Saturday, August 18, 2018

PRO/AH/EDR> MERS-CoV (26): Saudi Arabia, abbatoir workers (Nigeria), primary camel exposure

A ProMED-mail post
ProMED-mail is a program of the
International Society for Infectious Diseases

In this update:
[1] Saudi Arabia (Al Bahah)
[2] MERS in camel workers: Eurosurveillance
[3] Review of camel exposure in reported cases: viruses

[1] Saudi Arabia (Al Bahah)
Date: Fri 17 Aug 2018
Source: Saudi MOH 17 Aug 2018 [edited]

17 August 2018
New [case no.] 18-1740
MERS in Buljorshy: An 80-year-old male living in Buljorshy city,
Albaha region.
Contact with camels: No
Case classification: Primary / community-acquired
Current Status: Hospitalized

Communicated by:
ProMED-mail Rapporteur Mary Marshall

[This is the 1st newly confirmed case of MERS-CoV infection reported
by Saudi Arabia since Sun 5 Aug 2018. It is difficult to discuss the
case further in the absence of more details, other than to conclude it
is classified as a primary case with community acquisition, in the
absence of known direct (or indirect) camel contact.

The newly revised website does not provide information on outcomes of
reported cases. One conclusion is that, in the absence of identified
contact with camels or known other cases in the community, these cases
are considered primary community-acquired cases.

Al Bahah is located in the south of Saudi Arabia surrounded on 3 sides
by Makkah Province and bordering with Asir on its southeast borders.

HealthMap/ProMED-mail map:
Saudia Arabia: <>. - Mod.MPP]

[2] MERS in camel workers: Eurosurveillance
Date: Thu 9 Aug 2018
Source: Eurosurveillance [edited]

Lack of serological evidence of Middle East respiratory syndrome
coronavirus infection in virus exposed camel abattoir workers in
Nigeria, 2016
Citation: So Ray TY, Perera Ranawaka APM, Oladipo Jamiu O, Chu Daniel
KW, Kuranga Sulyman A, Chan Kin-ho, Lau Eric HY, Cheng Samuel MS, Poon
Leo LM, Webby Richard J, Peiris Malik. Lack of serological evidence of
Middle East respiratory syndrome coronavirus infection in virus
exposed camel abattoir workers in Nigeria, 2016. Euro Surveill. 2018;
23(32): pii=1800175.

Middle East respiratory syndrome coronavirus (MERS-CoV) is an ongoing
threat to global public health [1]. Serological and virological
studies have shown evidence of MERS-CoV infection in camels in the
Middle East, as well as in East, North, and West Africa [2-5] and in
Central Asia [6]. In spite of MERS-CoV being enzootic in camels in
Africa, zoonotic MERS has not been reported from the African
continent. Our recent genetic and phenotypic analysis of MERS-CoV from
camels in West (Burkina Faso, Nigeria) Africa has shown that West
African viruses were phylogenetically and phenotypically distinct from
those associated with human disease in the Arabian Peninsula [7],
raising the possibility that virus strain differences may be
associated with differences in zoonotic potential.

Abattoir workers with exposure to infected camels are a high-risk
group for MERS-CoV infection in the Arabian Peninsula [8]. However,
there is a paucity of serological data on MERS-CoV infection in people
occupationally exposed to camels in Africa, a knowledge gap identified
as a priority research question at a Food and Agriculture Organization
of the United Nations-World Organisation for Animal Health-World
Health Organization (FAO-OIE-WHO) Global Technical Meeting on MERS in
September 2017 [1]. A previous study in Egypt in 2013 showed no
serologic evidence of MERS-CoV among 179 serum samples from humans
working in 2 camel abattoirs [3]. None of 760 people with household
exposure to seropositive camels in Kenya in 2013 had evidence of
MERS-CoV antibody [9]. Another study in Kenya in 2013-14 of 1122
people (not with necessarily high exposure to camels) found 2 sera
with low and inconclusive levels of neutralising antibody to MERS-CoV
[10]. It remains important to carry out more sero-epidemiological
studies on humans with occupational exposure to infected camels to
understand whether or not zoonotic transmission is taking place in
Africa. We therefore investigated for serological evidence of MERS-CoV
infection of humans occupationally exposed to infected dromedary
camels in an abattoir in Kano, Nigeria.

