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Tropical Animal Health and Production (2022) 54:346
https://doi.org/10.1007/s11250-022-03342-0
REGULAR ARTICLES
Investigation oftheoutbreaks ofabortions andorchitis inlivestock
inNamibia during2016–2018
AlasterSamkange1 · JolandievanderWesthuizen2· AnselmSiegfriedVoigts3· FrankChitate1· IsraelKaatura1·
SiegfriedKhaiseb2· EmmanuelH.Hikufe2· JulietKabajani2· AlecS.Bishi1· PricillaMbiri1· NdahafaN.Hawanga1·
BordenMushonga1
Received: 9 January 2022 / Accepted: 4 October 2022
© The Author(s), under exclusive licence to Springer Nature B.V. 2022
Abstract
This study investigated outbreaks of seemingly related abortions and orchitis which occurred in the Khomas, Omaheke
and Otjozondjupa regions of Namibia from 2016 to 2018, affecting cattle, sheep and goats. Fifty-nine questionnaires were
administered, and 48 were completed giving an 81.4% return. The outbreaks were limited to Namibia’s east and central
regions, mainly on farms rearing cattle, sheep and goats and on farms with a mixture of these species. There was no signifi-
cant difference between Khomas and other regions on abortion reporting at the farm level [X2(1,N = 48) = 0.0002,p = 0.9
87851]. However, there was a significant difference in the abortions at the animal level among the three regions [X2(2,N
= 6246) = 239.8339,p = .00001]. In addition, the proportions of abortions calculated at the animal level at each farm were
significantly different when the Khomas region was compared to the other regions. Seventeen cattle sera, 35 sheep sera, 52
caprine sera, 18 bovine liver samples, one caprine liver, five aborted cattle foetuses, two cattle placentas, 18 testes (one bull,
eight bucks and nine rams) and ten bull sheath scrapings were collected and tested. Histopathology, microbiology, serology,
immunohistochemistry, real-time PCR and mineral analytical techniques were used to establish the aetiology of the abortion
and orchitis outbreaks. The gross and histopathological findings on the 18 testicles were characteristic of chronic orchitis.
In aborted foetuses, significant histopathological findings included meconium aspiration, funisitis and cardiomyopathy.
Placentitis and endometritis were the primary pathologies observed in cows. The bacteria isolated from microbiological
samples included Enterococcus spp. (65.5% [19/29]), Enterobacter spp. (6.9% [2/29]) and Streptococcus spp. (10.3% [3/29]),
Trueperella pyogenes (3.4% [1/29]), Stenotrophomonas maltophilia (3.4% [1/29]), Staphylococcus epidermidis (3.4% [1/29]),
Providencia rettgeri (3.4% [1/29]) and Acinetobacter lwoffii (3.4% [1/29]), mostly opportunistic bacteria. On mineral analysis,
28%, 33%, 83%, 33% and 17% (n = 18) of cattle livers were low in copper, zinc, manganese, selenium and iron, respectively.
Twenty-three percent (12/52) of the caprine sera were positive for Brucella melitensis on the Rose Bengal and complement
fixation tests. Thirty-five ovine sera were tested for B. melitensis, B. ovis and Coxiella burnetii, and the prevalence for each
was 2.9% (1/35). PCR tests on foetuses were all negative for Brucella spp., Coxiella burnetii, Chlamydia spp., Listeria
monocytogenes, Salmonella spp., Campylobacter fetus spp., Leptospira pathogenic strains, bovine viral diarrhoea virus,
Rift Valley fever virus, Anaplasma phagocytophilum and bovine herpes virus 4 Campylobacter fetus spp. and Trichomonas
foetus spp. The authors concluded that Brucella spp., Enterococcus spp., Escherichia coli, Streptococcus spp., Trueperella
pyogenes and Coxiella burnetii could have contributed to this outbreak. Micronutrient imbalances and pathogenic abiotic
nanoparticles were also identified as possible contributors to the abortion outbreaks.
Keywords Abortions· Orchitis· Outbreak· Cattle· Sheep· Goats· Namibia
Introduction
Tibary (2021) defined abortion as the termination of preg-
nancy before the foetus is viable and after organogenesis has
been completed (Tibary, 2021). In cattle, abortion is defined
as an expulsion of a non-viable foetus between days 43 and
* Alaster Samkange
alastersamkange@gmail.com
Extended author information available on the last page of the article
Tropical Animal Health and Production (2022) 54:346
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260 of pregnancy, whilst stillbirth is the expulsion of a foetus
after gestation day equal to or greater than 260days (Wolf-
Jäckel etal., 2020). Causes of livestock abortions can be clas-
sified into infectious and non-infectious causes, including
physical, chemical and biological causes. Chemical causes
include nutritional and toxic, whilst biological non-infectious
causes include genetic, hormonal, immunological and iatro-
genic (Ghalmi etal., 2009; Derdour etal., 2017).
