Bacterial Causes of Small Ruminant Abortion:
A systematic Review and Meta-Analysis
Gezahegn Alemayehu, Gemechu Chala, Samson Leta, Gezahegne
Mamo and Barbara Wieland
ISVEE 15, Thailand, Nov. 12-16, 2018

Introduction
• Abortion in sheep and goat cause significant wastage and
financial losses worldwide, affect productivity (lambs/kids)
• Infectious agents are the most common causes
• Common bacterial causes
• Chlamydia abortus
• Brucella spp.
• Coxiella burnetii
• Campylobacter spp.
• Listeria spp.
• Leptospira spp.
Most causes are zoonotic,
thus are a public health risk,
with high risk of exposure for
farmers

Objective
Improve understanding of relative importance of
bacterial abortion causes
• To conduct a comprehensive literature search
• To preform systematic review and meta-analysis of
reports which identify bacterial agents from
abortion cases in small ruminants

Methodology
Literature search strategy
• Review protocol based on PRISMA guideline
• Search in PubMed and Google Scholar databases
• Keywords:(list of hazards) and (animal species) and (Abortion).
• Titles and abstracts were screened by two independent reviewers.
• Duplicates were identified and removed

Inclusion criteria
• Study conducted on small ruminants
• Samples collected from aborted ewes and doe (not sero-survey
in healthy population!)
• Observational studies
• Published in English and after 2000
• The presence of the following data
a. location (country) of study
b. type and number of sample examined
c. pathogen detection technique
d. type of pathogen identified and
e. number of positive samples for each pathogen in each
animal species

Data extraction
• Using data extraction template:
✓ first author
✓ year of publication
✓ year of study
✓ location(country)
✓ number positive
✓ number negative
✓ continent
✓ study design
✓ bacteria species
✓ animal species
✓ test method
✓ type of sample
✓ number of abortion cases

Data analysis
• Descriptive analysis
• Fitting a random effects model
• Meta-regression
• Inter-study heterogeneity –chi2 statistic (Cochrane’s Q-test)-
p-value.
• Degrees of heterogeneity among studies(I2), ranges from 0%
to 100%–
➢ 0% to 40%: might not be important;
➢ 30% to 60%: moderate heterogeneity
➢ 50% to 90%: may represent substantial heterogeneity
➢ 75% to 100%: considerable heterogeneity.

Results
Flow diagram of the selection of eligible studies
→ Resulted in 176 animal level reports, representing 33,066 animals

Publication year of the included studies
0
5
10
15
20
25
30
35
40
45
2001
2002
2003
2004
2005
2006
2007
2008
2009
2010
2011
2012
2013
2014
2015
2016
2017

Origin of included studies

Type of samples used
0
2000
4000
6000
8000
10000
12000
14000
16000
18000
20000
Brucella spp. C.abortus C. burnetti Campylobacter
Spp.
Leptospira spp. Listeria spp.
fecal sample fetal fluid blood fetal tissue
sera aborting ewe/doe milk placenta stomach content

Diagnostic tests used
0
2000
4000
6000
8000
10000
12000
14000
16000
18000
20000 Brucella C.abortus
C.burnetii Campylobacter
Leptospira Listeria

Proportion of SR abortion cases with bacterial causes
21.47
26.56
16.83
21.47
18.64
3.77
0
5
10
15
20
25
30
0
2,000
4,000
6,000
8,000
10,000
12,000
14,000
16,000
18,000
20,000
Number negative Number Positive Pooled Prevalence

