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. 2021 Oct 20;53(6):520. doi: 10.1007/s11250-021-02926-6

Abortive diseases and their various associated risk factors in small ruminants in Algeria: a systematic review

Asma Haif 1, Nadjet Amina Khelifi-Ouchene 2,3,✉, Manal Khelifi 4, Imane Ouchetati 5, Fayçal Zeroual 1, Nassim Ouchene 2,3
PMCID: PMC8526997  PMID: 34669051

Abstract

Abortive infections are a major health challenge affecting productive and reproductive performance of sheep and goats. However, there is no comprehensive summary on the occurrence and distribution of these infections in Algeria. This systematic review provides a comprehensive summary on the prevalence of different abortive diseases and assesses potential risk factors in small ruminants in Algeria. Five databases were used to search epidemiological data on the prevalence of different abortive diseases (bacterial, parasitic, and viral). Data were collected from 25 papers published between 2003 and 2020. The total mean sample size was 53,080 small ruminants. The majority of the diseases/infections were diagnosed by serological and molecular tests. The overall prevalence of brucellosis was 0.39% in sheep and 5.31% in goats. Chlamydia and Q fever were observed in 32.72% and 20.62% of small ruminants, respectively. The prevalence of peste des petits ruminants was 15.76% and the overall prevalence of bluetongue in sheep and goats was, respectively, 13.41% and 44.50%. Border disease and bovine viral diarrhea were detected in 22.68% and 1.01% of sheep examined, respectively. Toxoplasma gondii infection prevalence among sheep and goats was 21.43% and 32.31% respectively. This study is a comprehensive epidemiological analysis of abortion diseases in small ruminants in Algeria and will therefore be a useful tool for researchers. Larger and more robust prevalence studies are needed to adequately support risk assessment and management of animal and public health threats.

Keywords: Algeria, Abortive diseases, Goats, Sheep, Prevalence, Systematic review

Introduction

Abortion in small ruminants is one of the major problems that can cause considerable economic losses due to the death of fetuses and reduced milk production and it may occur sporadically or as enzootic outbreaks. The etiology may be infectious or non-infectious (Vidić et al. 2007; Entrican et al. 2009). Infectious abortions are the most common and are caused by bacteria (Chlamydia abortus, Campylobacter spp., Listeria spp., Coxiella burnetii, Brucella melitensis), virus (bluetongue virus; plague of small ruminants virus, border disease virus), and parasites (Toxoplasma gondii) (Celli and Gorvel 2004; Khan et al. 2011; Kaufmann et al. 2012; Martin et al. 2015; Tegegne et al. 2016; Elhaig et al. 2018; Tejedor-Junco et al. 2019). Abortions are also caused by non-infectious etiologies such as toxicities, genetic factors, metabolic and nutritional problems, and physical factors (Vidić et al. 2007).

The breeding of small ruminants is a primordial activity of the North African breeder (Rondia 2006) and is the main source of red meat in Algeria (Mebirouk-Boudechiche et al. 2014). Small ruminants are farmed under the traditional extensive system in Algeria, and intensive farming systems have recently been introduced in the country. The total number of sheep and goats in Algeria has been estimated in 2017 at 26.4 million and 4.8 million heads, respectively, which constitutes an important wealth for the country (MADR 2018) and contribute substantially to food security, to the economy of mountain households, to their maintenance in poor and inaccessible territories, and require a human presence in regions exposed to rural exodus (Ouchene-Khelifi et al. 2015; 2018). However, the breeding of small ruminants in Algeria is subject to several constraints, including abortions. Khaled and Bouyoucef (2013) have reported that 90% of Algerian farmers had observed abortions on their farms.

Therefore, a comprehensive overview of abortive diseases in small ruminants has become crucial for the development of effective prevention and control measures and for a better prevention of human contamination since most of these diseases are zoonoses.

A recent systematic review, pertaining to small ruminants diseases (Kardjadj 2017), concluded that the epidemiological status of small ruminant diseases in Algeria is striking and the main infectious diseases threatening its small ruminant industry are peste des petits ruminants, bluetongue, foot and mouth disease, sheep pox/goat pox, brucellosis, and Rift Valley fever.

This systematic review is solely focused on the prevalence of abortion causes in sheep and goats in Algeria and its association with several risk factors.

