Research Article Prevalence and Risk Factors of Cervical ... · Cervical cancer is one of the leading cancers among women globally [1]. It is the third most common cancer in women

Journal of Comprehensive Cancer Research Volume 1 , Issue 1 Article ID: 100002

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Research Article

Prevalence and Risk Factors of Cervical Intraepithelial Neoplasia and

Cervical Cancer among Ever Married Adult Females in Egypt: A

Survey Study

El-Moselhy EA1*, Salim SA2, and Hagrass SA3

1Department of Community Medicine, Al-Azhazr University, Egypt

2Department of Obstetrics and Gynecology, Al-Azhazr University, Egypt

3Department of Community Health Nursing, Zgazig University, Egypt

*Corresponding Author: El-Moselhy EA, Department of public Health & Community Medicine, Al-Azhar University,

Egypt, E-mail: [email protected] and [email protected]

Received: April 13, 2017; Accepted: June 20, 2017; Published: June 27, 2017

Copyright: ©2017 El-Moselhy EA et al. This is an open access article distributed under the Creative Commons

Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original

work is properly cited.

Citation: El-Moselhy EA, Salim SA, and Hagrass SA (2017) Prevalence and Risk Factors of Cervical Intraepithelial

Neoplasia and Cervical Cancer among Ever Married Adult Females in Egypt: A Survey Study. J Compr Cancer Res 1(1):

100002.

Abstract

Background: Cervical cancer is one of the leading cancers among women globally. In Egypt, prevalence of cervical

cancer is increasing, however prevalence and risk factors of its precursors; cervical intraepithelial neoplasia (CIN)

were not fully defined. Aim of the Study: To define the prevalence of CIN and cervical cancer among ever married

adult females in Assiut, Egypt and to define their risk factors. Patients and Methods: A cross-section, analytic,

survey study design was used. One thousand and six hundred normal married adult females were recruited.

Conventional Pap smears were taken and examined, those with abnormal smear results were subjected to colposcopic

biopsy taking for pathologic examination. Results: Prevalence of epithelial abnormalities was 8.25%. Prevalence of

CIN and cervical cancer was 3.18%; CIN I, II, III, and cervical cancer were 2.25%, 0.69%, 0.18%, and 0.06%;

respectively. The mean ages of women in CIN I, II, and III/CIS/cancer were 41.7, 46.5, and 56.7 years; respectively

(P=0.005). The significant socio-demographic risk factors were the lowest education (OR=3.82), occupation

(OR=3.67), and social level (OR=2.16). The significant sexual behavior risk factor was sexual partner with STIs or

symptomatic (OR=4.47). The significant reproductive risk factors were vaginal delivery (OR= 8.77), birth spacing < 2

years (OR=6.04), OCs usage >5 years (OR=3.39), and multiparity >5 (OR= 2.81). History of STIs (OR=2.78) and BMI

≥ 30 (OR=2.22) were significant risk factors. Significant lifestyle risk factors were ever smoked (OR=4.52), low fruits

and vegetables intake (OR=3.67), and poor genital hygiene (OR=2.39). Conclusions and Recommendations:

CIN is prevalent in Assiut, Egypt. CIN risk factors are fully preventable. More surveys must be conducted to define the

exact prevalence, epidemiology, and situation of CIN and cervical cancer in Egypt. Efforts must be doubled to prevent

them through a national program.

Keywords: CIN, Cervical cancer, Prevalence, Risk factors, Egypt

Abbreviations: Pap: Papanicolaou; CIN: Cervical Intraepithelial Neoplasia; OCs: Oral Contraceptives; CIS:

Carcinoma in Situ; BMI: Body Mass Index; FE: Fisher Exact; OR: Odds Ratio; ANOVA: Analysis of Variance; CI:

mailto:[email protected]

mailto:[email protected]

Journal of Comprehensive Cancer Research


Confidence Interval; ECL: Exact Confidence Limits; STIs: Sexually Transmitted Infections; SES: Socioeconomic

Status; HPV: Human Papilloma Virus; +ve FH: Positive Family History; -ve: Negative

Introduction

Cervical cancer is one of the leading cancers among women globally [1]. It is the third most common cancer

in women and the seventh most common cancer overall [2]. Global cervical cancer incidence increased from 1980 to

2010 with 0.6% annual rate of increase. Cervical cancer killed up to 276,000 women in 2010, of which up to 64,000

were in developing countries [3]. The lowest rates (< 6/100,000 populations) are found in Australia, New Zealand,

and Northern America [2]. Developed countries have achieved high reductions in cervical cancer incidence and

mortality due to effective screening with Papanicolaou (Pap) smears [4]. On the other hand, the highest incidence

rates are found in Eastern and Western Africa; 34.5 and 33.7 cases/100,000 populations, respectively [2,5].