In general, infectious causes of abortions include bacterial,
viral, protozoal, rickettsial, chlamydial or mycotic causes (Par-
kinson etal., 2019). Specifically, common infectious causes
of abortion in cattle and small ruminants (sheep and goats)
include viruses: bovine herpesvirus 1 (IBR/IPV) (Vermunt
etal., 2019), bovine herpesvirus 4 (Derdour etal., 2017),
bovine viral diarrhoea virus-1 (BVDV) (Bulut etal., 2017;
Derdour etal., 2017; Tulu etal., 2018), bluetongue, Akabane
virus (Parkinson etal., 2019), Rift Valley fever (Gerdes,
2004), Q-fever (Derdour etal., 2017; Bishi etal., 2018; Tulu
etal., 2018), Schmallenberg virus (Molini etal., 2018; Sibhat
etal., 2018) and Border disease virus (Dun, 2019). Bacte-
rial causes of abortion in cattle and small ruminants include
Leptospira interrogans serovar Hardjo (Grooms, 2006; Der-
dour etal., 2017; Tulu etal., 2018), Brucella (Derdour etal.,
2017; Ndazigaruye etal., 2018; Tulu etal., 2018, 2020),
listeriosis (Tulu etal., 2018), Salmonella Dublin (Derdour
etal., 2017; Dun, 2019), Campylobacter jejuni (Dun, 2019)
and Chlamydophila (Chlamydia) abortus (Samkange etal.,
2010; Dun, 2019). Protozoal causes include Neospora cani-
num (Reichel etal., 2013; Derdour etal., 2017; Tulu etal.,
2018; McAllister, 2020) and trichomoniasis (Dąbrowska
etal., 2019). In addition, Aspergillus fumigatus has also been
reported to cause abortions (Tulu etal., 2018).
In addition to abortions, Chlamydophila (Chlamydia)
abortus, Trueperella pyogenes (Ponnusamy etal., 2017),
Brucella spp. (Saxena etal., 2018) and Corynebacterium
pseudotuberculosis can also cause epididymitis and orchitis
(Bell, 2006; Kováčová etal., 2007; Umer etal., 2017; Stewart
etal., 2018). Actinobacillus seminis is also known to cause
epididymo-orchitis in rams and bucks (Dos Santos etal.,
2014), whilst Salmonella enterica serovar Typhimurium
caused epididymo-orchitis in a bull (Mahmoud etal., 2020).
During 1991–1992, Namibia had an outbreak of abor-
tions, stillbirths and neonatal deaths in cattle, sheep and
goats on 119 commercial farms in the central regions (P.A.
Basson, unpublished information). Enterococcus casselifla-
vus was the primary pathogen isolated in 30 of the 91 speci-
mens. However, experimental inoculation of this bacterium
into pregnant cows did not cause abortions (P.A. Basson,
unpublished data). From late 2016 until early 2018, many
farms in the central regions of Namibia experienced out-
breaks of abortions and orchitis in cattle, sheep and goats.
These were so widespread and caused very high reproduc-
tive losses, which in turn caused an outcry in the country to
such an extent that it made news headlines in the local press
(Staff Reporter, 2017).
This study aimed to investigate the possible causes of the
outbreaks of abortion associated with orchitis that occurred
in the central regions of Namibia from 2016 to 2018 in cat-
tle, sheep and goats by collating and analysing all available
data and information.
Materials andmethods
Study area
The study area included some commercial farms in the
Khomas, Omaheke and Otjozondjupa regions of Namibia
(Fig.1).
Study animals
The study animals were breeding cattle (Bos taurus) in the
affected regions, which experienced reproductive losses like
abortions, stillbirths, orchitis or epididymo-orchitis. In addi-
tion, sheep (Ovis aries) and goats (Capra aegagrus hircus)
which experienced similar signs were also included.
Data collection
Questionnaires were administered at 59 commercial farms
in the affected regions.
Two questionnaire-based surveys were conducted by
the Directorate of Veterinary Services (DVS) (Annexure
1) of Namibia and the Namibia Agricultural Union (NAU)
(Annexure 2), mainly in the Khomas region as well as
in three other regions (Otjozondjupa, Omaheke and
Kunene). Farms that had recorded abortions and those
not affected were purposively selected for investigation.
The number of questionnaires returned to DVS and NAU
was 21 and 27, respectively. All the selected farmers were
visited by DVS staff and interviewed; hence, the turnout
was 100%. Conversely, questionnaires sent out to farmers
for completion by NAU were 38, and the response rate
was 71%. Both questionnaires are annexed (Annexure 1
and Annexure 2) and were pretested initially to ensure
clarity and a good understanding of the questions. There
were no challenges in responding to the questionnaires.
The questionnaires administered by DVS and NAU were
different but had similar content, enabling the merging of
the statistical fields. The questionnaires from DVS and
NAU were sent to different farmers. The DVS question-
naires were administered by veterinarians and veterinary
para-professional staff, whereas the farmers completed
the NAU questionnaires. However, the data was later
merged. Data from 48 questionnaires were eventually
Tropical Animal Health and Production (2022) 54:346
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analysed. The data collected included the location of
the farm (region), types of animals on the farm and their
numbers, history of abortions and orchitis, feeding and
grazing status, water sources, vaccination history and
details of any new animals brought into the establish-
ment. The data collected was captured onto a Microsoft
Excel 2013 spreadsheet and analysed.