Material and methods

Literature search strategy

This systematic review and meta-analysis was structured according to the recommendations of the Preferred Reporting Elements for Systematic Reviews and Meta-analysis (PRISMA; Moher et al. 2009). The study included only articles published in English that analyzed the causes of abortion infection in small ruminants in Algeria. The search was conducted using five literature databases, including PubMed, Thomson Reuters, ScienceDirect, Scopus, and Google Scholar. The search criteria were specified in advance, and was executed on April 8, 2020, and last updated on July 7, 2020. The following keywords with different combinations were used for the search: “abortion” and “brucellosis” or “Brucella melitensis” or “chlamydiosis” or “Chlamydia abortus” or “Q fever” or “Coxiella burnetii” or “Campylobacteriosis” or “Campylobacter spp” or “salmonellosis” or “Salmonella spp” or “leptospirosis” or “Leptospira spp” or “listeriosis” or “Listeria spp” or “mycoplasmosis” or “Mycoplasma spp” or “pestivirus” or “peste des petits ruminants (PPR)” or “bluetongue virus (BTV)” or “Border disease virus (BDV)” or “Bovine virus diarrhea virus (BVDV)” or “toxoplasmosis” or “Toxoplasma gondii” or “neosporosis” or “ Neospora caninum” or “trichomonosis” or “Trichomonas fœtus” or “mycosis” or “Aspergillus spp” and “prevalence” or “epidemiology” and “risk factors” and “sheep” or “goat” or “small ruminants” and “Algeria.” The collected bibliographic references were screened carefully in order to eliminate duplicates. Also, the reference lists of reviews, and all the retrieved articles, were manually searched during the same period to maximize article recovery.

Eligibility criteria

An article was included if it fulfilled the following criteria: (1) Full text in the English language published online up to July 2020; (2) descriptive or cross-sectional study (or clarity of objective/s) (estimation of prevalence or otherwise); (3) research reporting the prevalence of different abortion causes in small ruminants and their risk factors using different methods (serological examination, parasite observation, or PCR detection of NA); (4) exact total sample size, positive samples, and the study period were available. Articles were excluded when any of the above criteria were not met. We did not consider redundant articles or data, conference abstracts, and review articles.

All identified studies from the searches were independently assessed for eligibility and inclusion by two different authors. Discrepancies were resolved by discussion and consensus. If required, authors were contacted for clarifying the eligibility of papers.

Data extraction

A suitable data extraction template was prepared to collect and organize information from each reviewed study. The information retrieved included first author, year of publication, animal species, geographical area of study, sample size (number of examined animals), number of cases, prevalence rate, type of simple, diagnostic tests used for the study, sensitivity and specificity of diagnostic tests, risk factors, and the year in which studies were carried out. If required, authors were contacted for additional information.

Results

Literature search result

Through this search, 25 papers published between 2003 and 2020 were identified, eligible to be included in our systematic review and meta-analysis study. The number of articles screened, excluded, and included in the meta-analysis is shown in the diagram (Fig. 1).

Fig. 1.

Fig. 1

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Flow diagram of the selection of eligible studies

Causes of abortion

Examination of these 25 studies revealed the existence of 10 different infectious and parasitic abortive diseases of small ruminants in Algeria, including four (4) bacterial diseases (brucellosis, chlamydiosis, Q fever, and salmonellosis), five (5) viral diseases (PPR, bluetongue, border disease, CAE, and BVDV), and one (1) parasitic cause (toxoplasmosis) (Table 1). No eligible studies were conducted on mycosis causes. Among the 25 studies, 3 reported multiple diseases (multiple pathogen survey).

Table 1.

Diseases categories, number of studies, and sample size of all eligible studies

Diseases categories No. of studies (%) Sample size (sheep and goats)
Bacterial diseases
  Brucellosis 06 (20) 33,205
  Chlamydiosis 05 (16.66) 1809
  Q fever 02 (6.66) 674
  Salmonellosis 01 (3.33) 43
Viral diseases
  PPR 04 (13.33) 8143
  Bluetongue 03 (10) 3022
  Border disease 01 (3.33) 2151
  CAE 01 (3.33) 105
  BVDV 01 (3.33) 197
Parasitic disease
  Toxoplasmosis 06 (20) 4980
  Total 25 (100) 54,330
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PPR pest des petits ruminants, CAE caprine arthritis encephalitis, BVDV bovine viral diarrhea virus

The total number of small ruminants included in these 25 studies was 54,330, of which 5080 (9.35%) were reported to be diseased and/or infected with one of the 10 reported infectious or parasitic diseases. The majority of diseases/infections were diagnosed by serological and molecular tests.