Proportion of C. abortus in SR abortion cases
Overall (I^2 = 95.53%, p = 0.00)
Masala et al. (2005)
Bagdonas et al. (2007)
Abdelkadi et al. 2017
Oporto et al. (2006)
Hazlett et al. (2013)
Tavares Clemente et al. (2011)
Moeller (2001)
Navarro et al. (2015)
Kalender et al. (2013)
Navarro et al. (2015)
Navarro et al. (2015)
Szeredi et al. (2006)
Szeredi et al. (2006)
Szeredi et al. (2006)
Kalender et al. (2013)
Szeredi et al. (2006)
Benkirane et al. (2015)
Krkalić et al.( 2015)
Bagdonas et al. (2007)
Oh et al. (2017)
Krkalić et al.( 2015)
van den Brom et al. (2012)
Bagdonas et al. (2007)
Špičić et al.( 2015)
Masala et al. (2005)
Špičić et al.( 2015)
Hazlett et al. (2013)
Masala et al. (2007)
author
Hazlett et al. (2013)
Hireche et al.2015
Ababneh et al.( 2014)
Kalender et al. (2013)
Masala et al. (2005)
Ababneh et al.( 2014)
Spilovska et al. (2009)
Masala et al. (2005)
Ababneh et al.( 2014)
Navarro et al. (2015)
Ababneh et al.( 2014)
Špičić et al.( 2015)
Bagdonas et al. (2007)
Szeredi et al. (2006)
Bisias et al. (2009)
Špičić et al.( 2015)
Kreizinger et al. (2015)
Heidari et al.2017
Kreizinger et al. (2015)
Marsilio et al. (2005)
Heidari et al.2017
Kalender et al. (2013)
Bagdonas et al. (2007)
Szeredi et al. (2006)
Masala et al. (2007)
Hässig et al. (2003)
Kalender et al. (2013)
Bisias et al. (2009)
van den Brom et al. (2012)
Abd et al. (2011)
Hazlett et al. (2013)
Masala et al. (2007)
Abd et al. (2011)
Tavares Clemente et al. (2011)
Hireche et al.2015
Benkirane et al. (2015)
0.27 (0.21, 0.32)
0.05 (0.02, 0.10)
0.44 (0.19, 0.73)
0.31 (0.24, 0.38)
0.12 (0.08, 0.18)
0.86 (0.60, 0.96)
0.47 (0.35, 0.60)
0.14 (0.10, 0.20)
0.39 (0.22, 0.59)
0.09 (0.04, 0.19)
0.43 (0.26, 0.63)
0.63 (0.46, 0.77)
0.67 (0.30, 0.90)
0.39 (0.26, 0.55)
0.56 (0.46, 0.65)
0.06 (0.03, 0.12)
0.68 (0.55, 0.78)
0.15 (0.10, 0.23)
0.25 (0.09, 0.53)
0.58 (0.32, 0.81)
0.02 (0.00, 0.11)
0.92 (0.65, 0.99)
0.10 (0.07, 0.13)
0.67 (0.35, 0.88)
0.12 (0.06, 0.21)
0.02 (0.01, 0.04)
0.20 (0.13, 0.30)
0.21 (0.16, 0.28)
0.02 (0.01, 0.05)
ES (95% CI)
0.61 (0.39, 0.80)
0.60 (0.31, 0.83)
0.40 (0.20, 0.64)
0.14 (0.03, 0.51)
0.09 (0.02, 0.38)
0.50 (0.30, 0.70)
0.14 (0.11, 0.17)
0.00 (0.00, 0.06)
0.47 (0.25, 0.70)
0.60 (0.44, 0.74)
0.61 (0.46, 0.74)
0.29 (0.12, 0.55)
0.67 (0.55, 0.77)
0.17 (0.10, 0.27)
0.15 (0.11, 0.19)
1.00 (0.21, 1.00)
0.76 (0.55, 0.89)
