International Journal of Animal and Veterinary Advances 4(2): 113-118, 2012
ISSN: 2041-2908
© Maxwell Scientific Organization, 2012
Submitted: January 19, 2012
Accepted: February 17, 2012
Published: April 20, 2012
Exposure to Zoonotic Abortifacients among Sheep and Goats in Grenada
1
Diana M. Stone, 1Sachin Kumthekar, 1Alfred Chikweto, 2Derek Thomas,
1
Keshaw Tiwari and 1Ravindra N. Sharma
1
Pathobiology Program, School of Veterinary Medicine, P.O. Box 7, St. George’s University, St.
George’s, Grenada, West Indies
2
Ministry of Agriculture, Forestry and Fisheries, St. George’s, Grenada, West Indies
Abstract: The aim of this study was to determine the prevalence of exposure to the zoonotic abortifacients
Brucella spp., Coxiella burnetii and Chlamydophila abortus among sheep and goats in the Caribbean Tri-Island
state of Grenada. Documentation of exposure to these important bacterial pathogens will facilitate instituting
appropriate prevention and control measures. Serum samples were collected from 582 animals from the islands
of Grenada and Carriacou during 2009-2010. Sera were tested by enzyme-linked immunosorbent assay (ELISA)
for determination of antibodies to smooth lipopolysaccharides (s-LPS) of B. abortus strain S-99, inactivated
C. abortus antigens and to C. burnetii phase I and II purified antigens. None of the animals examined tested
positive for antibody to C. burnetii. Evidence of Brucella exposure was noted in 13 (3.6%) of 362 sheep,
representing animals from both islands of Grenada and Carriacou, whereas none of the 220 goats examined
tested positive. Exposure to either Brucella abortus or B. melitensis could account for the detected antibody
to Brucella s-LPS antigens. Antibody to C. abortus was detected in 6.0% of animals tested (24 sheep and 10
goats), representing animals from Carriacou and all 6 parishes of Grenada. Taken together, our results indicate
moderate widespread exposure of small ruminants to the zoonotic abortifacients Brucella spp. and
Chlamydophila abortus in the tri-island state of Grenada and is the first report documenting such exposures in
any animal species in this region of the Caribbean.
Key words: Brucella, Caribbean, Chlamydophila, Coxiella, Grenada, small ruminants
et al., 2002; Lucero et al., 2008), C. abortus (Borde et al.,
2006) or C. burnetii (Adesiyun and Cazabon, 1996;
Adesiyun et al., 2011). To our knowledge there are no
published reports from Grenada on exposure of animals or
humans to any of these agents. The objective of the study
reported here was to determine whether there is serologic
evidence of exposure to these zoonotic and economically
important reproductive pathogens in sheep and goats in
Grenada. Documentation on whether any of these agents
is currently being maintained in small ruminants in
Grenada will allow for appropriate prevention and control
measures to be instituted and may impact small ruminant
production, human health and livestock import and export
regulations in the region.
INTRODUCTION
Small ruminants are very important livestock species
in the Caribbean, including the tri-island state of Grenada.
The rearing of sheep and goats for both meat and milk is
increasing in Grenada and includes “back-yard” as well as
a few commercial enterprises (Ministry of Agriculture,
Forestry and Fisheries, Grenada, West Indies, 2009). Most
sheep and goat production systems are characterized as
small-scale and low-input and few breeding or
productivity records are kept.
