|Year : 2015 | Volume
| Issue : 3 | Page : 110-116
Evaluation of pattern of tubo-peritoneal abnormalities potentially responsible for infertility in Zaria, Nigeria: hysterosalpingographic assessment
Reuben Omokafe Lawan1, Philip Oluleke Ibinaiye1, Polite Onwuhafua2, Ahmed Hamidu1
1 Department of Radiology, Ahmadu Bello University Teaching Hospital, Zaria, Kaduna State, Nigeria
2 Department of Obstetrics and Gynecology, Ahmadu Bello University Teaching Hospital, Zaria, Kaduna State, Nigeria
|Date of Submission||03-Dec-2014|
|Date of Acceptance||21-May-2015|
|Date of Web Publication||3-Sep-2015|
Philip Oluleke Ibinaiye
Department of Radiology, Ahmadu Bello University Teaching Hospital, Zaria, Kaduna State
Background: Structural abnormalities on hysterosalpingography (HSG) are among the important factors in the evaluation of female infertility. Aim and Objective: This study is mainly concerned with the pattern of tubal and peritoneal abnormalities and their effects on fertility outcome. Materials and Methods: A prospective study of 220 consecutive patients who underwent HSG between December, 2011 and May, 2013, at Department of Radiology, Ahmadu Bello University Teaching Hospital, Zaria. Clinical notes and radiological findings were analyzed for demographic data, tubal and peritoneal pathologies. Fertility outcome in patients with abnormal findings was compared with those with normal findings. Results: A total of 121 (55.0%) patients had normal tubes on HSG. Tube abnormalities were found in 99 (45.0%) patients; 37 (37%) patients with primary and 62 (63%) patients with secondary infertility. Totally, 203 (92.3%) patients had normal peritonea contrast medium spillage on HSG. Peritoneal cavity abnormality (pelvic adhesion) affected 17 (7.7%) patients; 8 (47%) patients with primary and 9 (53%) patients with secondary infertility. The fertility outcome showed that after 1-year of follow-up, 3 (2.6%) of the 116 patients with abnormal findings (tubal and peritoneal abnormalities) got pregnant, while 25 (34.7%) of the 72 patients with normal findings (tubal, peritoneum, cervical canal and endometrial cavity) got pregnant. The difference noted was statistically significant (P = 0.0000). Conclusion: Fertility outcome in patients with tubo-peritoneal abnormalities at HSG was low.
Keywords: Abnormalities, hysterosalpingography, infertility, peritoneal, tubal
|How to cite this article:|
Lawan RO, Ibinaiye PO, Onwuhafua P, Hamidu A. Evaluation of pattern of tubo-peritoneal abnormalities potentially responsible for infertility in Zaria, Nigeria: hysterosalpingographic assessment
. Sub-Saharan Afr J Med 2015;2:110-6
|How to cite this URL:|
Lawan RO, Ibinaiye PO, Onwuhafua P, Hamidu A. Evaluation of pattern of tubo-peritoneal abnormalities potentially responsible for infertility in Zaria, Nigeria: hysterosalpingographic assessment
. Sub-Saharan Afr J Med [serial online] 2015 [cited 2021 Apr 15];2:110-6. Available from: https://www.ssajm.org/text.asp?2015/2/3/110/164418
| Introduction|| |
Infertility is a major global problem and is regarded as a social stigma in the Nigerian society, affecting 5-15% of couples in developed countries and 10-20% of couples in developing countries. , Infertility is a failure of a couple of reproductive age to conceive after 12 months or more of regular coitus without the use of contraception.  It is considered primary infertility when it occurs in a woman who has never established a pregnancy and secondary infertility when it occurs in a woman who has a history of one or more previous pregnancies. 
Factors from either or both partners may contribute to infertility. Factors in male account for 35%, while female factors account for 60-65% of causes of infertility.  In the female, ovulatory dysfunction accounts for 40% of causes of infertility, with uterine, tubal and pelvic pathologies accounting for the remaining 60% of causes. 
The major cause of tubal pathology and infertility in sub-Sahara Africa is pelvic inflammatory disease (PID), usually due to Neisseria More Details gonorrhea. Other causes include chlamydia and tuberculosis.  This usually results to tubal occlusion, hydrosalpinx, peritubal adhesion or salpingitis isthmica nodosa (SIN).  Other causes of tubal occlusion include, endometriosis, pelvic adhesions, mucus plugging, surgical ligation, salpingectomy, and tumors. 
