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Comparative studies on genital infections and antimicrobial susceptibility patterns of isolates from camels (Camelus dromedarius) and cows (Bos indicus) in Maiduguri, north-eastern Nigeria

  • Gideon Dauda Mshelia
  • Godfrey Okpaje
  • Yepmo Andre Casimir Voltaire
  • Godwin Onyeamaechi Egwu
Open Access
Research
Part of the following topical collections:
  1. Biomedical and Life Sciences

Abstract

A total of 160 genitalia of Camels and cows were investigated in Maiduguri, north-eastern Nigeria to compare bacterial isolates and the antibacterial susceptibilities of some of the isolates. Streptococcus (Str.) pyogenes (31%), Escherichia (E.) coli (24%) and Staphylococcus (S.) aureus (20%) were the most common vaginal bacterial isolates in camels; while E. coli (73%), Str. pyogenes (18%) and S. aureus (11%) were the most frequent isolates in the cows. Of the 78 uterine isolates recovered in this study, E. coli was the most prominent in camels (8%) and cows (54%). The overall weight of genital infection in all camels and cows examined was highest (P < 0.05) with E. coli (79%), but there was no difference (P > 0.05) between vaginal and uterine bacterial isolates from camels and cows in this study. The Relative Risk (RR) for an infection of the vagina with E coli (3.04, 95% Confidence Interval (CI): 2.104 to 4.398, P < 0.0001) is more in cows compared to the camel, but the RR for vaginal infection with S. aureus and Str. pyogenes were lower in cows compared to Camels. The E. coli and S. aureus isolates were highly susceptible to the antimicrobial agents tested. Therefore effective management of reproductive disorders associated with these pathogens can be achieved with proper use of these antimicrobial agents in these animal species

Keywords

Antimicrobial susceptibility Bacteria Camels Cows Genitalia Nigeria 

Introduction

The camelidae family has been described previously (Mouchira2009). The camelidae are resilient to adverse weather conditions and are able to stay long without water and food, which have made them to become more important as a source of meat and draught power in sub-Saharan Africa (Mouchira2009). Camel meat is daily being accepted in northern Nigeria and they may likely replace cattle as the main animal protein source for human population in Nigeria (Srikandakumar et al.2001).

At the moment these two livestock resources provide the meat consumed in northern Nigeria, so there is need to continue to intensify their production to meet up with the ever increasing demand for this product in the country. These animals are bred majorly using natural mating which is characterized by low reproductive performance, mostly associated with puerperal infections of the genital tracts (Sheldon et al.2006). Therefore, it is important to routinely assess the genital bacterial status of breeding animals as part of custom reproductive improvement programme.

The bacteria colonizing the genital tract of the female camel (Camelus dromedarius) have been shown to be the major causes of reproductive disorders in this species (Ali et al.2010; Tibary et al.2006; Wernery and Kumar1994). Evidence for the presence of a variety of uterine bacterial isolates has been demonstrated from studies using slaughterhouse materials. Some were isolated from the uterus of barren camels, but their responsibility as primary causes of uterine infections has been doubted (Enany et al.1990; Hussein et al.2006). Postpartum infections in cattle are eliminated within 2–4 weeks of parturition (Hussain et al.1990). However, some uterine pathogens persist to cause subclinical endometritis in this species (Fourichon et al.2000; Heuwieser et al.2000).

The disruption of the immune status during the periparturient period in cattle renders the uterus vulnerable to ascending infections with opportunistic bacteria from the vagina and the animals’ environment. These infections rise during this period compared with other stages of the reproductive cycle (Sheldon et al.2002; Singh et al.2008) requiring antimicrobial treatment for clearance (Drillich2006; Sheldon et al.2009) and improvement in subsequent fertility in these species. However, the inappropriate use of antimicrobial agents for the treatment of infective reproductive disorders in camels and cows led to increased bacterial contaminations of the genital environment (Tibary and Anouassi2001; Potter et al.2010; Gani et al.2008). The pattern in the pastoral husbandry system is changing particularly in the semi-arid regions in Nigeria (Blench1999), associated with the scarcity of food resources and drinking water at certain times of the year. So, camels could often be seen being herded together with cattle, donkeys and other small ruminant species at some watering points and market places (El-Yuguda et al.2010; Markemann and Zarate2010), which facilitates the transmission of infections between these species. Unlike cattle, there is dearth of information regarding infective pathogens colonizing the genital tracts in camels. This study was therefore designed to identify and compare the bacterial species colonizing the vagina and uterus of camels and cows in north-eastern Nigeria; and to determine their antimicrobial susceptibilities for effective management of reproductive disorders in these species.