Three pathogens that are infectious causes of
significant reproductive loss in sheep and goats and of
global importance are Brucella melitensis, Chlamydophila
abortus and Coxiella burnetii. These agents are also
zoonotic and can be associated with abortion and systemic
flu-like disease with occasional debilitating chronic
manifestations in humans. Domestic ruminants and in
particular, sheep and goats are the major animal reservoir
that leads to human exposure to all three of these agents
(Acha and Szyfres, 2001). There are few published
reports from the Caribbean on evidence of exposure to
Brucella spp. (Ahl et al., 1993; Corbel, 1997; Fosgate
MATERIALS AND METHODS
Study population and sample collection: Peripheral
blood samples from 582 small ruminants (362 sheep and
220 goats) from the islands of Grenada and Carriacou,
islands in the tri-island state of Grenada, were obtained
between December, 2009 and December, 2010. The much
smaller island of Carriacou is similar in land mass and
Corresponding Author: Diana M. Stone, Pathobiology Program, School of Veterinary Medicine, P.O. Box 7, St. George’s
University, St. George’s, Grenada, West Indies, Tel.: +1 473 444 4175; Fax: 1 473 439 5068
113
Int. J. Anim. Veter. Adv.,4(2): 113-118, 2012
population to the individual parishes in Grenada
(Government of Grenada, 2010) and thus, for the
purposes of this study the island of Carriacou was
considered as an island consisting of one parish. Groups
of sheep and/or goats owned by one person or family
were defined as a production unit. Sheep, goat or mixed
sheep and goat production units were selected with the
assistance of the Grenada Ministry of Agriculture,
Forestry and Fisheries and with oral confirmation of
owner informed consent. Sixty five production units were
selected from the 6 parishes of Grenada and 9 production
units were selected from the sister island of Carriacou.
Production units ranged in size from 1 to 150 animals. For
production units consisting of less than 4 animals, all
animals were sampled. For production units of $4 but #30
animals, 60% of the animals were sampled. For
production units of >30 animals, 40% of the animals were
sampled. Samples were from clinically healthy animals at
least 6 months of age. Based on the Grenada Ministry of
Agriculture, Forestry and Fisheries report on the number
of sheep and goats inspected in Grenada in 2009, we
estimated a population size of at most 1700 sheep and
2000 goats on these 2 islands at the time of our sampling.
Based on these maximum population estimates we
sampled greater than 10% of the sheep and goats on these
two islands. Our sample size was sufficient to detect a
minimum exposure rate of 1±2% at a 95% confidence
interval in both sheep and goats for the 3 infectious agents
evaluated in this study (Anonymous, 2010).
All animals sampled were determined by physical
examination to be healthy. Approximately 5 mL of blood
were collected by jugular venipuncture and allowed to
clot. Samples were centrifuged in the field within 2 h of
collection and 2-3 mL of serum was harvested from each
sample and kept on ice until arrival at the veterinary
diagnostic laboratory at St. George’s University School of
Veterinary Medicine for storage at -80ºC until tested.
after addition of the stop solution were then evaluated
using a microplate photometer to measure the Optical
Density (OD) of the yellow color at 450 nm. Results of
the microplate photometer reading were expressed as
either positive or negative. This was determined by
calculating a Percent Positivity (PP) value where PP
equals the OD of the sample divided by the OD of the
positive control X100. A PP value of <15 was considered
negative and a PP value of $15 was considered positive.
The PP of the negative control was also calculated for
each plate and confirmed to be <15.
Commercial ELISA kits were used to screen 564 of
the 582 serum samples for IgG antibodies to Coxiella
burnetii phase I and II purified antigens (IDEXX ChekitQ-fever, IDEXX Laboratories, Inc. Westbrook, Maine,
USA) and to inactivated Chlamydophila abortus antigens
(IDEXX Chekit Chlamydophila abortus, IDEXX
Laboratories, Inc. Westbrook, Maine, USA) according to
the manufacturer’s instructions. The manufacturer reports
a 100% relative sensitivity and specificity for the ChekitQ fever test in comparison with the complement fixation
test. The manufacturer reports a 89-95% diagnostic
sensitivity and a 100% diagnostic specificity for the
Chekit- Chlamydophila abortus test. Briefly, test sera
were prepared at 1:400 dilution and specific antibodies
were measured using a horseradish peroxidase-labeled
anti-ruminant IgG conjugate. Results were expressed as
a percentage of the OD reading at 450 nm of the test
sample (S) calculated by dividing the absorbance of the
sample (corrected by subtraction of the mean negative
control absorbance) by the mean absorbance of the
positive control (P) (corrected by subtraction of the mean
negative control absorbance), giving an S/P value. The
S/P value multiplied by 100 gives a % value. Samples
with a value <30% were considered negative, while
samples with a value $40% were considered positive.
