Abstract
Objectives
The oncogenic human papilloma virus (HPV) causes transient infections of the cervix, hence other co-factors can potentiate the formation of cervical epithelial cell abnormalities. This study was aimed at determining the seroprevalence of Chlamydia trachomatis infection among women with normal and abnormal Papanicolaou smear cytology results.
Methods
This was a hospital-based cross-sectional comparative study in which study participants were conveniently recruited from January to June,2021. The 50 cases and 50 controls were women with abnormal and normal Papanicolaou smear cytology results respectively. Both groups had blood samples collected for anti- Chlamydia trachomatis antibody test. The data was analyzed with the Statistical Product and Service Solutions (IBM SPSS, Armonk, New York, USA) version 24.0 for windows. The categorical and continuous variables were analyzed with chi square(X2) and Student’s t tests respectively. Binary logistic regression analysis was used to determine the associated factors for Chlamydia trachomatis infection among the respondents. P-value < 0.05 was accepted as statistically significant.
Results
The overall seroprevalence of Chlamydia trachomatis infection was 27%. Positive Chlamydia infection had a significant association with cervical epithelial cell abnormalities (P- value = 0.001). Positive history of multiple sexual partners and coitarche at age of < 18 years were associated factors for Chlamydia trachomatis infection.
Conclusion
This study identified an association between history of Chlamydia trachomatis infection and cervical epithelial cell abnormalities.
Supplementary Information
The online version contains supplementary material available at 10.1186/s12879-026-12994-4.
Keywords: Cervical cytology, Chlamydia trachomatis, Screening, Enugu
Introduction
Sub-Saharan Africa accounts for the highest incidence and mortality from cervical cancer [1]. Cervical cancer is the cause of most cancer deaths in low and middle income countries [2]. It is also associated with anxiety and depression [3]. Some oncogenic genital Human Papilloma Viruses (HPV) that are usually sexually transmitted have been implicated to be necessary but not sufficient cause of cervical premalignant lesion/ cancer [4]. These oncogenic HPV most often result in transient infections of the cervix and only a small proportion of persistently exposed women eventually progresses to cervical premalignant lesion/cancer [5]. Other co-factors, in addition to HPV, promote the development of cervical premalignant lesion and cancer.
One such possible co-factor is Chlamydia trachomatis infection. C. trachomatis is an obligate intracellular Gram- negative bacterium and is one of the most common sexually transmitted disease agents [5]. Genital infection caused by C. trachomatis is largely asymptomatic [6]. Approximately 50% and 80% of infected males and females respectively are asymptomatic [7]. It is highly prevalent among sexually active young women. Its worldwide pooled prevalence is 2.9% [8]. If proper epidemiological survey is done in sub-Saharan Africa, C. trachomatis prevalence may be higher in this region. In Africa, a C. trachomatis infection prevalent rates of 13.2% and 28.5% among female sex workers were found in Nairobi, Kenya and Dakar, Senegal respectively [9, 10]. Prevalent rates of 6% and 8.6% were reported among women attending antenatal clinics in Tanzania and Uganda, respectively [7]. The prevalence of C. trachomatis in the general population in Nigeria ranges between 6.5% and 66.8% [11, 12]. The possible reasons for this variation may be due to different demographic parameters, localities of the surveyed population and diagnostic methods used in those studies. A study in Lagos, Nigeria, showed the prevalence of C. trachomatis among women with abnormal and normal Papanicolaou smear cytology results as 50% and 16.7% respectively, with an overall prevalence of 27.7% [11].
Risk factors for C. trachomatis infection are similar to those of genital HPV infections. These risk factors include a history of multiple sexual partners, a recent new sexual partner, early age at first intercourse, and unprotected sexual intercourse [13, 14]. The possible mechanisms of how C. trachomatis potentiate the formation of premalignant and malignant lesions of the cervix from HPV infection have been adduced. These mechanisms include chronic cervicitis and immune inhibition [14–17]. The persistence of the oncogenic HPV leads to transformation of normal to abnormal cervical epithelial cells [15–18].
Previous studies showed an association between C. trachomatis infection and cervical intraepithelial lesion/cancer [15–18]. A recent literature search using PubMed and Medline revealed limited studies on the association between C. trachomatis and cervical lesions in Nigeria, particularly in the South-East region. This underscored the need for the study in order to fill the knowledge gap and may help strengthen the policy formulation towards incorporation of HPV and C. trachomatis screening in Nigeria. This study was therefore aimed at determining the seroprevalence of C. trachomatis infection among women with normal and abnormal Papanicolaou smear cytology results and its implications for cervical cancer screening in Enugu, South-East Nigeria.