Materials and methods

Animals and samples collection

The study was conducted in Maiduguri, Borno State in north eastern Nigeria. The parity and other reproductive histories of the she-camels (Camelus dromedarius) and cows (Bos indicus) were unknown, but they were culled from pastoral herds using natural breeding. The size of the samples collected was determined according to the formula provided by Thrustfield (2005):
n = 1.96 2 Pexp 1 - Pexp d 2 Open image in new window

where n = required sample size, Pexp = expected prevalence and d = desired precision. The calculation was based on 95% level of confidence (CL), 5% margin of error, and with the assumption that 50% of the genitalia will be infected with bacteria, Accordingly, a total of 160 (80 each from camels and cows) were collected in Maiduguri municipal abattoir. The genital tracts were collected twice weekly and transferred on ice in clean polyethelyne bags to the diagnostic laboratory within two hrs of collection. This study was approved and carried out in accordance with the ethical provisions of the faculty of Veterinary Medicine, University of Maiduguri.

Bacterial culture and isolation

Bacteriological examination was carried out on the vagina and uterus using standard protocols (Cheesbrough2000). Swab samples were collected routinely from the vagina (Amin et al.1996) and uterus (Azawi et al.2010). All the samples were inoculated onto blood and MacConkey’s agar plates, and incubated at 37°C for 24–48 hrs. Suspect colonies were examined for colony morphology, Grams characteristics and motility. Gram negative bacilli and Gram positive cocci were further subjected to catalase, oxidase and coagulase tests as well as standard biochemical tests (Cowan and Steel1993; Koneman et al.2005) to identify the isolates.

Antimicrobial susceptibility test

The disk diffusion test was used to determine the antimicrobial susceptibility of the confirmed bacterial isolates against panels of antimicrobial agents. This test was performed on the E. coli and S. aureus isolates recovered in the present study. The antimicrobial agents tested were Amoxycillin (25 μg), Ampicillin (10 μg), Amoxycillin-Clavulanate (30 μg), Cephalexin (30 μg), Ciprofloxacin (10 μg), Clindamycin (10 μg) and Co-trimoxazole (25 μg). Others include Erythromycin (5 μg), Gentamycin (30 μg), Nalidixic acid (30 μg), Norfloxacin (10 μg), Ofloxacin (5 μg), Pefloxacin (5 μg) and Streptomycin (10 μg). The antimicrogram pattern was determined according to the Kirby Bauer procedure described by Demissie (2011). Briefly, pure colonies of bacterial growth were suspended in tubes containing 5mls of Brain Heart infusion broth (Sigma-Aldrich, UK) and adjusted to 0.5 McFarland turbidity standards. 10 μl of the diluted bacterial suspensions were transferred to Mueller Hinton agar plates (BBL®, Becton Dickinson, USA) using sterile cotton swab applicator sticks. Excess fluid was squeezed out by rotating the swabs against the sides of the tubes. The plates were then inoculated uniformly by rubbing the swabs against the entire agar surfaces and allowed to dry. The impregnated antimicrobial discs (Optun Laboratories Nig Ltd., Lagos, Nigeria) were applied to the surfaces of the inoculated plates using sterile forceps. All the discs were gently pressed with forceps to ensure complete contact with the agar surface. The discs were placed 1.5 cm away from the edges of the plates and 3 cm away from each other with the guide of a template placed under the petri-dish. The plates were then inverted and incubated aerobically for 24 hr at 37°C. The zones of inhibition of bacteria by the antimicrobial discs were measured in millimeters using a caliper on the underside of the plates. The susceptibility of the bacteria was determined based on the breakpoints recommended by the Clinical Laboratory Standards Institute (CLSI2011).

Data analysis

The data on the genital bacteria and their isolation rates were analysed using descriptive statistics. The Chi-square test was used to test the differences in the percentages of the isolates, while the relative risks (RR) for an infection with bacteria were analysed and the significance tested with the Fisher’s Exact Test using Graph Pad Prism Statistical Software version 5.04 (GraphPad Software2010). Unless otherwise stated P value was considered significant at <0.05.

