This is a cross-sectional, descriptive and analytical study carried out in women who came to a gynecological consultation for cervical cancer screening during the period from January 1, 2017 to December 31, 2018 at the Panzi GRH (South Kivu, DR Congo). In total, we recorded 625 women, all of whom had Pap smears.

Pregnant women, those with a sexually transmitted disease other than HIV, those already receiving cervical cancer treatment and those who refused to respond to the questionnaire were excluded from the study.

A pre-established form was completed by the clinical physician during the interview with the women who consented to the study, and gathered information on socio-demographic characteristics (age, marital status, occupation, level of education, socio-economic level, etc.), sexual and gynecological obstetrics (age at menarche, age at first sexual intercourse, number of previous sexual partners, type of sexual intercourse, age at first pregnancy, notion of sexual violence involving rape with penetration, notion of smoking, hormonal contraception, parity and HIV antecedent).

All the women included in the study benefited from cervical uterine smear sampling. This sampling was carried out after sensitization by a qualified medical staff and in respect of all ethical considerations. The cytopathological results made it possible to describe the different cytopathological aspects of cervical lesions.

The following variables were studied:

· Dependent variable:

It was represented by the cytopathological results. The cytopathological examination of the smear revealed the following aspects: normal and inflammatory smear, atypical lesions (ASC-US and AGC), low-grade squamous intraepithelial lesions (LSIL) and high-grade squamous intraepithelial lesions (HSIL). These results were grouped into two classes: atypical, low-grade and high-grade intraepithelial lesions (ASC-US + AGC + LSIL + HSIL) that are precancerous and those related to normal smear (normal + inflammatory smear; the latter being a lesion non-precancerous).

· Independent variables:

They were constituted by socio-demographic, sexual and gynecological characteristics of the women examined.

Data analysis was done using Epi Info version 7 software. Descriptive statistics were used to describe women by sociodemographic, sexual and gynecological variables. The associations between the dependent variable and the set of explanatory variables (in terms of proportions observed in the contingency tables) were tested using Pearson’s Chi-2 test and Fisher’s exact test for qualitative variables. Odds ratios (ORs) with a 95% confidence interval were used to measure the level of association between variables. For multivariate analysis, logistic regression was used to calculate adjusted ORs to identify possible determinants of dysplastic lesions. The materiality threshold was set at p < 0.05.

Ethical considerations were taken into account, as mentioned above, after favorable opinion of the local ethics committee and UNILU (University of Lubumbashi).

Nearly half of the women surveyed were aged 35 and over (49.1%), with a median age of 34 and married (47.0%). The housewife accounted for 39.7% of the respondents, while 40.2% had a low socio-economic level (Table 1).

Just over half of the women had menarche between 14 and 15 years of age (51.8%), with an average age of 13.9 ± 1.6 years. The majority of them had their first sexual intercourse between the ages of 15 and 20 (67.5%), and a number of former sexual partners estimated at 1 - 5 (87.8%). Normal sex was the most common type (94.7%). The age at first pregnancy was in most cases between 15 and 20 years (68.8%). The majority of women did not experience sexual violence (73.9%), did not use tobacco (97.4%) and did not use contraception (78.1%). Several of them (59.0%) were multiparous. Those who reported an antecedent of HIV accounted for 21.9% (Table 2).

For all the respondents (Table 3), the cervical uterine smear was normal in 82.88% and inflammatory in 2.4% of the cases, whereas the cytological abnormalities, which were found in 14.72% of the cases, included 9.44% of atypia (8.8% of ASC-US, 0.48% of AUC-H and 0.16% of AGC), 4.48% low-grade squamous intraepithelial lesions (LSIL) and 0.8% high-grade squamous intraepithelial lesions (HSIL).

· Cytopathological results in the respondents.

Thus, out of a total of 625 women examined, 92 or 14.7% (95% CI: 12.1% - 17.8%) had dysplastic lesions (ASC-US, ASC-H, LSIL, HSIL and AGC) against 85.3% with normal and inflammatory smear.

