coxiella burnetii Infection: a Paradigm Change. Clin Microbiol Rev. 2017;30 (1 ):115–90. doi: 10.1128/CMR.00045-16 27856520
6 Angelakis E , Raoult D . Q Fever. Vet Microbiol. 2010;140 (3–4 ):297–309. doi: 10.1016/j.vetmic.2009.07.016 19875249
7 Rodolakis A , Berri M , Héchard C , Caudron C , Souriau A , Bodier CC , et al . Comparison of Coxiella burnetii shedding in milk of dairy bovine, caprine, and ovine herds. J Dairy Sci. 2007;90 (12 ):5352–60. doi: 10.3168/jds.2006-815 18024725
8 Anderson A , Bijlmer H , Fournier PE , Graves S , Hartzell J , Kersh GJ , et al . Diagnosis and management of Q fever—United States, 2013: recommendations from CDC and the Q Fever Working Group. MMWR Recomm Rep. 2013;62 (Rr-03 ):1–30. 23535757
9 Cunha BA , Nausheen S , Busch L . Severe Q fever community-acquired pneumonia (CAP) mimicking Legionnaires’ disease: Clinical significance of cold agglutinins, anti-smooth muscle antibodies and thrombocytosis. Heart Lung. 2009;38 (4 ):354–62. doi: 10.1016/j.hrtlng.2008.07.003 19577708
10 Maurin M , Raoult D . Q fever. Clin Microbiol Rev. 1999;12 (4 ):518–53. doi: 10.1128/CMR.12.4.518 10515901
11 Morroy G , Keijmel SP , Delsing CE , Bleijenberg G , Langendam M , Timen A , et al . Fatigue following Acute Q-Fever: A Systematic Literature Review. PLoS One. 2016;11 (5 ):e0155884. doi: 10.1371/journal.pone.0155884 27223465
12 Škultéty L. Q fever and prevention. Epidemiol Mikrobiol Imunol. 2020;69 (2 ):87–94.32819108
13 Wright D , Kortekaas J , Bowden TA , Warimwe GM . Rift Valley fever: biology and epidemiology. J Gen Virol. 2019;100 (8 ):1187–99. doi: 10.1099/jgv.0.001296 31310198
14 Fontenille D , Traore-Lamizana M , Diallo M , Thonnon J , Digoutte JP , Zeller HG . New vectors of Rift Valley fever in West Africa. Emerg Infect Dis. 1998;4 (2 ):289–93. doi: 10.3201/eid0402.980218 9621201
15 Baudin M , Jumaa AM , Jomma HJE , Karsany MS , Bucht G , Näslund J , et al . Association of Rift Valley fever virus infection with miscarriage in Sudanese women: a cross-sectional study. Lancet Glob Health. 2016;4 (11 ):e864–e71. doi: 10.1016/S2214-109X(16)30176-0 27692776
16 Cavalerie L , Wardeh M , Lebrasseur O , Nanyingi M , McIntyre KM , Kaba M , et al . One hundred years of zoonoses research in the Horn of Africa: A scoping review. PLoS neglected tropical diseases. 2021;15 (7 ):e0009607–e. doi: 10.1371/journal.pntd.0009607 34270551
17 Gumi B , Firdessa R , Yamuah L , Sori T , Tolosa T , Aseffa A , et al . Seroprevalence of Brucellosis and Q-Fever in Southeast Ethiopian Pastoral Livestock. J Vet Sci Med Diagn. 2013;2 (1 ): doi: 10.4172/2325-9590.1000109 24350302
18 Ibrahim M , Schelling E , Zinsstag J , Hattendorf J , Andargie E , Tschopp R . Sero-prevalence of brucellosis, Q-fever and Rift Valley fever in humans and livestock in Somali Region, Ethiopia. PLoS neglected tropical diseases. 2021;15 (1 ):e0008100–e. doi: 10.1371/journal.pntd.0008100 33493173
19 Tesfaye A , Sahele M , Sori T , Guyassa C , Garoma A . Seroprevalence and associated risk factors for chlamydiosis, coxiellosis and brucellosis in sheep and goats in Borana pastoral area, southern Ethiopia. BMC Vet Res. 2020;16 (1 ):145–.32434500
20 Asebe G , Mamo G , Michlmayr D , Abegaz WE , Endale A , Medhin G , et al . Seroprevalence of Rift Valley Fever and West Nile Fever in Cattle in Gambella Region, South West Ethiopia. Vet Med (Auckl). 2020;11 :119–30. doi: 10.2147/VMRR.S278867 33244452