Results

Vaginal and uterine bacterial isolates

The bacteria colonizing the vagina and uterus in camels and cows are shown in Table 1. Out of a total of 75 bacterial isolates from camels (n = 80), 66 of those were recovered from the vagina and made up of 25 (31.3%) Str. pyogenes, 19 (23.8%) E. coli, 16 (20%) S. aureus, 5 (6.3%) Proteus spp and 1 (1.3%) Corynebacterium spp. Nine of the isolates were recovered from the uterus. Out of these number, 6 (7.5%) were E. coli, 1 (1.25%) S. aureus, 1 (1.25%) Str. pyogenes and 1 (1.25%) Corynebacterium spp. There were four gravid camelidae uteri examined from this specie, but no bacteria were isolated from them.
Table 1

Vaginal and uterine bacterial isolates from Cows and Camels slaughtered in north-eastern Nigeria

Isolates

Cows (n = 80)

Camels(n = 80)

RR

 

n

%

n

%

 

VAGINA

     

Streptococcus pyogenes

14

18

25

31

(0.58, 95% CI: 0.3485 to 0.9674, P = 0.0479),

Staphylococcus aureus

9

11

16

20

(0.55, 95% CI: 0.2782 to 1.087, P = 0.1170)

*Staphylococcus spp

19

23

NI

  

Escherichia coli

58

73

19

24

(3.04**, 95% CI: 2.104 to 4.398, P < 0.0001)

Proteus spp

11

14

5

6

 

Corynebacterium spp

NI

 

1

1

 

UTERUS

     

Streptococcus pyogenes

11

14

1

1

(14.0**, 95% CI: 1.875 to 104.51, P = 0.0006)

Staphylococcus aureus

9

11

1

1

(11.0**, 95% CI: 1.446 to 83.652; P = 0.0050)

*Staphylococcus spp

6

8

NI

  

Escherichia coli

43

54

6

8

(6.750**, 95% CI: 3.389 to 13.444, P < 0.0001)

Proteus spp

3

4

NI

  

Corynebacterium spp

NI

 

1

1

 

Abbreviations: NI, not isolated, *other Staphylococcus species, RR, relative risk for an infection with bacteria in cows compared to camels, CI, Confidence Interval, **within a column, values are statistically significant.

In the cows (n = 80), there were 111 isolates recovered from the vagina which include 14 (17.5%) Str. pyogenes, 9 (11.3%) S. aureus, 58 (72.5%) E. coli, 11 (13.8%) Proteus spp and 19 (23.3%) other Staphylococcal spp. The uterine cultures yielded 69 bacterial isolates, 43 (53.8%) of which were E. coli, 11 (13.8%) Str. pyogenes, 9 (11.3%) S. aureus, 3 (3.8%) Proteus spp and 6 (7.5%) other Staphylococcal spp. Two gravid uteri were examined from this specie, from which, E coli and Staphylococcal spp were isolated from 2/2 and 1/2 of the uteri. The overall weight of genital infection was calculated; and the highest infection rate was associated with E. coli (79%) followed by Str. pyogenes (32%) and S. aureus (25%) in all the animals investigated in the present study (Table 2).
Table 2

The overall weight of genital infection with bacteria isolated from Cows and Camels slaughtered in north-eastern Nigeria

Isolates

E. coli

Str. pyogenes

S. aureus

COWS (n = 80)

101

25

23

CAMELS (n = 80)

25

26

17

Total isolates (Infection rate)

126 (79%)

51 (32%)

40 (25%)

Abbreviation: n, number of animals investigated.

Relative risk (RR) analysis

The risks of infection of the vagina and uterus with bacteria were calculated for the cow and camels. The RR for an infection of the vagina with E. coli (3.04, 95% CI: 2.104 to 4.398, P < 0.0001) is higher in cows compared to camels, while the RR for S. aureus (0.55, 95% CI: 0.2782 to 1.087, P = 0.1170) and Str. pyogenes (0.58, 95% CI: 0.3485 to 0.9674, P = 0.0479) were lower in cows compared to camels. However, the RR for uterine infection with Str. pyogenes (14.0, 95% CI: 1.875 to 104.51, P = 0.0006) is higher in cows compared to camels, so also with E. coli and S. aureus (Table 1).