Spatial distribution of eligible studies

Out of the 25 studies, 9 (36%) were conducted in several regions across the country. Six (24%) studies were carried out in northeastern Algeria: 2 (8%) studies each in Constantine and Tebessa; 1 (4%) in Mila; and 1 (4%) study in the eastern highlands (Batna and Setif).

Five studies (20%) were conducted in north-central Algeria and the highlands: one study (4%) each in Djelfa, Tiaret, and Ksar El-Boukhari; and 2 studies (8%) were conducted along the highlands of central Algeria.

Two studies (8%) were carried out in the north-west of the country: one study (4%) in Mostaganem and the other in Sidi Belaabes.

The other three studies (12%) were carried out in the south of the country (the Sahara) and were distributed as follows: one study (4%) in the north of the Sahara (Ghardia) and two studies (8%) in the south-west of the Sahara (Tindouf and Beni-Abbes).

Distribution of studies over time

Examining the distribution of published studies over time, it was found that 23 studies (92%) were conducted and published from 2011 to the present. However, only two studies (8%) were published before this date.

Determination of abortive diseases

Bacterial diseases

A total of 14 papers (Table 2) reported the prevalence of bacterial abortive diseases, and their risk factors in small ruminants included 4 infections: brucellosis, chlamydiosis, Q fever, and salmonellosis (Tables 1, 2). Most of these investigations were serological studies using different laboratory methods (RBPT, BAPAT, CFT, ELISA, PCR, and card test) (Table 2), while no publications have documented the prevalence of campylobacteriosis, leptospirosis, and listeriosis.

Table 2.

Characteristics of the included studies concerning abortive bacterial diseases in small ruminants

Diseases Reference Region Species Sample type Lab diagnostic Individual level Flock level
Sample size Positive case (%) CI (95%) Sample size Positive case (%) CI (95%)
Brucellosis Aggad 2003 Tiaret Sheep Blood RBPT 142 06 (4.22) [0.92–7.53] - - -
Aggad 2003 Tiaret Goats Blood RBPT 230 02 (3.07) [0.00–2.07] - - -
Aggad 2003 Tiaret Sheep Blood BAPAT 142 02 (1.42) [0.00–3.35] - - -
Aggad 2003 Tiaret Goats Blood BAPAT 230 07 (3.05) [0.82–5.26] - - -
Bachir Pacha et al. 2009 The north and the high plateaus Sheep Blood Card test, CFT 4594 03 (0.06) [0.00–0.14] - - -
Bachir Pacha et al. 2009 The north and the high plateaus Goats Blood Card test, CFT 19,568 1224 (6.2) [5.92–6.59] - - -
Gabli et al. 2015 The eastern Algerian high plateaus Goats Blood RBPT, CFT 4955 49 (0.98) [0.71–1.26] 101 16 (15.84) [8.72–22.96]
Gabli et al. 2015 The eastern Algerian high plateaus Goats Vaginal swabs RBPT, CFT 38 26 (68.42) [53.64–83.20] - - -
Kardjadj et al. 2016a, 2016b Different region of the country Sheep and goats Blood RBPT 2421 - - 150 05 (3.33) [2.41–4.25]
Kouri et al. 2018 The arid zones of Algeria Goats Blood RBPT, CFT 105 25 (23.8) [15.66–31.96] 23 09 (39.1) [19.18–59.08]
Kouri et al. 2018 The arid zones of Algeria Goats Milk Ring test 43 6 (14) [3.60–24.31] 10 03 (3.33) [1.60–58.40]
Rechidi-Sidhoum et al. 2018 Mostaganem Sheep Blood RBPT, CFT 450 10 (2.22) [0.86–3.58] 65 5 (7.69) [1.21–14.2]
Rechidi-Sidhoum et al. 2018 Mostaganem Goats Blood RBPT, CFT 287 15 (5.23) [2.65–7.80] 40 7 (17.5) [5.72–29.3]
Chlamydiosis Hireche et al. 2014 Constantine Sheep Blood i-ELISA 552 135 (24.5) [20.87–28.04] 54 38 (70.4) [58.19–82.55]
Hireche et al.  2014 Constantine Sheep Blood i-ELISA 552 40 (7.2) [5.08–9.41] 54 18 (33.3) [20.76–45.91]
Hireche et al. 2014 Constantine Sheep Placentas PCR–RFLP 08 04 (50) [15.35–84.65] - - -
Hireche et al. 2014 Constantine Sheep Fetuses PCR–RFLP 10 06 (60) [29.64–90.36] - - -
Merdja et al. 2015a Different areas of Algeria Sheep and goats Blood i-ELISA 164 14 (8.5) [4.26–12.81] 20 06 (30) [9.92–50.08]
Merdja et al. 2015a Different areas of Algeria Sheep and goats Vaginal swabs rt- PCR 199 30 (15) [10.10–20.05] 20 16 (64) [62.47–97.53]
Merdja et al. 2015b The region of Ksar El-Boukhari Sheep and goats Blood i-ELISA 144 51 (35.41) [27.61–43.23] 17 15 (88.23) [72.92–100]
Abdelkadir et al. 2017 Sidi Belabbes Sheep Blood i-ELISA 180 55 (30.56) [23.92–37.84] 39 29 (74) [58–86]
Q fever Khaled et al. 2016 Different regions of Algeria Sheep and goats Blood i-ELISA 227 32 (14.1) [11.8–16.4] 35 17 (58) [32.01–65.13]
Khaled et al. 2016 Different regions of Algeria Sheep and goats Genital swabs rt-PCR 267 57 (21.3) [16.43–26.26] 35 21 (60) [43.77–76.23]
Abdelkadir et al. 2017 Sidi Belabbes Sheep Blood i-ELISA 180 50 (27.78) [21.37–34.93] 39 28 (72) [57.67–85.92]
Salmonellosis Kouri et al. 2018 The arid zones of Algeria Goats Milk Culture (CONDA media) 43 00 (00) - - - -
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RBPT Rose Bengal plate test, BAPAT buffered acidified plate agglutination test, CFT complement fixation test, ELISA enzyme-linked immunosorbent assay test, i-ELISA indirect enzyme-linked immunosorbent assays, The antigen plugged on plate or “card test”, rt-PCR real-time polymerase chain reaction

