Infertility in the Moroccan population: major risk factors encountered in the reproductive health centre in Rabat

Infertility is responsible for a major cost burden for patients and health care systems. Therefore identifying preventable risk factors for infertility may contribute to the development of more cost-effective approaches to solving the infertility problem. However, such investigations have never been conducted in Morocco. Thereby, the objective of the present study was to determine the occurrence and distribution of these factors among Moroccan infertile couples. This retrospective study included 1265 infertile couples who attended the Assisted Reproductive Technology Unit of the Reproductive Health Centre of the University Hospital Ibn Sina in Rabat. All couples had been infertile for at least 1 year and both partners were fully investigated. Couples had primary and secondary infertility in 77.2% and 22.8% of cases, respectively. Women were overweight in 47.9% of cases and obese in 25.8% of cases while men were overweight in 44.6% of cases and obese in 14.7% of cases. 18.9% of women and 17.5% of men had a previous abdominopelvic or urogenital surgery. A history of sexually transmitted infection was reported by 7% of men and 5.8% of women. A history of tuberculosis was found 9.3% of women and 4.8% of men. In addition, 31.7% of men were cigarette smokers and 8.4% consumed alcohol. The study showed that preventable risk factors of infertility are common among Moroccan infertile couples. However, additional studies are required to investigate each factor and its relation to infertility in the Moroccan population.