Samples with a value $30% and <40% were considered
suspect and were retested.
Indirect enzyme-linked immunosorbent assays
(iELISA): The commercial solid phase indirect Brucella
ELISA antibody test (SAVNOVIR® Brucella-Ab-IELISA, Svanova biotech Ab, Uppasala, Sweden) was
used to screen all 582 serum sample for detection of IgG
antibodies to inactivated Brucella antigen according to the
manufacturer’s instructions. The antigen used is derived
from the smooth lipopolysaccharides (s-LPS) of the B
abortus strain S-99. The reported diagnostic sensitivity
and specificity from the manufacturer for this test is 94.3100% and 100%, respectively, which is in close
agreement with an independent report on Brucella
iELISA tests (Minas et al., 2005). Briefly, test sera and
positive and negative control samples were prepared at
1:400 dilution and specific antibodies were measured
using a horseradish peroxidase-conjugated anti-ruminant
IgG monoclonal antibody. Results were first screened by
visual inspection for a color change. Samples resulting in
the development of a blue color which changed to yellow
Data analysis: For each serologic test the Chi-squared
test of significance was used to compare differences in
percent positive animals between sheep and goats,
between the two islands of Grenada and Carriacou and
among the parishes of Grenada. The Chi-squared test of
significance was also used to compare differences
between the percent positive Brucella spp. animals and
percent positive C. abortus animals.
RESULTS
Serum from 582 sheep and goats was tested for
antibodies against Brucella antigen (Table 1). Five
hundred and sixty four of the 582 samples were also
tested for antibodies against C. abortus (Table 2) and C.
burnetii antigens. Of the 74 production units sampled, 38
were sheep only, 20 were goat only and 16 were mixed
sheep and goat units.
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Int. J. Anim. Veter. Adv.,4(2): 113-118, 2012
Table 1: Seroprevalence of IgG antibodies against Brucella spp. in
sheep and goats from Grenada and Carriacou
Animal
No. sampled
No. positive
Prevalence (%)1
Sheep
362
13
3.6
Goats
220
00
0.0
Total
582
13
2.2
1
: Significant difference (p<0.05) between sheep and goats
which contained only sheep (Table 2). Seven of the
remaining 8 production units in Carriacou contained
sheep and all sampled sheep from these production units
tested negative. For both islands together, the percent of
sheep that tested positive within production units with
more than a single animal ranged from 4.3 to 25%. Two
single-animal production units each had one sheep that
tested positive for Brucella antibodies. There was no
significant difference between the percent Brucella
antibody-positive sheep in Grenada compared to the
percent positive sheep in Carriacou (Table 2).
Antibody to C. abortus was detected in 6.0% of the
564 animals tested and included both sheep and goats
(Table 3). Positive animals were identified in all 6
parishes of Grenada and on the island of Carriacou (Table
4). Twenty four sheep tested positive (6.7%) and 10 goats
tested positive (4.7%) (Table 3). Among all sheep tested,
2 of 33 males tested positive (6.0%) and 22 of 322
females tested positive (6.8%). Among all goats tested,
none of the 31 males tested positive and 10 of the 178
females tested positive (5.6%). Twenty animals from
Grenada tested positive (5.6%) consisting of 12 sheep (10
females and 2 males) and 8 goats, all females. In
Carriacou 14 animals tested positive (6.7%) consisting of
12 sheep and 2 goats, all of which were females. In
Grenada, 14 of the 65 production units contained C.
abortus antibody-positive animals. The percent positive
animals within production units ranged from 4.5 to 33.3%
with a mean of 11.5%. In Carriacou, 6 of the 9 production
units tested had animals positive for C. abortus
antibodies. The percent positive animals within
production units ranged from 4.0 to 18.8% with a mean of
8.9%. There was no significant difference between the
percent positive sheep and goats or between the percent
positive animals in Grenada compared to the percent
positive animals in Carriacou. Further, there were no
significant differences among the 6 parishes of Grenada
and the island of Carriacou for the percent positive
animals (Table 4).