21 Endale A , Michlmayr D , Abegaz WE , Geda B , Asebe G , Medhin G , et al . Sero-prevalence of West Nile virus and Rift Valley fever virus infections among cattle under extensive production system in South Omo area, southern Ethiopia. Trop Anim Health Prod. 2021;53 (1 ):92. doi: 10.1007/s11250-020-02506-0 33415465
22 Tschopp R , Gebregiorgis A , Tassachew Y , Andualem H , Osman M , Waqjira MW , et al . Integrated human-animal sero-surveillance of Brucellosis in the pastoral Afar and Somali regions of Ethiopia. PLOS Neglected Tropical Diseases. 2021;15 (8 ):e0009593. doi: 10.1371/journal.pntd.0009593 34358232
23 Greter H , Jean-Richard V , Crump L , Béchir M , Alfaroukh IO , Schelling E , et al . The benefits of ’One Health’ for pastoralists in Africa. Onderstepoort J Vet Res. 2014;81 (2 ):E1–3. doi: 10.4102/ojvr.v81i2.726 25005234
24 Peyre M , Chevalier V , Abdo-Salem S , Velthuis A , Antoine-Moussiaux N , Thiry E , et al . A Systematic Scoping Study of the Socio-Economic Impact of Rift Valley Fever: Research Gaps and Needs. Zoonoses Public Health. 2015;62 (5 ):309–25. doi: 10.1111/zph.12153 25256804
25 Tschopp R , GebreGiorgis A , Abdulkadir O , Molla W , Hamid M , Tassachew Y , et al . Risk factors for Brucellosis and knowledge-attitude practice among pastoralists in Afar and Somali regions of Ethiopia. Preventive Veterinary Medicine. 2022;199 :105557. doi: 10.1016/j.prevetmed.2021.105557 34902652
26 Abebe S , Melaku H , GebreGiorgis Kidanu A , Tschopp R . Pastoral mobility and challenges for disease surveillance and control in National Parks in Afar, Ethiopia. Ecohealth. 2024; doi: 10.1007/s10393-024-01687-6 38819755
27 Sergeant ESG . Epitools Epidemiological Calculators: Ausvet. 2018. Available from: http://epitools.ausvet.com.au.
28 Nanyingi MO , Muchemi GM , Thumbi SM , Ade F , Onyango CO , Kiama SG , et al . Seroepidemiological Survey of Rift Valley Fever Virus in Ruminants in Garissa, Kenya. Vector Borne Zoonotic Dis. 2017;17 (2 ):141–6. doi: 10.1089/vbz.2016.1988 27929928
29 Eisa M. Preliminary survey of domestic animals of the Sudan for precipitating antibodies to Rift Valley fever virus. J Hyg (Lond). 1984;93 (3 ):629–37. doi: 10.1017/s0022172400065207 6512261
30 Wielders CC , Hackert VH , Schimmer B , Hodemaekers HM , de Klerk A , Hoebe CJ , et al . Single nucleotide polymorphisms in immune response genes in acute Q fever cases with differences in self-reported symptoms. Eur J Clin Microbiol Infect Dis. 2015;34 (5 ):943–50. doi: 10.1007/s10096-014-2310-9 25577174
31 Knobel DL , Maina AN , Cutler SJ , Ogola E , Feikin DR , Junghae M , et al . Coxiella burnetii in humans, domestic ruminants, and ticks in rural western Kenya. Am J Trop Med Hyg. 2013;88 (3 ):513–8. doi: 10.4269/ajtmh.12-0169 23382156
32 de Bronsvoort BMC , Bagninbom JM , Ndip L , Kelly RF , Handel I , Tanya VN , et al . Comparison of Two Rift Valley Fever Serological Tests in Cameroonian Cattle Populations Using a Bayesian Latent Class Approach. Front Vet Sci. 2019;6 :258. doi: 10.3389/fvets.2019.00258 31475162
33 Gebremichael B , Girmay S , Gebru M . Camel milk production and marketing: Pastoral areas of Afar, Ethiopia. Pastoralism. 2019;9 (1 ):16.