0.08 (0.05, 0.13)
0.40 (0.12, 0.77)
0.05 (0.02, 0.11)
0.15 (0.10, 0.23)
0.06 (0.02, 0.15)
0.63 (0.31, 0.86)
0.46 (0.40, 0.52)
0.07 (0.03, 0.14)
0.15 (0.05, 0.36)
0.14 (0.03, 0.51)
0.21 (0.16, 0.28)
0.04 (0.03, 0.07)
0.06 (0.04, 0.08)
0.49 (0.40, 0.59)
0.13 (0.02, 0.47)
0.05 (0.03, 0.06)
0.48 (0.37, 0.60)
0.50 (0.22, 0.78)
0.27 (0.22, 0.34)
100.00
1.79
1.20
1.81
1.79
1.36
1.71
1.81
1.52
1.72
1.52
1.62
1.03
1.63
1.77
1.77
1.71
1.77
1.31
1.31
1.67
1.31
1.84
1.20
1.73
1.84
1.76
1.80
1.83
Weight
1.45
1.24
1.39
1.09
1.27
1.48
1.83
1.71
1.39
1.62
1.67
1.36
1.72
1.74
1.82
0.41
1.49
1.81
0.95
1.78
1.78
1.72
1.15
1.82
1.74
1.48
1.09
1.80
1.83
1.84
1.76
1.15
1.85
1.72
1.15
1.81
%
0.27 (0.21, 0.32)
0.05 (0.02, 0.10)
0.44 (0.19, 0.73)
0.31 (0.24, 0.38)
0.12 (0.08, 0.18)
0.86 (0.60, 0.96)
0.47 (0.35, 0.60)
0.14 (0.10, 0.20)
0.39 (0.22, 0.59)
0.09 (0.04, 0.19)
0.43 (0.26, 0.63)
0.63 (0.46, 0.77)
0.67 (0.30, 0.90)
0.39 (0.26, 0.55)
0.56 (0.46, 0.65)
0.06 (0.03, 0.12)
0.68 (0.55, 0.78)
0.15 (0.10, 0.23)
0.25 (0.09, 0.53)
0.58 (0.32, 0.81)
0.02 (0.00, 0.11)
0.92 (0.65, 0.99)
0.10 (0.07, 0.13)
0.67 (0.35, 0.88)
0.12 (0.06, 0.21)
0.02 (0.01, 0.04)
0.20 (0.13, 0.30)
0.21 (0.16, 0.28)
0.02 (0.01, 0.05)
ES (95% CI)
0.61 (0.39, 0.80)
0.60 (0.31, 0.83)
0.40 (0.20, 0.64)
0.14 (0.03, 0.51)
0.09 (0.02, 0.38)
0.50 (0.30, 0.70)
0.14 (0.11, 0.17)
0.00 (0.00, 0.06)
0.47 (0.25, 0.70)
0.60 (0.44, 0.74)
0.61 (0.46, 0.74)
0.29 (0.12, 0.55)
0.67 (0.55, 0.77)
0.17 (0.10, 0.27)
0.15 (0.11, 0.19)
1.00 (0.21, 1.00)
0.76 (0.55, 0.89)
0.08 (0.05, 0.13)
0.40 (0.12, 0.77)
0.05 (0.02, 0.11)
0.15 (0.10, 0.23)
0.06 (0.02, 0.15)
0.63 (0.31, 0.86)
0.46 (0.40, 0.52)
0.07 (0.03, 0.14)
0.15 (0.05, 0.36)
0.14 (0.03, 0.51)
0.21 (0.16, 0.28)
0.04 (0.03, 0.07)
0.06 (0.04, 0.08)
0.49 (0.40, 0.59)
0.13 (0.02, 0.47)
0.05 (0.03, 0.06)
0.48 (0.37, 0.60)
0.50 (0.22, 0.78)
0.27 (0.22, 0.34)
100.00
1.79
1.20
1.81
1.79
1.36
1.71
1.81
1.52
1.72
1.52
1.62
1.03
1.63
1.77
1.77
1.71
1.77
1.31
1.31
1.67
1.31
1.84
1.20
1.73
1.84
1.76
1.80
1.83
Weight
1.45
1.24
1.39
1.09
1.27
1.48
1.83
1.71
1.39
1.62
1.67
1.36
1.72
1.74
1.82
0.41
1.49
1.81
0.95
1.78
1.78
1.72
1.15
1.82
1.74
1.48
1.09
1.80
1.83
1.84
1.76
1.15
1.85
1.72
1.15
1.81
%
-.5 0 .5 1
Forest plot on proportion
of C. abortus in aborted
small ruminants
Chi2,P = 0.00
Degrees of heterogeneity (I2)=
95.53%