Brucella spp.

Six papers discussed the prevalence, and the risk factors of brucellosis in small ruminants’ flocks. Most of these investigations were based on serological test: 5 studies performing RBPT; 1 study performing BAPAT, 1 study performing card test, and 1 study performing ring test. The total number of individual samples was 7260 sheep and 25,945 goats. The reported prevalence ranged from 0.06 to 2.22% and from 3.05 to 68.42% in sheep and goats respectively. The overall estimated prevalence was 0.39% (0.23–0.56%; 95% CI) in sheep (21/5328) and 5.31% (5.04–5.59%; 95% CI) in goats (1354/25,456).

For the culture and the identification of Brucella spp., twenty-six (68.42%) bacterial isolations were characterized by Gabli et al. (2015) in goats’ vaginal swabs. Only Biovar 3 B. melitensis strains were identified.

Risk factors associated with Brucella spp. seropositivity in small ruminants were identified: age, sex of animal, herd size, management system (nomadic/sedentary systems), gestation rank, and parity (Gabli et al. 2015; Kardjadj et al. 2016a, 2016b; Kouri et al. 2018).

Chlamydia spp.

Information on Chlamydia infection in small ruminants was obtained from 5 studies using indirect ELISA, real-time PCR, and PCR–RFLP methods. Analysis included a total of 1809 sheep and goats. The reported seroprevalence ranged from 08.5 to 35.41%. Meta-analysis showed that the prevalence of chlamydiosis in small ruminants was 32.72% (27.61–37.82%; 95% CI). Chlamydia abortus (43.3%) was the species most frequently detected, followed by C. pecorum (20%) (Merdja et al. 2015a).

The most potential risk factors associated with chlamydiosis infection in small ruminants were age, reproductive disorders (stillbirth problem, mortality rate in young lambs, and septicemia in lambs), management system (not using disinfectants, availability of veterinary service, and visit of adjacent farm-workers), and the region (Hireche et al. 2014; Hireche et al. 2016; Abdelkadir et al. 2017).

Coxiella burnetii

Few studies have targeted Coxiella burnetii infection in small ruminants. A total number of individual samples were 674 sheep and goats. The overall estimated prevalence in small ruminants was 20.62 (17.57–23.68%; 95% CI) (139/674). The first report was conducted by Khaled et al. (2016). Indirect ELISA was used to detect specific antibodies against C. burnetii, and real-time PCR was used to detect bacterial DNA. The survey indicated that individual seroprevalence was estimated at 14.1% and 21.3% of females have proved C. burnetii excretion. Abdelkadir et al. (2017) were reported a prevalence of 27.78% in aborted ewes.

