Study and Identification of Uterine Bacterial Flora of She-Camel During Postpartum ^†

Abstract

To identify the uterine bacterial flora and for a deeper understanding of pathologies related to the female genital tract, 10 camels were monitored during the postpartum period, and uterine swabs were collected. From the 84 samples, 354 bacterial strains were isolated and identified, including 80.2% Staphylococcus species and 19.8% Streptococcus species. No Gram-negative bacteria could be isolated. The bacterial load was very high during the first week, and then regressed and increased by day 30. The uterine bacterial flora of the camel is rich in lactic acid bacteria, ensuring a high level of local defense of the uterus.

1. Introduction

The dromedary (Camelus dromedarius) is a species naturally adapted to desert and Saharan regions, which meets the challenge of global warming [1]. In Algeria, 4/5 of the territory is represented by an arid and semi-arid climate where a dromedary population estimated at 426,000 heads lives [2], but that remains below the country’s production capacity [2]. The increase in the dromedary population depends on mastering its reproductive physiology, in particular the monitoring of gestation, parturition and factors related to uterine involution, which is key to the resumption of ovarian activity [2]. During and after parturition, the uterus remains exposed to risks of infections.

A literature review showed that uterine bacteriological studies in She-camels were carried out on females who had developed metritis and endometritis or on the aforementioned matrices after slaughtering [1]. The main germs isolated were Staphylococcus aureus, Streptococcus pyogenes, Escherichia coli, Corynebacterium pyogenes, Klebsiella spp., Proteus spp. and Salmonella spp. [3]. These organisms are responsible for uterine infections and should be detected in order to prevent the risks of infertility or even sterility. The occurrence of these infections depends on the balance between contaminating germs and the state of local defense of the uterus.

2. Materials and Methods

This study was conducted on 10 Sahrawi She-camels aged 10 to 12 years. The females were clinically monitored for 6 weeks after natural parturition at 1-week intervals. Before any manipulation, each female received an intravenous injection of 50 to 120 mg Xylazine^® 20% (Accentra Health, Gustav Mahlerplein 90, Amsterdam, The Netherlands, 1082 MA (KEPRO Holland) [4].

Samples were taken from the uterus using sterile single-use swabs (Equivet 663021) that were then transferred to a transport medium (nutrient broth) and immediately transported, under cold conditions, to the laboratory for bacterial cultures.

Bacterial identifications were performed using API_ system (Bio-Mérieux): API staph, API 20 strep and API 20 E strips.

3. Results and Discussion

Dystocia associated with human interventions are the main sources of uterine infection after parturition in females [5]. This work reports the uterine macrobiota in She-camels after parturition. To the best of our knowledge, no description has been reported in this species, except for some aspects related to uterine pathology after parturition [1]. The total number of isolated bacterial strains is high (

Table 1. Rates of bacterial species in the uterine microbiota in She-camels over 6 weeks postpartum.

	Species	Rate (%)
Streptococci	Lactococcus lactis Subsp. Lactis	13
	Lactococcus lactis Subsp. Cremoris	8.6
	Leuconostoc ssp.	8.6
	Aerococcus viridans 1	8.7
	Aerococcus viridans 2	8.7
	Aerococcus viridans 3	8.7
	Streptococcus dysgalactiae subsp. equisimilis	8.7
	Streptococcus pyogenes	4.6
	Streptococcus pneumoniae	4.36
	Enterococcus faecium	4.34
	Streptococcus bovis	4.34
	Enterococcus faecalis	4.34
	Enterococcus avium	4.34
	Streptococcus uberis	4.34
	Streptococcus mitis 1	4.34
Staphylococci	Staphylococcus lentus	50
	Staphylococcus xylosus	50

). Compared to the number of bacterial species, which is relatively low, only two species of negative coagulase Staphylococci (Table 1) are generally nonpathogenic in animals and are likely to be contaminants of the skin [6]. On the other hand, 15 species of Streptococci have been identified (Table 1). These bacteria seem to belong to the uterine microbiota and can be contaminants of fecal and urine origins. During our study, no sign of pathology was observed on the animals and the resumption of heat associated with fertilizing matings argues in favor of the absence of uterine pathological states. It would seem that the composition of the uterine microbiota of our She-camels is, for the majority, lactic bacteria (Table 1) belonging to Leuconostocaceae, Aerococcaceae, Enterococcaceae, and two species of Streptococcaceae. Other species of Streptococcaceae are listed in Table 1.

For convenience, all these bacteria have been considered as Streptococci in Table 1. Our results show a rate of 30.2% of bacteria of the genus Lactococcus and Leuconostoc (Table 1). The three species identified are homofermentative lactic acid bacteria producing lactic acid [7]. It is known that lactic acid bacteria play a determining role in the acidification of the vaginal and uterine environment that is unfavorable to the development of pathogenic bacteria [8]. They have been considered as the main microbiological barrier to infections by genital pathogens [9]. They exert a protective role through a combination of steric exclusion and production of inhibitory substances, such as hydrogen peroxide, and bacteriocin substances that can affect undesirable or pathogenic strains [10].

4. Conclusions

This work represents the first report on the uterine bacterial flora in postpartum camels. This flora, rich in 15 species of streptococci and 2 species of staphylococci, is not accompanied by clinical or subclinical metritis. The females experienced heat followed by natural matings, and the latter were fertile upon ultrasound examination. These bacteria identified using the API 20 strep and API staph galleries appear to be commensals of the uterus and constitute the uterine microbiota in female dromedaries. The absence of clinical signs is likely due to competition between the different bacteria in this microbiota, which contributes to the camel’s resistance to bacterial proliferation and postpartum metritis. It is therefore suggested that female camels should be bacteriologically evaluated to prevent uterine infections before their breeding seasons.