Antimicrobial susceptibility test

The antimicrobial susceptibility of E. coli was highest (100%) against Pefloxacine and Ofloxacin, and 96% against Amoxycillin-clavulanate, Ciprofloxacin, Gentamycin and Streptomycin. This pathogen was susceptible to the other antimicrobial drugs at rates ranging from 73–82%. The lowest susceptibility was observed against Nalidixic acid (64%; Figure 1A). S. aureus had the highest susceptibility against Ampicillin 100%, followed by Cephalexin (98%) and Ciprofloxacin (93%) and Ofloxacin (88%). The susceptibility of S. aureus against most of the other drugs ranged from 81–83%, with the lowest susceptibility recorded against Gentamycin (79%; Figure 1B).
Figure 1

Antimicrobial susceptibility patterns for bacterial isolates. (A) Shows the susceptibility of E. coli, and (B) the susceptibility of S. aureus.

Discussion

The information regarding bacteria causing genital infections in female dromedary camels is scarce (Ali et al.2010). However, evidence implicating bacterial infections as causes of endometritis has been reported, and a variety of these bacterial species have been recovered from the uteri of infertile camelids (Tibary et al.2006; Wernery and Kumar1994). Out of the vaginal bacterial isolates recovered from camels in this study, Str. pyogenes, S. aureus and E. coli were the most common. The isolation rate of Str. pyogenes (31%) alone was higher (P < 0.0%) compared to the rates for E. coli and S. aureus. This bacteria has been isolated previously in camels (Tibary and Anouassi2001) suffering from endometritis (Wernery and Kumar1994) and in those with mucopurulent or purulent vaginal discharges (Ali et al.2010). Proteus spp and Corynebacterium spp were also isolated, with the later having the lowest isolation rate (1%).

In cows, E. coli was the most commonly isolated bacteria from the vagina. Other isolates including Staphylococcal organisms, Str. pyogenes and Proteus spp were moderately isolated from this species, but Corynebacterium spp was not isolated. The rate of isolation of E. coli observed in the present study (73%) was highly significant, and accounted for more than all the other bacterial isolates put together. Previously, E. coli was thought to be a non-specific pathogen associated with endometritis in mares and cows (Arthur et al.2000), but they were recently isolated in camels with purulent discharges (Ali et al.2010). The presence of this bacterium at the present level of infection in the vagina could likely lead to metritis as a consequence of ascending uterine infection during breeding. Specific strains of E. coli have recently been shown to be pathogenic for the endometrium, causing Pelvic Inflammatory Disease (PID) in cattle (Sheldon et al.2010). But the role of this bacterium in the pathogenesis of metritis especially in camels merits further studies.

The uterine bacterial isolates observed in camels in the present study are similar to those observed in the vagina, and they concurred with the findings of Yagoub (2005) who reported S. aureus, E. coli, Klebsiella sp, Proteus sp, Corynebacterium sp and Streptococcus sp as the main bacterial isolates from several cases of uterine infections in camels. The most common isolate in the present study was E. coli with an isolation rate of 6%. The isolation rates of the uterine bacteria observed in the present study were lower compared to those from the vagina, and more so in the camels than the cows. Unlike the cows, Proteus sp was not isolated in the camelids uterus, but Str. pyogenes, S. aureus and Corynebacterium sp were isolated at a minimal rate of 1% from all the camels examined. The result from the cows also showed that E. coli was the major bacteria isolated from the uterus. The isolation rate of this bacterium (54%) accounted for more than all the rates for the other bacteria isolated from the bovine uterus. Although uterine infection with E. coli is significant in the present study, the rate is lower in the uterus compared to the vagina, which is likely due to the continuous clearance of bacteria from the uterine lumen (Singh et al.2008). Despite this low isolation rate, it is important to note that the isolation of pathogenic bacteria such as E. coli in the present study portends a risk factor for lowered reproductive efficiency because of increased inflammatory reactions and possible damages to the uterine tissues (Sheldon and Dobson2004) by direct action of the bacteria or its toxins.

The data in the present study has shown that there was no difference (p > 0.05) between the bacterial species colonizing the vagina and uterus in camels and cows. But on the overall, the weight of infection with E coli (79%) in all the animals examined was more than the rates for Str. pyogenes and S. aureus put together.

