Utilization of cervical cancer screening by cytology and the burden of epithelial abnormalities: A tertiary-center 42-year study

doi:10.21203/rs.3.rs-4078436/v1

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Utilization of cervical cancer screening by cytology and the burden of epithelial abnormalities: A tertiary-center 42-year study

https://doi.org/10.21203/rs.3.rs-4078436/v1

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published 17 Jul, 2024

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Background: Cytological screening remains a high-impact practice, particularly in low-resource settings, for preventing cervical cancer. The examination of screening practices over time and the prevalence of epithelial abnormalities have not been investigated in longitudinal studies in one of the largest countries in the Middle East and Africa.

Methods: Routine healthcare data were collected from March 1981 to December 2022 at the Early Cancer Detection Unit in a tertiary referral university hospital in the Greater Cairo Region, Egypt. Cervical smears were obtained using a standardized technique and sent to the cytopathology laboratory for conventional cytology examination by expert pathologists. The data were analyzed to determine the temporal trend of the number of women screened each year and the prevalence of epithelial abnormalities.

Results: Data included the results of satisfactory smears from 95120 women. The mean age (SD) of the women at the time of screening was 38.5 (10.5). None of the included women received an HPV vaccine. Abnormal epithelial cells were reported in 5174 women (5.44%). Of these epithelial abnormalities, the majority were low-grade squamous intraepithelial lesions in 4144 women (4.36%). Other abnormalities included atypical squamous cells in 378 women (0.40%), high-grade squamous intraepithelial lesions in 226 women (0.24%), atypical glandular cells not otherwise specified in 184 women (0.19%), adenocarcinoma in 165 women (0.17%), squamous cell carcinoma in 70 women (0.07%), and atypical glandular cells favoring neoplasms in 7 women (0.01%). Women who were at an early age at first intercourse, those who opted for routine cervical cytology screening, and those who were older at screening were more likely to have epithelial abnormalities. The yearly number of screened women was positively associated with the detection of low-grade squamous intraepithelial lesions (correlation coefficient [95% CI] = 0.84 [0.72, 0.91]) and negatively associated with the detection of squamous cell carcinoma (correlation coefficient [95% CI] = -0.55 [-0.73, -0.29]).

Conclusions: The small number of annually screened Egyptian women and the temporal trend in epithelial abnormalities critically demonstrate the need for establishing and scaling up a structured population-based program to achieve the goal of eliminating cervical cancer.

Early detection of cancer

Cancer screening

Uterine cervical neoplasms

Cervical cancer

Squamous intraepithelial lesions of the cervix

Cervical cancer, a matter of public health concern, is the fourth most prevalent form of cancer in women worldwide and ranks as the 14th in Egypt. [1]

The natural history of cervical cancer has a multistep carcinogenesis model, wherein the critical stages are Human Papilloma Virus (HPV) infection, progression to a precancerous state, and subsequent development of invasive cancer. [2, 3]

The incidence of cervical cancer, a largely preventable cancer, has decreased over the past few decades in most countries, although the extent of this reduction varies. HPV vaccination and screening for precursor lesions, followed by appropriate follow-up and treatment contribute to this reduction. [4, 5] This laid the foundation for the World Health Organization (WHO) global initiative to eliminate cervical cancer. One cornerstone of this initiative aims at achieving a target of 70% screening coverage of women aged 30–49 years with a high-performance test. [6]

Screening forms the initial mandatory step of the two approaches towards the prevention of cervical cancer, whether the screen-and-treat approach or the screen, triage and treat approach. [4]

Screening is available in many countries through either population-based (organized) or non-population-based (unorganized) programs, as well as through opportunistic screening. Participation rates and coverage vary significantly across countries and settings. The key factors influencing participation are socioeconomic status, health insurance coverage, public awareness, and level of education. Additionally, some women may face barriers to accessing these services due to a lack of power, authority, or control, which can be major obstacles to their participation. [7–9]

According to the 2015 Egypt Health Issues Survey, the knowledge and utilization of Pap smears for cervical cancer screening among women are quite limited. Only 7 percent of women between the ages of 15 and 59 had ever heard of a pap smear, and a very small percentage (0.3 percent) had undergone the procedure. The proportion of women who were aware of pap smears exceeded 10 percent only among women residing in urban governorates (14 percent), women working for cash (13 percent), and women in the highest wealth quintile (11 percent). In all subgroups, one percent or less of women reported ever having had a Pap smear. [10]

Given the limited knowledge and low utilization of cervical screening among Egyptian women, coupled with the absence of a national population-based screening program, there is a lack of comprehensive understanding regarding the trends of epithelial abnormalities in cervical cytology within the largest population in Africa and the Middle East. Previous research has not thoroughly investigated the outcomes of cervical cancer screening initiatives among Egyptian women or how they evolve over time. Therefore, our objective was to examine the temporal trends in cervical cytology practice and the observed epithelial abnormalities.