Laboratory samples were collected from 10 farms, all
of which had reported cases of abortions, stillbirths or
orchitis. The samples were sent to the Central Veterinary
Laboratory (CVL) located in Windhoek (Namibia). Some
were sent to Diagnostix—Veterinary Pathology Services
(South Africa) or Onderstepoort Veterinary Institute in
South Africa. These samples included sera, placentas,
foetuses, testicular swabs, organs in 10% formalin, liver
samples, sheath washes and orchitic testes (Table1). The
CVL could not perform all the required tests; therefore,
some samples were sent to South African diagnostic
laboratories. Laboratory tests on submitted samples
included immunohistochemistry, real-time polymerase
chain reaction (RT-PCR), bacterial culture, histopathol-
ogy, mineral analyses on liver samples and serology tests
(Rose Bengal test and complement fixation test). Post-
mortem examinations of orchitic testicles collected from
culled animals (bulls, rams and bucks) were also done;
appropriate microbiology and histopathology samples
were collected and sent for laboratory analysis. A total
of 18 testes (one bull, nine rams and eight bucks) were
examined this way. A total of 226 samples were analysed
at the CVL, Vet Diagnostix—Veterinary Pathology Ser-
vices (South Africa) or Onderstepoort Veterinary Insti-
tute (South Africa) or Pathcare (South Africa) (Table1).
The laboratory test results were collected, collated and
then captured on Microsoft Excel and analysed.
Fig. 1 The map of Namibia depicting all the regions of the country; the three regions of Otjozondjupa, Omaheke and Khomas are shown in the
central areas of the country (source: https:// www. mappr. co/ count ies/ namib ia/; used with permission)
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Data analysis
Descriptive statistics, Fisher’s exact test and Student’s t test
were used for analysing the data.
Results
Questionnaire data
A total of 72.9% (35/48) of the respondents were from the
Khomas region, and the remaining 27.1% (13/48) were from
Kunene, Omaheke and Otjozondjupa regions. About 72.9%
(35/48) of the respondents reported abortions on their farms
(Table2). The data were analysed using the Chi-square test
for a 3 × 2 contingency table to determine the association
between region and abortion. Regarding reporting abor-
tion, there was no significant difference between Khomas
and other regions [X2(1,N = 48) = 0.0002,p = 0.987851].
Table3 shows the 25 farms that experienced abortions
and reported the number of breeding cows on their respec-
tive farms, excluding farms that did not provide the num-
ber of breeding cows. There was a significant difference in
the abortions at the animal level among the three regions
when the data was subjected to a Chi-square test for a 3 × 2
contingency table [X2(2,N = 6246) = 239.8339,p = 0.0000
1]. However, there was no significant difference at the farm
level.
The Khomas region had the highest average animal-level
percentage of abortions (Table4). At the worst affected
farm, 77.6% (180/232) of the breeding cows aborted, fol-
lowed by others which had 47.3% (52/110), 37.4% (40/70)
and 15% (15/100). The second highest affected area at the
animal level was the Omaheke region (4.2%), ranging from
2.5 to 12%.
Twelve farms reported abortions according to par-
ity (Table5). Most abortions were observed in heifers 98
Table 1 A summary list of types and numbers of samples collected
and analysed
* Foetal organs, uterine contents, placentas, lymph nodes and testicles
** Foetal organs
*** Foetal organs, testes, livers, uterus and placentas
Samples Bovine Ovine Caprine Totals
Bacterial culture* 22 16 5 43
Liver mineral analysis 18 1 - 19
Histopathology** 14 6 4 24
PCR/RT-PCR*** 4 1 2 7
IHC (foetuses) 1 - - 1
Gross pathology (testes) 1 9 8 18
Sheath washes 10 - - 10
Sera 17 35 52 104
Totals 87 68 71 226
Table 2 Summarised abortion
figures on cattle farms that
responded
Region No. of
respond-
ents
Number of farms
reporting abortions
% of farms
reporting abor-
tions
Number of
abortions
Average number of
abortions per farm
Khomas 35 26 74.3% 782 30.1
Kunene 1 0 0.0% 0 0
Omaheke 7 5 71.4% 31 6.2
Otjozondjupa 5 4 80.0% 9 2.3
Total 48 35 72.9% 822 23.5
Table 3 Animal-level abortions
at farms where abortions were
reported
Region Number of breed-
ing cows
Number of farms
reporting abortion
Number of abor-
tions in 2017
Percentage of
abortions in
2017
Khomas 4092 16 569 13.9%
Omaheke 736 5 31 4.2%
Otjozondjupa 1418 4 9 0.6%
Grand Total 6246 25 609 9.8%
Table 4 Summary of distribution of abortions at the animal level
comparing Khomas to other regions
Region Number of
farms
Min percentage
abortion at farm
Max percentage
abortion at farm
Khomas 16 0.3% 77.6%
Others 9 1.0% 12.0%
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(49.5%), followed by second calvers 82 (41.4%) and, lastly,
third or later calvers 20 (10%). Unfortunately, the total num-
ber of animals in each parity category was unavailable for a
valid comparison.
Orchitis was reported in only three cattle farms in the
Khomas region. On one of the farms with eight affected
bulls, 5.5% (12/220) of the cows aborted, whilst on the
other farm with four cases of orchitis, 77.6% (180/232) of
the cows had aborted. The third farm, which did not specify
the number of orchitis cases, had four cows which aborted.
Pregnancy andcalving percentages
Focusing on 2017 data, the year when most abortions were
reported, the pregnancy percentage between farms that
reported abortion and those that did not, the one-tail t test
showed no significant difference (p = 0.14). However, there
was a significant difference in calving percentages between
the two categories of farms (p = 0.047), indicating that abor-
tion significantly impacted calving percentages in that year.
Potential risk factors investigated
The questionnaire surveys investigated other potential risk
factors and management practices that could have contrib-
uted to abortion outbreaks. These included introducing new
breeding animals and contact with other animal species;
non-vaccination against brucellosis; whether bull testing
for campylobacteriosis and trichomoniasis was practised;
comorbidity; continuous breeding; provision of supplemen-
tary feeding; grazing; and watering conditions (Table6).