It has been estimated that PID related tubal adhesions, causes 30-50% of all cases of female infertility, bilateral tubal occlusion was noted in 20% of cases in a study carried out in Kenya.  In Nigeria, tubo-peritoneal factors have been shown to be the commonest cause of infertility, contributing to as much as 64% in some series due to high prevalence of sexually transmitted infection. 
Hysterosalpingography (HSG) is a diagnostic procedure in which there is radiographic visualization of the endocervical canal, the endometrial cavity and lumina of the Fallopian tube More Detailss by the injection of radiopaque contrast medium.  Despite the development of other radiological methods of visualizing the female reproductive tract, HSG remains the main radiological method used in evaluation of infertile women in developing countries. 
There is paucity of information in our environment on the effects of tubo-peritoneal abnormalities on fertility outcome in women with infertility.
This study is mainly concerned with the pattern of tubal and peritoneal abnormalities and their effects on fertility outcome.
| Materials and methods|| |
This prospective study was carried out at the Ahmadu Bello University Teaching Hospital (ABUTH), which is a tertiary health institution located in Shika-Zaria, Kaduna State, Nigeria. The city has a population of 975,153. 
This prospective study was carried out between December, 2011 and May, 2013 on 220 consecutive patients referred from infertility clinics of the ABUTH for HSG. Patients were counseled on the procedure and possible complications. Consent was duly obtained. Demographic data such as age, parity, and duration of infertility were extracted from specially designed data collection form. After the HSG, the patients were followed up for a period of 1-year in the infertility clinic, during which details of the therapeutic intervention and fertility outcomes were extracted from their medical records.
Those that were excluded from the study included: Patients with vaginal discharge, recent history of intrauterine instrumentation, ongoing vaginal bleeding, history of previous salpingectomy, pregnancy, palpable adnexa masses.
Technique of hysterosalpingography
Patient referred for HSG reports at the radiology department for booking, where the patients were educated about the examination. All their questions concerning the examination were fully answered. An explanation of the procedure,  including that placement of the speculum, vulsellum and cannula may cause cramping, was done to help reduce anxiety and prepare their state of mind. The patients were told of likely risk of contrast reaction and postprocedural bleeding. Also, patients were asked to abstain from sexual intercourse after the last menstruation until the procedure is carried out to prevent pregnancy, and patient to fast on the day of examination to prevent vomiting and aspiration in case of contrast reaction.
HSG was performed on 10 th day of the menstrual cycle, to ensure a thin endometrium, which prevents intravasation of contrast medium and makes interpretation of the images easier, and also to be sure that the patient was not pregnant. In patients with irregular menstrual cycle and amenorrhea, HSG was done after pelvic ultrasonography to ensure a thin endometrium (<6 mm) and also to rule out pregnancy. An intravenous line is secured prior to the procedure, for resuscitation in case of contrast reaction and injection of Hyoscine-N-butylbromide. Sterile gowns were provided for the patients to wear after removing their cloths.
Scout films (antero-posterior [AP] of the pelvis) were obtained to ascertain good radiographic factors settings and also to detect any premorbid condition.
The patients were placed in the lithotomy position, with the thighs flexed and abducted, the feet resting in stirrups, and the buttocks extending slightly beyond the edge of the examining table for ease of examination. The patients were premedicated with IV Hyoscine-N-butylbromide (20 mg) 5 min before the beginning of the procedure to prevent fallopian tube spasm.
The perineum and vagina were cleaned with savlon (containing; cetrimide 3% w/v, chorhexidine gluconate 0.3% w/v. Dilution ratio; 60 mL in 1 L of sterile water), using a sponge holding forceps and sterile gauze. The cleaning process starts from the vagina then the perinea area last.
Before insertion of the speculum, external genitalia of the patients were inspected. With a sterile gloved hand, the labium was separated to inspect the vaginal orifice and introitus for any induration, inflammation, or ulcerations that will make placement of a speculum difficult and painful. In situation where inflammation was suspected, the examination was put on hold and the patient's physician notified. A digital examination with lubricated fingers was done to determine the position, depth, and orientation of the cervix.