Generally the pre-breeding and peri-parturient periods are known as the most critical for bacterial infection of the genital tract. This is due to the hormonal changes that make the uterus susceptible for ascending infections with resident bacteria colonizing the vagina (Singh et al.2008). During these periods, the vagina is constantly being contaminated with bacteria from the environment and from faecal droppings that smear the vagina during breeding seasons. These and other contaminants from the male genitalia are introduced into the female vagina by stud bulls which can lead to uterine infections in vulnerable animals (Singh et al.2008; Tibary and Anouassi2001). Also, during the immediate period post partum the cervix is dilated (Sheldon and Dobson2004) which allows bacteria to ascend from the vagina into the uterus, causing infections in 90% of cows by 21 days post partum (Sheldon et al.2006). This could possibly explain the similarity between the types of vaginal and uterine bacteria isolated in the present study.

The occurrence of ovulation prior to the expulsion of exudates and debris from the uterus has been shown to favor heavy growth of bacteria in the uterine environment which leads to the retention of the corpus luteum (CL) and consequent impairment of the ability of the uterus to secret PGF2α (Kaneko et al.2013). Although, there is continuous bacterial clearance and recontamination of the uterine lumen for up to 7 weeks postpartum (Singh et al.2008), some bacteria still persist in the uterus triggering inflammatory responses and pathological changes. This delays uterine involution (Williams et al.2005) thereby lowering fertility. The types of bacteria colonizing the uterus are likely to influence the severity of this condition (Singh et al.2008) in countries where natural breeding is common practice.

The result of the present study also showed that E. coli and S. aureus were isolated from pregnant bovine uteri. This finding is interesting considering that the uterus is thought to be sterile during pregnancy (Singh et al.2008), when the cervix is closed. Infections of the uterus carrying life pregnancies are the common causes of repeat breeding occasioned by conception failures (Ferreira et al.2008; Gani et al.2008). Furthermore, the isolation of E. coli from a gravid uterus is particularly important in this study because the bacterium is most frequently associated with uterine disease in cattle (Sheldon et al.2002; Williams et al.2005). Infections in the pregnant female could lead to abortion, prenatal-neonatal loss and stillbirth (Tibary et al.2006). The persistence of such infections post partum is likely to contribute to the early demise of the CL with decrease in secretion of progesterone (P4) in the affected animal (Williams et al.2007) which could also lead to pregnancy failures.

The number of bacteria colonizing the uterus and the level of uterine immune response are important determinants of uterine infections (Azawi2008; Singh et al.2008). When the immune status is lowered, the pathogenic bacteria adhere to the endometrial mucosa, get internalized and penetrate the epithelium. Alternatively, the bacteria can also release toxins that cause uterine diseases (Azawi2008). The findings in the present study have shown that the risk of an infection of the vagina with E. coli is higher in the cows compared to the camels, but inversely so with S. aureus and Str. pyogenes.

Antimicrobial agents are commonly used in the management of reproductive failures in livestock (Drillich2006). In Nigeria, they are used concurrently with prophylactic de-worming regimen in beef bull fattening schemes, but there is no special attention given to antibiosis with replacement heifers or breeding cows. The findings in the present study showed that S. aureus was highly susceptible to most of the antimicrobial agents tested, among which Ampicillin, Cephalexin, Ciprofloxacin and Ofloxacin were the most effective. This finding concurs with the observations made by Gani et al. (2008) who found Ciprofloxacin as one of the most effective antimicrobial agent against Staphyloccocal uterine infections in dairy cows. In one study, Fazlani et al. (2011) showed that S. aureus isolates from camels milk was moderately susceptible to amoxicillin, ampicillin, cephalexin and ofloxacin within the range of 64-86%. Serin et al. (2010) also demonstrated that S. aureus isolate from wrestling dromedary bulls was 100% susceptible to ciprofloxacin.

For E. coli, the susceptibility pattern to most of the antimicrobial agents tested was similar to what was observed with the S. aureus isolates, but the susceptibility was higher compared to those observed with the S. aureus isolates. The most effective antimicrobial agents observed include Ofloxacin and Pefloxacin, also Amoxycillin-clavulanate, Ciprofloxacin, Gentamycin and Streptomycin. This finding is similar to previous reports with isolates associated with genital infections in cattle and sheep (Gani et al.2008; Goncuoglu et al.2010), and from mastitic milk samples of camels (Fazlani et al.2011).

Amongst the factors that have been reported to be contributing to uterine infections in camelids are overbreeding (excessive matings during the period of receptivity), postpartum complications and unhygienic gynaecological examination and manipulation (Tibary and Anouassi2001). It has been highlighted that antimicrobial treatments have some beneficial effects on reproductive performance in livestock (Drillich et al.2003). Therefore, at the current level of susceptibility of these bacteria to the antimicrobial agents tested in the present study, effective treatment could be achieved if these antimicrobial agents are used appropriately.