None of the animals tested were positive for both
Brucella s-LPS and C. abortus antibodies. One production
unit on the island of Grenada had one Brucella antibodypositive sheep and one C. abortus antibody-positive
sheep. There was no significant difference between the
percent positive animals for Brucella spp. antibodies and
percent positive animals for C. abortus antibodies. Nor
was there a significant difference between the percent of
sheep testing positive for Brucella spp. antibodies and
percent of sheep testing positive for C. abortus antibodies
(data not shown).
Among all animals evaluated only one serum sample
tested as a suspect for antibody to C. burnetii. The one
suspect animal was a female goat from the parish of St.
Andrews in Grenada. This goat tested negative for
antibodies to both Brucella antigen and C. abortus
antigen.
Table 2: Seroprevalence of IgG antibodies against Brucella spp. in
sheep by parish/region
Parish/
No.
No.
Prevalence
Island
region
sampled
positive
(%)1
Grenada
St. George
17
01
5.8
St. David
26
01
3.8
St. Andrew
120
05
4.1
St. John
34
03
8.8
St. Mark
24
00
0.0
St. Patrick
----------Total
221
10
4.5
Carriacou
Carriacou
141
03
2.1
Total
362
13
3.6
1
: Not significantly different (p>0.05) among parishes or between
Grenada and Carriacou; 2: All samples collected from St. Patrick were
from goats
Table 3: Seroprevalence of IgG antibodies against C. abortus in sheep
and goats from Grenada and Carriacou
Animal
No. sampled
No. positive
Prevalence (%)1
Sheep
355
24
6.7
Goats
209
10
4.7
Total
564
34
6.0
1
: Not significantly different (p>0.05) between sheep and goats
Table 4: Seroprevalence of IgG antibodies against C. abortus in
healthy sheep and goats (combined) according to island and
parish location
Parish/
No.
No.
Prevalence
Island
region
sampled
positive
(%)1
Grenada
St. George
82
04
4.8
St. David
59
04
6.8
St. Andrew
120
03
2.5
St. John
44
03
6.8
St. Patrick
26
031
1.5
St. Mark
24
03
12.5
Total
355
20
5.6
Carriacou
Carriacou
209
14
6.7
Total
564
34
6.0
1
: Not significantly different (p>0.05) among parishes or between
Grenada and Carriacou
None of the goats tested were positive for antibodies
to s-LPS Brucella antigen using the I-ELISA. However,
3.6% of the 362 sheep tested were Brucella I-ELISA
positive (Table 1). Of the 13 positive sheep, 10 were from
the island of Grenada representing sheep from 4 of the 6
parishes (Table 2). There were no significant differences
for the percent positive sheep among the 4 parishes with
positive sheep (Table 2). Four of the 67 male sheep
(6.0%) and 9 of the 295 female sheep (3.0%) tested were
Brucella antibody-positive. On the island of Grenada 46
of the 65 production units tested contained sheep and 7 of
these production units had Brucella I-ELISA positive
sheep. Of these 7 production units 4 contained only sheep
and 3 units had both sheep and goats. Three of the 13
Brucella antibody-positive sheep resided on the island of
Carriacou and all were from the same production unit
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Int. J. Anim. Veter. Adv.,4(2): 113-118, 2012
DISCUSSION
were also present in some of the production units with
positive sheep. Abortion is a recognized problem in small
ruminant production in Grenada but few cases are
evaluated by veterinarians (B. Louison, Grenada Ministry
of Agriculture, Forestry and Fisheries, personal
communication, 2011). There are no data on brucellosis
in humans in Grenada which may reflect that few flu-like
disease cases are laboratory confirmed. It will be
important to determine the species of Brucella responsible
for exposure in Grenadian sheep and the impact that
brucellosis is having on animal production and human
health in this region of the Caribbean.