Accordingly, 85.0% of cervical cancer cases and 80.0% of deaths occurred in developing countries; where it accounts

for at least 13.0% of all women's cancers [2,6]. These high rates are mostly attributed to the lack of effective screening

programs with a high coverage [7]. So, it is not surprisingly that cervical cancer incidence is anticipated to increase by

more than 75.0% in developing countries by the year 2025 [5]. Thus, prevention, screening, and early detection

efforts have limited or no success in these areas [6,8].

In Egypt, incidence rate of cervical cancer is 6.6 cases/100,000 populations [2], while prevalence of pre-

invasive high-grade lesions represents ~0.3% among the Egyptian females [9]. Cervical cancer ranked 8th among the

most common females' cancers registered in the National Cancer Institute registry for the years 2002- 2004, with

increasing incidence from 2002 to 2004 [10]. Further, it is estimated that cervical cancer cases will be increases in

Egypt by 34.0% from 2013 to 2050 [11].

The Pap smear has remained the most successful screening test ever developed for cervical cancer. It can

detect precursor epithelial changes, called cervical intraepithelial neoplasia (CIN) or cervical dysplasia, long before

visible abnormalities appear on the cervix uteri epithelium. All cervical cancers arise from such precursor lesions [12].

Thus, CIN are the precursor lesions for a potentially fatal disease, cervical cancer [7]. The usual 10-20 year natural

history of progression from mild dysplasia to carcinoma makes it relatively easily preventable disease and provides

the rationale for screening [8]. So, CIN is a term for a continuum of epithelial lesions of the cervix uteri ranked in

three grades that are progressive and consecutive stages in the development of cervical cancer; based on increasing

degrees of cellular change and disorganization [7,13]. On histological basis, these lesions are graded as CIN I (mild

dysplasia), CIN II (moderate dysplasia), and CIN III (severe dysplasia and carcinoma in situ, CIS) [12].

Prevalence of premalignant cervical lesions varies greatly among populations. In unscreened populations

estimates for CIN I prevalence ranges from 3.0%-10.0%, and for CIN II and CIN III/CIS from 1.0%-5.0%. Further, the

number of premalignant lesions is related to the frequency of the disease itself, the age of the screened women and

previous screening status [8]. In Zaira, cervical cancer high-risk area, prevalence was 4800/100,000 [14]. Further, it

is estimated that 1.4 million women live with cervical cancer; this means at least 2.8-7 million women harbor

premalignant lesions that need to be detected and treated [15]. In Egypt, it is evident from the available sources that

about 866 women are diagnosed with cervical cancer per year and about 373 death cases are recorded on an average

[16]. Also, it is found that pre-invasive high-grade lesions and invasive cervical carcinoma represent 0.5% and 0.04%,

respectively [17].

Many studies have documented CIN and cervical cancer's risk factors. These factors are the lowest social

status [18] including education [19], occupation [19], and rural residence [20], sexual partner with sexually



transmitted infections (STIs) [18], vaginal delivery [21], poor birth spacing [22], oral contraceptive (OC) usage

[20,23], high multiparity [24], history of STIs [25], obesity [26], smoking [18], and poor genital hygiene [21].

Aim of the Study

The aim of this study is to determine prevalence of CIN and cervical cancer and to define their socio-

demographic, sexual behavior, reproductive, associated diseases, and lifestyle risk factors among ever married adult

females in Assiut Governorate, Egypt.

Patients and Methods

Study design

A cross-section, analytic, survey study design was chosen to conduct this research.

Study settings and patients

This study was conducted purposively in Bany Ady Village, Manfalout District, Assiut Governorate, Egypt,

where the gynecologist researcher colleague lives and practices. Bany Ady Village situated ~20 Km north Assiut, there

are 20,641 females in it [27]. A sample of 1475 women, according to Fisher’s formula of sample size equation [28],

and it was increased by ~8.0% to be 1600 apparently normal ever married adult females. The village was mapped and

its houses were numbered; accordingly, the women in the chosen houses were interviewed, with help of the

Community Health Nurse researcher's colleague to insure their cooperation, to explain aim of the study and

procedures that will be taken, and asked them to participate in the study. The women were examined in a Charity

Clinic there and cervical smears were taken. During the women waiting for examination; the Community Health

Nurse colleagues gave them a health education session about importance of CIN screening and cervical cancer risk

factors. The women with positive smears were asked to go to the Gynecology Clinic, Al-Azhar University Hospital at

Assiut, to follow up them (the cases group). A control group, doubling the number of cases, was randomly selected

from the negative (-ve) Pap cases.