Materials and methods
Study area
It is the University of Nigeria Teaching Hospital (UNTH), Ituku-Ozalla, Enugu, Nigeria. UNTH has a well-established Department of Obstetrics and Gynaecology. The Department runs functional gynaecology, family planning, and cervical cancer screening clinics, among other service delivery points, which offer services to patients from Enugu and other South-East states. It also receives referrals from neighboring states including Delta, Benue, Kogi, Rivers, Cross river, Bayelsa, Edo and from any other part of this country and beyond. Because of the availability of radiotherapy services, cervical cancer cases are referred from other parts of Nigeria to UNTH for chemo-irradiation. This study was performed at the cervical cancer screening clinic.
Study design
It was a cross-sectional comparative study in which women who had normal(controls) and abnormal (cases) Papanicolaou smear cytology results were conveniently recruited at the cervical cancer screening clinic, UNTH, Enugu from January to June,2021. To ensure quality assurance, two cytopathologists independently read each of the cytology slides. Both groups of the study participants were approximately matched for age, parity and level of education. The eligible participants were given information leaflets and counselled appropriately on the objectives of the study. For the purpose of this study, normal and abnormal Papanicolaou smear cytology reports were defined using the Bethesda 2001 classification [19]. The cases were those who had cervical epithelial cell abnormalities while the controls were the women that had negative to squamous intraepithelial lesion or malignancy, from Papanicolaou smear cytology. Information on the socio-demographic, sexual and reproductive variables, was obtained using interviewer-administered semi-structured questionnaires. The questionnaire for this study was designed by the authors. Serial numbers were assigned to each participant to protect her identity and eliminate bias. These questionnaires were administered by the authors and the trained research assistants.
Procedure for C. trachomatis testing
Blood samples were collected from consenting women with either negative or positive Papanicolaou smear cytology results, for detection of antibodies to C. trachomatis using human chlamydia immunoglobulin G (IgG) enzyme-linked immunosorbent assay (ELISA) kit manufactured by Sigma Aldrich, St. Louis, Missouri, United States of America and the catalogue number was SE120030. This was an indirect solid phase enzyme. The blood samples were allowed to clot and centrifuged at 3000 revolutions per minute. The resulting sera were stored at -20°c in a deep freezer until analyzed for antibody to Chlamydia using IgG ELISA kit. The ELISA technique was done according to the manufacturer’s instructions on containing leaflet. The optical density of the test well was determined at 450 nm(nm) with a spectrophotometer. A specialist microbiologist cross- checked the results and instruments at regular intervals which helped to increase the quality assurance of the results. The C. trachomatis IgG ELISA test kit result was considered negative and positive if the absorbance value was < 0.9 and ≥ 0.9 respectively. However, the use of an IgG ELISA kit is a significant limitation. IgG antibodies indicate past or chronic infection but not necessarily current and active infection that could be acting as a co-factor.
Estimation of sample size
The sample size was calculated using the formula for quantitative cross-sectional comparative study [20], and figures for power used from a nearby similar study in Lagos [11].
 |
Zα/2 = Z-score for the desired alpha level (1.96 for 95% CI)
Zβ = Z-score for the desired power (0.84 for 80% power)
P* = Average proportion exposed =proportion of exposed case + proportion of control exposed/2
P1 is proportion in cases (50%) and P2 is proportion in control (16.7%) [11]
P* = (0.5 + 0.167)/2 = 0.3335
r=ratio of the cases to controls = 1
1 - P* = 0.6665
P1- P2 = Effect size or difference in proportion expected based on previous studies
P1- P2 =0.50-0.167= 0.333
N = 31
After adding 10% attrition, the sample size for each of the groups was 34. However, the sample size of 50 was used for each of the groups in this study in order to increase power of the study.
Inclusion criteria
These consisted of women who gave written consent to participate in the study and those who were aged 21 years old and above.
Exclusion criteria
These consisted of pregnant women, those who had hysterectomy, smokers, Human Immuno-deficiency Virus positive women and diabetics. Others were women on medications like steroids, Azithromycin, Erythromycin, doxycycline or tetracycline in the past three months, women who were less than 21 years old, cervical cancer patients and those who, despite adequate counseling, declined to participate in the study. This was to eliminate confounding effects such as immunosuppression and recent antibiotic exposure.