Salmonella spp.

There was only one study that treated salmonella infection in goats. Forty-three milk samples were tested using CONDA media for bacterial culture and the results were all negative.

Viral diseases

Viral causes have been reported in eight papers that have concerned PPRV, BTV,BDV, CAEV and BVDV (Table 3).

Table 3.

Characteristics of the included studies concerning abortive viral diseases in small ruminants

Diseases Reference Region Species Sample type Lab diagnostic Individual level
Sample size Positive case Prevalence % CI (95%)
PPRV De Nardi et al. 2011 Tindouf Sheep and goats Nasal swabs, ocular swabs, whole blood rt-PCR 09 03 33.3 [2.53–64.13]
Kardjadj et al. 2015a Ghardaïa Sheep Blood c-ELISA 30 06 20 [5.69–34.31]
Kardjadj et al. 2015a Ghardaïa Goats Blood sera c-ELISA 32 11 34.37 [17.92–50.83]
Kardjadj et al. 2015a Ghardaïa Sheep Blood rt-PCR 30 6 20 [5.69–34.31]
Kardjadj et al. 2015a Ghardaïa Goats Blood rt-PCR 32 8 25 [10.00–40.00]
Kardjadj et al. 2015a Ghardaïa Sheep Oculo-nasal swabs rt-PCR 30 15 50 [32.11–67.89]
Kardjadj et al. 2015a Ghardaïa Goats Oculo-nasal swabs rt-PCR 32 21 65.62 [49.17–82.08]
Kardjadj et al. 2015b Algeria Sheep Blood c-ELISA 3336 362 10.85 [9.80–11.91]
Kardjadj et al. 2015b Algeria Goats Blood c-ELISA 1216 214 17.59 [15.46–19.74]
Baazizi et al. 2017 Algeria Sheep Blood c-ELISA 2786 484 17.4 [15.97–18.78]
Baazizi et al. 2017 Algeria Goats Blood c-ELISA 610 152 24.9 [21.49–28.35]
BTV Madani et al. 2011 Different regions of Algeria Sheep Blood ELISA 359 52 14.48 [10.84–18.13]
Madani et al. 2011 Different regions of Algeria Goats Blood ELISA 71 15 21.12 [11.63–30.62]
Madani et al. 2011 Different regions of Algeria Sheep Blood rt-PCR 51 03 20 [0.00–12.34]
Madani et al. 2011 Different regions of Algeria Goats Blood rt-PCR 15 00 00 [0.00–0.00]
Kardjadj et al. 2016a, 2016b Different regions of Algeria Sheep and goats Blood c-ELISA 2421 138 5.70 [4.78–6.62]
Kouri et al. 2018 The arid zones of Algeria Goats Blood c-ELISA 105 70 66.7 [57.65–75.68]
BDV Feknous et al. 2018 Different regions of Algeria Sheep Blood Ag-ELISA 689 00 00
Feknous et al. 2018 Different regions of Algeria Sheep rt-PCR 689 00 00
Feknous et al. 2018 Different regions of Algeria Sheep Blood Ab-ELISA 576 344 60.17
Feknous et al. 2018 Different regions of Algeria Sheep VNT 197 144
CAEV Kouri et al. 2018 The arid zones of Algeria Goats i-ELISA 105 00 00
BVDV Feknous et al. 2018 Different regions of Algeria Sheep VNT 197 02
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PPRV pest des petits ruminants virus, BTV bluetongue virus, BDV border disease virus, CAEV caprine arthritis encephalitis virus, BVDV bovine viral diarrhea virus, i-ELISA indirect enzyme-linked immunosorbent assays, c-ELISA enzyme-linked immunosorbent assay competitive, VNT virus neutralization test, rt-PCR real-time polymerase chain reaction

Peste des petits ruminants virus (PPRV)

Four articles were revealed reporting information on the prevalence of peste des petits ruminants (PPR) in Algeria. Two (2) testing methods were used: c-ELISA and rt-PCR. The total number of investigations performed was 8134 sheep and goats of which 1282 were positive (15.76%), (14.97–16.55%; 95% CI). The prevalence varied from 10.58 to 65.62%.