Study sites and sample collection
Around 70 camels are slaughtered daily at the abattoir in Kano,
Nigeria. We collected around 20 nasal swabs daily from [12 Oct 2015 to
2 Dec 2015] and from [11 Jan 2016 to 29 Feb 2016]. Swab samples were
placed in viral transport medium and stored at -80 deg C/-112 deg F.

Abattoir workers with and without occupational exposure to camels were
recruited for a serological study after obtaining informed consent,
during April-November 2016. A questionnaire was administered to each
participant to ascertain demographic information, type and duration of
occupational exposure to camels or other livestock, practices such as
consuming camel milk, or use of camel urine for food or health
purposes. Camel exposures in the abattoir were classified as "direct"
(exposure to live or freshly slaughtered camels or camel meat) or
"indirect" (no exposure to live camels or freshly slaughtered camels
or meat; exposure only being to cooked meat or dried bones, etc., as
further described in the table). Duration of exposure to camels in the
abattoir was categorised as less than one year, 1-5 years,
or greater than 5 years. These workers used no personal protective

Virological and serological analysis
Total nucleic acid was extracted from camel nasal swabs using EasyMag
(Biomerieux, France) and screened for MERS-CoV RNA using a
reverse-transcription qPCR (RT-qPCR) assay targeting the upstream
elements of the Envelope (UpE) gene. Positive samples were confirmed
by testing with a 2nd RT-qPCR targeting the open reading frame 1a
(ORF1a) gene [3,11].

Human sera were tested for MERS-CoV antibody using a MERS-CoV S1 spike
enzyme-linked immunosorbent assay (ELISA; Euroimmun, Lubeck, Germany)
according to manufacturer's instructions and by a pseudoparticle
neutralisation (ppNT) assay as described previously [12]. A greater
than or equal to 90 percent reduction of signal was considered as
evidence of neutralisation in the ppNT assay.

Overall, 2529 camels were tested, 38 of them being calves less
than 2 years, 1400 aged 2-4 years, and 1091 aged greater than 4
years. None of the 1300 camels tested from [12 Oct 2015 to 2 Dec 2015]
were positive for MERS-CoV RNA. Those tested in the week of [11 Jan
2016 (n = 142) remained virus RNA negative. MERS-CoV was detected
in subsequent weeks, 5 (2.6percent) of 190 swabs in the week of [18
Jan 2016], 2 (1 percent) of 199 in the week of [25 Jan 2018], 12 (6.6
percent) of 183 in the week of [1 Feb 2016], 16 (8.4 percent) of 190
in the week of [8 Feb 2016], 12 (7.4 percent) of 162 in the week of
[15 Feb 2016], and 8 (5.2 percent) of 155 in the week of [22 Feb
2016]. None of 8 tested in the week of [29 Feb 2016] were positive. Of
the 2529 camels tested, MERS-CoV RNA was detected in 4 (10.5 percent)
of 38 aged less than 2 years, 31 (2.2 percent) of 1400 aged 2-4
years and 20 (1.8 percent) of 1091 aged greater than 4 years.

A total of 311 abattoir workers were recruited for the serological
study. Of these, 261 had occupational exposure to camels, with 243
workers having direct exposure to live camels, freshly killed camels,
or camel meat and 18 having indirect exposure to camels. Fifty persons
recruited in the study worked in the slaughterhouse with no
occupational camel exposure. Many workers in the abattoir, including
those without direct occupational exposure to camels, reported
drinking fresh (unboiled) camel milk, drinking camel urine, using
camel urine for medicinal purposes ([table available at source URL]).
Irrespective of these modes of exposure, none of the 311 humans tested
had any evidence of MERS-CoV antibody in their serum.