Our results on detection of antibody to C. abortus in
sheep and goats indicate that exposure is present in both
species and is wide spread, as demonstrated by
seropositive animals in all 6 parishes of Grenada and the
island of Carriacou. This was not unexpected, as C.
abortus infection in small ruminants is recognized almost
globally and is considered to be one of the most
economically important production animal pathogens in
the world (Aitken and Longbottom, 2007), including the
US, Mexico and parts of South America (World
Organization for Animal Health, 2011a, b). The
seroprevalence rate for sheep in our study was higher
(6.7%) than that in goats (4.7%), but the difference was
not statistically significant (Table 3). Importantly, only 14
of the 65 production units in the study contained
seropositive animals and seroprevalence rates were as
high as 33.3% within production units with positive
animals, suggesting that although exposure is widely
distributed, it is not evenly distributed. Other published
reports of estimated prevalence of infection, as measured
by anti-C. abortus antibodies, vary considerably as noted
by an 8.6% prevalence in the UK (Leonard et al., 1993),
a 19% prevalence in Switzerland (Borel et al., 2004), a
21.8% prevalence in Spain (Mainar-Jaime et al., 1998)
and a 50.5% prevalence in Jordan (Al-Qudah et al., 2004).
However, these studies represent different types of
antibody tests and some represent samples only from
sheep and goats with a history of abortion. There are a
few published reports comparable to ours of C. abortus
seroprevalence as determined by ELISA on randomly
selected, healthy sheep or goats. These studies report
seroprevalence rates from as low as 3.03% in Sovak
Republic („isláková et al., 2007) to as high as 31.1% in
Mexico (Jiménez-Estrada et al., 2008). Only one
published report was identified from the Caribbean and in
this study from the island of Tobago only one of 89 goats
tested was antibody positive by ELISA (Borde et al.,
2006).
Due to the demonstrated 100% specificity of the C.
abortus ELISA test used in this study (IDEXX Animal
Health Updates, 2007), our results confirm that sheep and
goats in Grenada are exposed to C. abortus. It is likely
that the rate of exposure may be higher than we detected
due to the reported sensitivity of the C. abortus ELISA
There are no vaccines commercially available for
protection of sheep and goats against C. burnetii and
although commercial vaccines against C. abortus and B
melitensis are available internationally, they are not
currently used in Grenada. Thus, positive serology
detected in the sheep and goats in this study reflect natural
exposure.
The Brucella antigens in the iELISA antibody test
used in this study are derived from the B. abortus S-99
strain (Svanova Biotech Ab, Uppsala, Sweden, 2011,
personal communication). Because this is a smooth
Brucella strain and contains only s-LPS, the test does not
detect antibodies to the rough B. canis and B. ovis strains.
Although B. suis is a smooth strain and has been reported
in the more northern Caribbean islands (Corbel, 1997), it
has not been documented in the Eastern Caribbean and
infections in sheep and goats with this species are rarely
reported anywhere (Špi…iƒ et al., 2010; Lucero et al.,
2008). Thus, the positive results from our study likely
reflect exposure to the smooth strains of B. abortus and/or
B. melitensis and are the first report of exposure to either
of these agents in Grenada. Our results further indicate
that exposure in sheep is moderately distributed (4 of 6
parishes) and occurs on both Grenada and Carriacou.
Although brucellosis in ruminants has been controlled in
many industrialized countries, it continues to have an
important economic and public health impact in many
parts of the world, including South and Central America
(OIE, 2011a, b; Corbel, 1997). It is of interest that the
neighboring Eastern Caribbean island state of Trinidad
and Tobago was classified free of brucellosis by (OIE,
2011a, b; Blajan and Melendez, 1984). However, in 2002
B. abortus biovar 1 was isolated from both cattle and
water buffalo from this region (Fosgate et al., 2002). The
only published reports of exposure to B. melitensis in the
Caribbean are from Cuba on samples from sheep
collected prior to 1991 (Lucero et al., 2008) and from St.