Age, herd mix, and contact with other herds were the main risk factors identified (Kardjadj et al. 2015b; Baazizi et al. 2017).

Bluetongue virus (BTV)

There were three papers published on BTV prevalence among small ruminants. The total number of sheep and goat samples was 3022. Prevalence levels ranged from 5.70 to 66.7%. The serotype identified was BTV-1. The overall estimated prevalence in sheep and goats was respectively, 13.41% (55/410) (10.12–16.71%; 95% CI) and 44.50% (85/191) (37.45–51.55%; 95% CI).

Risk factor analysis indicated that grazing system, mixed flocks, presence of wetlands nearby the flocks, and lack of Culicoides control strategies were the major risk factors associated with bluetongue seropositivity in Algerian small ruminants (Kardjadj et al. 2016a, 2016b).

Border disease virus (BDV)

Information on border disease virus in sheep was obtained from one study only using four (4) different test methods (Ag-ELISA, RT-PCR, Ab-ELISA, and VNT). The total number of individual samples was 2151. The overall estimated prevalence was 22.68% (488/2151) (20.92–24.46%, 95% CI).

Several risk factors were identified as linked to BDV such as climate, landscape, flock management and presence of goats and other diseases in the farm (Feknous et al. 2018).

Bovine viral diarrhea virus (BVDV-1 and BVDV-2)

Prevalence of anti-BVDV antibody in sheep was obtained from one study only which was performing by VNT. The total number of individual samples was 197 and the prevalence was 1.01% (Feknous et al. 2018).

Caprine arthritis encephalitis virus (CAEV)

One study was obtained about CAEV seroprevalence using i-ELISA method. The study was conducted on 105 goats which were all free of CAEV (Kouri et al. 2018).

Parasitic causes

Parasitic causes have been reported in six papers that have concerned only toxoplasmosis (Table 4). There are no data available on other parasitic causes that may induce abortion in small ruminants such as Neospora caninum and Trichomonas fœtus.

Table 4.

Characteristics of the included studies concerning abortive parasitic diseases in small ruminants

Disease Reference Region Species Simple Lab diagnostic Individual level Flock level
Total animals Positive case (%) CI (95%) Total animals Positive case (%) CI (95%)
Toxoplasma gondii Dechicha et al. 2015 Djelfa Sheep Blood serum IFAT 276 32(11.59) [8.07–15.97] 19 11 (57.89) 36.28–76.86
Dechicha et al. 2015 Djelfa Goats Blood serum IFAT 106 14 (13.21) [7.41–21.17] 6 04 (66.66) 30–90.32
Dahmani et al. 2018 The north of Algeria Sheep Blood serum ELISA 580 48 (8.28) [6.03–10.52] - - -
Dahmani et al. 2018 The north of Algeria Sheep Esophagi and diaphragms Histological technique 335 02 (0.59) [0.00–1.42] - - -
Benlakehal et al. 2019 Tebessa Sheep Blood serum i-ELISA 376 133 (35.37) [30.54–40.21] 39 33 (84.61) 73.29–95.94
Mohamed-Cherif et al. 2019 The central of Algeria Sheep Blood serum i-ELISA 2144 549 (25.6) [23.8–27.4] 70 70 (100) 10–100
Mohamed-Cherif et al. 2019 The central of Algeria Goats Blood serum i-ELISA 478 57 (11.9) [9–14.8] 47 41 (87.2) 77.7–96.8
Dahmane et al. 2020 Mila Goats Blood serum i-ELISA 184 132 (71.73) [64–79.4] 25 24 (96) 83.30–99.92
Dahmane et al. 2020 Mila Goats Blood serum LAT 184 117 (63.58) [56.43–70.20] 25 25 (100) 78.58–99.21
Ait Issaad et al. 2020 Tebessa Sheep Blood PCR 227 80 (35.24) [29.03–41.46] 20 - -
Ait Issaad et al. 2020 Tebessa Goats Blood PCR 91 17 (18.68) [10.67–26.69] 20 - -
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IFAT indirect fluorescent antibody test, ELISA enzyme-linked immunosorbent assay, i-ELISA indirect enzyme-linked immunosorbent assay, LAT latex agglutination test, PCR:polymerase chain reaction

Information on Toxoplasma gondii infection in small ruminant was obtained from 6 different studies. Four studies performing ELISA; one study performing IFAT; one study performing LAT; one study performing PCR; and one study performing histological technique. The total number of individual samples was 3938 sheep and 1042 goats. T. gondii infection prevalence among sheep and goats was 21.43% (844/3938) (20.15–22.71%, 95% CI) and 32.31% (337/1043) (29.47–35.15%; 95% CI) respectively.