A Cusco's speculum of appropriate size is selected. Under aseptic condition and bright illumination, the speculum was inserted into the vagina with the blades held obliquely and pressure exerted toward the posterior vaginal wall to avoid the more sensitive anterior wall and urethra. Appropriate measure was taken not to pull on the pubic hair or to pinch the labia with the speculum. Holding the labia apart with the fingers of the free hand enables the speculum to be placed without dragging or pulling the labia into the vagina. After the speculum was successfully placed in the vagina, the blades were rotated into a horizontal position, and opened after full insertion, then maneuvered so that the cervix comes into full view. The speculum was secured with the blades open by tightening the thumbscrew.
The anterior lip of the cervix was held with a vulsellum forceps, and uterine sound was introduced to determine uterine size and direction. An appropriate size Leech Wilkinson's cannula was selected and inserted into the distal end of the cervical canal, after prefilled with contrast medium to eliminate air bubbles. While maintaining a tight seal between the cervical canal and the cannula, a water soluble contrast medium, urografin 76% (20 mL contains sodium amidotrizoate 200 g and meglumine amidotrizoate 1320 g, with iodine concentration of 370 mg l/mL. Diluted with water for injection in ratio 1:1, to prevent peritoneal irritation) was injected slowly into the uterine cavity and the fallopian tubes under fluoroscopic guidance. About 7-10 mL of contrast medium produces good uterine visualization; larger quantity usually obscures subtle filling defects. However, in a grossly dilated uterine cavity, larger volume of contrast medium was used.
Before film exposure, the position of the marker was ascertained, and then a gentle traction was applied on the cervix to bring the uterus to horizontal position relative to X-ray tube. The contrast medium was injected in a slow and steady fashion while watching its progress under fluoroscopy.
Early radiograph of the uterine cavity when it first fills with contrast medium was obtained because further injection of contrast medium can sometimes obscure intracavitary pathology. Continuous contrast medium injection and intermittent fluoroscopy screening were done and film exposed when the tube fills and spills into the peritoneal cavity. Patients were turned to right or left oblique position to delineate the fallopian tubes better if necessary.
Pelvic radiographs were obtained in AP supine and right and left oblique positions during the injection of the contrast medium. Delayed radiographs were obtained 30 min after completion of the procedures when necessary, to assess the degree of loculation of contrast medium in the peritoneal cavity.
Prior to the commencement of the study, approval was giving by the ethical and research committee of ABUTH. In addition, informed and written consent was obtained from the participants in the study.
Data were analyzed using Statistical Package for Social Sciences version 16 (SPSS Inc, Chicago, Illinois, USA), computer software for statistical analysis. Analyses test used in this study was Pearson's Chi-square statistic. Primary infertility, secondary infertility, normal findings, pattern and prevalence of tubal and pelvic peritoneal abnormalities as demonstrated on HSG among patients with infertility were summarized in figures and percentages (%). Also, reproductive outcome in patients with structural abnormalities and normal HSG findings were compared to determine the effect of HSG findings on fertility outcome. Findings were presented in graphical and tabular forms. All tests of significance were two-tailed, and P < 0.05 was considered as statistically significant.
| Results|| |
Two hundred and twenty patients with infertility were interviewed and investigated. The age ranged from 18 to 40 years and shows a normal age distribution curve, with mean age of 27.37 ± 1.4 [Figure 1]. The duration of infertility ranges from 1 to 8 years with a mean duration of 4.48 years as shown in [Table 1].
[Table 2] shows that patients with secondary infertility were 133 (60.5%) and primary infertility were 87 (39.5%). The young aged group, 18-30 years, had a high proportion of primary infertile participants (46.4%) while high proportion of secondary infertile patients, 78.8% were in age group 31-40 years. However, there was more secondary infertility in both age groups.