Inclusion criteria: Ever married female, age ≥ 20 year, neither currently pregnant nor menstruated, haven't a

history of any cancer, and accept to participate in the study.

Exclusion criteria: Virgin female, age <20 year, either currently pregnant or menstruated, with past history of total

hysterectomy or cervix uteri operations, with past history of pelvic radiation therapy or refuse to participate in the

study.

Study tools

A specially designed comprehensive interviewing form contains data relevant to topic of the study was used

to collect data.

Samples of exfoliated cervical cells for conventional Pap smear were taken during the gynecologic

examination. Results were classified according to the Bethesda System [29]; the test based on those neoplastic cells

are less attached than normal cells and shed easily, the cells can be collected and tested for anaplasia characters [30].

Pap test has low sensitivity, leading to many false -ve results, but its specificity is high. Other disadvantage is the need

for repeat smears, recall of patients [7]. Cases who showed +ve cytology, atypical squamous cells of undetermined

significance or more severity were interviewed by the Gynecologist and Community Health Nurse researchers to

explain result of the report and asked them to be subjected for colposcopic guided punch biopsy. Results of the

histopathology were categorized into negative (normal or inflammation), CIN I, CIN II, CIN III, carcinoma in situ

(CIS) or invasive cervical cancer.

All the cases and controls had undergone anthropometric measurements; height (cm) and weight (kg) were



measured with participants standing without shoes and heavy garments. Body mass index (BMI) was calculated and

classified according to WHO [31].

Ethical consideration

The study was approved by the Departments' Councils and Al-Azhar University Hospital Ethics Committee.

The purpose and procedures of the study were explained to the participants, confidentiality was guaranteed, and

consents were taken before starting the work. Also, the females with abnormal Pap smears were properly managed.

The study complies with the ethical principles for medical research involving humans were taken into the account

(Helsinki Declaration).

Statistical analysis

The collected data were organized, tabulated and statistically analyzed using statistical package for social

sciences (SPSS) version 20 (SPSS, Inc., Chicago, USA). For categorical data, frequency and percent were calculated;

Chi-square (χ2) or Fisher exact (FE) test was used as appropriate to detect significance of differences. In case of

numerical data; F-test (analysis of variance, ANOVA) was used to detect significance of differences. Odds ratio (OR)

test with 95% confidence interval (CI) or exact confidence limits (ECL) was used to detect significance of risk factors.

The significance level in χ2, FE, and F tests was accepted at P-value <0.05.

Results

Figure (1) shows clear prevalence of EA among the studied females was 8.25%; 3.18% of them proved to have

CIN and cervical cancer. In detail, CIN was 3.12%; 2.25% CIN I, 0.69% CIN II, 0.18% CIN III/CIS, and invasive

cervical cancer was 0.06%.

Figure 1: Distribution of the detected prevalence of +ve Pap, CIN, and cervical cancer among the studied ever

married adult females screened with Pap smear and pathology.

Table 1 clarifies 77.8% of CIN I cases were in age group 40-59 year; 72.7% of CIN II cases in age group 40-59

year; and 50.0% of CIN III/CIS/cancer cases were in age group 50-59 year. Further, there were 2 (50.0%) cases CIN

III, 1 (25.0%) CIS, and 1 (25.0%) case cervical cancer. All differences between groups were statistically insignificant.

But, the mean ages of women in CIN I, II, and III/CIS/cancer were 41.7, 46.5, and 56.7 years, respectively with

statistically significant differences, P=0.005.



Age Groups

(year)

CIN grades and cervical cancer (n=51) Total

χ2F* P- Value CIN I

(n=36=70.6%)

CIN II

(n=11=21.6%)

CIN III/Cancer

(n=4=7.8%) No. %

No. % No. % No. %

20-29 2 5.6 1 9.1 0 0.0 3 5.9 0.461 0.793

30-39 3 8.3 1 9.1 0 0.0 4 7.8 0.376 0.828

40 49 14 38.9 3 27.3 1 25.0 18 35.3 0.699 0.705

50-59 14 38.9 5 45.4 2 50.0 21 41.2 0.289 0.865

≥ 60 3 8.3 1 9.1 1 25.0 5 9.8 1.139 0.565

Mean ± SD 41.7 ± 8.3 46.5 ± 9.8 56.7 ± 11.2 --- --- 5.788* 0.005

Table 1. Distribution of the CIN and cervical cancer group of ever married adult females screened to Pap smear and

pathology according to their age groups.