Role of animal species, continent, sample type and
diagnostic test:
• No significant difference between sheep and goat
• Differences between continents: range from 14.51%
(Asia) to 42.29% (North America), P=0.54
• Most positives were detected in placenta samples
(p=0.04)
• Highest proportion of positives with CFT
C. abortus

Proportion of C. burnetii in SR abortion case
Overall (I^2 = 96.68%, p = 0.00)
Navarro et al. (2015)
Abdelkadi et al. 2017
Vaidya et al. (2010)
Masala et al. (2004)
Vaidya et al. (2010)
Jones et al. (2013)
Jones et al. (2013)
Vaidya et al. (2010)
Masala et al. (2007)
Benkirane et al. (2015)
Filioussis et al.2017
Vaidya et al. (2010)
Bisias et al. (2009)
Oporto et al. (2006)
Hazlett et al. (2013)
Abiri et al. (2016)
Pritchard et al. (2014)
Masala et al. (2004)
Navarro et al. (2015)
Hazlett et al. (2013)
Rousset et al. (2007)
Hazlett et al. (2013)
Vaidya et al. (2010)
Kreizinger et al. (2015)
Oh et al. (2017)
Oh et al. (2017)
Kreizinger et al. (2015)
Vaidya et al. (2010)
Szeredi et al. (2006)
Heidari et al.2017
Vaidya et al. (2010)
Masala et al. (2004)
van den Brom et al. (2012)
Abiri et al. (2016)
Szeredi et al. (2006)
Navarro et al. (2015)
Jones et al. (2013)
van den Brom et al. (2012)
Kreizinger et al. (2015)
Navarro et al. (2015)
Vaidya et al. (2010)
Vaidya et al. (2010)
Benkirane et al. (2015)
Heidari et al.2017
Masala et al. (2007)
Asadi et al. (2013)
Masala et al. (2004)
Vaidya et al. (2010)
Hazlett et al. (2013)
Masala et al. (2004)
Abdel-Moein and Hamza (2017)
Vaidya et al. (2010)
Abdel-Moein and Hamza (2017)
Vaidya et al. (2010)
Filioussis et al.2017
Moeller (2001)
Masala et al. (2004)
Kreizinger et al. (2015)
Asadi et al. (2013)
Oporto et al. (2006)
Bisias et al. (2009)
author
16.83 (13.12, 20.87)
17.39 (4.95, 38.78)
27.78 (21.37, 34.93)
11.63 (3.89, 25.08)
16.67 (2.09, 48.41)
5.88 (0.15, 28.69)
60.00 (14.66, 94.73)
57.14 (18.41, 90.10)
11.11 (2.35, 29.16)
10.96 (7.62, 15.12)
27.36 (19.15, 36.87)
8.00 (6.22, 10.10)
2.78 (0.07, 14.53)
63.22 (55.59, 70.39)
2.70 (0.74, 6.78)
74.19 (55.39, 88.14)
17.39 (10.28, 26.70)
11.11 (0.28, 48.25)
10.75 (7.79, 14.35)
11.43 (3.20, 26.74)
66.67 (59.14, 73.62)