The Fisher’s exact test was used to establish any association
between sixteen risk factors and the occurrence of abortions.
None of these factors was statistically significant except the
introduction of new breeding animals (p < 0.05).
Gross pathology
The bulls, rams and bucks with orchitis had bilateral or
unilateral hard or doughy swollen testes (Figs.2 and 3).
The gross lesions included severe enlargement of the scro-
tal contents (Figs.2, 3 and 8), fibrous adhesions between
testicular tunics (Figs.4, 5, 9, 13, 14and15), multiple
testicular and epididymal abscesses with purulent exudate
(Figs.9 and 14) and foci of fibrosis and calcification
(Figs.4 and 11). Some affected testes appeared necrotic
and oedematous (Figs.6, 7, 8, 10 and 11). Necrosis of
the testicular parenchyma with caseous and haemorrhagic
exudate and some epididymis revealed multifocal sper-
matic granulomas affecting the normal tubular architec-
ture (Fig.12). Some of the testes showed fibrosis of the
tunica vaginalis (Figs.4, 5, 6, 9, 10, 11, 12, 13, 14 and
15). Some testicular samples had multiple haemorrhagic
foci on the cut surface; peri-testicular ecchymotic haem-
orrhages around the tunica vaginalis were also observed
(Figs.6, 7 and 15).
Histopathology
Histopathological findings of various tissues examined in
the laboratory are summarised in Table7. Testicular samples
were diagnosed with chronic orchitis, testicular degeneration
and chronic epididymitis. Abnormalities in histopathology
included the abnormal architecture of the testicular struc-
tures, large foci of necrotic testicular tissue with minerali-
sation, moderate-to-severe presence of fibrous connective
tissue and prominent interstitial mononuclear inflammatory
cell infiltration with a few multinucleated inflammatory
cells. In addition, some testicular samples showed subacute
testicular degeneration with seminiferous tubules containing
mainly desquamated germinal epithelial cells and very few
spermatozoa and mineralisation.
Histopathological diagnoses for other samples mainly
included necrotising placentitis and meconium aspiration.
Bacterial culture
As shown in Tables8 and 9, twenty-one different bacte-
rial species were isolated from the 43 microbiological
samples (Table1) submitted to the laboratory. These sam-
ples included placentas, foetal organs and swabs collected
from orchitic testes. The bacterial isolates in abortion cases
(Table9) were mostly Enterococcus spp. (65.5% [19/29]),
Enterobacter spp. (6.9% [2/29]) and Streptococcus spp.
(10.3% [3/29]). The rest were at (3.4% [1/29]) each and
included Trueperella pyogenes, Stenotrophomonas malt-
ophilia, Staphylococcus epidermidis, Providencia rettgeri
and Acinetobacter lwoffii.
Eleven species of bacteria were isolated from cases of
epididymo-orchitis in bulls, rams and bucks (Table9).
The main genera of pathogens that were cultured included
Streptococcus spp. (47.4% [9/19]), Brucella spp. (10.5%
[2/19]), Enterococcus spp. (21.1% [4/19]) and E. coli
(5.3% [1/19]). Enterococcus spp. were isolated from cat-
tle and goats; Streptococcus spp. were cultured from all
three species (cattle, sheep and goats), but Brucella spp.
and E. coli were both isolated from bucks. The rest of
Table 5 Distribution of abortions by parity
Parity 1st calver 2nd calver 3rd or more Total
No. of reporting farms 6 4 2 12
No. of abortions 98 (49.5%) 82 (41.4%) 20 (10.0%) 200
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the isolates included Staphylococcus pseudintermedius
(bull), Sphingomonas paucimobilis (ram) and Pantoea
spp. (ram), which were isolated once, each 5.3% across
the two livestock species.
Polymerase chain reaction (PCR)
A total of five aborted foetuses and two placentas from
two farms were tested using PCR. The reason was that
those were the only farms that availed specimens deemed
suitable for the test. The following pathogens were tested
using either PCR or real-time PCR: Brucella spp., Cox-
iella burnetii, Chlamydia spp., Listeria monocytogenes,
Salmonella spp., Campylobacter fetus spp., Leptospira
pathogenic strains, bovine viral diarrhoea virus, Rift Val-
ley fever virus, Anaplasma phagocytophilum and bovine
herpes virus 4. In addition, sheath scrapings from 10
bulls were also tested for Campylobacter fetus spp. and
Trichomonas foetus spp., with negative results. All sam-
ples yielded negative results for the pathogens tested.
Mineral analysis
A total of 19 liver samples (18 bovine and 1 ovine)
from 19 farms were each tested for levels of copper,
zinc, manganese, selenium and iron (Table10). For the
bovine samples, 28% (5/18), 33% (6/18), 83% (15/18),
33% (6/18) and (17%) 3/18 were low in copper, zinc,
manganese, selenium and iron, respectively; another
33% (6/18) were high in iron.
The one ovine liver sample was low in zinc and man-
ganese but high in iron.