Data analysis
The data was analysed with the Statistical Product and Service Solutions (IBM SPSS, Armonk, New York, USA) version 24.0 for windows. The categorical and continuous variables were analyzed with chi square(X2) and Student’s t-tests respectively Binary logistic regression analysis was used to determine the associated factors for C. trachomatis infection among the respondents. The dependent variable was the C. trachomatis result. The covariates were age, marital status, social class, parity, history of multiple sexual partners, age at coitarche and cervical cytology results of the participants. P-value < 0.05 was accepted as statistically significant. The reporting of this study conformed to the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statements [21].
Results
Figure 1 shows the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) [21], Flow chart for this study. A total of 100 participants (50 cases and 50 controls) were conveniently enrolled in this study. The socio demographic characteristics of the cases and controls are shown in Table 1. There was no statistically significant difference between the participants with abnormal and normal cytology results on the socio-demographic characteristics (P-value = > 0.05). Table 2 shows comparison of the sexual history of the respondents between both groups of participants. The participants with cervical epithelial cell abnormalities had younger age at onset of sexual intercourse and history of higher multiple sexual partners than those with normal cervical cytology results(P-value = < 0.001). Table 3 shows the types of cytology results of participants with cervical epithelial cell abnormalities. A total of 7,23,12,5 and 3 participants with cervical epithelial cell abnormalities had atypical squamous cell of undetermined significance (ASC-US), atypical squamous cell of undetermined significance high grade (ASC-H), atypical glandular cells (AGC), low grade squamous intraepithelial lesion (LSIL) and high grade squamous intraepithelial lesion (HSIL) respectively. The comparison of C. trachomatis infection between women with positive versus negative Papanicolaou smear cytology results is shown in Table 4. The seroprevalences of C. trachomatis infection among the participants with normal and abnormal Papanicolaou smear cytology results were 12% and 42% respectively. The overall seroprevalence of C. trachomatis infection among the participants was 27%. There was an association between cervical epithelial cell abnormalities and history of C. trachomatis infection [Odds ratio (OR),5.310, 95% confidence interval (CI), 1.913–14.715, P-value = 0.001]. Table 5 shows association between C. trachomatis infection and socio-demographic characteristics/Papanicolaou smear cytology results among the respondents. History of multiple sexual partners [OR 1.112, 95% CI 0.375–3.294, P-value = 0.048], younger age (< 18 years) at onset of sexual intercourse [OR 0.335, 95% CI 0.116–0.963, P-value = 0.013] and cervical epithelial cell abnormalities [OR 5.088, 95% CI,1.556–16.639, P-value = 0.009] were associated factors for C. trachomatis infection.
Fig. 1.
STROBE Flow chart shows the STROBE flow chart for the participants’ selection. Each group of the participants was conveniently recruited at the ratio of 1:1. A total of 100 participants completed the study
Table 1.
Socio-demographic characteristics of the cases and controls
| Socio-demographic Characteristic | Case (Cervical smear positive) (N = 50) | Control (Cervical smear negative) (N = 50) | X2 | P value |
|---|---|---|---|---|
| freq (%) | freq (%) | |||
| Age in years | ||||
| 21–30 | 4 (8) | 4(8) | 0.16 | 0.691 |
| 31–40 | 8 (16) | 6(12) | ||
| 41–50 | 16 (32) | 15(30) | ||
| 51–60 | 18 (36) | 19(38) | ||
| 61–70 | 4(8) | 6(12) | ||
| Level of education | ||||
| No formal education | 3(6) | 2(4) | 0.82 | 0.372 |
| Primary | 5(10) | 3(6) | ||
| Secondary | 16(32) | 20(40) | ||
| Post secondary | 26(52) | 25(50) | ||
| Marital status | ||||
| Single | 9(18) | 3(6) | 9.35 | 0.053 |
| Married | 33(66) | 44(88) | ||
| Divorced | 0(0) | 1(2) | ||
| Separated | 1(2) | 0(0) | ||
| Widowed | 7(14) | 2(4) | ||
| Religion | ||||
| Christianity | 46 (92) | 47(94) | 1.011 | 0.603 |
| Islam | 3(6) | 3(6) | ||
| African Traditional religion | 1(2) | (0) | ||
| Parity | ||||
| nulliparous | 12 (24) | 7(14) | 11.44 | 0.407 |
| 1–4 | 11(22) | 19(38) | ||
| ≥ 5 | 27(54) | 24(48) |
Table 2.