This observational study used routinely collected health data from the Early Cancer Detection Unit (ECDU) following Institutional Review Board approval from the Department of Obstetrics and Gynecology, Ain Shams University, Cairo, Egypt. Informed consent from participants was not obtained, as all analyses were conducted using deidentified data collected during the process of healthcare administration at the University Hospital.

Study Population and Data Source

The ECDU began opportunistic screening and treatment for cervical cancer in March 1981. The ECDU provides the service at a subsidized cost that is much cheaper than women would find at other healthcare facilities in Egypt. Participants included all adult women who did not have any prior screening in the past 10 years and who underwent conventional cervical screening in the ECDU from March 1981 to December 2022.

No formal referral process exists between healthcare facilities in Egypt. However, the resources available at the ECDU for the detection and treatment of cervical cancer make screening at the ECDU an essential step in the continuum of cancer prevention and control within the country. As a result, many women are referred to the ECDU from public or private healthcare facilities across Egypt to obtain a pap smear to obtain follow-up evaluations after a suspicious screening using other methods, such as visual inspection aided by acetic acid or Lugol’s iodine, or to begin the process of cancer treatment. The ECDU does not employ a systematic method of recruiting women to undergo cervical cancer screening; therefore, the women were either self-referred or referred by a healthcare provider for screening. Data identifying the source of referral for screening as the individual or a healthcare provider were not captured in this dataset. According to ECDU institutional practice, women who have low-grade infections at the time of a Pap smear are screened again within 6 months of the prior visit, indicating that women often have multiple screening visits.

The ECDU started to use an electronic database in 1986, in addition to paper records, to capture relevant demographics (i.e., age, address, marital status, number of pregnancies), risk factors for cervical cancer (i.e., previous sexually transmitted infections, parity, oral contraceptive use), and clinical outcomes (outcomes of Pap smear) of women who were screened at the clinic. In the first Pap smear, a unique identifying number was used to update each woman’s record. The database has been maintained since its inception, making it a reliable source of longitudinal data for examining trends in cervical cancer screening in a tertiary university healthcare facility in Egypt. All paper records, prior to the establishment of the electronic records system, were transcribed into a database.

Cervical cytology (Pap smear) was obtained using an Ayer spatula and spread over a marked glass slide, which was placed in 95% ethyl alcohol and sent to the cytopathology laboratory for conventional cytology examination. The data were recorded using a structured form. The results of the examined smears were reported according to the Bethesda System for Reporting Cervical Cytology. The terminology “CIN1”, “2”, and “3” was used in the ECDU until 2004. Following the adoption of the Bethesda system, the ECDU transformed all the data to match the new system terminology.

Data analyses

The ECDU provided a deidentified dataset spanning a 42-year period. We used this dataset to describe the clinical and demographic characteristics of screened women, to examine longitudinal trends in screening utilization and to report trends in epithelial abnormalities.

Epithelial abnormalities captured at screening were categorized into normal results, low-grade abnormalities (Atypical Squamous Cells of Undetermined Significance or AS-CUS, and Low-grade Squamous Intraepithelial Lesion or LSIL classifications), and high-grade abnormalities (Atypical Squamous Cells, High-grade Lesion or ASC-H, Atypical Glandular Cells or AGUS, High-grade Squamous Intraepithelial Lesion or HSIL, and Invasive Cancer).

We conducted analyses summarizing patient characteristics, including age at screening, parity, reporting means and standard deviations. We also assessed marital status and Pap smear outcome by the Bethesda classification system as categorical variables, reporting proportions for each variable. The primary outcome of interest was the number of pap smears completed by year, including the cytological results of those screenings.

The data were analyzed using the Statistical Package for the Social Science (SPSS), Version 20 (IBM Corp., Armonk, USA).