The rate of dysplastic lesions was significantly higher among women in the age group ≥ 35 years, the risk being doubled compared to their counterparts aged 25 - 34 (OR 95% CI: 2.1 [1, 10 - 4.24], p = 0.0245). The difference was also significant (p = 0.0183) for brides and other marital statuses (widowed, divorced, polygamous) compared to single women, with the risk of having a dysplastic lesion being multiplied by about two, respectively (OR 95% CI: 1.97 [1.003 - 4.12]) and three (95% OR: 2.61 [1.28 - 5.62]). On the other hand, there was no significant difference (p < 0.05) in women’s occupation, education level and socio-economic level (Table 4).

The rate of dysplastic lesions was very significantly higher in nulliparas and in primiparous and pauciparous patients, the risk being respectively nearly five and three times higher compared to multiparas (OR 95% CI: 4.73 [1.69 - 18.36] and 3.33 [1.08 - 13.75], p < 0.0042). In contrast, there was no significant difference in dysplastic lesions between menarche age groups (p = 0.9794), age groups at first intercourse (p = 0.8144). ), number of previous sexual partners (p = 0.4448), type of sexual intercourse (p = 0.4496), age at first pregnancy (p = 0.7535), notion of sexual abuse (p = 0.3552), smoking concept (p = 0.5734), hormonal contraception (p = 0.1181) and HIV antecedent (p = 0.158) among respondents (Table 5).

To measure accurately the linkage power between factors associated with dysplastic lesions, a multivariate analysis (logistic regression) was performed as advertised in the methodology and took into account significant independent variables following the bivariate analysis of dysplastic lesions cases observed in the respondents (Table 4 and Table 5).

Multivariate analysis revealed statistically insignificant ORs (p < 0.05) for the age, marital status and parity variables of the respondents (Table 6).

The immunosuppression (HIV infection, immunosuppressive therapy, etc.) plays a major role in the occurrence of dysplastic lesions of the cervix [1] [46]. Several studies have supported the coexistence between HIV infection and human papillomavirus [34] [47] [48] [49] [50].

In our series, about a quarter of women, or 21.9%, was HIV positive. This non-insignificant frequency of HIV infection is explained by the low standard of living of the population, pushing girls and women into unsafe sexual practices and unprotected sex.

Smoking is one of the risk factors for cervical cancer [1] [46]. Our study reveals a low rate of women consuming tobacco (2.5%). Shin SS et al. [23] had a slightly lower rate than ours of 1.8% of women who had used tobacco in the past.

Other authors had far greater results than ours regarding women who had used tobacco in the past: Godfrey M.A.L et al. [42] in the United Kingdom (41.9%), Pokomandy A et al. [51] in Canada (54.1%); Agorastos A et al. [52] in Greece (77.45%), Wudtisan J et al. [35] in Thailand (26.7%) and Bogani G et al. [53] in Italy (20.9%).

This very low rate of women consuming tobacco in our environment is explained by the absence of this habit in the community, as smoking is considered to be the preserve of men.

Pap smear is the screening tool currently recommended for precancerous and cancerous cervix lesions. The technique developed by Papanicolau and Babès is inexpensive, simple and acceptable, painless and reproducible, non-invasive, with no contraindications [46]. For more than half a century, it has been effective since its introduction, the invasive carcinoma of the cervix has seen its frequency considerably decreased. However, the biopsy remains the gold standard, it is she who confirms the lesions after detection by cytology and orientation by colposcopy [46]. Biopsy is therefore indicated in cytological lesions of low and high grade [46].

In our series, cervical-uterine pap smears was normal in 82.88% and inflammatory in 2.4% of cases, while cytological abnormalities, which were found in 14.7% of cases, included: 9.44% atypia (8.8% ASC-US, 0.4% ASC-H and 0.16% AGC); 4.48% low-grade squamous intraepithelial lesions (LSIL) and 0.8% high-grade squamous intraepithelial lesions (HSIL). Wang JJ et al. [54] in China found: normal cervical-uterine pap smears in 71.7% of cases versus 14.8% ASCUS; 8.7% of LSIL and 2.3% of HSIL. Kasap B et al. [55] found in their study in Turkey: a rate of 84.9% normal cervical-uterine pap smears; 1.55% ASC-US; 5.3% LSIL and 4.0% HSIL. Garbuglia AR et al. [50] in Italy had the following results: normal cervical-uterine pap smears in 76.4% of cases; ASC-US, LSIL and HSIL in 24.4% of cases while Correa CM et al. [56] obtained a normal cervical-uterine pap smear in 63.2% in Brazil. Agaba AP et al. [57] reported, in Nigeria, 31.7% of normal cervical-uterine pap smears; 39.3% ASC-US; 15.2% of LSIL and 13.8% of HSIL. Takamatsu R et al. [58] in Laos resulted in the following results: 90.7% normal cervical-uterine pap smears; 5.3% ASC-US; 0.6% ASC-H; 2.3% of LSIL; 0.9% HSIL and 0.07% SCC.