Table 6 Summary of risk
factors SN Factors No. of farms expe-
riencing abortion
No. of farms not
experiencing abor-
tion
1 New breeding cattle introduced 14 7
No new breeding cattle introduced 3 2
2 Contact with other cattle 9 5
No contact with other cattle 8 4
3 Contact with other animal species 12 8
No contact with other animal species 19 6
4 Not vaccinated against brucellosis 23 8
Vaccinated against brucellosis 12 5
5 No bull, rams and bucks testing for reproductive disease 14 9
Bull, rams and bucks testing for reproductive disease 17 8
6 Comorbidity present 7 5
Comorbidity not present 10 5
7 Continuous breeding throughout the year 17 7
Defined breeding season 14 9
8 Supplementation 26 8
No supplementation 5 3
9 Good grazing 2015 8 6
Poor grazing 2015 9 4
10 Poor grazing 2016 11 5
Good grazing 2016 6 5
11 Water not tested 4 5
Water tested 13 5
12 No water abnormality detected 9 2
Water abnormality detected 1 0
12 Dam water present 11 3
No dam water present 6 7
14 Surface water present 3 1
No surface water present 14 9
15 Presence of game on farm 7 2
Absence of game on farm 9 5
16 Presence of poisonous plants 14 6
Absence of poisonous plants 2 1
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Serology
Table11 summarises the serological test results of 104 sam-
ples collected from one of the farms severely affected by
abortions and epididymo-orchitis in cattle, sheep and goats.
The 17 bovine sera were tested for Brucella abortus
and B. melitensis using the Rose Bengal test (RBT), with
negative results. A total of 23% (12/52) caprine sera were
positive for Brucella melitensis on both the RBT and com-
plement fixation test (CFT) but were negative for Brucella
ovis. An ELISA test was also used to test the 52 caprine
samples for Chlamydia abortus, which were all negative.
The 35 ovine sera were tested for B. melitensis (RBT), B.
ovis (RBT) and Coxiella burnetii (ELISA); there was one
positive case in each.
Other tests
Samples of one cow and its foetus’ organs sent to South
Africa were tested for Coxiella burnetii and Chlamydia
abortus using immunohistochemistry, and the results were
Fig. 2 A swollen globular shaped right testicle of a ram with orchitis
Fig. 3 A fistulous tract through the scrotum of a ram with severe
epididymitis and orchitis
Fig. 4 Fibrous hypertrophy of tunica vaginalis and fibrotic testicular
parenchyma in the testes from a buck
Fig. 5 A ram testicle showing bulges on the cut surface, testicular
parenchyma appears uniformly necrotic and reddish in colour; the
tunica vaginalis is hyperplastic and fibrotic
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negative. Tissues from another aborted foetus were also
sent to South Africa, where they were subjected to modi-
fied Ziehl–Neelsen staining and culture for Mycobacterium
spp. The results were also negative.
Discussion
According to Bagley (1999) and Tulu et al. (2018),
abortion levels of up to 2% in cattle are acceptable, but
upwards of 3–5% warrant investigation and intervention
to curtail further losses (Bagley, 1999; Tulu etal., 2018).
Some studies have reported average abortion rates ranging
from 4.55% in sheep to 5.61–11.86% in cattle (Abdelhadi
etal., 2015; Dechicha etal., 2020). There is, therefore, no
question that abortion figures of up to 77.6% at the animal
level, which are reported in this study, were very high and,
therefore, constituted an outbreak that warranted further
investigation.
A definitive diagnosis of the cause of abortion often pre-
sents a challenge because of the many infectious and non-
infectious causes which may be involved (Kumar etal., 2015;
Tulu etal., 2018). Abortion also often follows an initial infec-
tion that may have occurred several weeks or months before.
Thus, the causal agent is often undetectable when the abor-
tion occurs (Tulu etal., 2018). The high cost of laboratory
work to diagnose abortion also compounds the problem (Tulu
etal., 2018). Some investigations on causes of abortions have
found that a significant proportion is due to unknown causes,
with some authors determining figures ranging from 47 to
67% (Macías-Rioseco etal., 2020; Wolf-Jäckel etal., 2020) in
cattle, 42% in sheep and 56% in goats (Van Den Brom etal.,
2012). Macías-Rioseco etal. (2020) investigated abortions in
dairy cattle in Uruguay and determined the aetiology in only
53% (54/102) of cases. Infectious agents implicated included
Neospora caninum, Coxiella burnetii, Campylobacter fetus
subsp. venerealis, bovine parainfluenza-3 virus, bovine viral
diarrhoea virus, Salmonella enterica serovar Newport and
Leptospira interrogans. In addition, opportunistic bacteria
like Escherichia coli, Streptococcus spp., Staphylococcus
spp., Mannheimia spp., Trueperella pyogenes and Providen-
cia stuartii were also found (Macías-Rioseco etal., 2020).
One study demonstrated serological evidence of mixed infec-
tions in cattle among abortifacient agents, raising the poten-
tial for their synergism (Okumu etal., 2019).
Fig. 6 A ram testicle showing a necrotic testicular parenchyma with
ecchymotic haemorrhages of the head of the epididymis; a necrotic
and oedematous tail of the epididymis with multiple fluid-filled cysts
Fig. 7 A buck testicle show-
ing necrosis and peri-testicular
ecchymotic haemorrhages
around the tunica vaginalis
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In the current study, most bacterial agents isolated are
opportunistic and not among the major abortifacient spe-
cies. This could be attributed to other underlying factors
predisposing the animals to these infections, as noted later
in this discussion. Furthermore, the high abortion rates
recorded in cattle in this study in the absence of Brucella
abortus as a prominent pathogen could be because, in
Namibia, cattle producers must vaccinate their cattle against
brucellosis. Therefore, this renders this pathogen an unlikely
significant contributor to this outbreak due to herd immunity.
