Hysterosalpingographic, ultrasonographic and clinical profile of infertile women in Butembo, Eastern Democratic Republic of Congo

Introduction infertility is a reproductive health issue in modern society. In developing countries, ultrasonography and hysterosalpingography (HSG) are first-line exams investigating infertility in women. It is a highly reported issue in Africa and is linked to abnormalities diagnosed by medical imagery investigations. Our research aimed to evaluate ultrasonography and HSG usage in female infertility investigation in eastern DR Congo, and to point out the most frequent lesions in infertile women in this area. Methods it was a cross-sectional research. It included 1024 patients in four equipped hospitals with HSG and ultrasonography, who consulted from January 1st, 2019 up to December 31st, 2021. Data were collected from consultation dossiers and imagery protocols. Results of 1024 patients, the mean age was 30.85±5.05 years, 41.79 % (n=428) had primary infertility and 57.71% (n=591) had secondary infertility with parity ranges 1.28±1.25, abortion 1.17±1.33. HSG usage rate was 26.85% (n=275) whereas ultrasonography was 66.01%(n=749). The prevalent diagnosed lesions were uterine myomas 10.51 % (n=71), polycystic ovary syndrome (PCOS) 8.28%(n=56), endometrial dysplasia 7.99% (n=54), ovarian cysts 5.03% (n=34) at ultrasonography and tubal obstructions 53.45 %(n=147), hydrosalpinx 4.73% (n=13), cervical impotence 3.27% (n=9), uterine synechias 2.55%(n=7), müllerian abnomalies 2.55%(n=7), uterine retroversion 2.18% (n=6) at HSG. History of upper genital infection was a risk factor aOR= 3.71, 95%CI 1,55-8,88; p <0.001 for tubal obstruction to HSG. Conclusion regarding the high prevalence of tubal and uterine abnormalities in infertile women of eastern DR Congo, ultrasonography, and HSG should be more performed exams in clinical practice in low-income countries.


Introduction
Infertility is defined as failure to get pregnant after 12 months or more of regular unprotected sexual intercourse [1,2].Worldwide, 186 million people suffer from infertility, the majority in developing countries [3].It affects 8 to 12% of reproductive-aged couples, with 20% to 35% due to women [4,5].In women, infertility is caused by abnormalities of the ovaries, uterus, fallopian tubes, and the endocrine system [6].After hormonal analysis, medical imagery is the main complementary exam in its investigation [7].Hysterosalpingography (HSG) and ultrasonography serve as the main tools to explore the anatomy and function of the reproductive system and then to rule out causes and factors of infertility in women [8].

Methods
Study design and setting: this research was conducted in Butembo, eastern DR Congo, in four referral hospitals: Teaching Hospital of Graben, Wanamahika Hospital, Matanda Hospital and FEPSI Hospital.The four hospitals selected have all a gynecologist and imaging equipment.The labels were « Zoncare-V3 2D» for ultrasonography in the four Hospitals and « Siemens Opti 150/12/50 C » for Rx HSG at Matanda Hospital and Wanamahika, and « Kimray Medical » for Rx HSG at Teaching Hospital of Graben and FEPSI.
Study population: our research was a descriptive cross-sectional that included 1024 patients aged 18 years to 45 years old who consulted for infertility in the 4 hospitals from January 1 st 2019 and December 31 st , 2021.Included in our research, were all the patients aged from 18 to 45 years, living with a partner with regular sexual intercourse for 1 year or more, who consulted for infertility.Our sample was exhaustive, taking all the patients who fulfilled the inclusion criteria.
Data collection: data were collected from medical records of patients, with a complete protocol of HSG and/or ultrasonography.
Statistical analysis: they were processed with Epi Info version 7.2.4.0.We included 9 variables: age, marital status, origin, type of infertility, medical and surgical background, history of genital infections, diagnosed lesions at ultrasonography, and HSG.The khi-2 test and odds ratio served to evaluate dependence among variables.
Ethical considerations: participant's identity was kept secret, and our research didn´t use any invasive procedure.Data were collected after the approval of the Ethical Committee of each selected hospital.

Results
General characteristics of the study population: our research included 1024 patients.The use of ultrasonography was at 66.01% (n=676) and HSG was at 26.85% (n=275).The age of patients ranged from 18 to 45 years with an average of 30.85 years; 97.46% were married and 2.54 % were single; 89.26% were from urban areas and 10.74 % from rural areas, 40.33% (n=413) consulted for primary infertility and 59.67% (n=611) had secondary infertility.The demographic characteristics and the histories of patients are presented in Table 1, depending on the type of infertility.