[Table 3] shows that a total of 72 patients (32.7%) had tubal occlusion. A total of 11 patients (5%) had bilateral tubal occlusion. Right tubal occlusion was noted in 33 patients (15%), this was slightly higher than the left tubal occlusion, which was observed in 28 patients (12.7%), the deference noted was statistically significant (P = 0.004). A total of 23 patients (10.5%) had hydrosalpinx. Left hydrosalpinx [Figure 2] was noted in 14 patients (6.4%), while right hydrosalpinx was noted in 9 patients (4.1%), the difference noted was not statistically significant (P = 0.297). A total of 4 patients (1.8%) had SIN, 2 (0.9%) were bilateral while the remaining 2 (0.9%) had left SIN.
|Figure 2: Hysterosalpingography showing dilated left fallopian tube (hydrosalpinx) without spillage of contrast medium into the peritoneal cavity. The right tube is proximally occluded|
Click here to view
[Table 4] shows that 17 patients (7.7%) had pelvic adhesion, seen as loculated spill, convoluted or crowded tubes and vertical oriented tubes. Bilateral pelvic adhesion was seen in 5 patients (2.3%). Right pelvic adhesion was seen in 8 patients (3.2%) while left pelvic adhesion was seen in 4 patients (1.8%). The difference noted was statistically significant (P = <0.0001).
[Table 5] shows that after 1-year of follow-up, 3 (2.6%) of the 116 patients with abnormal findings (tubal and peritoneal abnormalities) got pregnant, while 25 (34.72%) of the 72 patients with normal findings (tubal, peritoneum, cervical canal and endometrial cavity) got pregnant. The difference noted was statistically significant (P = 0.0000).
In total, 28 patients became pregnant. A total of 14 (50%) patients were spontaneous pregnancies after HSG while 14 (50%) patients had therapeutic intervention before they conceived.
[Table 6] shows the distribution of pregnancy occurrence and therapeutic intervention in patient with abnormal HSG findings. Unilateral tubal occlusion was seen 61 patients, 2 (3.3%) became pregnant spontaneously. Unilateral hydrosalpinx was noted in 23 patients, 1 (4.3%) came pregnant after salpingectomy.
|Table 6: Summary of the distribution of fertility outcome and therapeutic intervention in patients with abnormal HSG fi ndings|
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| Discussion|| |
The mean age of participants in this study was 27.37 years; this was similar to the mean age of infertile women in another study by Bello  in Ilorin, Nigeria. However, this value is lower than that of Okafor et al.  in Nnewi, Southeastern Nigeria where the mean age of their study was 32.41. The difference may be due to cultural differences influencing the age at marriage.
The mean duration of infertility was 4.48 years which is similar to previous study done in Nigeria.  The mean duration of infertility is reported low in other previous studies conducted in India.  Most of the patients in this study had 4-8 years of infertility with the majority of these patients, showing significant number of abnormalities (74%). This long duration could be attributed to lack of awareness of the importance of early treatment among the infertile couple. The presence of enormous local traditional healing practices and religious believes could be an important contributory factor for the delay in presentation to health facilities.
In this study, more patients had secondary infertility than those with primary infertility, which is similar to other previous studies. , However, this differs from other studies where it was found that primary infertility was commoner. ,, This higher rate of patients with secondary infertility compared to primary infertility can be used as a crude indicator of the possible effects of PID, postabortal sepsis and puerperal sepsis in our setting. ,
The prevalence of tubal abnormalities demonstrated in the present study was 45%, which was similar to what was reported by Bello  in Ilorin, Nigeria (40%). This is much lower than that found by Baramki  in Lagos (61.8%). This discrepancy between Northern and Southern part of Nigeria may be due to cultural differences as par exposure to premarital and extra-marital sex and its sequelae such as sexually transmitted diseases and PID. The common tubal abnormality found was tubal blockage (32.7%), which was similar to the report of Kiguli-Malwadde and Byanyima.  Bilateral tubal blockage was noted in 5% of the total patients while right tubal blockage occurred in 15% and left in 12.5% of the total patients. It may, however, be difficult to differentiate bilateral tubal bockage from bilateral cornual spasm or underfilling from technical inadequacies. Radiographically, cornual spasm is characterized by a taper and smooth cornual margin, which is pointed or blunted and irregular in cases of occlusion.  However, the use of antispasmodics and a gentle technique were employed to minimize the effect of spasm in this study.