Over a 42-year period from March 1981 to December 2022, 100155 Pap smears were collected from women attending the ECDU at the Department of Obstetrics and Gynecology, Ain Shams University, Cairo, Egypt. Following data cleaning, 95120 smears were obtained for data analysis.

The mean age of the women screened was 38.48 years (10.45). Most of the women were married and were examined routinely Table 1. Among women who opted for screening due to clinical symptoms, vaginal discharge (26%) was the most common indication. Most smears (57072/95120 [60.00%]) were obtained following referral from a healthcare provider to the ECDU for screening.

Table 1: Demographic characteristics of women screened at ECDU, Ain Shams University, 1981– 2022

Demographic and clinical characteristics	Mean (SD) or number (%)	Valid number
Age at screening (years)	38.48 (10.45)	95120
Age at first intercourse (years)	20.05 (1.39)	89490
Marital status		95120
Married	93709 (98.52)
Widow	819 (0.86)
Divorced	506 (0.53)
Separated	86 (0.09)
Indication for screening		95120
Not reported	53354 (56.09)
Symptomatic	30352 (31.91)
Routine asymptomatic	11414 (12.00)

The temporal trend of screening is depicted in Fig. 1. The median [IQR] number of women who underwent cervical cytology screening was 1982 [1674, 2928].

Epithelial abnormalities were absent in 94.56% of women (89946/95120; with or without inflammatory cells 71971 and 17975, respectively).Table 2

Table 2: Results of cervical cytology among women screened at ECDU, Ain Shams University, 1981– 2022

Finding	Frequency	Relative frequency
NILM	89946	94.56%
LSIL	4144	4.36%
ASC	378	0.40%
HSIL	226	0.24%
AG cells NOS	184	0.19%
Adenocarcinoma	165	0.17%
Malignant SCC	70	0.07%
AG cells favor neoplastic	7	0.01%
Total	95120	100.00%

Pap smears revealed epithelial abnormalities in 5.44% of the participants (5174/95120). Epithelial cell abnormalities included LSIL (low-grade squamous intraepithelial lesion) in 4144 women (4.36%) (condyloma in 3113 (3.27%) and CIN I in 1031 (1.08%) women), atypical squamous cell (ASC) in 378 (0.40) (ASCUS in 351 (0.37%) and ASC-H in 27 (0.03%) women), HSIL (high-grade squamous intraepithelial lesion) in 226 (0.24%) (HSIL-CIN II in 202 and HSIL-CIN III in 24 women), and squamous cell carcinoma in 70 (0.07%) women. There were 184 women (0.19%) with atypical glandular lesions not otherwise specified and 165 women (0.17%) with adenocarcinoma (malignant endocervical cells in 155 and malignant endometrial cells in 10 women).

During the period from 1981 to 2004, the percentage of condylomas decreased from 4–1%, and that of CIN I decreased from 9–0.52%.

The detection of LSIL decreased from 6.9% in 1981 to 4.3% in 2022, while that of HSIL decreased from 1.2–0.13%.

Preinvasive lesions (ASC, LSIL, and HSIL) declined from 10% in 1981 to 5% in 2022. The temporal trends are depicted in Fig. 2 and Fig. 3.

Patients with abnormal cells had a significantly older mean age than those with normal cells (40.5 versus 38.4 years, P < 0.001). Patients with ASC were significantly older than those with LSIL and younger than those with HSIL, and there were more patients with glandular cells (favor neoplastic) (P < 0.001). The mean age of patients with LSILs was significantly younger than that of patients with other abnormal cells (P < 0.001). Patients with LSILs and AGUS were significantly younger than patients with malignant squamous cell carcinoma, HSILs or adenocarcinoma (P < 0.05).

Rates of epithelial abnormalities increased significantly with each decade of age. Rates flattened in the middle age groups and then showed a significant increase in the older age groups.

Epithelial abnormalities were significantly more common in women who underwent routine check-ups than in symptomatic women (OR [95% CI] 1.2 [1.11, 1.30], P < 0.001). Women with epithelial abnormalities were significantly younger at first intercourse (P < 0.001).

The yearly number of screened women was positively associated with the observed LSIL (correlation coefficient [95% CI] = 0.84 [0.72, 0.91]) (Fig. 4), not significantly associated with the HSIL (correlation coefficient [95% CI] = 0.26 [-0.05, 0.52]) (Fig. 5), and negatively associated with the observed suspected invasion (correlation coefficient [95% CI] = -0.55 [-0.73, -0.29]) (Fig. 6).

