Low-Level Middle East Respiratory Syndrome Coronavirus among Camel Handlers, Kenya, 2019

Abstract

Although seroprevalence of Middle East respiratory coronavirus syndrome is high among camels in Africa, researchers have not detected zoonotic transmission in Kenya. We followed a cohort of 262 camel handlers in Kenya during April 2018–March 2020. We report PCR-confirmed Middle East respiratory coronavirus syndrome in 3 asymptomatic handlers.

Since the first human case of Middle East respiratory syndrome coronavirus (MERS-CoV) was identified in 2012, the World Health Organization has reported 2,494 infections and 858 deaths (case-fatality ratio 34.4%) in persons across 27 countries in the Middle East, Europe, Asia, and North America (1). Dromedary camels (Camelus dromedarius) are the known reservoirs of the virus (2,3). Most human cases result from direct or indirect transmission of virus from camels or human-to-human transmission in healthcare settings; researchers have also documented limited secondary transmission to household contacts (4). Occupational direct contact with camels is a risk factor for primary MERS-CoV infection (5). Camel workers and herders have a 0%–50% seroprevalence of MERS-CoV, generally higher than that of the general population in Saudi Arabia (4,6).

Although infection is widespread among dromedary camels, zoonotic transmission from camels to humans is sporadic, and disease prevalence among humans is not directly proportional to potential exposure to infected camels (4,5,7). Although >65% of the world’s dromedary camels live in Africa, on that continent MERS-CoV seroprevalence in humans is low (0.2%), with no documented cases of acute human infection (8,9). Furthermore, studies in the Africa region have identified MERS-CoV RNA in 11%–16% of camels and in 80%–95% of seropositive camels (9–11). To determine whether MERS-CoV infections occur in humans in a region with high seroprevalence among camels, we studied a cohort of 262 camel handlers in Kenya.

The Study

During April 2018–March 2020, we enrolled participants on a rolling basis from 32 camel-owning households in Marsabit County, northern Kenya (Figure 1). We defined a camel handler as any person in the household who had contact with camels (Figure 2). This study was approved by the Scientific and Ethical Review Committee of Kenya Medical Research Institute (approval no. SSC3472), the Institutional Review Board of Washington State University (approval no. 16245), and the US Centers for Disease Control and Prevention (approval no. 7065). We obtained written informed consent from all participants.

Figure 1.

Locations of enrolled households in study on MERS-CoV, Marsabit County, Kenya, 2018–2020. Black circles indicate participating households; red circles indicate households with cases. Inset shows location of Marsabit County within Kenya. MERS-CoV, Middle East respiratory syndrome coronavirus.

Figure 2.

Types and frequency of contacts with camels among participants in study on Middle East respiratory syndrome coronavirus, Marsabit County, Kenya, 2018–2020.

We conducted monthly visits with the participants. At each visit, we collected nasopharyngeal and oropharyngeal swab samples from each participant. We also administered a questionnaire to each participating camel handler to identify signs and symptoms of possible respiratory illness during the previous 30 days. In addition, we recorded occurrences of respiratory illness among their household members. Participants belonged to 32 households with a median of 6 persons (interquartile range [IQR] 1–8 persons) and 32 camels (IQR 2–48 camels) at enrollment. The median age of these participants was 19 years (IQR 11–38 years). Most (67.2%) participants were male, of whom 39.3% were employed as camel workers and 38.2% were school going household members (Table 1). All participants handled camels. The most frequent interactions were herding (74.4%), cleaning barns (67.9%), feeding (67.6%), and milking (63.7%) (Figure 2).

Table 1. Characteristics of camel handlers enrolled in a study on Middle East respiratory syndrome coronavirus, Marsabit, Kenya, 2018–2020*.

Characteristic	Value, n = 262
Sex
M	176 (67.2)
F	86 (32.8)
Age, y
<19	131 (50)
20–39	73 (27.9)
40–59	41 (15.6)
>60	17 (6.5)
Median participant age, y (IQR)	19 (11–38)
Work engagement in the previous 30 d
Camel farm worker	103 (39.3)
Primary/secondary school student	100 (38.2)
Housewife	28 (10.7)
Farm owner	22 (8.4)
Pastoralist	6 (2.3)
Not currently engaged	2 (0.8)
Retiree	1 (0.4)
Median household size (IQR)	6 (1–8)
Median camel herd size (IQR)	32 (2–48)
History of chronic respiratory symptoms†	5 (1.9)
History of other chronic conditions‡	1 (0.4)
History of travel in the previous 5 y	0
Past tobacco use	72 (27.5)
Current tobacco use	72 (27.5)
Respiratory symptoms during the 2-year follow-up period	25 (9.5)
Fever	5 (1.9)
Running nose	39 (14.9)
Cough	25 (9.5)
Nasal stuffiness	23 (8.8)
Sore throat	16 (6.1)
Chest pain	2 (0.8)

*Values are no. (%) except as indicated.
†Respiratory symptoms include cough, sore throat, running nose, nasal stuffiness, chest pain.
‡Other chronic medical conditions include diabetes, cancer, liver disease, kidney disease, and tuberculosis.