The main risk factors associated with toxoplasma infection were age, sex, region, season management system (herd size, presence of goats in sheep flocks) (Dechicha et al. 2015; Dahmani et al. 2018; Benlakehal et al. 2019; Mohamed-Cherif et al. 2019; Ait Issaad et al. 2020), and reproductive disorders (abortion stage, and flocks with a history of abortion) (Benlakehal et al. 2019; Dahmane et al. 2020; Ait Issaad et al. 2020).

Discussion

Abortion in small ruminants can be caused by a variety of infectious and non-infectious agents. It can cause great economic losses (Givens and Marley 2008; Holler 2012). Despite preventive recommendations made by veterinarians of the State for several years, abortion in small ruminants remains a difficult problem in Algeria. The first publication on the causes of abortions in small ruminants in Algeria was published in 2003 which concerned brucellosis (Aggad 2003) and since then no study has been carried out until 2009 when a study on the same pathology was published (Bachir Pacha et al. 2009).

To the best of our knowledge, this systematic review is the first in Algeria which provides a comprehensive concept regarding the etiology of abortions in small ruminants through the pooling of data from studies published from the beginning in 2003 to 2020. A total of 25 studies were eligible for this review which included a number of 54,330 small ruminants of which 5080 were revealed positive (9.35%). The review indicates that there was very little research on abortive infectious and parasitic diseases of sheep and goats until 2011 when a marked increase in prevalence studies was noted.

The prevalence of different abortion diseases varies according to the studies. This difference could be attributed to several factors, the most important of which are difference in sampling technique, herd management, and the climate and diagnostic test used (Selim et al. 2018a; Tesfaye et al. 2020; Mamlouk et al. 2020).

Chlamydia and Q fever were observed in 32.72% and 20.62% of small ruminants, respectively. The prevalence of peste des petits ruminants was 15.76% and the overall prevalence of bluetongue in sheep and goats was, respectively, 13.41% and 44.50%. Toxoplasma gondii infection prevalence among sheep and goats was 21.43% and 32.31% respectively. Border disease and bovine viral diarrhea were detected in 22.68% and 1.01% of sheep examined, respectively. The overall prevalence of brucellosis was 0.39% in sheep and 5.31% in goats. All samples were found to be free of salmonellosis and Caprine arthritis encephalitis virus (CAEV).

Chlamydia abortus, causing enzootic abortion in sheep, is considered one of the major causes of abortion in small ruminants worldwide (Tejedor-Junco et al. 2019). Abortion is observed in particular during the last 2 or 3 weeks of gestation (Arif et al. 2020). The prevalence reported herein ranges from 08.5 to 35.41% with an average of 32.72%, which is in agreement with the previous prevalence of 27.2% in Morocco (Benkirane et al. 2015), 14.9% in Egypt (Selim et al. 2018a), 21.8% in Jordan (Al-Qudah et al. 2014), and 21.5% in Brazil (Pinheiro Junior et al. 2010). It is higher than that reported in other studies in Tunisia: 1.9% (Rekiki et al. 2005), 6.6% (Mamlouk et al. 2020), and 3.2% (Elandalousi et al. 2015).

The prevalence of Border disease virus (BDV) revealed herein is lower than reported elsewhere (Valdazo-Gonzalez et al., 2006; Krametter-Froetscher et al. 2010; Martin et al. 2015; Mishra et al. 2016). There are significant regional variations in the prevalence of the disease in small ruminants which are attributed to the levels of movement, regional differences in management practices, and herd density (Nettleton et al. 1992).