Introduction polycystic ovary syndrome.Among the female partners, 18.9% had previous abdominal or pelvic surgical treatments. Appendicitis, peritonitis, and intestinal occlusions were reported in 33 (2.6%), 7 (0.5%) and 2 (0.2%) cases, respectively. In 9 cases, the patients could not remember the type of surgery. Fifteen (1.2%) women who had appendectomies and all the women who were operated for peritonitis and intestinal occlusions presented a tubo-peritoneal factor. The history of surgical treatment showed that 17.5% of men had abdominal or urogenital surgery. Eighteen (1.4%) men had surgery for inguinal hernia. Twenty-six (2.1%) men had unilateral or bilateral orchiopexy for undescended testicle diagnosed at an advanced age among them 3 patients (0.2%) had unilateral orchiectomies. Unilateral or bilateral varicocele ligations were performed in 117 (9.2%) men and 2 (0.2%) patients had orchiectomies after a testicular injury.
A history of sexually transmitted infections was found in 73 (5.8%) women and 13 (1%) of them had a pelvic inflammatory disease. A tubo-peritoneal factor was found in 44 (3.5%) women with a previous history of sexually transmitted infections, and in all patients with a previous history of pelvic inflammatory disease. On the other hand, 118 women reported a history of tuberculosis, 82 (6.5%) of these women had a tubo-peritoneal factor. For men, sexually Thirty-nine women reported that they previously had an induced abortion and 2 women had a history of molar pregnancy (  Furthermore, all our patients who had a previous pelvic inflammatory disease had a tubal factor. This is a very high frequency compared to the literature [4]. In a Nigerian study, 52.8% of women with a history suggestive of pelvic inflammatory disease had tubal pathology [15]. The proportion of previous sexually transmitted diseases in our patients might be underestimated for two reasons. First, men and women are usually unaware of the infection due to its asymptomatic character. Second, sexual behaviors in Morocco are still to some extent a social taboo and therefore sexually transmitted diseases are denied and hidden.
In addition to sexually transmitted pathogens, other infectious diseases can also impair fertility such as genital tuberculosis whose incidence ranges from less than 1% in developed countries to almost 13% in the developing world [4,16]. The insidious nature of genital tuberculosis allows it to persist and evolve without detection and infertility might be the first sign of the infection [4,17]. In women, Mycobacterium tuberculosis affects the fallopian tubes in 92-100% of cases, the endometrium in 50% of cases and the ovaries in 10-30% of cases [16]. Thus, this pathogen not only provokes irreversible tubal obstructions, but also affects endometrial implantation and may induce ovulatory failure [16]. In men, genital tuberculosis affects mainly the epididymis rather than the testis.
Less commonly, the prostate might be involved [13,17]. This infection causes severe structural obstruction or anatomic distortion of the epididymis, vas deferens or ejaculatory duct with consequently in most cases obstructive azoospermia [17]. In our study, 20.2% of men with an obstructive azoospermia had a history of tuberculosis. In addition, the study women with a tubal infertility had a history of tuberculosis in 24.3% of cases, which is low compared to India where the reported frequency of genital tuberculosis is 41% in tubal factor infertility [16] and Iran where a study found that 81% of women with tubal factor had a history of tuberculosis [18]. Tubal infertility can also result from pregnancyrelated infections and previous laparotomy [15]. In fact, up to 50% of all abdominal and pelvic surgery elicits adhesions [15]. Peri-tubal and para-ovarian adhesions can cause "follicular entrapment, reduced motility and mechanical blockage of the fallopian tubes thereby limiting oocyte transport" [15]. In a recent study performed by Famurewa investigating the connection between abdominal surgery and tubal infertility, a tubal pathology was found in all the women who have had upper abdominal surgery, surgery for ectopic pregnancy and appendectomy [15]. Similarly, our findings showed that all the women operated for peritonitis and intestinal occlusions presented a tubo-peritoneal factor. However, 45.5% of the women who had appendectomies and 67.6% of women with ectopic pregnancy had a tubal pathology. Among women who had cesarean section, 45.7% had tubal infertility. However, according to previous studies, it seems that cesarean section has no relationship with tubal pathology [15]. Concerning induced abortion, some studies have shown its association with a high risk of tubal infertility while other studies did not [15]. In our study, 38.5% of the women who had an induced abortion had a tubal infertility.
Another factor increasingly associated with the inability to conceive is obesity and overweight. In Morocco, 22% of women and 8% of men are obese [19]. This phenomenon is attributable to the shift in diet and the change to a more sedentary lifestyle [5,19]. This study kg/m 2 . Secondly, obesity has a negative impact on assisted reproductive technologies outcomes [20]. Studies have shown that obese women require higher doses of gonadotrophins and longer duration of ovarian stimulation [6,20]. Cycle cancellation for inadequate response was more frequent, and the number of oocytes retrieved was lower. There was no evidence of an effect on embryo quality [20]. However, pregnancy rates were lower in obese women [6,20]. Thirdly, obesity is associated with a high risk of pregnancy loss [20]. Indeed, Studies investigating the outcomes of pregnancies achieved with assisted reproductive technologies reported an increasing risk of pregnancy loss in overweight and obese women compared with normal weight women [20]. In order to decrease all these negative effects, all patients treated in the assisted reproductive center with a body mass index of more than 25 kg/m 2 are enrolled in a weight loss program. In men, although high body mass index has been identified by large population studies as an independent risk factor for infertility, its relationship with sperm quality remains controversial. In fact, some studies According to the World Health Organisation 2008 report, the current prevalence of smoking among Moroccan adults is 14.2%, with a rate of 29.5% for males and 0.3% for females [22]. In this study, 31.7% of men were smokers while in Bayasgalan's study 48.9% of infertile men were smokers. Many studies investigating the role of cigarette smoking in the reduction of semen quality found a negative relationship between smoking and semen parameters while other studies did not observe any impact [23,24]. However, despite the lack of decisive evidence, "the latest American Society for Reproductive Medicine Committee opinion stated that smoking can affect basic semen parameters in a dose-dependent manner".
Smoking has also a negative impact on sperm function particularly its fertilization abilities. This means that even in the presence of normal semen parameters, sperm functions could still be impaired in smokers [23]. In addition, cigarettes are responsible for increased seminal oxidative stress [24], reduced vesicular and prostatic parameters and increased risk of erectile dysfunction. With regard to male sex hormones, the results of various studies were conflicting [23]. In women, cigarette smoking has been shown to negatively affect folliculogenesis and ovarian reserve. Thus, it is related to earlier menopause, menstrual disorders, and difficulty conceiving.
Studies have reported that smoking women have a reduced menopausal transition by 1 to 1.5 years leading to early menopause [24]. Moreover, smoking is associated with an increased risk of assisted reproductive treatment failure, as well as pregnancy loss [4]. Indeed, increased doses of gonadotrophines are required in smoking women under ovarian stimulation for assisted reproductive treatments [24]. Frequently associated with smoking, chronic alcoholism has a deleterious impact on male and female fertility. In fact, in women, heavy alcohol consumption has been shown to be associated with a decline in ovarian function; and therefore, is responsible for infertility and reduced in vitro fertilization cycle success [25]. In the present study, only men consumed alcohol in 8.4% of cases this frequency is low compared to other countries. In the Mongolian study, 14.9% of men reported alcohol consumption.
In men with chronic alcohol intake, male reproductive hormones are altered, semen quality is impaired and sexual disorders are frequent with a prevalence ranging from 8% to 58% [26]. What is known about this topic  Sexually transmitted diseases represent the most important and most preventable risk factors for infertility;  The incidence of tuberculosis ranges from less than 1% in developed countries to almost 13% in the developing world;

Conclusion
 Obesity and overweight are a global and major concern to public health.

What this study adds
 All the study women with a previous pelvic inflammatory disease had a tuboperitoneal infertility;  There is a high frequency of overweight and obesity among the study population;  The study women with a tubo-peritoneal factor had a history of tuberculosis in 24.3% of cases.

Competing interests
The authors declare no competing interest.

Authors' contributions
All the authors contributed to the conduct of this work. All authors also declare that they have read and approved the final version of the manuscript. Tables   Table 1: History of the study couples  Values are given as number (percentage of the 1265 of the study women). Some women had more than one infertility factor.