Comparison of the sexual history of the respondents
| Positive cervical cytology[N = 50] | Negative cervical cytology[N = 50] | T-test/X2 | P value | |
|---|---|---|---|---|
| Mean age at sexual debut (Mean ± SD) Years | 17.96 ± 3.21 | 20.66 ± 4.07 | -3.682 | < 0.001 |
| History of multiple sexual partners | ||||
| Yes | 24(48) | 7(14) | 13.51 | < 0.001 |
| No | 26(52) | 43(86) | ||
Table 3.
The cytology results of respondents with cervical epithelial cell abnormalities
| Cervical epithelial cell cytology | Frequency (N = 50) | Percentage (%) |
|---|---|---|
| ASC-US | 7 | 14% |
| LSIL | 23 | 46% |
| HSIL | 12 | 24% |
| ASC-H | 5 | 10% |
| AGC | 3 | 6% |
AGC-Atypical glandular cells
ASC-H=Atypical squamous cell of undetermined significance high grade
ASC-US=Atypical squamous cell of undetermined significance
HSIL=High grade squamous intraepithelial lesion
LSIL = Low grade squamous intraepithelial lesion
Table 4.
Comparing Chlamydia trachomatis infection between women with positive versus negative Papanicolaou smear cytology results
| Chlamydia trachomatis infection | Cervical smear result Positive Negative |
B | Wald X2 | OR | 95% CI | P value | |
|---|---|---|---|---|---|---|---|
| Freq(%) | Freq(%) | Lower Upper | |||||
| Positive | 21(42) | 6 (12) | 1.670 | 10.268 | 5.310 | 1.913 14.745 | 0.001 |
| Negative | 29(58) | 44(88) | |||||
B= Unstandardized regression weight ; Wald X2 =Wald chi square; OR=Odds ratio; CI= Confidence Interval
Table 5.
Association between Chlamydia trachomatis infection and socio-demographic characteristics/Papanicolaou smear cytology results among the respondents
| Factors | Chlamydia Negative Positive |
B | Wald X2 |
Odds Ratio | 95% CI | P value | |
|---|---|---|---|---|---|---|---|
| Freq(%) | Freq(%) | ||||||
| Age | |||||||
| ≤ 45 | 27(64.3) | 15(35.7) | -0.537 | 0.964 | 0.584 | 0.209–1.637 | 0.307 |
| > 45 | 46(79.3) | 12(20.7) | |||||
| Marital status | |||||||
| Married | 61(79.2) | 16(20.8) | -0.591 | 0.450 | 0.502 | 0.371–3.233 | 0.870 |
| Not Married | 12(52.2) | 11(47.8) | |||||
| Social class | |||||||
| High | 47(81.0) | 11(19.0) | -0.491 | 0.749 | 0.612 | 0.201–1.861 | 0.612 |
| Low | 26(61.9) | 16(38.1) | |||||
| Parity | |||||||
| Nulliparous | 15(78.9) | 04(21.1) | 0.658 | 0.647 | 1.931 | 0.389–9.597 | 0.421 |
| Parous women | 58(71.6) | 23(28.4) | |||||
| History of multiple sexual partners | |||||||
| Yes | 16(51.6) | 15(48.4) | 0.106 | 1.076 | 1.112 | 0.375–3.294 | 0.048 |
| No | 57(82.6) | 12(17.4) | |||||
| Age at coitache | |||||||
| < 18 years | 18(64.3) | 10(35.7) | -1.094 | 6.176 | 0.335 | 0.116–0.963 | 0.013 |
| ≥ 18 years | 54 (75.0) | 18(25.0) | |||||
| Cervical cytology result | |||||||
| Negative | 29(58.0) | 21(42.0) | 1.627 | 6.885 | 5.088 | 1.556–16.639 | 0.009 |
| Positive | 44(88.0) | 06(12.0) | |||||
B= Unstandardized regression weight ; Wald X2 =Wald chi square; OR=Odds ratio; CI=Confidence Interval
Discussion
This study showed that the overall seroprevalence of C. trachomatis infection among the participants was 27%. The seroprevalences of C. trachomatis infection in women with normal and abnormal Papanicolaou smear cytology results were 12% and 42% respectively. There was an association between history of C. trachomatis infection and cervical epithelial cell abnormalities. This study also showed that positive history of multiple sexual partners and early age at coitarche were associated with C. trachomatis infection.
The overall C. trachomatis infection seroprevalence of 27% obtained from this study is similar to previous reports in Southwest and Southeast, Nigeria [11, 22]. The association between history of C. trachomatis infection and cervical epithelial cell abnormalities established in this study is essentially similar to previous reports in Lagos, Nigeria and Brazil [11, 23]. However, Safaeian et al. [24], de Castro-Sobrinho et al. [25], and de Paula et al. [26] in their different studies reported no association between positive Chlamydia infection with cervical intraepithelial neoplasia in women for all age groups. This disparity could be due to the fact that they recruited only HPV positive participants. Furthermore, Bhatla et al. [27] in a cross-sectional study in India using antibody test stated that C. trachomatis infection was not significantly associated with cervical intraepithelial lesion.