Discussion
Our research aimed to evaluate the rate of HSG and ultrasonography usage in the clinical investigation of infertility in women of Butembo DR Congo and the most frequently diagnosed lesions.It included 1024 patients who consulted for infertility; the average age was 30.85 years.Ultrasonography usage was 66.01% and HSG 26.85%.The most prevalent findings at ultrasonography were myomas at 10.50%, endometrial dysplasia at 7.99%, uterine hypoplasia at 1.78% and tubal obstructions at 53.45%, hydrosalpinx 4.73%, cervical impotence at 3.27 % at HSG. History of upper genital infection was a risk factor aOR= 3.71, 95%CI 1,55-8,88; p <0.001) for tubal obstruction to HSG.In general, female fertility decreases from the age of 35 years, due to ovulatory dysfunctions and other hormonal pathologies [21].Our results were similar to other research in Kisangani DR Congo, Uganda, Cameroon, and Ghana with average ages between 31.7 to 33.52 years [16][17][18]22].The rate of ultrasonography usage was 66.01% in our research and 26.85% for HSG.In normal conditions, these exams should be performed as the first line in female infertility investigation after hormonal screening [23].Nevertheless, the low rate of HSG use in clinical practice may be related to the economic burden of this exam and its invasive character in our context; by the way, Maggie Williams et al. [24] in the United Kingdom and La Fianza A et al. [25] in Italy reported that HSG constitutes a source of anxiety for patients due to its invasive aspect, besides it is an economic burden for African health system [26].However, there was no major difference in proportion neither between a number of ultrasonographies nor HSG performed, based on the sociodemographic background of patients.
Clinical history (Table 1), came to be a factor in infertility onset in women.It is the case of endouterine curettage, tubal surgery, or genital infection [27], especially endo-uterine curettage is reported to be a risk factor of Asherman syndrome, characterized by endo-uterine adherence after traumatic or inflammatory reactions [28,29].Regarding the prevalence of reproductive system anomalies on ultrasound Table 2), uterine anomalies were most prevalent (20.27%), with a significant association between endometrial dysplasia and secondary infertility (p=0.01) and between uterine hypoplasia and primary infertility in patients (p=0.02).The specific uterine lesions on ultrasound were 20.27% (myomas 10.50%, endometrial dysplasia 7.99%, uterine hypoplasy 1.78%), ovarian lesions 13.3% (PCOS 8.28%, and ovarian organic cysts 5.03%) and a normal ultrasonographic result 66.42%.As it has been found in our research, Porcu G and Heckenroth H reported a prevalence of 5 to 10% of myomas in infertile females [30].It is nevertheless an exceptionally isolated cause of infertility [31].Myomas can lead to infertility by hampering the normal process of nidation and abortion induction by reducing the uterine capacity to carry the pregnancy [32].Otherwise, among ovarian lesions, PCOS was most prevalent at 8.28%.This was similar to the results of Brassard et al.where PCOS represented 10 % of causes of infertility in women, in particular primary infertility [33].Polycystic ovary syndrome (PCOS) leads to infertility by anovulation; thus 50% of women with PCOS present primary infertility and 25% secondary infertility; it is reported the cause of 70% of infertility by ovulation [34,35].In the literature, it is reported a prevalence of 5% of adenomyosis in female infertility [36].Yet, our research didn´t report any.This can be related to ultrasonographic sensitivity in our context, its diagnosis requires supplementary skills of the radiologists.
For HSG results, we found the following results (Table 3): tubal obstructions 53.45%, hydrosalpinx 4.73%, cervical impotence 3.27%, endometrial polyps 2.8%, uterine synechia 2.55% and uterine abnormalities 2.55%.These results were similar to those reported in Kisangani, DR Congo, where a prevalence of tubal obstructions of 72.31% was reported at HSG in infertile women [18]; and in Goma Mushabaa K et Labama L reported a prevalence of 67.6% of tubal obstructions in etiology of female infertility [19].In other African countries: in Ghana, Nigeria, Cameroon, and Uganda tubal obstructions were reported respectively at a rate of 43.50%, 30.01%, 36.60%, and 52.90 % in infertile females [12,16,17,22].Hysterosalpingography (HSG) comes as an important exam taking into account the high proportion of tubal factors in infertile females throughout African countries [16,17,37].Many factors explain this high prevalence, in particular concern, genital infection (Table 4) constituted a risk factor of tubal obstruction with 3.71 à IC 95% (1.55-8.88)risk of tubal occlusion in patients with a history of upper genital infection.In general, it is assumed that genital infections represent a high risk of post-infectious adherence, particularly the infection of chlamydia trachomatis [38,39].That way, our results fitted with Egbe TO et al. who reported a risk of 7.3 of tubal occlusion in patients with a history of genital infections in Cameroon, mostly due to complications of postpartum or post-abortum in low asepsis settings [40].In this research, we had the limitation of low rate of HSG performed compared to ultrasonography, to get more statistical significance.Nevertheless, it gave an overview on the clinical investigation of infertility in Eastern DR Congo and the prevalence of subsequent lesions in infertile women.This can serve as a springboard for prospective studies and an orientation for medical professionals in this area, investigating infertility.

Conclusion
Our research included 1024 patients who consulted for female infertility in four gynecological referral hospitals of Butembo, eastern DR Congo, from the 1 st January 2019 to 31 st December 2021.The rate of ultrasonography use was higher than HSG use.The most prevalent lesions in our patients were uterine myomas and PCOS at ultrasonography; tubal obstructions and hydrosalpinx at HSG. Tubal obstructions came as a prevalent lesion in infertile women in Butembo, with genital infection as a major risk.
Matumo, Charles Posite, Alexandre Amini and Ahuka Ona Longombe.Supervision: Olivier Mulisya, Baraka Munyanderu, Philemon Matumo, Charles Posite, Alexandre Amini and Ahuka Ona Longombe.Guarantor of the study: Dieumerci Kaseso.All the authors have read and agreed to the published version of the manuscript.

Table 1 :
demographic characteristics and patients' histories based on type of infertility

Table 3 :
abnormalities observed at HSG based on type of infertility

Table 4 :
risk of tubal obstructions at HSG based on history of genital tract infections

Table 1 :
demographic characteristics and patients' histories based on type of infertility

Table 2 :
abnormalities observed on ultrasonography based on type of infertility

Table 3 :
abnormalities observed at HSG based on type of infertility Hysterosalpingography (

Table 4 :
risk of tubal obstructions at HSG based on history of genital tract infections