Table 2 shows significant socio-demographic risk factors for CIN/cervical cancer were lowest education (OR=3.82,

95% CI: 1.69-8.75), occupation (OR=3.67, 95% CI: 1.47-9.23), and social levels (OR=2.16, 95% CI: 1.03-4.56).

Socio-demographic

Characteristics

CIN/CIS and cervical

cancer group (n=51)

Normal epithelium

group (n=100) OR* (95%CI)**

OR* (95%ECL)# No. % No. %

Educational level:

Illiterate and d read & write 39 76.5 46 46.0 3.82 (1.69-8.75)

Up to secondary 9 17.6 43 43.0 0.28 (0.11-0.69)

University 3 5.9 11 10.0 0.51 (0.09-2.05)#

Occupational level:

House wife 21 41.2 47 47.0 0.79 (0.38-1.65)

Unskilled 17 33.3 12 12.0 3.67 (1.47-9.23)

Semi-skilled & skilled 10 19.6 34 34.0 0.47 (0.19-1.13)

Professional 3 5.9 7 7.0 0.83 (0.13-3.85)#

Social class:

Low 28 54.9 36 36.0 2.16 (1.03-4.56)

Middle 19 37.3 48 48.0 0.64 (0.3-1.35)

High 4 7.8 16 16.0 0.45 (0.1-1.5)#

Religion:

Muslim 37 72.5 63 63.0 1.55 (0.7-3.47)

Christian 14 27.5 37 37.0 0.64 (0.29-1.43)

Table 2. Distribution of the studied group of CIN and cervical cancer of ever married adult females compared to

controls according to socio-demographic risk factors. *Odds ratio; **Confidence intervals; #Exact confidence limits.



Table 3 illustrates significant sexual behavior risk factors for CIN/cervical cancer was partner with STIs or

symptomatic (OR=4.47, 95% ECL: 1.11-21.15). On the other hand, the insignificant risk factors were age at marriage

<20 years, premarital sexual practice, none circumcised partner, and ≥ 2 lifetime sexual partners.

Sexual behavior risk

factors

CIN/CIS Cancer group

(n=51)

Normal epithelium

group (n=100)

OR* (95% CI)**

OR (95% ECL)#

No. % No. %

Age at marriage (year):

< 20 12 23.5 13 13.0 2.06 (0.79-5.35)

≥ 20 39 76.5 87 87.0 0.49 (0.19-1.26)

Premarital sexual practice:

Yes 4 7.8 2 2.0 4.17 (0.57-47.15)#

Partner with STIs or symptomatic:

Yes 8 15.7 4 4.0 4.47 (1.11-21.15)#

None circumcised male partner:

Yes 5 9.8 3 3.0 3.51 (0.65-23.39)#

Number of lifetime sexual partners:

1 39 76.5 87 87.0 0.49 (0.19-1.26)

≥ 2 12 23.5 13 13.0 2.06 (0.79-5.35)

Table 3. Distribution of the studied group of CIN and cervical cancer of ever married adult females compared

to controls according to sexual behavior risk factors. * Odds ratio; ** Confidence intervals; # Exact confidence

limits.

Table 4 reports significant reproductive risk factors for CIN/cervical cancer were multiparity >5 (OR=2.81,

95% CI: 1.15-6.89), vaginal delivery (OR=8.77, 95% ECL: 2.0-79.08), birth spacing < 2 years (OR=6.04, 95% ECL:

1.68-32.67), and OCs usage >5 years (OR=3.39, 95% CI: 1.53-7.56).



Reproductive history risk factors CIN group (n=51) Normal group

(n=100)

OR* (95%CI)**

OR (95% ECL)#

No. % No. %

Age at first full term labor (year):

< 20 18 35.3 23 23 1.83 (0.82-4.08)

≥ 20 33 64.7 77 77 0.55 (0.25-1.22)

Parity:

0 2 3.9 8 8 0.47 (0.05-2.49)#

1-5 33 64.7 78 78 0.52 (0.23-1.16)

> 5 16 31.4 14 14 2.81 (1.15-6.89)

Mode of delivery: (n=49) (n=92)

Normal vaginal 47 95.9 67 72.8 8.77 (2.0-79.08)#

Caesarean section 2 4.1 25 27.2 0.11 (0.01-0.5)#

Birth spacing (year): (n=49) (n=92)

< 2 46 93.9 66 71.7 6.04 (1.68-32.67)#

Oral contraceptives (OCs) usage:

Yes 49 96.1 92 92 2.13 (0.4-21.27)#

Duration of OCs use (year): (n=49) (n=92)

≤ 5 23 46.9 69 75 0.29 (0.13-0.65)

> 5 26 53.1 23 25 3.39 (1.53-7.56)

Table 4. Distribution of the studied group of CIN and cervical cancer of ever married adult females compared to

controls according to reproductive history risk factors. * Odds ratio; ** Confidence intervals; # Exact confidence

limits.