Table: Exposure to camels and history of camel product consumption in
abattoir workers recruited for a Middle East respiratory syndrome
coronavirus serological study, Kano, Nigeria, April-November 2016
(n = 311)

Camels (n = 132) in this abattoir in Kano had been previously
studied in January 2015, and MERS-CoV RNA was detected in 11 percent
of samples, while 96 percent were antibody positive [2]. In 2016 (this
study), virus RNA detection in January-February ranged from 0-8.4
percent of camels sampled. The peak period of MERS-CoV activity in
Kano appeared to be in February, about 2 months later than the peak of
virus activity previously reported in Egypt [13].

The high rates of virus detection in camels during January-February in
2015 and 2016 suggest that workers in the abattoir had prolonged and
intensive occupational exposure to MERS-CoV-infected camels and camel
carcasses, very likely over many years, without the use of any
personal protective equipment. In addition to occupational exposure to
camels in the slaughtering process, of the 50 workers in the abattoir
with no occupational exposure to camels or camel meat (table) 15
reported frequent drinking of fresh camel milk, 10 drank fresh camel
urine, and 10 used camel urine as medicine. The complete absence of
MERS-CoV antibodies in workers is striking. Although the serological
assays were carried out using the spike protein of the prototype
MERS-CoV strain EMC, we have shown that MERS-CoV from diverse parts of
Africa, including Nigeria/NS004/2015, do not differ antigenically from
the prototype MERS-CoV EMC strain [7]. Thus antigenic diversity is
unlikely to explain the lack of seropositivity observed in
camel-exposed individuals in Nigeria. The MERS-spike protein
pseudoparticle neutralisation assay has comparable sensitivity to
plaque neutralisation tests in detecting antibody in humans infected
with MERS-CoV [14].

MERS-CoV seroprevalence in persons with occupational exposure to
camels in the Arabian Peninsula was significantly higher than in the
general population; 5 (3.6 percent) of 140 workers occupationally
exposed to camels in Saudi Arabia investigated in 2013-14 and 2 of 5
camel slaughterers in a central animal market in Qatar tested in 2014
were MERS-CoV seropositive [8,15]. Two of 22 camel barn workers at a
camel race track in Qatar were seropositive [15]. In our study, of 261
workers exposed to camels in the abattoir in Kano, Nigeria, none were
seropositive. This seropositivity rate is significantly lower than
that of the camel abattoir workers in Saudi Arabia (p = 0.0049,
Fisher's exact test) and that of the camel barn workers at a race
track in Qatar (p = 0.0058). The finding of only negative test
results in 113 camel slaughterers in this study yields a significantly
different rate of seropositivity than that in camel slaughterers in an
animal market in Qatar (p = 0.0014). Our results are concordant
with that of a study in Kenya, East Africa, where there was no
evidence of antibody in serum of 760 people with household or
occupational exposure to MERS-CoV seropositive camels [9]. Another
study of the general population from Kenya found evidence of
neutralising MERS-CoV antibody at very low antibody titre in 2 of 1122
sera (0.18 percent) [10], comparable with a general population
seroprevalence of 0.15 percent of sera from Saudi Arabia [8]. But it
is unclear if these low antibody titres reflect actual infection with
MERS-CoV. MERS-CoV from West Africa, including Nigeria, were
genetically and phenotypically distinct from those in East Africa [7],
and thus, zoonotic potential of viruses from Nigeria may be different
from those in Kenya. Overall, these data may suggest that the risk of
MERS infection from exposure to infected camels may be lower in some
African countries.