Conclusions

The bacteria colonizing the genital tract are similar in camels and cows reared in north-eastern Nigeria. E. coli and S. aureus were amongst the most prevalent bacteria isolated, and they were found to be susceptible to the antimicrobial agents tested. It is advised that effective gynaecological evaluations should precede the initiation of antimicrobial treatments in order to minimize the development of antimicrobial resistant pathogenic strains in these species.

Notes

Acknowledgements

We are grateful to Isa A. Gulani of the Department of Veterinary Medicine, University of Maiduguri, Nigeria, for technical assistance; and the staff of the Maiduguri municipal abattoir, for their support with sample collection.

Supplementary material

40064_2013_836_MOESM1_ESM.tiff (664 kb)
Authors’ original file for figure 1

References

  1. 1.
    Ali A, Hassanein KM, Al-Sobayil FA, Tharwat M, Al-Hawas A, Ahmed AF: Relationship between characters of vaginal discharges and uterine bacterial isolates recovered from repeat breeding female camels ( Camelus dromedarius ). J Agric Vet Sci 2010, 2: 87-97.Google Scholar
  2. 2.
    Amin JD, Zaria LT, Malgwi RW: Vaginal aerobic bacterial flora of apparently healthy cattle in various stages of reproductive cycle in the Sahel region of Nigeria. Bull Anim Hlth Prod Afr 1996, 44: 15-18.Google Scholar
  3. 3.
    Arthur GH, Pearson H, Noakes DE: Veterinary Reproduction and Obstetrics. English Language Book Society and Bailliere. London: Tindall; 2000.Google Scholar
  4. 4.
    Azawi OI: Postpartum uterine infection in cattle. Anim Reprod Sci 2008, 105: 187-208. 10.1016/j.anireprosci.2008.01.010CrossRefGoogle Scholar
  5. 5.
    Azawi OI, Al-Abidy HF, Ali AJ: Pathological and bacteriological studies of hydrosalpinx in buffaloes. Reprod Domest Anim 2010, 45: 416-420.CrossRefGoogle Scholar
  6. 6.
    Blench R: Traditional livestock breeds: Geographical distribution and dynamics in relation to the ecology of West Africa. 1999, 44-50. Available from(Assessed 31st January 2014) http://www.odi.org.uk/publications/2041-traditional-livestock-breeds-geographical-distributiondynamics-relations-ecology-west-africa Available from(Assessed 31st January 2014)Google Scholar
  7. 7.
    Cheesbrough M: District Laboratory Practice in Tropical Countries Part 2. Cambridge, UK: Cambridge University Press; 2000.Google Scholar
  8. 8.
    CLSI: Clinical and Laboratory Standards Institute, Performance Standards For Antimicrobial Disk Susceptibility Testing. Wayne, PA: 21st International Supplement CLSI Document. M100-S21; 2011.Google Scholar
  9. 9.
    Cowan SJ, Steel KJ: Manual of Identification of Medical Bacteria. 3rd edition. Cambridge, UK: Cambridge University Press; 1993.Google Scholar
  10. 10.
    Demissie M: Isolation and identification of aerobic, septicaemia bacteria from cattle in and around Sebeta town and antimicrobial susceptibility testing. Afr J Microbiol Res 2011, 5: 87-92.Google Scholar
  11. 11.
    Drillich M: An update on uterine infections in dairy cattle. Slovakia Vet Res 2006, 43: 11-15.Google Scholar
  12. 12.
    Drillich M, Pfützner A, Sabin HJ, Sabin M, Heuwieser W: Comparison of two protocols for the treatment of retained foetal membranes in dairy cattle. Theriogenology 2003, 59: 951-960. 10.1016/S0093-691X(02)01132-9CrossRefGoogle Scholar
  13. 13.
    El-Yuguda AD, Abubakar MB, Baba SS, Ngangnou A: Competitive ELISA rinderpest virus antibody in slaughtered camels (Camelus dromedarius): implication for rinderpest virus elimination from Nigeria. Afr J Biomed Res 2010, 13: 83-85.Google Scholar
  14. 14.