Hydrosalpinx is seen as a dilated convoluted tubular structure on HSG which gradually increase in size due to distal tubal occlusion.  It is a result of fallopian tubes inflammation following infections such as gonococcal, chlamydial or tuberculosis of the genital tract. The fimbrial ends are eventually occluded due to adhesions leading to collection of the secretions in the lumen with gradual distension of the fallopian tube.  The incidence of hydrosalpinx (10.5%) is less in this study than similar studies done in Ilorin by Adetiloye  (44.5%) and Bello  (23.3%). This might be due to the conservative culture in Zaria predisposing the patients less to sexually transmitted diseases and postabortal complications responsible for hydrosalpinx. The lower value may also be due to the improvement in the health care delivery system over the years. A lot of researchers suggested that the presence of the appendix on the right side may predispose to increased PID on the right side with resultant hydrosalpinx.  However, in this study, the left hydrosalpinx (6.4%) was more than the right (4.1%), and therefore, the above theory does not apply. However, the appendix theory could explain the statistically higher prevalence of right tubal occlusion than the left.
Salpingitis isthmica nodosa is a rear condition involving the fallopian tube due to chronic salpingitis. It is usually seen on HSG as small diverticular extending from the lumen of the tubes, involving the isthmus and associated with infertility and ectopic pregnancy.  In this study, 1.8% of the total patients had SIN. This is similar to the finding of Troell  (1.1%) but less than the finding of Creasy et al.,  who reviewed 1184 HSG and identified only 45 patients with SIN (3.8%).
Pelvic adhesions are usually formed as a result of inflammation from PID. Adhesion disturbs the delicate anatomical relationship between the tubes and ovaries, interfering with the normal ovulation or preventing the normal capture and transport of the ovum.  In this study, patients with features of pelvic adhesions accounted for 7.7% of all infertile patients. A study conducted previously in Uganda showed that the peritubular adhesion was higher (28%) while that done in Pakistan was lower, 7% of all patients. , This high incidence of tubo-peritoneal related pathologies may be due to PID, which is reported to be the most common gynecological disease affecting many African women. , Also, noncompliance to PID treatment, which may lead to sub-acute or chronic PID with deleterious effects on the fallopian tubes, may also be a contributory factor. This indicates that PID is still common in our environment and makes it a common cause of infertility.
The fertility outcome show that after 1-year of follow-up, 3 (2.6%) of the 116 patients with abnormal findings (tubal and peritoneal abnormalities) got pregnant, while 25 (34.7%) of the 72 patients with normal findings (tubal, peritoneum, cervical canal and endometrial cavity) got pregnant. The difference noted was statistically significant (P = <0.0001). This is different from the findings in the work of Schankath et al.,  in Switzerland, where they observed a higher pregnancy rate in patients with pathological HSG. The poor fertility outcomes associated with patients with structural abnormalities in this study are multifactorial. This includes lack of appropriate expertise necessary for infertility management, nonavailability of advance equipment required for proper management of infertility and financial constrain on the part of the patients.
Among the 28 patients that conceived, 14 had spontaneous pregnancies after HSG; while 14 patients had therapeutic interventions (adhesiolysis, salpingectomy, ovulatory induction, timed-intercourse, and intrauterine insemination) before they conceived. High pregnancy rate noted in patients without therapeutic intervention may be due to the therapeutic effect of HSG. It is a known and undisputable fact that HSG also has therapeutic value. Following HSG, certain mild uterine adhesion and partial tubal occlusion are lysed and hitherto infertile women have conceived months after HSG without any other gynecological intervention. 
| Conclusion|| |
Fertility outcome in patients with tubo-peritoneal abnormalities at HSG was low. The high spontaneous pregnancy rate in patients with unexplained infertility may be due to therapeutic effect of HSG.
| Acknowledgment|| |
The authors acknowledged the contribution of staff of departments of Radiology and Obstetrics and Gynecology, Ahmadu Bello University Teaching Hospital, Zaria, Nigeria while carrying out this research work.
Financial Support and Sponsorship
Conflicts of Interest
There are no conflicts of interest.
| References|| |
Irinia P. A Guide to Reproduction: Social Issues and Human Concern. Cambridge: Cambridge University Press; 1994. p. 3-17.
Belsey MA. The epidemiology of infertility: A review with particular reference to sub-Saharan Africa. Bull World Health Organ 1976;54:319-41.