It should be noted that seroconversion is not invariable even in
patients with MERS. In a cohort of patients with RT-PCR-confirmed MERS
in the South Korean outbreak in 2015 who were serologically followed
up for one year, 4 of the 6 patients who had mild disease (i.e., did
not require supplemental oxygen or mechanical ventilation) were
negative by S1 ELISA, 2 were positive by plaque reduction
neutralisation test (PRNT) 90 (titre 1:10), and of these 2, only one
was positive by ppNT (titre of 10) [16]. Although designated as having
mild disease, with one exception, these patients, had chest
infiltrates on X-ray, indicating lung parenchymal pathology. In
another cohort of South Korean MERS patients, none of 3 persons with
asymptomatic infection and only 6 of 10 patients with symptomatic
disease without pneumonia seroconverted, whereas most patients with
severe pneumonia did seroconvert [17]. Therefore, it is possible that
camel-exposed individuals who get asymptomatic or mild infections may
not seroconvert. Even in those who do develop detectable antibody,
waning antibody titres may lead to negative serological results. Thus
sero-epidemiological studies may well underestimate the true extent of
MERS-CoV infection in humans. A recent study showed that
virus-specific CD8 +  T-cell responses were detected in mild or
asymptomatic patients with MERS-CoV infection, even in the absence of
serologic responses [18]. T-cell responses and their specificity for
MERS-CoV should also be investigated in future studies for identifying
evidence of zoonotic MERS-CoV infection in high-risk groups.

In conclusion, we found no serological evidence of MERS-CoV infection
in abattoir workers with extensive exposure to dromedaries with
documented virus infection in winter months. lt is possible that
MERS-CoV from West Africa may have lower zoonotic potential than
current virus strains in the Arabian Peninsula [7]. Studying MERS-CoV
in humans in Africa is an urgent priority. There is also a need for
additional studies to genetically and phenotypically characterise
MERS-CoV in Nigeria and other parts of Africa.

References available at source URL.

Communicated by:
ProMED-mail Rapporteur Mary Marshall

[In a nutshell, in spite of having documented exposure to the MERS-CoV
infected animals, there were no identifiable seroconversions amongst
abbatoir workers in Nigeria, thereby highlighting the enigma of "Why
Saudi Arabia?" - Mod.MPP]

[3] Review of camel exposure in reported cases: viruses
Date: Tue 14 Aug 2018
Source: Viruses [edited]

Reported Direct and Indirect Contact with Dromedary Camels among
Laboratory-Confirmed MERS-CoV Cases
Citation: Conzade R, Grant R, Malik MR,Elkholy A, Elhakim M, Samhouri
DD, Embarek PKB and Van Kerkhove MD. Reported Direct and Indirect
Contact with Dromedary Camels among Laboratory-Confirmed MERS-CoV
Cases. Viruses. 2018; 10(8): 425. doi:10.3390/v10080425

Dromedary camels (_Camelus dromedarius_) are now known to be the
vertebrate animal reservoir that intermittently transmits the Middle
East respiratory syndrome coronavirus (MERS-CoV) to humans. Yet,
details as to the specific mechanism(s) of zoonotic transmission from
dromedaries to humans remain unclear. The aim of this study was to
describe direct and indirect contact with dromedaries among all cases,
and then separately for primary, non-primary, and unclassified cases
of laboratory-confirmed MERS-CoV reported to the World Health
Organization (WHO) between 1 January 2015 and 13 April 2018. We
present any reported dromedary contact: direct, indirect, and type of
indirect contact. Of all 1125 laboratory-confirmed MERS-CoV cases
reported to WHO during the time period, there were 348 (30.9 percent)
primary cases, 455 (40.4 percent) non-primary cases, and 322 (28.6
percent) unclassified cases. Among primary cases, 191 (54.9 percent)
reported contact with dromedaries: 164 (47.1 percent) reported direct
contact, 155 (44.5 percent) reported indirect contact. Five (1.1
percent) non-primary cases also reported contact with dromedaries.
Overall, unpasteurized milk was the most frequent type of dromedary
product consumed. Among cases for whom exposure was systematically
collected and reported to WHO, contact with dromedaries or dromedary
products has played an important role in zoonotic transmission.

[I've excerpted the discussion and conclusion sections. Interested
readers are pointed to the source URL for the full article, including
helpful tables supporting the conclusions and observations below. -

4. Discussion
This is the first study to describe contact among all MERS-CoV
infections reported to WHO with the known animal reservoir of
MERS-CoV: dromedary camels. We report that among all of the 1125
MERS-CoV cases reported to WHO between 1 January 2015 and 13 April
2018, 30.9 percent were primary cases. Among primary cases, 191 (54.9
percent) reported direct or indirect contact with dromedaries, 164
(47.1 percent) reported direct, physical, contact with dromedaries,
and 155 (44.5 percent) reported contact with products derived from
dromedaries, namely unpasteurized camel milk.