Our results indicate that 72.9% of surveyed farms
experienced abortions, which is relatively high compared
to 37.3% in Algeria (Ghalmi etal., 2009). The higher
abortion percentage in the current study could be due
Fig. 8 Multiple haemorrhagic foci on the cut surface of a buck’s testi-
cle; the head of the epididymis appears haemorrhagic
Fig. 9 A buck testicle with a cavity containing purulent exudate; the
tunica vaginalis appears fibrotic
Fig. 10 Severe and diffuse
necrotic testicular parenchyma
in a ram with orchitis
Fig. 11 A ram testicle with focal testicular cavity filled with suppura-
tive exudate; the testicular parenchyma appear fibrotic
Fig. 12 A buck’s left testicle with multiple necrotic cavities with
nodular raised lesions in the testicular parenchyma with suppurative
exudate; epididymal spermatic granulomas
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to the outbreak of abortions experienced at the time of
the survey.
Twenty-three percent (12/52) of the caprine sera tested
were positive for B. melitensis. This pathogen is a known
cause of abortions in sheep and goats (Das etal., 2008;
Ndazigaruye etal., 2018). B. melitensis is an impor-
tant cause not only of abortions but also of orchitis and
epididymitis in sheep and goats. Furthermore, it has been
demonstrated that B. melitensis can be a significant cause
of abortion in cattle in mixed farming practices (Deng etal.,
2020). In the areas covered in the current study, mixed
farming practices involving cattle and small ruminants
(sheep and goats) are the norm rather than the exception.
This might explain the abortions observed in cattle and
small ruminants on some farms.
Di Blasio and coworkers isolated several of what they
referred to as neglected opportunistic infections as causes
of abortion. These included Escherichia coli, Acinetobac-
ter lwoffii, Staphylococcus spp., Streptococcus spp., Strep-
tococcus uberis, Streptococcus suis, Trueperella pyogenes,
Mannheimia haemolytica, Bacillus cereus and Nocardia
spp. The authors concluded that these pathogens should be
considered emerging and considered alongside the major
infectious players in bovine and caprine reproductive failure
(Di Blasio etal., 2019).
In the current study, Trueperella pyogenes was isolated
only once from a cow abortion case (Table9). T. pyogenes
is a normal inhabitant of domestic animals’ respiratory, uro-
genital and gastrointestinal tracts, and it, therefore, causes
opportunistic infections (Ponnusamy etal., 2017; Di Blasio
etal., 2019; Macías-Rioseco etal., 2020). However, it is rec-
ognised as a critical etiological agent in bovine endometritis
and metritis (Goldstone etal., 2014); it has also been impli-
cated in sporadic abortions (Ponnusamy etal., 2017; Wolf-
Jäckel etal., 2020). In some studies, T. pyogenes was found
Fig. 13 Buck testicle with oedematous fluid within the epididymis,
the tunica vaginalis and the testicular parenchyma appears fibrotic
Fig. 14 Ram testicle with a focal necrotic lesion in the testicular
parenchyma with caseous exudate; there is haemorrhagic exudate of
the head of the epididymis
Fig. 15 Haemorrhagic exudate of the epididymis head of a ram testi-
cle; the testicular parenchyma and tunica vaginalis are fibrotic
Table 7 Summary of histopathological features in the samples exam-
ined
Histopathological diagnosis Bovine Ovine Caprine Total
Necrotising placentitis 2 - - 2
Meconium aspiration 2 - - 2
Hyperplastic goitre 1 - - 1
Foetal cardiomyopathy 1 - - 1
Thymic atrophy 1 - - 1
Chronic epididymitis 1 - - 1
Chronic orchitis & testicular
degeneration
1 5 4 10
Total 9 5 4 18
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Page 11 of 15 346
to account for 3% (5/162) to 10% (27/280) of cases of bovine
abortions which were studied (Syrjälä etal., 2007; Wolf-
Jäckel etal., 2020). It is, therefore, reasonable to assume that
T. pyogenes was the cause of abortion in this particular case.
A total of 63.3% (19/30) of bacterial culture results yielded
various species of Enterococcus as the abortive agents, pre-
dominantly E. mundtii 26.7% (8/30), E. casseliflavus and E.
gallinarum each at 10% (3/30). In an earlier study on livestock
abortion outbreaks in Namibia from 1991 to 1992, E. casselifla-
vus was isolated in 33% (30/91) of the culture samples (Basson,
unpublished data). In another study of the causes of abortions in
small ruminants, E. casseliflavus was identified as an abortive
agent, among other infectious causes (Schnydrig etal., 2017).
In another study, Enterococcus species were isolated in mastitic
cow milk and from the genital tracts of aborted women (Hamzah
and Kadim, 2018). It is, therefore, possible that Enterococcus
spp. could cause abortions in women and livestock. Enterococ-
cus spp., therefore, cannot be ruled out as being responsible for
at least some of the abortions encountered in the current study.
Streptococcus suis was only isolated from one bovine foe-
tus in the current study and is also generally regarded as an
opportunistic infection in ruminants (Macías-Rioseco etal.,
2020). There is, however, a report where it was implicated
as the cause of a bovine abortion case (Higgins etal., 1990).
It is, therefore, plausible that S. suis was a possible cause of
abortion in this case.