Phleps JY, Thomas AU. Diagnosis and cotemporary management of infertility. Clin Obstet Gynecol 1978;18:1-7.
Speroff L, Gass GI, Constantine RH, Kase GN. Female infertility. In: Clinical Gynaecological Endocrinology and Infertility. 7 th
ed. Baltimore: William and Walkin; 1992. p. 1013-68.
Seibel MM. Diagnostic evaluation of infertile couple. In: A Comprehensive Text of Infertility. 2 nd
ed. New York, USA: Appletan and Lange; 1997. p. 3-11.
Lapido OA. Tests of tubal patency: Comparison of laparoscopy and hysterosalpingography. Br Med J 1976 27;2:1297-8.
Bhatla N. Infection as they infect individual organs. In: Jeffcoates Principles of Gynaecology. 6 th
ed. The University of Michigan, Michigan, USA: Butterworths; 2001. p. 355-74.
Idrisa A, Ojiyi E. pattern of infertility in North-Eastern Nigeria. Trop J Obstet Gynaecol 2000;17:27-9.
Lindheim SR, Sprague C, Winter TC 3 rd
. Hysterosalpingography and sonohysterography: Lessons in technique. AJR Am J Roentgenol 2006;186:24-9.
Ubede B, Marta P, Enric A, Ramonm AA. Pictoral essay: Hysterosalpingography: Spectrum of normal variant and pathological findings. AJR Am J Roentgenol 2001;177:133-5.
National Population Commission. National Demographic Survey; 2006. Available from: http://www.population.gov.ng/. [Last accessed on 2014 Nov 25].
Oh DJ, Faye JA. Hysterosalpingogram. In: Normal Radiographic Anatomy. 4 th
ed. Baltimore: Blackwell Scientific Publication; 1999. p. 29-39.
Bello TO. Pattern of tubal pathology in infertile women on hysterosalpingography. Ann Afr Med 2004;3:72-9.
Okafor CO, Okafor CI, Okpala OC, Umeh E. The pattern of hysterosalpingographic findings in women being investigated for infertility in Nnewi, Nigeria. Niger J Clin Pract 2010;13:264-7.
Oluwaseun OF. Reproductive outcome following hysteroscopic adhesiolysis in patient with Asherman's syndrome. Wold J Laparosc Surg 2011;4:31-9.
Akinola RA, Akinola OI, Fabamwo AO. Infertility in women: Hysterosalpingographic assessment of the fallopian tubes in Lagos, Nigeria. Educ Res Rev 2009;4:86-9.
Watson A, Vandekerckhove P, Lilford R, Vail A, Brosens I, Hughes E. A meta-analysis of the therapeutic role of oil soluble contrast media at hysterosalpingography: A surprising result? Fertil Steril 1994;61:470-7.
Obejide AO, Ladigo OA, Otolorin FO, Makamagola JD. Infertility in Nigerian women. A study of related physiological factors. J Obstet Gynaecol East Cent Africa 1986;5:61-3.
Mesbazri S, Pourissa M, Refahi S, Tabarraei Y, Dehgha MH. Hysterosalpingographic abnormalities in infertile women. Res J Biol Sci 2009;4:430-2.
Kiguli-Malwadde E, Byanyima RK. Structural findings at hysterosalpingography in patients with infertility at two private clinics in Kampala, Uganda. Afr Health Sci 2004;4:178-81.
Baramki TA. Hysterosalpingography. Fertil Steril 2005;83: 1595-606.
Adetiloye VH. Radiological patterns of diseases on Hysterosalpingography. Dissertation. National Postgraduate Medical College of Nigeria, Lagos; 1988. p. 64-100.
Troell S. Diverticula of the walls of the Fallopian tubes. Acta Obstet Gynecol Scand 1970;49:17-20.
Creasy JL, Clark RL, Cuttino JT, Groff TR. Salpingitis isthmica nodosa: Radiologic and clinical correlates. Radiology 1985;154:597-600.
Naula U. Hysterosalpingography. Prof Med J 2005;12:386-91.
Schankath AC, Fasching N, Urech-Ruh C, Hohl MK, Kubik-Huch RA. Hysterosalpingography in the workup of female infertility: Indications, technique and diagnostic findings. Insights Imaging 2012;3:475-83.
[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]