We found primary human cases more likely to be older, with a higher
proportion of males compared to all cases, and compared to non-primary
or unclassified cases. This likely reflects differences in cultural
practices and exposures to dromedaries between men and women in the
Middle East, rather than a difference in infection susceptibility. In
this study, all primary MERS-CoV infections have occurred in countries
in the Middle East, including KSA, which accounts for 96.3 percent of
primary infections reported between 1 January 2015 and 13 April 2018
(table 1). In this region, dromedary ownership, herding, and farming
practices have increased in recent decades, and camel farms are
increasingly concentrated close to major cities, with camel workers
often living inside or in close proximity to camel barns. As
culturally important animals, dromedaries are celebrated in camel
races, sales, beauty competitions, and parades, and often kissed,
hugged, and greeted, intensifying frequency of direct contact with
dromedaries [23,24,39,43]. In addition, unpasteurized camel milk and
meat are widely consumed, despite current WHO recommendations for
people living in areas with reported MERS-CoV circulation to avoid
drinking raw camel milk [44], and camel urine, which is believed to
have therapeutic benefits. The risk of MERS-CoV infection from the
consumption of unpasteurized camel milk has been evaluated in Qatar,
and the authors found evidence of MERS-CoV RNA and neutralizing
antibodies in the milk but could not determine if MERS-CoV was in the
milk or contaminated during the milking process [35].

Although it is clear that contact with infected dromedaries are the
primary source of recurrent introduction of MERS-CoV into the human
population, mitigating spillover from dromedaries to humans has been
limited by a lack of clarity on the modes of transmission between
dromedaries and humans, the extent of spillover to humans, and the
epidemiology of MERS-CoV circulation in dromedaries in large parts of
Africa and South Asia. A deeper understanding of why zoonotic
transmission has been undetected in many countries in Africa, the
Middle East (outside the Arabian Peninsula), and South Asia, despite
high seroprevalence in dromedaries in such countries, is required
[45]. WHO, the Food and Agriculture Organization of the United Nations
(FAO), in collaboration with technical partners in these regions, are
currently working to implement field studies at the animal/human
interface, to further understand the extent of circulation in
dromedaries, zoonotic transmission, dromedary husbandry practices, and
trade patterns of dromedaries in a number of countries across Africa
and South Asia (personal communication, with permission, Van

Our study applied a One Health vision to retrospective analysis of
epidemiological data to determine if we could better understand
infection at the animal/human interface. The findings show clearly
that contact with dromedaries has likely played an important role in
the continued introduction of MERS-CoV into the human population from
the dromedary camel reservoir. While there have been notable
improvements in surveillance and reporting of human cases since 2015,
multidisciplinary research, cross-sectoral collaboration at country
level, public awareness about the disease, and laboratory and
surveillance capacity in affected countries, particularly since 2015,
there is still a need to further understand frequency and patterns of
contact between infected dromedaries and humans that lead to zoonotic
transmission, best achieved through multisite anthropological studies
in areas across which MERS-CoV is known to circulate, not only in
human populations, but also in dromedary populations. Interrupting
zoonotic transmission could also be achieved through the ongoing
development and application of dromedary and/or human vaccine

The results of our study are strengthened by the size of the study,
which includes all laboratory confirmed cases reported to WHO since [1
Jan 2015]. We were not able include all laboratory confirmed cases
reported to WHO since 2012, because prior to 2015, there were
inconsistencies in the way exposure information for each human
MERS-CoV infection was collected. For example, at the start of this
epidemic in 2012, a comprehensive data collection tool was not used by
all countries identifying MERS cases and potential risk factor data,
and disease/outcome information about individual patients after the
time of reporting was not systematically reported to WHO. Even among
data reported since 2015, there is some missing data for contact with
dromedaries and there is a complete absence of information on the use
of personal protective equipment (PPE; e.g., gloves, boots, coveralls,
masks/respirators) when in direct contact with dromedaries, and on
hygiene practices following contact with dromedaries. This limits our
ability to draw conclusions from our dataset, as to how each case was
infected and the exact route(s) of transmission. The use of PPE,
however, has been evaluated in a detailed case-control study in Qatar
evaluating specific types of dromedary contact among seropositive vs
seronegative occupational workers, which found that hand washing
before and after contact with the dromedary was protective against
infection with MERS-CoV [46].