34 Abebe A. Prevalence of Q fever infection in the Addis Ababa abattoir. Ethiopian medical journal. 1990;28 (3 ):119–22. 2209579
35 Özcelik R , Abakar MF , Counotte MJ , Zakaria FA , Kimala P , Issa R , et al . Seroprevalence and associated risk factors of brucellosis, Rift Valley fever and Q fever among settled and mobile agro-pastoralist communities and their livestock in Chad. PLoS Negl Trop Dis. 2023;17 (6 ):e0011395. doi: 10.1371/journal.pntd.0011395 37352362
36 Jaleta MB , Tefera M , Negussie H , Mulatu T , Berhe T , Belete F , et al . Entomological survey of the potential vectors of Rift Valley fever virus and absence of detection of the virus genome from the vectors in various niches in the southern half of the Great Rift Valley of Ethiopia. Vet Med Sci. 2022;8 (6 ):2716–25. doi: 10.1002/vms3.941 36104829
37 Consultative Group for RVF Decision Support. Decision-support tool for prevention and control of Rift Valley fever epizootics in the Greater Horn of Africa. Am J Trop Med Hyg. 2010;83 (2 Suppl ):75–85. doi: 10.4269/ajtmh.2010.83s2a03 20682910
38 Kersh GJ , Fitzpatrick KA , Self JS , Priestley RA , Kelly AJ , Lash RR , et al . Presence and persistence of Coxiella burnetii in the environments of goat farms associated with a Q fever outbreak. Appl Environ Microbiol. 2013;79 (5 ):1697–703. doi: 10.1128/AEM.03472-12 23315737
39 Bonfoh B , Kasymbekov J , Dürr S , Toktobaev N , Doherr MG , Schueth T , et al . Representative seroprevalences of brucellosis in humans and livestock in Kyrgyzstan. Ecohealth. 2012;9 (2 ):132–8. doi: 10.1007/s10393-011-0722-x 22143553
40 Hartman A. Rift Valley Fever. Clin Lab Med. 2017;37 (2 ):285–301. doi: 10.1016/j.cll.2017.01.004 28457351
41 Delsing CE , Kullberg BJ , Bleeker-Rovers CP . Q fever in the Netherlands from 2007 to 2010. Neth J Med. 2010;68 (12 ):382–7. 21209463
42 Vellema P , Santman-Berends I , Dijkstra F , van Engelen E , Aalberts M , Ter Bogt-Kappert C , et al . Dairy Sheep Played a Minor Role in the 2005–2010 Human Q Fever Outbreak in The Netherlands Compared to Dairy Goats. Pathogens. 2021;10 (12 ). doi: 10.3390/pathogens10121579 34959534
43 Leta S , Mesele F . Spatial analysis of cattle and shoat population in Ethiopia: growth trend, distribution and market access. SpringerPlus. 2014;3 (1 ):310. doi: 10.1186/2193-1801-3-310 25019048
44 Cleaveland S , Sharp J , Abela-Ridder B , Allan KJ , Buza J , Crump JA , et al . One Health contributions towards more effective and equitable approaches to health in low- and middle-income countries. Philos Trans R Soc Lond B Biol Sci. 2017;372 (1725 ). doi: 10.1098/rstb.2016.0168 28584176
45 Metaferia F , Cherenet T , Gelan A , Abnet F , Tesfay A , Abdi J , et al . A review to improve estimation of livestock contribution to the national GDP. Addis Ababa, Ethiopia: Ministry of Finance and Economic Development, Ministry of Agriculture. 2011.
46 Dreyfus A , Ruf MT , Goris M , Poppert S , Mayer-Scholl A , Loosli N , et al . Comparison of the Serion IgM ELISA and Microscopic Agglutination Test for diagnosis of Leptospira spp. infections in sera from different geographical origins and estimation of Leptospira seroprevalence in the Wiwa indigenous population from Colombia. PLoS Negl Trop Dis. 2022;16 (6 ):e0009876. doi: 10.1371/journal.pntd.0009876 35666764