Table 5 shows BMI ≥ 30 (OR=2.22, 95% CI: 1.01-4.86) and history of STIs (OR=2.78, 95% CI: 0.97-8.01)

were significant risk factors for CIN and cervical cancer. Whilst, significant lifestyle risk factors were low fruits and

vegetables intake (OR=3.67, 95% CI: 1.59-8.57), ever smoked (OR=4.52, 95% CI: 2.07-9.97), poor genital hygiene

(OR=2.39, 95% CI: 1.13-5.07).



Medical and family history risk factors

CIN group

(n=51)

Normal group

(n=100) OR* (95% CI)**

OR (95% ECL)# No. % No. %

Associated diseases and family history risk factors

Obesity (BMI, kg/ m²):

Normal <25 12 23.5 34 34.0 0.6 (0.26-1.37)

Pre-obese 25- 29.9 18 32.3 42 42.0 0.75 (0.35-1.6)

Obese ≥ 30 21 41.2 24 24.0 2.22 (1.01-4.86)

History of STIs:

Yes:0 12 23.5 9 9.0 3.11 (1.11-8.83)

Positive family history of CIN or cervical cancer:

Yes: 2 3.9 1 1.0 4.04 (0.28-240.74)#

Positive family history of other cancer types:

Yes 3 5.9 2 2.0 3.06 (0.34-37.5)#

Lifestyle risk factors

Low fruits and vegetables intake:

Yes 21 41.2 16 16.0 3.67 (1.59-8.57)

Tobacco smoking:

Never smoked 21 41.2 76 76.0 0.22 (0.1-0.48)

Ever smoked 30 58.8 24 24.0 4.52 (2.07-9.97)

Alcohol intake:

Yes 3 5.9 2 2.0 3.06 (0.34-37.5)#

Genital hygiene:

Poor 27 52.9 32 32.0 2.39 (1.13-5.07)

Neglect medical advice for initial symptoms:

Yes 39 76.5 71 71.0 1.33 (0.57-3.11)

History of Pap smears testing:

No 50 98.04 98 98.0 1.02 (0.05-61.39)#

Table (5): Distribution of CIN and cervical cancer cases of ever married adult females compared to controls according to

associated diseases, family history, and lifestyle risk factors. * Odds ratio: ** Confidence intervals; # Exact confidence limits.

Discussion

Cervical cancer is fully preventable and curable at low cost and risk when screening to facilitate timely

detection of early precursor lesions in asymptomatic women is available together with appropriate diagnosis,

treatment, and follow-up [6,8]. Despite these advances, it is still a major cause of morbidity and mortality in

developing countries [5-7].



Cytology-based screening is a highly effective method of secondary prevention and control of cervical cancer

in developed countries [6,8]. Incidence of this cancer has lowered in many areas since its use. Nearly all cervical

cancer cases arise from CIN lesions, but not all CIN lesions progress to cancer. Actually, many persist without change

or even regress [7]. It is believed that CIN I and II are more likely to regress than to progress; only 10.0%-15.0% of

CIN I lesions are progress to CIN II and III/CIS, and 50.0% of CIN II and 30.0% of CIN III regress spontaneously

[13]. On the contrary, the higher the grade of the precursor lesion, the greater the chance it will progress to cancer;

the progress of CIN I to invasive cancer can take decades [7].

In the present study, prevalence of EA was 8.25%; this figure is comparable with 7.8% [17] and 9.6% [23]

prevalence of EA by Pap test, while it is higher than 1.63% [32] and 1.07% [9]. This study high EA figure might be

attributed to that the present study included all apparently normal women. While, other studies' [9, 32] figures that

are lower than this study figure (8.25%) may be explained, they excluded women presenting with cervical disorders.