Key results

By analyzing routinely collected healthcare data from 95,120 satisfactory cervical smear records in the ECDU, this study reported trends in screening uptake and in the observed epithelial abnormalities. A notable increase in the number of annually screened women occurred from 1981 to 1992, after which the number of screened women declined. Women who engaged in sexual intercourse at a young age and who made the conscious decision to undergo routine cytological screening exhibited a greater probability of presenting with epithelial abnormalities. Furthermore, these abnormalities were more prevalent among women who underwent the screening process at a relatively advanced age than among their counterparts. The most common epithelial abnormality was LSILs. The yearly utilization of cervical screening by cytology was positively associated with LSIL and negatively associated with invasive lesions.

This discrepancy between the recommended cervical cancer screening guidelines and actual clinical practice was identified in a recent systematic review. Only six of 11 countries across North America, Europe, and the Asia-Pacific region have implemented comprehensive population-based screening programs. [11] This observation highlights a potential gap between policy recommendations and real-world implementation of cervical cancer prevention strategies.

Current consensus does not recommend the initiation of cervical cancer screening before the age of 21 years in immunocompetent females due to the very low rate of cervical cancer among women aged 20 to 24 years (0.8 per 100,000). [12] In Egypt, there is a social tendency for early marriage, and the results of this study revealed that epithelial abnormalities are associated with earlier sexual activity. This might have implications for practice.

This study revealed a 5.44% prevalence of epithelial abnormalities in cervical smears. This finding aligns with reports from other Arab countries, such as Saudi Arabia (4.27%) [13], Jordan (3.8%) [14], the United Arab Emirates (3.3%) [15], and Kuwait (4.4%) [16]. This similarity might be related to shared cultural and religious factors. This prevalence in our study is much lower than that reported in sub-Saharan Africa, as reported in studies from southwestern Nigeria (34.6%) [17] and Northwest Ethiopia (14.1%) [18]. Coexisting HIV infection in these regions is a potential explanation for the higher rates.

In the current study, epithelial abnormalities were significantly more common in women who underwent routine check-ups than in symptomatic women. Other reports have not found such a significant difference. [13] This finding suggests that routine cervical cancer screening may be more effective in detecting precancerous changes than relying solely on the presence of symptoms.

In an age-stratified analysis of the distribution of cytological abnormalities, we found that women older than 60 had the highest prevalence of epithelial abnormalities, possibly due to the limited organized screening programs in Egypt in younger women with accumulation of epithelial abnormalities over time.

Our results indicate that women with ASC were significantly older than those with LSIL and younger than those with HSIL and glandular cells. Patients with LSILs and AGUS were significantly younger than patients with malignant squamous cell carcinoma, HSILs or adenocarcinoma. This was consistent with the findings of previously published results showing that the incidence of ASC, LSIL, and HSIL peaked in the 30–39-year age group, while the incidence of AGUS peaked among individuals aged 40–49 years. The incidence of malignant lesions further increased after the age of 50 years. The mean ages at diagnosis for patients with LSILs and HSILs were 34.7 and 37.7 years, respectively, while patients with malignant lesions presented with a mean age at diagnosis of 51.8 years. [19] This might have implications for screening practice. [20]

Over a 42-year period, the prevalence of SIL abnormalities decreased from 6.9–4.3% for LSILs and from 1.2–0.13% for HSILs. The relative frequency of preinvasive abnormalities (ASC, LSIL, and HSIL) started at approximately 10% in 1981 and decreased to 5% in 2022. While the observed decline appears to be reassuring, it does not necessarily reflect the direct effectiveness of a comprehensive preventive strategy. This is because screening services in ECDUs currently operate on an opportunistic basis rather than through a structured, population-based approach.

The effectiveness of structured, population-based preventive strategies in reducing the incidence rates of preinvasive and invasive lesions of the cervix cannot be overstated. [21–24] However, in the vast majority of low- and middle-income countries (LMICs), including Egypt, researchers have identified a diverse array of obstacles to the process of screening [25]. Therefore, LMICs need prompt and immediate execution of unambiguous regulations, which should be fortified by the ability of the healthcare system to put these regulations into action. We need widespread advocacy within the community and the dissemination of information, alongside the strengthening of policies that promote the well-being of women and ensure gender equality.