The associated factors for C. trachomatis infection in this study such as positive history of multiple sexual partners, early age at coitarche and cervical epithelial cell abnormalities were similar to the previous studies in the subject matter [13, 14]. However, Nwankwo and Magaji, in Kano, Nigeria observed younger age group and marital status in addition to multiple sexual partners and early coitarche as the associated factors for Chlamydia infection [28]. This study’s participants were much older than the participants in Kano study. More so, the disparity in marital status between this and Kano studies could be due to high preponderance of polygamy in Kano, northern Nigeria as opposed to Enugu, southern Nigeria where this study was conducted. These factors also buttress the point by some authors [10, 17], who had earlier shown that Chlamydia infection and cervical epithelial cell abnormality have similar associated factors.
Strengths and limitations of the study
This study was strengthened by the quality assurance employed at the detection of antibodies to C. trachomatis using human chlamydia IgG ELISA kit and Papanicolaou smear cytology in order to reduce errors. However, the use of an IgG ELISA kit is a significant limitation. IgG antibodies indicate past or chronic infection but not necessarily current and active infection that could be acting as a co-factor. The choice of this test makes it difficult to establish a direct, causal-temporal relationship between C. trachomatis infection and the concurrent cytological findings. These ELISA tests could not differentiate antibodies against different chlamydia serotypes. The sample size calculation was based on a previous study that used polymerase chain reaction (PCR) and not serology [11]. Therefore the prevalence (50% vs. 16.7%) [11], were likely for active infection, which may not be comparable to seroprevalence in this study. The HPV status and history of contraceptive use among these study participants were not assessed and these are critical confounding variables in cervical epithelial cell abnormalities/cancer studies. The absence of HPV data significantly limits the interpretability of the association between C. trachomatis infection and cervical epithelial cell abnormalities. The participants were recruited through convenience sampling which could introduce bias hence limiting the external validity of the results. The convenience sampling method used in this study may also have influenced the distribution of sexual and reproductive characteristics of the participants. Some confidence intervals in the data that were analysed with binary logistics regression were wide which suggested limited precision in the data. This was a tertiary hospital-based study, hence generalizability could be affected. Some of the information sought from the participants were prone to recall bias.
In conclusion, this study identified an association between history of C. trachomatis infection and cervical epithelial cell abnormalities. However further research using PCR-based testing or longitudinal study to confirm the role of active infection is necessary before any routine screening policy recommendation is considered. Further studies to detect the specific serotypes of C. trachomatis antibodies implicated and HPV strains among participants with cervical epithelial cell abnormalities in this environment is also recommended.
Supplementary Information
Below is the link to the electronic supplementary material.
Acknowledgements
We wish to acknowledge Drs. Ezeoke, Aqua and Eze, the trained research assistants, for helping us in sample collection.
Author contributions
TDI was involved in the concept, design, planning, conduct, data analysis, and manuscript writing of this research project. MIA was involved in the design, planning, conduct, data analysis, and manuscript writing of this research project. LOA was involved in the concept, design, planning, conduct, data analysis, and manuscript writing of this research project. HUE was involved in the design, planning, conduct, data analysis, and manuscript writing of this research project. AOM was involved in the conduct, data analysis, and manuscript writing of this research project. VCD was involved in the conduct, data analysis, and manuscript writing of this research project. AAI was involved in the conduct, data analysis, and manuscript writing of this research project. IJA was involved in the conduct, data analysis, and manuscript writing of this research project.
Funding
The authors bore every aspect of funding for this project.
Data availability
The data for this study is available within the manuscript or the supplementary Information file.
Declarations
Human ethics and consent to participate
Informed written consent was obtained from all the eligible participants in the study. The ethical principles of autonomy, beneficence, non-maleficence and justice were observed while obtaining and handling information/data from the eligible participants. Ethical approval for this study was obtained from the Human Research and Ethics Committee of UNTH with reference number UNTH/CSA/327/vol.5/010 and its date was 26th November,2020. Data collection from the eligible participants was in compliance with Helsinki declaration [29].
Competing interests
The authors declare no competing interests.
Footnotes
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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Data Availability Statement
The data for this study is available within the manuscript or the supplementary Information file.