Regarding prevalence of CIN, the current study figure (3.12%) is higher than 1.3% [33], 1.74% [34], 0.703% [9], and

0.12% [32]; while it is lower than 5.9% [23]. As regard prevalence of CIN grades, this study figures were 2.25% CIN I,

0.69% CIN II, and 0.18% CIN III/CIS. These figures are higher than 0.359% CIN I, 0.228% CIN II, and 0.116% CIN

III [9]; 0.5% pre-invasive high-grade lesions [17]; and 1.04% CIN I, and 0.5% CIN II [34]; and 0.08% CIN I, 0.03% II,

0.01% III, and 0.01% adenocarcinoma in-situ [32]. Further, this study figure (0.18% CIN I) is similar to 0.2% CIN

III/CIS [34]. Also, this study figure (2.25% CIN I) is similar to 2.6% CIN I [35]. On the other hand, this study figures

are lower than 2.6% prevalence for each of CIN II plus CIN III/CIS [35], and prevalence of 4.7% CIN I and 1.2% CIN

II + [23]. Respecting invasive cervical cancer, the current study figure was 0.06%. It is cleared that cervical cancer in

Egypt ranks the 13th most frequent cancer among women [16]. This figure is similar to 0.04% invasive cervical cancer

[17] and 0.07% the US SEER prevalence [36], while it is higher than 0.027% prevalence of cervical cancer in Egyptian

women [36]. Lastly, the differences observed between this study and other studies could be attributed to the

differences in technical screening methods, geographic, environmental, genetic diversity, and sociodemographic and

cultural background of the study population.

In this study, 77.8% of CIN I cases were 40-59 year; 72.7% of CIN II 40-59 year; and 50.0% of CIN

III/CIS/cancer 50-59 year. Regarding CIN III/CIS/cancer; CIN III was 50.0%, CIS 25.0%, and cervical cancer 25.0%.

Whilst, mean ages of women in CIN I, II, and III/CIS/cancer were 41.7, 46.5, and 56.7 years; respectively. It is

believed that cervical cancer in Egypt ranks the 10th most frequent among women in age group 15-44 [16]. This study

results are consistent with what is shown that women with CIS/cervical cancer are significantly older than those with

dysplasia [34], so succession of malignant changes in cervical epithelium is a function of age [7]. Most of cervical

cancer cases are found in women less than 50 years and >15.0% of cancer cases are found in women over 65 [40].

Screening in resource-limited countries is age targeted screening with cytology; the ideal age is 25-65, which can be

narrowed to 30-39 years according to the resources [8]. It has been shown that a mean age of 39 years for the low-

grade lesions, the significant older women (mean age 43) for the high-grade lesions, and mean age 53 for cervical

cancer [37]. Also, it is cleared that the mean age in the patients was 49.9±11.7 years [20]; meanwhile data showed

70.5% of the CIN II or CIN III lesions are found in women aged 30-40 [33]. As regard cases of cervical cancer; 62.0%

of the cases were 30-59 years. Most women screened for EA are about the same age, with a tendency for high-grade

lesions to occur in somewhat older women; the women with the highest risk are those aged 30-49 [34]. The cancer

incidence rate increased after age 30 and peaked in 55-65 [38]. Further, Hammad et al. [9] found prevalence of the

disease very low below 35 years but significantly increase above that age. Also, mean age for CIN was 44.2 years, while

that for cervical cancer was 54.3. Recently, it is observed that 60.0% of CIN I were 30-39 year, 50.0% of CIN II and III

were in 30-39 and the other half were in 50-64 [32].



In the current study, low socioeconomic status (SES) was risk factor for CIN and cervical cancer. There is

great difference between developed and developing countries related to CIN and cervical cancer issues; the

differences in socio-demographic factors have great role in disease causation [7]. An inverse relation was found

between SES and the incidence of CIN and cervical cancer worldwide [18,19, 32, 39] and it was stronger in

low/middle income countries [39]. Further, health care differences may arise from interplay of economic [20], social,

and cultural factors. The main causes for the great risk in lower SES group are related to sexual behavior (may leads

to a greater chance to acquire and/or a carrier of Human papilloma virus, HPV) and less access to early screen. Also,

an increased risk of ~100% between high and low SES for the occurrence of cancer and of ~60% for dysplasia,

includes CIS, are noticed [39]. The result of this study is agreement with Irimie et al. [20]; they showed most of

patients had poor SES. Hispanic women, in the US, are more likely to get cervical cancer than whites [40]. Further,

SES factors might influence other risk factors as tobacco use, poor nutrition, and obesity [18]. The effect of low SES

may be due to poor sexual hygiene, multiparity or early age of first coitus. The incidence by at least 3-fold was

occurred in the wives of the lower SES [21]. However, an insignificant slight increase incidence of EA and CIN among

women from low SES was found [32]; also, it is showed that SES had no significant effect on cervical dysplasia/cancer

[41].