We stored the swab samples in virus transport media and tested them for MERS-CoV by reverse transcription PCR (RT-PCR) at the Kenya Medical Research Institute (Nairobi, Kenya) as described previously (12). We conducted real-time RT-PCR selective for the upstream region envelope and 2 distinct regions of nucleocapsid genes on total nucleic acid extracted from 200 μL of sample. We defined a positive sample by positivity of all 3 PCRs.

We tested 1,369 samples from 262 camel handlers during the 2-year follow-up period. Participants had a median of 43.6% of monthly follow-up visits (IQR 8%–75%). Three (1.1%) participants (cases 1–3) tested positive for MERS-CoV by RT-PCR. The cycle threshold (C_t) values for case 1 were 38.9 for the upstream envelope, 37.7 for the nucleocapsid 2, and 39.3 for the nucleocapsid 3 genes; for case 2, the values were 39.7 for the upstream envelope, 36.9 for the nucleocapsid 2, and 39.8 for the nucleocapsid 3 genes; for case 3, the values were 35.6 for the upstream envelope, 36.0 for the nucleocapsid 2, and 36.8 for the nucleocapsid 3 genes. We detected all 3 cases during July–September 2019 (Table 2).

Table 2. Characteristics of persons with Middle East respiratory syndrome coronavirus, Kenya, 2019.

Case	Age, y/sex	Occupation	No. household members in study	No. of camels owned by household	Enrollment date	Diagnosis date	Type of camel contact at time of positive sample
1	20/F	Spouse to herder	11	37	2019 Jun 23	2019 Jul 31	Herding, milking, feeding, petting/playing, grooming, cleaning barn
2	49/M	Herder	6	2	2019 May 21	2019 Aug 13	Herding, milking, feeding, grooming, cleaning barn, administering medications
3	22/M	Herder	3	32	2018 May 2	2019 Sep 12	Herding, milking, feeding, grooming, cleaning barn, assisting in birth

Case 1 was in a woman 20 years of age who enrolled in June 2019 and had 9 monthly follow-up visits. She participated in the study with 11 other members of the household, all of whom tested negative for MERS-CoV throughout the follow-up period. Case 2 was in a man 49 years of age who enrolled in May 2019 and had 7 monthly follow-up visits. He participated in the study with 6 of his 10 household members; all the participants in his household tested negative for MERS-CoV. Case 3 was in a man 22 years of age who enrolled in May 2018 and had 12 monthly follow-up visits. He participated in the study with 3 of his 9 household members; the participants in his household tested negative for MERS-CoV. None of the 3 with positive results tested positive for MERS-CoV in the subsequent months.

All of the 3 with positive results were asymptomatic at diagnosis and had no concurrent conditions or histo-ry of travel outside of the county or country in the previ-ous month. None of them or their household members had respiratory illness before or after diagnosis.

Conclusions

We report 3 PCR-confirmed cases of MERS-CoV in humans in Kenya; these cases met the World Health Organization case definition of MERS-CoV infection (13). All 3 persons were asymptomatic before and after diagnosis; this finding supports previous data suggesting that the virus causes no or mild disease in Africa compared with the Middle East and Asia, perhaps because of the younger age of most camel herders in Africa (4,8,9). Our findings are limited by the high C_t values (>35) of all cases, a level which some experts might not consider to be positive. However, because these patients had C_t values <40 for 3 distinct MERS-CoV genes, we feel confident that these are unlikely to be false positive results. Researchers have observed low upper respiratory tract RNA concentrations in asymptomatic patients and contacts of MERS-CoV patients (14). In contrast to studies conducted in the Middle East, we found no evidence of human-to-human transmission; a total of 20 household members of the 3 patients tested negative for MERS-CoV before and after their household member’s diagnosis. However, we might have missed some infections that occurred between follow-up visits. Furthermore, not all household members were enrolled in the study. In addition, serologic assessment of MERS-CoV T-cell responses might detect mild and asymptomatic MERS-CoV cases (15). Finally, the low (0.2%) seroprevalence among participants who had high exposure to camel herds with MERS-CoV circulation suggest a low level of zoonotic camel-to-human transmission. We previ-ously found no antibodies against MERS-CoV in camel herders despite high seroprevalence among camels in this community (9).

In conclusion, we confirmed zoonotic transmis-sion of MERS-CoV from camels to handlers in Kenya. Focused surveillance is needed to detect these rare in-fections when they occur.

Biography

Dr. Munyua is an epidemiologist within the Division of Global Health Protection, Global Health, US Centers for Disease Control and Prevention, Nairobi. Her research interests include infectious and zoonotic diseases.