In view of the results of the above studies, we can say that cervical cytopathology was normal in the majority of cases in our series. This normality of the cervical-uterine pap smears is explained by the sensitivity of this examination which is about 70% to 80%.

The study of the association between socio-demographic characteristics and cytology (Table 4) shows that the proportion of dysplastic lesions was significantly higher in women ≥ 35 years of age (18.6%), more particularly compared to the 25 - 34 age group (9.8%) with almost twice the risk of having dysplastic lesions (p < 0.0245, OR = 2.1, 95% CI [1.10 - 4.24]). With regard to marital status, brides (15.3%) and widows, divorced and women in polygamous unions (19.3%), compared with single men (8.4%), had a significantly higher (p = 0.0183) dysplastic lesions of the cervix with respectively two and three times more risk of developing this type of lesions (OR = 1.97, 95% CI [1.003 - 4.12] and OR = 2.61, 95% CI [1.28 - 5.62]).

On the other hand, we did not note a statistically significant difference according to the occupation, the level of education and the socio-economic level, notwithstanding the risk more or less high to present dysplastic lesions highlighted in the women farmers (OR = 1.23, 95% CI [0.65 - 2.28], p = 0.7725), women with a higher level of education (OR = 1.41, 95% CI [0.52 - 3.45], p = 0.8515) and women of low socioeconomic status (OR = 1.15, 95% CI [0.71 - 1.87], p = 0.3095).

Several studies have been done and have revealed the correlation between socio-demographic characteristics and cytopathology in case of precancerous lesions of the cervix.

Indeed, Adenis A et al. [59] found in their study in Guyana a higher risk of developing dysplastic lesions in women aged 50 to 64 than in all women (OR = 4.8, 95% CI [0.6%] 39.5]); it was the same for those with a low level of education (OR = 2.1, 95% CI [0.5 - 8.9]) without the difference being significant. Berraho M et al. [60] have observed in their series in Morocco a high risk of cervical cancer in divorced women (OR vs. married women = 2.4, 95% CI [1.3 - 4.6]), women with (95% CI 95%), women living in rural areas (OR = 10.7, 95% CI [5.3 - 21.8]) and those with a low socio-economic level (OR = 3.1, 95% CI [1.8 - 5.4]).

Vinodhini K et al. [61] found in their study in India that the proportion of dysplastic lesions was statistically higher among illiterate women (OR = 8.28, 95% CI [5.51 - 12.83], p < 0.004).

We find that the results are slightly different according to the authors, this would be related to the sample size of each study, a key element for statistical significance.

The proportion of dysplastic lesions in our series was very significantly (p = 0.0042) higher in multiparous (17.9%) and primiparous-pauciparas (13.3%) than in nulliparous (4.4%), the risk being multiplied by nearly five (OR = 4.73, 95% CI [1.69 - 18.36]) and three (OR = 3.33, 95% CI [1.08 - 13.75]).

In contrast, we did not find a statistically significant difference in the proportion of dysplastic lesions: between age groups at menarche (p = 0.9794); between age groups at first intercourse (p = 0.8144, the risk being slightly higher among women who had their first sexual intercourse beyond 20 years (OR = 1.46, 95% CI [0.55 - 3.68]), based on the number of previous sexual partners (p = 0.4448) and the type of intercourse (p = 0.4496), with the risk being slightly higher among women reporting normal sexual intercourse (OR = 1.26 95% CI 0.42 - 5.07), depending on the age at first pregnancy (p = 0.7535), the risk being slightly higher for women who had first pregnancy beyond 20 years (OR = 1.27, 95% CI [0.51 - 3.41]), compared to the notion of sexual violence (p = 0.3552), smoking ( p = 0.5734) and hormonal contraception (p = 0.1118), with a slightly higher risk for women who used hormonal contraception (OR = 1.43, 95% CI [0.80 - 2.47]) as well as according to the antecedent HIV infection (p = 0.1584).