    Enany M, Hanafi MS, El-Ged AGF, El-Seedy FR, Khalid A: Microbiological studies on endometritis in she-camels in Egypt. J Egypt Vet Med Assoc 1990, 50: 229-243.Google Scholar
  15. 15.
    Fazlani SA, Khan SA, Faraz S, Awan MS: Antimicrobial susceptibility of bacterial species identified from mastitic milk samples of camel. Afr J Biotechnol 2011, 10(15):2959-2964.Google Scholar
  16. 16.
    Ferreira R, Oliveira JFC, Antoniazzi AQ, Pimentel CA, Moraes JCF, Henkes LE, Bordignon V, Gonçalves PB: Relationship between clinical and postmortem evaluation in repeat breeder beef cows. Ciência Rural, Santa Maria 2008, 38: 1056-1060. 10.1590/S0103-84782008000400023CrossRefGoogle Scholar
  17. 17.
    Fourichon C, Seegers H, Malher X: Effect of disease on reproduction in dairy cows: a meta-analysis. Theriogenology 2000, 53: 1729-1759. 10.1016/S0093-691X(00)00311-3CrossRefGoogle Scholar
  18. 18.
    Gani MO, Amin MM, Alam MGS, Kayesh MEH, Karim MR, Samad MA, Islam MR: Bacterial flora associated with repeat breeding and uterine infections in dairy cows. Bangladesh J Vet Med 2008, 6: 79-86.CrossRefGoogle Scholar
  19. 19.
    Goncuoglu M, Seda F, Ormanci B, Ayaz ND, Erol I: Antibiotic resistance of Escherichia coli O157:H7 isolated from cattle and sheep. Ann Microbiol 2010, 60: 489-494. 10.1007/s13213-010-0074-8CrossRefGoogle Scholar
  20. 20.
    GraphPad: GraphPad Prism Version 5.04, GraphPad Software Inc. 2010. http://www.graphpad.comGoogle Scholar
  21. 21.
    Heuwieser W, Tenhagen BA, Tischer M, Luhr J, Blum H: Effect of three programmes for the treatment of endometritis on the reproductive performance of a dairy herd. Vet Rec 2000, 146: 338-341. 10.1136/vr.146.12.338CrossRefGoogle Scholar
  22. 22.
    Hussain AM, Daniel RCW, O’Boyle D: Post-partum uterine flora following normal and abnormal puerperium in cows. Theriogenology 1990, 34: 291-302. 10.1016/0093-691X(90)90522-UCrossRefGoogle Scholar
  23. 23.
    Hussein FM, El-Amrawi GA, El-Bawab IE, Metwally KK: Bacteriological and haematological studies in the camel genitalia. Proceedings of the International Scientific Conference on Camels, Qassim University 10–12 May 2006, 491-500.Google Scholar
  24. 24.
    Kaneko K, Nakamura M, Reiichiro-Sato R: Influence of Trueperella pyogenes in uterus on corpus luteum lifespan in cycling cows. Theriogenology 2013, 79: 803-808. 10.1016/j.theriogenology.2012.12.007CrossRefGoogle Scholar
  25. 25.
    Koneman WK, Allen SD, Janda WM, Schreckenberger PC, Propcop GW, Woods GL, Winn WC Jr: Color Atlas and Textbook of Diagnostic Microbiology. 6th edition. Philadelphia, USA: Lippincott-Raven Publisher; 2005.Google Scholar
  26. 26.
    Markemann A, Zarate AV: Traditional llama husbandry and breeding management in the Ayopaya region, Bolivia. Trop Anim Health Pro 2010, 42: 79-87. 10.1007/s11250-009-9388-6CrossRefGoogle Scholar
  27. 27.
    Mouchira MM: Pathological Studies on Ascariasis in Dromedary ( Camelus dromedarius ) and Llama ( Lama glama ) Camelidae. Eur J Sci Res 2009, 38: 159-171.Google Scholar
  28. 28.
    Potter TJ, Guitian J, Fishwick J, Gordon PJ, Sheldon IM: Risk factors for clinical endometritis in postpartum dairy cattle. Theriogenology 2010, 74: 127-134. 10.1016/j.theriogenology.2010.01.023CrossRefGoogle Scholar
  29. 29.
    Serin I, Ceyland A, Kirklan S, Parin U: Preputial bacterial flora and antibiotic susceptibility in wrestling dromedary bulls in Aydin region, Turkey. J Anim Vet Adv 2010, 9(3):482-485.CrossRefGoogle Scholar
  30. 30.
    Sheldon IM, Dobson H: Postpartum uterine health in cattle. Anim Reprod Sci 2004, 82–83: 295-306.CrossRefGoogle Scholar