88.00 (75.69, 95.47)
66.67 (50.45, 80.43)
4.65 (0.57, 15.81)
20.00 (0.51, 71.64)
42.55 (28.26, 57.82)
76.60 (61.97, 87.70)
0.00 (0.00, 52.18)
0.00 (0.00, 6.72)
1.33 (0.03, 7.21)
2.73 (0.89, 6.26)
5.66 (1.18, 15.66)
12.58 (11.20, 14.05)
8.61 (5.93, 12.00)
0.00 (0.00, 84.19)
2.03 (0.66, 4.68)
13.04 (2.78, 33.59)
93.33 (68.05, 99.83)
1.78 (0.82, 3.35)
47.62 (25.71, 70.22)
11.43 (3.20, 26.74)
9.30 (2.59, 22.14)
7.55 (2.09, 18.21)
15.35 (10.67, 21.07)
0.85 (0.02, 4.67)
9.21 (3.78, 18.06)
19.55 (17.24, 22.01)
6.00 (1.25, 16.55)
10.71 (2.27, 28.23)
70.00 (60.02, 78.76)
10.84 (5.08, 19.59)
3.45 (0.09, 17.76)
1.89 (0.05, 10.07)
3.45 (0.09, 17.76)
2.33 (0.06, 12.29)
14.38 (12.02, 17.00)
9.00 (5.51, 13.70)
9.06 (8.41, 9.75)
14.29 (3.05, 36.34)
27.22 (20.87, 34.34)
2.70 (0.74, 6.78)
48.79 (42.89, 54.71)
ES (95% CI)
16.83 (13.12, 20.87)
17.39 (4.95, 38.78)
27.78 (21.37, 34.93)
11.63 (3.89, 25.08)
16.67 (2.09, 48.41)
5.88 (0.15, 28.69)
60.00 (14.66, 94.73)
57.14 (18.41, 90.10)
11.11 (2.35, 29.16)
10.96 (7.62, 15.12)
27.36 (19.15, 36.87)
8.00 (6.22, 10.10)
2.78 (0.07, 14.53)
63.22 (55.59, 70.39)
2.70 (0.74, 6.78)
74.19 (55.39, 88.14)
17.39 (10.28, 26.70)
11.11 (0.28, 48.25)
10.75 (7.79, 14.35)
11.43 (3.20, 26.74)
66.67 (59.14, 73.62)
88.00 (75.69, 95.47)
66.67 (50.45, 80.43)
4.65 (0.57, 15.81)
20.00 (0.51, 71.64)
42.55 (28.26, 57.82)
76.60 (61.97, 87.70)
0.00 (0.00, 52.18)
0.00 (0.00, 6.72)
1.33 (0.03, 7.21)
2.73 (0.89, 6.26)
5.66 (1.18, 15.66)
12.58 (11.20, 14.05)
8.61 (5.93, 12.00)
0.00 (0.00, 84.19)
2.03 (0.66, 4.68)
13.04 (2.78, 33.59)
93.33 (68.05, 99.83)
1.78 (0.82, 3.35)
47.62 (25.71, 70.22)
11.43 (3.20, 26.74)
9.30 (2.59, 22.14)
7.55 (2.09, 18.21)
15.35 (10.67, 21.07)
0.85 (0.02, 4.67)
9.21 (3.78, 18.06)
19.55 (17.24, 22.01)
6.00 (1.25, 16.55)
10.71 (2.27, 28.23)
70.00 (60.02, 78.76)
10.84 (5.08, 19.59)
3.45 (0.09, 17.76)
1.89 (0.05, 10.07)
3.45 (0.09, 17.76)
2.33 (0.06, 12.29)
14.38 (12.02, 17.00)
9.00 (5.51, 13.70)
9.06 (8.41, 9.75)
14.29 (3.05, 36.34)
27.22 (20.87, 34.34)
2.70 (0.74, 6.78)
48.79 (42.89, 54.71)
ES (95% CI)
-50 0 50 100 150
Proportion
Chi2, P = 0.00
I2 = 96.68%
Forest plot of proportion
of C. burnetii in aborted
small ruminants