In this study, the lowest education and occupation levels were significant risk factors for CIN and cervical

cancer. The association noticed between CIN/cervical cancer and low SES is likely related to education. Again, the

association may be due to the influence of low access to early detection and treatment of CIN [20]. Also, a consistent

increasing trend in cervical cancer incidence with various indicators of low SES, including education and occupation

is reported [19]. In UK, 0.7% of cervical cancer cases are due to occupation [42]. Whilst, a lower risk is associated with

higher level of education; 7.3% and 23.7% of patients had a low and high level of education, respectively [20]. Further,

it is noticed that low education level is significant risk factor [23]. In Egypt, there is still persistent gap regarding SES

between rural and urban areas; the inhabitants in rural areas are facing large problems of poverty and a more difficult

access to health care services [18].

In this study, Christians were insignificant risk. This might be due to uncircumcised male partners;

circumcision is a tradition in Muslim countries. In Egypt, all Muslims' males and most Christians' male are

circumcised, so the risk of uncircumcised male partners could be more in Christians' females. In a study on 5000

Indians with cervical cancer, it is reported that incidence of the disease is low in Muslims' women compared to

Hindus and Christians [43].

Studies have shown an increased risk of CIN and cervical cancer attributable to sexual behaviors [20]. This

study illustrated that partner with STIs was significant risk factor; this agreed with our previous work [18]. On the

other hand, age at marriage <20, premarital sexual practice, none circumcised partner, and ≥ 2 lifetime sexual

partners were insignificant risk factors. Cervical cancer is unknown in nuns [44], while it is common in prostitutes

[45], so it has been thought that sexual behavior is major factor in its occurrence [44]. The still low incidence of CIN

in Egypt could be attributed to many factors as benign sexual behavior, male circumcision, and religious culture.

Woman tends to monogamous relation unless she remarried due to divorce or death of her husband. Also,

extramarital relationship is rare in almost all social standards due to strong religious beliefs [32]. This study results is

inconsistent with what is cleared that young age at first coitus and high number of sexual partners have emerged as

significant risk factors for CIN/cervical cancer [18,24,45]. This inconsistent may be due to small number of our cases.

Further, it is cleared that the association between cervical cancer and early age at first coitus as biological activity in

cervix cells are at the highest level during adolescence [45]. Also, it is assumed that sperm act as the carcinogen in

cervical cancer; two basic types of protein are found in the ejaculate of human sperm; histone and protamine [46].



They might have a role in the etiology of cervical carcinoma. It is found that more than 40.0% of patients have

become sexually actives before the age of 18, and 66.7% and 33.3% had one and >1 sexual partners during lifetime,

respectively [20]. Majority of the patients’ life partners had multiple partners that increase the risk of acquiring HPV

infection. Also, a significant association between early age (<17) at marriage and cervical cancer is reported [22,41].

Regarding circumcised partners, male circumcision is significant factor in lowering incidence of cervical cancer

[18,43,47]. Also, cervical cancer may be induced by smegma, lake of hygiene or by some mutagenic factor in sperm

[48]. So, uncircumcised sexual partner is associated with CIN/cervical cancer [44]. Again, male circumcision is an

Islamic tradition among Egyptians; all Muslims and most of Christian's follow this [18].

In this study, multiparity >5, vaginal delivery, birth spacing < 2 years, and OCs usage >5 years were

significant risk factors. Early age at first pregnancy is associated with CIN/cervical cancer [18,44]. This study results

are consistent with what is shown that a significant relative risk of acquiring disease is 6-fold more in women who had

first parity at age <18 compared to those who had first parity after that age [49]. Also, it is observed that 19.2% of

women with cancer had their first child at age <20 and 9.5% their age ≥ 20 with significant difference [41]. While,

high parity appeared as a constant significant risk for CIN/cervical cancer [24]. Further, multiparty with poor birth

spacing between pregnancies is risk factor [22]. It is found that 37.5% of the patients had ≥ 3 childbirth [20], a

significant association between parity >4 and CIN/cervical cancer [41], and association is strongest for women with

parity ≥ 7 full term pregnancies [50]. Further, parity ≥ 7 increases the risk 4-fold compared to the nulliparous [51].

Our result regarding vaginal delivery agrees with Skegg et al. [21]. These women were exposed to more cervix trauma

during vaginal delivery especially multipara women with low SES. Also, OCs usage has been found to increase the risk

of cervical cancer; studies have suggested an increased risk [20,23,52] or a shorter time of transition from dysplasia to

CIS [20]. OCs usage might encourage sexual promiscuity and increase the exposure to carcinogenic agents, but the

mitotic inhibitory effect of OCs on cervical epithelium may offset this [52]. In UK, 10.0% of cervical cancer cases

linked to OCs use [42]. Further, cervical cancer is found in 31.4% of patients who used OCs, although no one of them

used for >5 years [20]. OCs usage for ≥ 5 years increases the risk to develop CIN/cervical cancer 3-fold, while their

use for >10 years increases the risk 4-fold compared to non-users [51]. In Egypt, OCs usage is a significant risk factor

[18].