  31. 31.
    Sheldon IM, Noakes DE, Rycroft AN, Pfeiffer DU, Dobson H: Influence of uterine bacterial contamination after parturition on ovarian dominant follicle selection and follicle growth and function in cattle. Reproduction 2002, 123: 837-845. 10.1530/rep.0.1230837CrossRefGoogle Scholar
  32. 32.
    Sheldon IM, Lewis GS, LeBlanc S, Gilbert RO: Defining post-partum uterine disease in cattle. Theriogenology 2006, 65: 1516-1530. 10.1016/j.theriogenology.2005.08.021CrossRefGoogle Scholar
  33. 33.
    Sheldon IM, Cronin J, Goetze L, Donofrio G, Schuberth HJ: Defining postpartum uterine disease and the mechanisms of infection and immunity in the female reproductive tract in cattle. Biol Reprod 2009, 81: 1025-1032. 10.1095/biolreprod.109.077370CrossRefGoogle Scholar
  34. 34.
    Sheldon IM, Rycroft AN, Dogan B, Craven M, Bromfield JJ, Chandler A, Roberts MH, Price SB, Gilbert RO, Simpson KW: Specific strains of Escherichia coli are pathogenic for the endometrium of cattle and cause pelvic inflammatory disease in cattle and mice. PLoS One 2010, 5: e9192. doi:10.1371/journal.pone.0009192 10.1371/journal.pone.0009192CrossRefGoogle Scholar
  35. 35.
    Singh J, Murray RD, Mshelia G, Woldehiwet Z: The immune status of the bovine uterus during the peri-partum period. Vet J 2008, 175: 301-309. 10.1016/j.tvjl.2007.02.003CrossRefGoogle Scholar
  36. 36.
    Srikandakumar A, Johnson EH, Mahgoub O, Kadim IT, Al-Ajmi DS: Anatomy and histology of the female reproductive tract of the Arabian camel. Emirates J Agric Sci 2001, 13: 23-26.Google Scholar
  37. 37.
    Thrustfield M: Veterinary Epidemiology. 3rd edition. Cambridge, USA: Black Well Science Ltd; 2005:225-228.Google Scholar
  38. 38.
    Tibary A, Anouassi A: Uterine infections in Camelidae. Vet Sci Tomorrow 2001. http://dspace.library.uu.nl:8080/handle/1874/28883Google Scholar
  39. 39.
    Tibary A, Fite C, Anouassi A, Sghiri A: Infectious causes of reproductive loss in Camelids. Theriogenology 2006, 66: 633-647. 10.1016/j.theriogenology.2006.04.008CrossRefGoogle Scholar
  40. 40.
    Wernery U, Kumar BN: Reproductive disorders in dromedary camels due to infectious causes and its treatment. J Camel Pract Res 1994, 1: 85-87.Google Scholar
  41. 41.
    Williams EJ, Fischer DP, Pfeiffer DU, England GCW, Noakes DE, Dobson H, Sheldon IM: Clinical evaluation of postpartum vaginal mucus reflects uterine bacterial infection and the immune response in cattle. Theriogenology 2005, 63: 102-117. 10.1016/j.theriogenology.2004.03.017CrossRefGoogle Scholar
  42. 42.
    Williams EJ, Fischer DP, Noakes DE, England GCW, Rycroft A, Dobson H, Sheldon IM: The relationship between uterine pathogen growth density and ovarian function in the postpartum dairy cow. Theriogenology 2007, 68: 549-559. 10.1016/j.theriogenology.2007.04.056CrossRefGoogle Scholar
  43. 43.
    Yagoub SO: Bacterial diseases of the reproductive system of camels ( Camelus dromedaries ) in Eastern Sudan. J Anim Vet Adv 2005, 4: 642-644.Google Scholar

Copyright information

© Mshelia et al.; licensee Springer. 2014

This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited.

Authors and Affiliations

  • Gideon Dauda Mshelia
    • 1
  • Godfrey Okpaje
    • 1
  • Yepmo Andre Casimir Voltaire
    • 1
  • Godwin Onyeamaechi Egwu
    • 2
  1. 1.Department of Veterinary Surgery and Theriogenology, Faculty of Veterinary MedicineUniversity of MaiduguriMaiduguriNigeria
  2. 2.Department of Veterinary Medicine, Faculty of Veterinary MedicineUniversity of MaiduguriMaiduguriNigeria

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