Berraho M et al. [60] reported from their study in Morocco: a higher risk of developing cervical dysplastic lesions in women who had menarche between 13 and 14 years than those who had menarche at 15 years and beyond (OR = 3.6, 95% CI [2.1 - 6.2] and OR = 2.4, 95% CI [1.3 - 4.4], respectively); and a higher risk in multiparous women starting from third parity and beyond (OR = 1.4, 95% CI [1.2 - 3.9]), in women practicing oral contraception (OR = 1.8, 95% CI [1.2 - 2.8]) and those with normal sexual intercourse (OR = 3.3, 95% CI [1.8 - 6.4]).

Adenis A et al. [59] had the following results in Guyana: a higher risk but no significant difference in large multiparas (OR = 2.1, 95% CI [0.5 - 11.2]), women with age at first intercourse ≥ 18 years (OR = 1.5, 95% CI [0.4 - 6.0]) and with only one sexual partner (OR = 8.2, 95% CI 0.8 - 84.5) as well as a higher risk with a significant difference in women taking non-oral contraception (OR = 3.3, 95% CI [1.1 - 10.4]).

As for Vidal AC et al. [62], they had noted in Tanzania a higher proportion of dysplastic lesions with a statistically significantly greater difference in oral contraceptives (p < 0.003) and HIV infection (p < 0.0001). However, the difference was not statistically significant in terms of number of sexual partners (p < 0.4), marital status (p < 0.6), and smoking status (p < 0.6).

Vinodhini K et al. [61] found in their study in India that the proportion of dysplastic lesions was higher, with a statistically significant difference, among women who had their first sexual intercourse at age 15 and below (OR = 4.21; 95% [3.82 - 8.82], p < 0.04), in case of menarche between the age of 13 and 14 years (OR = 4.19, 95% CI [2.87 - 6.11 P < 0.04), in multiparous women with a delivery number ≥ 3 (OR = 19.2, 95% CI [10.78 - 34.44], p < 0.001) and in women with at least three intercourse per week (OR = 6.70, 95% CI [4.41 - 10.16], p < 0.01). On the other hand, they did not note any significant statistical difference with respect to socioeconomic level (p < 0.44), marital status (p < 0.12) and number of sexual partners (p < 0.45).

Ali-Risasi C et al. [9], after their study in the city of Kinshasa, the following results with respect to HIV infection: the risk of developing low grade dysplastic lesions (LSIL) was higher among HIV-negative widows compared to HIV-positive widows compared to same-status spouses (OR = 8.33, 95% CI [0.41 - 170.67] and OR = 1.16, 95% CI [0.45 - 2.94]), seronegative multiparas than seropositive (OR = 10.01, 95% CI [1.18 - 75.36] and OR = 1.31, 95% CI [0.49 - 3.51]) in comparison with women with gestations ≤ 2 sharing the same serological status. Also in their study, multivariate analysis revealed a slightly elevated risk for HIV-positive women who had aborted in the past (risk increased by about two-fold) compared to women with gestationality ≤ 2 sharing the same serologic status (OR = 1.98, 95% CI [0.83 - 4.75]). It also noted a significantly higher risk for HIV-negative single (OR = 5.26, 95% CI [0.27 - 102.32]) and seronegative widows (OR = 4.34, 95% CI [0.18 - 105.99]) compared to brides with the same serological status.

Thus, several studies have been conducted on the correlation between cytopathology and the sexual or behavioral and gynecological characteristics of women, but the results are slightly different. It has to be said that in the majority of studies the same theoretically documented risk factors predisposing to the development of dysplastic lesions of the cervix are incriminated, even if, according to the studies, the rib ratios look slightly different with various statistics meanings.