Croix in 1993 on serum samples from goats (Ahl et al.,
1993). Documented importation of sheep into Grenada
during the last 20 years has only occurred from the island
of Barbados and prior to 2004. There is only one
documented shipment of goats into Grenada during the
past 20 years and this was in 2007 from the United States
(B. Louison, Grenada Ministry of Agriculture, Forestry
and Fisheries, personal communication, 2011). Because
there has been little effort to detect Brucella exposure in
the Caribbean and because undocumented importation of
sheep and goats from neighboring countries may have
occurred, it is impossible to say how Brucella spp. might
have been introduced into Grenada and whether B.
abortus and/or B. melitensis account for the seropositive
results observed in our study.
Of interest is that only sheep were identified as
Brucella seropositive in our study, even though goats
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Int. J. Anim. Veter. Adv.,4(2): 113-118, 2012
used as being between 89-95% (IDEXX Animal Health
Updates, 2007). Further, serologic tests may fail to detect
infection prior to pregnancy or abortion (Stuen and
Longbottom, 2011).
C. burnetii is considered to have a worldwide
distribution with higher prevalence in areas with
concentrated numbers of sheep and goats (Raoult et al.,
2005)). Thus, it was unexpected that none of the 564
sheep and goats tested in this study were seropositive.
C. burnetii has also not been detected in New Zealand, a
much larger sheep producing island country and where
several C. burnetii serosurveys have been conducted
(Hilbink et al., 1993; Fournier et al., 1998; Greenslade et
al., 2003). This suggests that some geographically
confined areas may be free of this organism. There are
only two publications from the Caribbean reporting
detection of C. burnetii exposure and both are from the
island of Trinidad. In Trinidad serologic evidence of
exposure was detected in livestock (Adesiyun and
Cazabon, 1996) and more recently in humans (Adesiyun
et al., 2011). Of interest, in the Trinidad report on
livestock the highest prevalence was in pigs (11.3%) and
none of the 16 sheep and 7 goats tested were seropositive
by the capillary agglutination test (Adesiyun and
Cazabon, 1996). A recent report from Antigua failed to
detect C. burnetii DNA in 100 ticks of two species that
are potential C. burnetii vectors (Robinson et al., 2009).
It is possible that Grenada and Carriacou are truly free of
C. burnetii. It is also possible that exposure in sheep and
goats is less than 1% and below our ability to detect with
our sample size. Alternatively, it is possible that the test
used was not sensitive enough to detect positive animals.
This is unlikely given our use of the indirect ELISA
which contains both phase 1 and phase 2 C. burnetii
antigens for the detection of both acute and chronic
infections and has a sensitivity of almost 100% (IDEXX
Animal Health Updates, 2007). These features of the
indirect ELISA led to its recent adoption as the standard
test used at the Veterinary Laboratories Agency in
England and Wales (Horigan et al., 2011). However, to
determine whether or not Grenada and Carriacou are free
of C. burnetii, more extensive testing of livestock will be
required and should include testing of swine as well as
small ruminants.
production units compared to Brucella spp. exposure. It is
likely that due to the prevalence of exposure identified in
this study to these two pathogens that infection is having
a significant negative impact on small ruminant
production and on human health. There is a critical need
for diagnostic workups on small ruminant abortions and,
in particular, surveillance of Brucella exposure in
Grenada. Identification of the Brucella species accounting
for exposure and the extent of exposure need to be
determined to appropriately design, implement and
evaluate control programs aimed at this important
zoonotic small ruminant abortifacient.
ACKNOWLEDGMENT
The authors would like to thank Dr. Bowen Louison,
Chief Veterinary Office, Ministry of Agriculture, Forestry
and Fisheries, Grenada, West Indies and Dr. Claude De
Allie, veterinary pathologist in the Department of
Veterinary Services, Ministry of Agriculture, Forestry and
Fisheries, Grenada, West Indies for their assistance in
identifying sheep and goat production units in Grenada
and Carriacou, for facilitating communications and
logistics with production unit owners and for providing
valuable information on small ruminant production in
Grenada.
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