Strengths and limitations

The present study has notable strengths. This study is among the limited number of reports that scrutinize longitudinal patterns in the use of cervical cancer screening in middle-income countries. This highlights the vital role that reliable data collected during routine healthcare can play in describing practice and identifying the potential challenges in accessing care. Our study has a large sample and spans 42 years of practice. Another strength of this work is that all cytologic findings were assessed and confirmed by highly competent pathologists and stored in the electronic database, reducing the chances of incorrect classification of screening results.

Limitations of this work includes missing data especially in certain demographic characteristics of women. This might reflect sensitive data in a conservative community or the lack of rigor or inconsistencies when collecting routine data. All demographic data were self-reported by women, which is prone to recall bias. The process of screening for cervical cancer is characterized by opportunistic practices rather than organized efforts. This implies that the subset of women who undergo screening differs from those who do not, as the former group has successfully surmounted various obstacles, such as financial constraints, social factors, cultural influences, and geographic limitations, to avail themselves of screening services. There is also a lack of information relating to the source of referral (e.g., self-referred or provider referred) for screening. Finally, the change in terminology used over time may have some implications for the assigned category of abnormality observed.

Our findings highlighted the use of cervical cancer screening and the burden of epithelial abnormalities among women in Egypt. Our results provide insights for policy makers who are shaping advanced testing or vaccination policies. The findings suggest the potential for national expansion and integration with universal health coverage. The findings clearly show the need for a population-based national program if we are keen to meet the World Health Organization’s 2030 targets for cervical cancer elimination.

AG-US

Atypical glandular cells of undermined significance

ASC

Atypical squamous cell

ASC-H

Atypical squamous cell-induced HSILs cannot be excluded

ASC-US

Atypical squamous cell of undetermined significance

CIN

Cervical intraepithelial neoplasia

ECDU

Early Cancer Detection Unit

HSIL

High-grade intraepithelial lesion

HPV

Human papillomavirus

LSIL

low-grade squamous intraepithelial lesion

NILM

Negative for intraepithelial lesion or malignancy

NOS

Not otherwise specified

SCC

squamous cell carcinoma

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Availability of data and materials

All data relevant to this study are publicly available. The data, analysis script and materials related to this study are publicly available on an open access registry. To facilitate reproducibility, this manuscript was written by interleaving regular prose and analysis code using R Markdown. The integrity of raw data is the responsibility of the first author Prof. Sahar Ezzelarab.

Competing interests

The authors declare that they have no competing interests.

Funding

This research received no specific grant from any funding agency in the public, commercial or not-for-profit sectors.

Authors’ contributions

All authors collaborated in conceiving the idea for this study and in conducting the work. S.E. and A.N. contributed to the data analysis and interpretation of the results. S.E., A.N., and R.A. wrote the first draft of the manuscript. All authors revised the manuscript critically for important intellectual content. All authors approved the final version of the manuscript. S.E. is the guarantor for the raw dataset integrity.

Acknowledgments

Early Cervical Cancer Detection Consortium

Maya Abdelrazek, Magda Abdelsalam, Reem Abdelsalam, Rehab Abdelrahman, Rania Ahmed, Radwa Ali, Amal Alloub, Hamdy Alqenawy, Amal Alshabrawy, Nahla Awad, Sohair Ayaad, Amro El-Husseiny, Hala El-Sallaly, Mortada El-Sayed, Sahar Ezzelarab, Ragia Fahmy, Asmaa Kasem, Ghada Moubarak, Hasan Morsi, Ashraf Nabhan, Magda Nasreldin, Ragaa Rifaat, Noha Sakna, Amal Zeinab Shehabeldin, Ahmed Zenhom

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No competing interests reported.

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You are reading this latest preprint version

Utilization of cervical cancer screening by cytology and the burden of epithelial abnormalities: A tertiary-center 42-year study

Status:

Journal Publication

Version 1

Abstract

Figures

Background

Methods

Study Population and Data Source

Data analyses

Results

Discussion

Key results

Strengths and limitations

Conclusion

Abbreviations

Declarations

Ethics approval and consent to participate

Consent for publication

Availability of data and materials

Competing interests

Funding

Authors’ contributions

Acknowledgments

Early Cervical Cancer Detection Consortium

References

Additional Declarations

Status:

Journal Publication

Version 1