Table 8 Summary of bacterial
culture results for abortion cases Bacteria isolated Bovine Ovine Caprine Total Percent
Enterococcus casseliflavus 3 0 0 3 10.3
Enterococcus mundtii 8 1 0 9 31.0
Enterococcus sulfureus 1 0 0 1 3.4
Enterococcus gallinarum 3 0 0 3 10.3
Enterococcus faecalis 1 0 0 1 3.4
Enterococcus faecium 2 0 0 2 6.9
Enterobacter spp. 2 0 0 2 6.9
Stenotrophomonas maltophilia 1 0 0 1 3.4
Staphylococcus epidermidis 1 0 0 1 3.4
Trueperella pyogenes 1 0 0 1 3.4
Providencia rettgeri 1 0 0 1 3.4
Acinetobacter lwoffii 1 0 0 1 3.4
Streptococcus agalactiae 1 0 0 1 3.4
Streptococcus suis 1 0 0 1 3.4
Beta and alpha Streptococcus group D 0 0 1 1 3.4
Total 27 1 1 29 100.0
Table 9 Summary of bacterial culture results for epididymo-orchitis
cases
Bacteria isolated Bovine Ovine Caprine Total
Enterococcus casseliflavus 1 0 0 1
Enterococcus gallinarum 1 0 0 1
Enterococcus faecium 1 0 0 1
Enterococcus spp. 0 0 1 1
E. coli 0 0 1 1
Staphylococcus pseudintermedius 1 0 0 1
Sphingomonas paucimobilis 0 1 0 1
Pantoea spp. 0 1 0 1
Streptococcus thoraltensis 0 3 0 3
Streptococcus spp. 1 3 2 6
Brucella spp. 0 0 2 2
Total 5 8 6 19
Table 10 Summary of mineral analysis results of 19 liver samples
from 19 farms
Mineral Level Bovine Ovine Totals
Low 5 - 5
Copper Normal 12 1 13
High 1 - 1
Low 6 1 7
Zinc Normal 3 - 3
High 9 - 9
Low 15 1 16
Manganese Normal 3 - 3
High - - 0
Low 6 - 6
Selenium Normal 12 1 13
High - - 0
Low 3 - 3
Iron Normal 9 - 9
High 6 1 7
Total 90 5 95
Tropical Animal Health and Production (2022) 54:346
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346 Page 12 of 15
Streptococcus spp., Enterococcus spp., Brucella spp. and
E. coli were the most significant bacteria isolated from cases
of epididymo-orchitis in bulls, rams and bucks. However,
Brucella spp. and E. coli were only isolated from bucks.
Streptococcus spp. can cause orchitis and overt testicular
abscessation in cattle (Mahmoud etal., 2020) and epididymi-
tis in rams (Searson, 1976). The genus Brucella has a great
tropism for the genitourinary system of cattle, goats, sheep
and pigs, which is caused by the high concentration of eryth-
ritol in the testicular and placentary tissues of these animals
(Colmenero etal., 2007). In particular, Brucella ovis has a
predilection for the genital tract of sheep where it causes
epididymitis and, rarely, abortions (Ridler and West, 2011).
Brucella abortus, Mycobacterium tuberculosis, Trueperella
pyogenes, Histophilus somni, bovine herpes virus 1 (IBR/
IPV) and Mycoplasma spp. have been implicated as the most
common causes of orchitis in bulls (Bell, 2006; Mahmoud
etal., 2020). Some authors contend that epididymo-orchitis
is rare (approximately 1%) in breeding bucks and that B.
melitensis and Corynebacterium pseudotuberculosis are the
commonest causes (Stewart and Shipley, 2014).
It is therefore reasonable to assume that the Brucella spp.
that were isolated in the current study were at least partially
responsible for some of the cases of epididymo-orchitis that
were observed in bucks in this study. Enterococcus spp. along
with other bacteria like Pseudomonas spp. and Klebsiella
spp. have also been implicated in causing epididymo-orchitis
in man (Ryan etal., 2018), but no study has implicated this
bacteria as a cause of the condition in domestic animals.
However, the current study has demonstrated that Entero-
coccus spp. should be considered as a cause of epididymo-
orchitis in bulls, rams and bucks, as well as abortions.
In the current study, the number of bovine liver samples
with low levels of copper, zinc, manganese, selenium or iron
ranged from 17%, for iron, to 83% for manganese. Trace ele-
ment deficiencies have also been implicated in causing abor-
tions (Kumar etal., 2015). Minerals such as copper, cobalt,
selenium, manganese, iodine, zinc and iron can influence the
reproductive performance of ruminants (Kumar etal., 2015;
Zekarias etal., 2019) and have been reported to be a predis-
posing factor for the occurrence of retention of placentas and
repeat breeding in dairy cows, abortion and weak calf syn-
drome (Yasothai, 2014; Balmurugan etal., 2017). However,
the progesterone metabolite allopregnanolone has also been
implicated in the pathogenesis of weak calf syndrome (Riedel
etal., 2018), although other authors suggest a genetic predis-
position (Zepeda-Batista etal., 2018). In another study, low
zinc and high copper serum levels were associated with an
increased risk of foetal loss (Graham etal., 1994). Copper
deficiency has also been reported to be associated with early
embryonic death and resorption of the embryo, increased
chances of retained placenta and necrosis of the placenta
(Yasothai, 2014).