Our dataset is also limited by our ability in classifying cases based
on available information reported to WHO at the time of reporting by
the country. For example, thorough outbreak investigations, which
include full genome sequencing of the virus, may find that cases which
were initially classified as non-primary cases, may in fact be primary
cases, and this information was not regularly relayed to WHO. More
complete case reporting, including exposures prior to symptom onset,
would improve our ability to assess non-human exposures that may have
led to primary MERS illness in humans. Efforts are currently being
made to retrospectively review and update the epidemiological data for
all cases reported to WHO to date, particularly prior to 2015. To aid
member states in more systematic data collection on suspected and
confirmed MERS cases, WHO has updated guidance on investigation of
cases, and has revised the MERS case reporting forms, which include
specific questions about contact with known MERS patients, healthcare
visits, travel, occupation, dromedary contact, other animal contact,
and underlying medical conditions within the 14 days prior to symptom
onset [47,48].

5. Conclusions
In conclusion, a lack of systematic reporting on exposures and risk
factors, including contact with dromedaries for each MERS case
identified since 2012, prevents a clear understanding of how infection
occurred in each case. However, it is clear from the data reported
that contact with dromedaries has played an important role in
transmission of MERS-CoV into the human population from the dromedary
reservoir. As a result, further understanding the geographic scope of
MERS-CoV circulation in dromedaries, and limiting direct and indirect
contact with infected dromedaries, remains important for reducing
zoonotic transmission of MERS-CoV.

Communicated by:
ProMED-mail Rapporteur Mary Marshall

[As I've said before, why Saudi Arabia? Why are the overwhelming
majority of cases reported from Saudi Arabia? What also awaits
addressing is what are the routes of transmission for the primary
community-acquired cases with no identifiable known contact with
camels. - Mod.MPP]

[See Also:
MERS-CoV (25): risk assessment, WHO
(24): Saudi Arabia, MoH reports
(23): Saudi Arabia, WHO, RFI
(22): Saudi Arabia, WHO
(21): EMRO/WHO update May 2018
(20): Saudi Arabia (NJ) susp. family cluster
(10): Oman, Saudi Arabia, WHO
(01): Malaysia (ex KSA), Saudi Arabia, UAE (ex Oman)
MERS-CoV (77): Saudi Arabia, camels, human, epidemiology, assessment
(01): Saudi Arabia (QS, RI, MD) RFI
MERS-CoV (123): Saudi Arabia (MK, AS) new cases
(01): Oman, Saudi Arabia
MERS-COV (167): acute management and long-term survival
(01): Saudi Arabia, new cases, new death
MERS-CoV (69): Saudi Arabia, new case, RFI
(01): Bangladesh, KSA, Algeria, UAE, Iran, WHO, RFI
- Eastern Mediterranean (82): anim res, camel,
- Eastern Mediterranean (01): Saudi Arabia, UAE, Oman, WHO
MERS-CoV - Eastern Mediterranean (106): animal reservoir, camel,
Qatar, OIE
- Eastern Mediterranean: Saudi Arabia, new case, RFI
Novel coronavirus - Eastern Mediterranean (29): MERS-CoV, ICTV
Novel coronavirus - Eastern Mediterranean: bat reservoir
Novel coronavirus - Eastern Mediterranean (06): comments
Novel coronavirus - Eastern Mediterranean: WHO, Jordan, conf., RFI
Novel coronavirus - Saudi Arabia (18): WHO, new cases, cluster
Novel coronavirus - Saudi Arabia: human isolate]
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