C. burnetii
Role of animal species, continent, sample type and
diagnostic test:
➢ Higher proportion was detected from goat(22.22%)
than sheep(13.10%), p=0.08
➢ Differences between continents: range from 9.93% (Asia
to 55.91%(North America), p=0.00
➢ Most positives was detected in feta fluid samples
(p=0.46).
➢ Highest proportion of positives with ElISA(P=0.24)

Proportion of Brucella spp. in SR abortion case
Overall (I^2 = 95.35%, p = 0.00)
Wareth et al. (2015)
Bisias et al. (2009)
Szeredi et al. (2006)
Wareth et al. (2015)
Bisias et al. (2009)
Ilhan and Yener (2008)
Moeller (2001)
Wareth et al. (2015)
Wareth et al. (2015)
Ocholi et al. (2005)
Wareth et al. (2015)
Oh et al. (2017)
Wareth et al. (2015)
Szeredi et al. (2006)
Benkirane et al. (2015)
Ocholi et al. (2005)
Benkirane et al. (2015)
Wareth et al. (2015)
İlhan et al. 2007
author
Wareth et al. (2015)
İlhan et al. 2007
Assadullah Samadi et al. (2010)
Ocholi et al. (2005)
Celebi and Atabay (2009)
Assadullah Samadi et al. (2010)
Celebi and Atabay (2009)
Celebi and Atabay (2009)
Celebi and Atabay (2009)
21.47 (13.28, 30.64)
33.33 (7.49, 70.07)
15.22 (11.29, 19.89)
0.00 (0.00, 9.25)
33.33 (7.49, 70.07)
22.41 (16.45, 29.34)
30.00 (21.63, 39.48)
0.00 (0.00, 1.73)
100.00 (2.50, 100.00)
100.00 (66.37, 100.00)
14.29 (4.03, 32.67)
33.33 (7.49, 70.07)
0.00 (0.00, 7.55)
100.00 (2.50, 100.00)
0.00 (0.00, 3.48)
13.21 (7.41, 21.17)
100.00 (47.82, 100.00)
13.37 (9.00, 18.85)
100.00 (2.50, 100.00)
18.52 (12.36, 26.11)
ES (95% CI)
100.00 (2.50, 100.00)
21.48 (14.88, 29.37)
34.57 (24.34, 45.96)
14.29 (4.03, 32.67)
36.75 (32.01, 41.68)
48.11 (38.30, 58.03)
33.75 (29.13, 38.62)
35.50 (30.81, 40.41)
34.75 (30.09, 39.64)
21.47 (13.28, 30.64)
33.33 (7.49, 70.07)
15.22 (11.29, 19.89)
0.00 (0.00, 9.25)
33.33 (7.49, 70.07)
22.41 (16.45, 29.34)
30.00 (21.63, 39.48)
0.00 (0.00, 1.73)
100.00 (2.50, 100.00)
100.00 (66.37, 100.00)
14.29 (4.03, 32.67)
33.33 (7.49, 70.07)
0.00 (0.00, 7.55)
100.00 (2.50, 100.00)
0.00 (0.00, 3.48)
13.21 (7.41, 21.17)
100.00 (47.82, 100.00)
13.37 (9.00, 18.85)
100.00 (2.50, 100.00)
18.52 (12.36, 26.11)
ES (95% CI)
100.00 (2.50, 100.00)
21.48 (14.88, 29.37)
34.57 (24.34, 45.96)
14.29 (4.03, 32.67)
36.75 (32.01, 41.68)
48.11 (38.30, 58.03)
33.75 (29.13, 38.62)
35.50 (30.81, 40.41)
34.75 (30.09, 39.64)
-50 0 50 100 150
Proportion
Q- Chi2, P = 0.00
I2 = 95.35%
T2= 0.17
Forest plot on proportion
of Brucella spp. in aborted
small ruminant

Brucella spp.
Role of animal species, continent, sample type and
diagnostic test:
➢ Higher proportion was detected from
sheep(23.48%), than goat (17.33%)p=0.063
➢ Differences between continents: range from 0.0
(North America) to 39.84(Africa), p=0.00
➢ Most positives detected in milk samples (p=0.1).
➢ Highest proportion of positives with PCR (P=0.01)

Conclusions
• Similar causes across continents, but with different importance
and roles they play
• No or limited data found on socio-economic impact caused by
these agents
• Overall few studies, especially for LMICs, even though
reproductive performance in these countries is lower
• Surveillance and routine diagnostic data not widely accessible,
and thus not included in the review
• Further research needed on the role of major pathogens that
cause abortion in small ruminants

This presentation is licensed for use under the Creative Commons Attribution 4.0 International Licence.
better lives through livestock
ilri.org
better lives through livestock
ilri.org