In the current study, BMI ≥ 30 and history of STIs were significant risk factors for CIN and cervical cancer.

Most studies reported an inverse relation between decreased cervical cancer screening and obesity [53]; obesity has

been associated with cervical adenocarcinoma through its hormonal actions; it might play a role in pathogenesis of

cervical cancer [26]. Obesity not only represents a risk factor, but also it may affect prognosis through numerous

pathways; associated adverse disease features, co-morbidities that can interfere with treatment, and hormonal

influences [20]. Also, women with STIs are at increased risk for CIN causation [22,25]. Chlamydia trachomatis

infection increases the risk of developing cervical cancer [54]. HPV is recognized as the major causative agent for

premalignant and malignant lesions of the cervix uteri [7]. Further, this study reported that positive family history

(+ve FH) was insignificant risk factor, while in our previous study we noticed it is a significant risk factor for cervical

cancer [18]. This controversy may be due to difference in the studied groups; in the earlier all patients have cervical

cancer, while in this study invasive cancer was 1.96% only. It has been documented that women with +ve FH of

cervical cancer, especially in first degree relatives, have 2-fold risk of developing cervical cancer, suggesting an

inherited susceptibility [55]. Also, +ve FH of cervical cancer is found among 13.3% of the patients [20], it is not clear

if the risk associated with +ve FH of cancer is due to a genetic susceptibility or to shared environmental and lifestyle

influences [56].



This work observed that low fruits and vegetables intake and ever smoked women were significant smoking is

the most consistent finding in risk factor studies; it is associated with a 2-fold increased risk for lifestyle risk factors.

Low intake of fruits and vegetables is risk factor for cervical cancer [18]. Cigarettes' smoking is the most consistent

finding in risk factor studies; it is associated with a 2-fold increased the risk for high-grade CIN lesions and invasive

cancer, and it increases with the number of cigarettes per day and the number of years a woman smoke [51,57,58].

The mechanism by which cigarette smoking leads to increase risk of cervical cancer is not known, it may act

independently or it may promote neoplastic transformation by interfering with normal host defense mechanisms

[58]. Further; cotinine, micotione, and other mutagens are found in cervical mucus of smokers that could support a

direct carcinogenic effect [59]. Also, this study cleared that poor genital hygiene is significant risk factor, this result is

agreed with many other studies [18,21,22].

This study noticed that no Pap screen is insignificant risk factor. Patient's unawareness of symptoms, neglect

initial symptoms, and lacking screening facilities is at risk for increase cervical cancer incidence [60]. Cervical cancer

rarely occurs in women who have been getting regular screening before they were 65 [40]. A low rate of participation

in cervical screening programs was shown; 39.9% of patients had screened for cervical cancer and those who reported

being screened were residents in urban setting [20]. Further, the difference probably reflects inequalities in health

care systems [7]. This is mainly attributed to the lack of awareness of cervical cancer in the community, policy-makers

and even health care providers, limited access to health care services, high costs of screening, lack of specific expertise

in sampling and interpretation of results, and the necessity of repeated visits by women [6-8]. Also, it relates to

consequence failure of treating pre-cancerous lesions and to the lack of knowledge about prevention of infections

[60]. In Egypt, preventive and screening behaviors are not lifestyle practice probably these related to socioeconomic

and cultural deeply rooted believes.

Conclusions and Recommendations

CIN is prevalent in Assiut, Egypt. CIN risk factors are fully preventable and CIN is more common among

younger age females. The significant risk factors were low education level, low occupation level, low social level,

sexual partner with STIs, multiparity >5, vaginal delivery, OCs use >5 year, obesity, history of STIs, low fruits and

vegetables intake, smoking, and poor genital hygiene. More surveys are needed in different geographical areas, on big

number of population to define magnitude of the problem, to identify the public health importance of the problem, to

understand the true epidemiology and current situation, to address high risk groups, and to address role of the

community health nurse in prevention of the disease. Health education must be tailored and targeted to all females.

Also, there is a need for an organized prevention program and integration of Pap test into the health-care services that

women use.

Acknowledgments

The authors want to thank Dr Saed A. Kher, MD, Pathology for his assistance in the cytological and

pathological diagnosis of the studied cases.

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