Therefore, it would appear from the mineral results that
micronutrient imbalances possibly contributed to the abor-
tion/stillbirth and epididymo-orchitis outbreak. Copper and
zinc deficiency appeared to be a common thread in all of
the results, and both minerals are essential for metabolism
and proper immune system function (Minatel, 2000; Fraker
and King, 2004). This might explain the many species of
bacteria which were isolated. The authors contend that in
utero growth retardation due to maternal malnutrition or
over-nutrition in conjunction with the immunosuppressive
effects of the micronutrient imbalances were significant
factors during this outbreak. The bull’s pathology could be
related to the underlying copper deficiency already noted.
Copper deficiency has a significant negative impact on the
male reproductive tract, and the immunosuppressive effects
would predispose to the development of epididymitis.
Swerczek and Dorton (2019) reported that mare
reproductive loss syndrome (MRLS) had been known to
affect horses in Kentucky for decades, causing, among
other things, outbreaks of spontaneous abortions. The
authors further noted that these foetal losses, with an
unknown aetiology but associated with MRLS, occurred
in mares and other livestock that were grazing in spring
pastures affected by climatic and environmental factors
like droughts, cold stress, nitrogenous fertilisers and
herbicides, factors that cause nitrate to accumulate in
these pastures. This excessive nitrate accumulation was
reported to result in toxic and pathogenic abiotic nano-
particles forming in the amniotic fluid and pathognomonic
placental lesions consistent with the MRLS. The authors
then hypothesised that this recently discovered mechanism
of action for the pathogenesis of foetal losses might be a
predisposing factor for a host of opportunistic diseases
Table 11 Serological test results
from one of the farms severely
affected by the outbreak of
abortions and epididymo-
orchitis
NT, not tested
Species No. of samples Brucella
abortus Brucella
melitensis Brucella ovis Chlamydia
abortus Coxiella
burnetii
Bovine 17 0 0 NT NT NT
Caprine 52 0 12 0 0 NT
Ovine 35 0 1 1 NT 1
Total 104 0 13 1 0 1
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Page 13 of 15 346
in livestock (Swerczek and Dorton, 2019). The Kentucky
scenario mirrors the circumstances of the outbreaks of
abortions in Namibia in 1991–1992 and 2016–2018.
The years 1991–1992 and 2015–2016 were marked by
severe droughts in Namibia (Devereux and Næraa, 1996;
Holloway, 2000; Kahiurika, 2016; van Rensburg and
Tortajada, 2021). It is, therefore, possible, as reported
by Swerczek and Dorton (2019), that these drought peri-
ods which preceded the major outbreaks of abortions in
the country could have resulted from excessive accumu-
lation of nitrate in the pastures, which when consumed
by pregnant animals, could have caused the formation of
toxic and pathogenic abiotic nanoparticles in the amniotic
fluid, thereby predisposing the pregnant animals to a host
of opportunistic infections resulting in the outbreaks of
abortions.
In conclusion, this study identified a multiplicity of
possible aetiologies of the reproductive problems that
occurred in the central regions of Namibia from 2016 to
2018. Any combinations of the causes identified in this
study could cause the observed outbreaks. However, why
these conditions occurred in these species, parts of the
country and during these related periods remains elusive.
Controlled focused studies of future abortions, orchitis and
epididymitis in specific animal species may shed light on
the temporal and spatial relationships of the reproductive
problems and their aetiologies.
Supplementary Information The online version contains supplemen-
tary material available at https:// doi. org/ 10. 1007/ s11250- 022- 03342-0.
Acknowledgements The authors would like to thank the Directorate
of Veterinary Services in Namibia for providing the data used for this
study. Our appreciation also goes to the Namibia Agricultural Union
and the University of Namibia for their tremendous support.
Author contribution All authors contributed to the study conception
and design. Material preparation and data collection and analysis were
performed by Alaster Samkange, Jolandie van der Westhuizen, Anselm
Siegfried Voigts, Frank Chitate, Israel Kaatura, Emmanuel H. Hikufe,
Juliet Kabajani, Alec S. Bishi and Ndahafa N. Hawanga. The first draft
of the manuscript was written by Alaster Samkange, and all authors
commented on previous versions of the manuscript. All authors read
and approved the final manuscript.
Data availability The datasets generated during and/or analysed during
the current study are not publicly available for confidentiality reasons
but are available from the corresponding author on reasonable request.
Code availability Microsoft Office 2013.
Declarations
Ethics approval The University of Namibia’s Research and Ethics
Committee provided a waiver for this study since it only involved the
use of secondary data.
Consent to participate Informed consent was obtained from all farmers
included in the study.
Consent for publication The authors affirm that the participating farm-
ers provided informed consent for publication of the data collected.
Conflict of interest The authors declare no competing interests.
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Authors and Aliations
AlasterSamkange1 · JolandievanderWesthuizen2· AnselmSiegfriedVoigts3· FrankChitate1· IsraelKaatura1·
SiegfriedKhaiseb2· EmmanuelH.Hikufe2· JulietKabajani2· AlecS.Bishi1· PricillaMbiri1· NdahafaN.Hawanga1·
BordenMushonga1
1 School ofVeterinary Medicine, Faculty ofHealth Sciences
andVeterinary Medicine, University ofNamibia, P. Bag
13301, Windhoek, Namibia
2 Directorate ofVeterinary Services, Central Veterinary
Laboratory, Private Bag 13187, Windhoek, Namibia
3 Windhoek Veterinary Clinic, 8 Lossen Street, P.O. Box5030,
Windhoek, Namibia
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