Toxoplasmosis, due to Toxoplasma gondii, is one of the major parasitic causes of reproductive failure associated with abortion, in sheep and goats (Weiss and Dubey 2009). The prevalence of toxoplasma-infection in small ruminants depends on the density of infected cats around the farm, the breeding conditions, the climate, the diagnostic technique used, and the sampling procedure (Liu et al. 2015; Hanif and Tasawar 2016; Tegegne et al. 2016). The reported prevalence in sheep (21.43%) is comparable to those previously recorded in Morocco (20.8%) (Benkirane et al. 2015) and Tunisia (19%) (Gharbi et al. 2013), but higher than those reported in Pakistan (11.1%) (Ramzan et al. 2009) and northeast China (3.0%) (Wang et al. 2011). Higher values were observed in Tunisia (40.2%) ( Lachkhem and Sakly 2015), Egypt (52.7%) (Ibrahim et al. 2017), and Morocco (27.6%) (Sawadogo et al. 2005). In goats, prevalence of T. gondii infection observed in this study was close to that recorded in Tunisia (34%) ( Lachkhem and Sakly 2015), and higher than that observed in Morocco (8.5%) (Benkirane et al. 2015), Pakistan (11.2%) (Ramzan et al. 2009), and central Ethiopia (11.6%) (Bekele and Kasali 1989). Other reports have shown higher prevalences than ours, such as those from Pakistan (41.8%) (Ahmed et al. 2016), Egypt (44.3%) (Shaapan et al. 2010), and southern Ethiopia (55.18%) (Tegegne et al. 2016).

Coxiella burnetii, is an obligate intracellular bacterium, which causes Q fever disease responsible for reproductive disorders such as abortion in ruminants (Elhaig et al. 2018). According to published data, the prevalence of Q fever in sheep and goats in Algeria was 20.62%, which is in agreement with 22.7% in Egypt (Selim et al. 2018b) and inferior to the results of Kalender (2001) who reported a prevalence of 38.59% in Turkey. Low results were recorded by Kilic and Kalender (2016) in Turkey (16% in aborted ewes and 7.6% in non-aborted ewes).

Bluetongue is an infectious viral disease of domestic and wild ruminants. It is transmitted between ruminants by the bite of Culicoides midge vectors (Breard et al. 2004; Kaufmann et al. 2012). In the present study, the prevalence of BTV was 13.41% in sheep which is lower than the reported prevalence of 39.4% in Thailand (Apiwatnakorn et al. 1996) and 90% in Turkey (Taylor et Mellor 1994) and higher than 6.57% in southeastern Iran (Mozaffari and Khalili 2012). The prevalence of BTV herein was 44.50% in goats which is lower than the reported prevalence of 73.0% in Thailand (Apiwatnakorn et al. 1996) and higher than the result of 3.9% in Brazile (Mota et al. 2011).

Peste des petits ruminants (PPR), is a highly contagious viral disease of small ruminants in many countries in Africa, the Middle East, and Asia. It has been reported by FAO and OIE as a class one disease to be eradicated (OIE and FAO, 2015). In Algeria, PPR has been reported only in sheep with a prevalence of 14.05%, which is significantly lower than other studies (Dhar et al. 2002; Ozkul et al. 2002; Khan et al. 2011 in Pakistan).

Bovine viral diarrhea virus (BVDV-1 and BVDV-2) has been identified in Algeria in sheep with a low prevalence (1.01%) which is much lower than the results of other studies (O’Neill et al. 2004; Valdazo-Gonzalez et al. 2006; Gaffuri et al. 2006).

Brucellosis is an important zoonosis that causes massive economic losses in small ruminant farming with great public health significance. In sheep and goats, it is mainly caused by Brucella melitensis of which the main symptom is abortion (Celli and Gorvel 2004). In Algeria, the prevalence revealed in this systematic review and meta-analysis in goats and sheep was 5.32% and 0.39% respectively, which is largely lower than reported elsewhere (Mrunalini et al. 2000 and Singh et al. 2000 performed in India; Al-Dabagh et al. 2014 and Tamadhir et al. 2020 performed in Iraq).

Conclusion

This meta-analysis is the first synthesis study on abortive diseases in small ruminants in Algeria. It provides important information that could be useful in managing and monitoring programs to control abortive diseases in small ruminants. The main abortive diseases in small ruminants in Algeria are brucellosis, chlamydiosis, Q fever, salmonellosis, PPR, bluetongue, border disease, CAE, BVDV, and toxoplasmosis. Considering that some of these diseases are zoonoses, farmers must take important hygienic precautionary measures. Further research and surveillance will be needed to reduce the prevalence of these infections and, consequently, reduce economic damage and public health risks in Algeria.

Author contributions

All authors read and approved the final manuscript.

Data availability

All data generated or analyzed during this study are included in this published article.

Declarations

Ethics approval

Not applicable.

Conflict of interest

The authors declare that they have no competing interests.

Footnotes

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

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