Factors Influencing Knowledge and Practice Regarding Cervical Cancer and Pap smear Testing among Omani Women

Background: Knowledge of cervical cancer and performance of Pap smear testing are influenced by several sociodemographic factors. This study aimed to describe the effect of relevant variables on knowledge and compliance with guidelines in Oman. Methods: In this cross-sectional survey, participants were divided into three groups: patients who attended Outpatient Gynecology Department, female medical staff and university graduate students. Results: There were 204 outpatients, 133 staff, and 157 students. Adequate knowledge among was seen in 38.7%, 35.3%, and 7.6%, respectively. Knowledge of cervical cancer and Pap smear was significantly lower among outpatients with secondary education, while those with high level of income were more likely to have adequate cancer knowledge. Uptake of Pap smear was significantly greater among outpatients aged ≥ 30 years, with high income and a positive history of cancer. Conclusion: Culturally tailored interventions that focus on improving cancer risk knowledge are needed to maximize screening uptake for cervical cancer.

Introduction from all participants and they were ensured about the confidentiality and that their participation is voluntary and they have full right to withdraw from the study at any time without reasons. They were also rewarded for their time with an informative gift cards given at the end of the interview.

Data Collection
Data collection was interview-based for the gynecology outpatients and self-administered online for female staff and students. The questionnaire survey, which consists of four parts with a total of 44 questions, was designed by the investigators based on the study's objectives and literature review (Al-Darwish et al., 2014;Ortashi et al., 2013). However, some of the questions were modified based on expert opinions addressing the cultural values. Knowledge items regarding warning signs and risk factors of cervical cancer were extracted from Cancer Awareness Measure (CAM) tool kit version 2.1 and modified to fit Omani culture.
Data included age, marital status, educational level, family income, husband's educational level, family history of cancer, average visits to gynecology clinic, parity, and abortion. The parity were classified into multiparous (Para ≥ 4 ) and non-multiparous (Para < 4 ) according to the average number of children in Omani families. Family income (Omani Rial (OMR/Month) was divided into ≤ 1,000 and > 1,000 based on Oman's average monthly household income that was reported by the National Center of Statistics and Information (NSCI) (Gulf Business., 2016). The awareness questions assessed whether or not participants had ever heard of cervical cancer, HPV, HPV vaccine and Pap smear testing, knowledge of warning signs and risk factors of cervical cancer, knowledge and performance of females regarding Pap smear testing.
For each question, the answer was coded as one for correct answer and zero for incorrect or (I do not know) answer. The total score represents the sum of the correct responses of the 29 questions. Knowledge of cervical cancer and Pap smear was categorized as "adequate" if approximately 2/3 (i.e. 19 ) of the 29 knowledge questions were correct. The cut-off point for knowledge adequacy was similar to other studies (Al-Shaikh et al., 2014;Jia et al., 2013).

Statistical analysis
Results of descriptive statistics were presented using Mean ±SD for knowledge score and frequency (N) and percentages (%) for the remaining categorical variables. Bivariate analyses were performed using χ 2 to test the association between sociodemographic characteristics and knowledge of cervical cancer and Pap smear as well as its uptake reporting odds ratios (OR) and 95% confidence intervals (CI). P-values of less than 0.05 were considered statistically significant. The data were analyzed using Statistical Package for Social Science (SPSS) version 23 program.

Results
A total of 494 females participated in this study, 204 gynecological outpatients, 133 staff, and 157 students. Participants' characteristics were shown in Table 1. Most of participants were educated and had educational degrees. A total of 56.4% outpatients and 77.4% staff reported to have a total family income of more than 1,000 OMR per month, whereas 63.7 % of participated students reported a family income of less than or equal to 1,000 OMR per month. Two-thirds of staff (92.5%) and students (72.6%) had not visited the clinic. Among the married females, 19.1% of the outpatients and 11.3% of staff were found to be multiparous (Para ≥4), while 8.3% of students were non-multiparous (Para< 4) Table 1.

Awareness and knowledge of cervical cancer and Pap smear
More than two-thirds of outpatients and students had heard of cervical cancer with less than one-third reported to have knowledge about HPV or HPV vaccine. Only 23.6% of students were aware of Pap smear testing in contrast to the high awareness among the outpatients (61.3 %) and staff (85.7%) Table 2.
Bivariate analysis using χ 2 showed no association between average visits to the gynecology clinic and hearing of cervical cancer, HPV, HPV vaccine and Pap smear among all participants (P> 0.05). Only 45.1% of the outpatients and 22.9% of students knew correctly HPV infection as a risk factor for cervical cancer compared to 72.9% in staff. Using cutoff score of 19 out of 29 as an adequate knowledge score, 61.3% of the outpatients and 64.7% of staff were found to have inadequate knowledge regarding cervical cancer and Pap smear versus 92.4% in students Table 2.

Factors contributing to knowledge of cervical cancer and Pap smear
Among outpatients, marital status, educational level, and family income were associated significantly with adequate knowledge scores (P's < 0.05) in contrast to age, family history of cancer, husband's educational level, parity, and abortion history (P> 0.05). Age, marital status, family income, family history of cancer, parity and abortion were not significantly associated with knowledge scores among staff. The same was true about the association of knowledge scores with marital status, family income, and family history of cancer among students Table 3.
A total of 36.8% and 23.3% of outpatients and staff had performed Pap smear, respectively, whereas none of students had a prior Pap smear. About 54% of postgraduates outpatients had performed Pap smear test versus 32.2% in females at secondary level of education and 33.3% in postgraduate staff Table 4.
Screening uptake increased with age among the outpatients (OR 1.86). Married females were four times more likely to perform Pap smear than unmarried females. Marital status was also a significant factor affecting the uptake of Pap smear test among staff. Husband's level of education was significantly correlated to Pap smear Factors Influencing Knowledge and Practice of Cervical Cancer and Pap Smear of cervical cancer and performance of Pap smear were influenced by several sociodemographic factors such as age, participants educational level, husband's qualification and family income (Strohl et al., 2015;Al-Shaikh et al., 2014;Al-Darwish et al., 2013;Jia et al., 2013;Obeidat et al., 2012). The findings of this study show an inadequate knowledge of Omani females with regard to cervical cancer warning signs and risk factors as well as Pap smear test. These findings are consistent with similar studies conducted on outpatients females (Barghouti et al., 2008), medical staff, e.g., nurses, doctors, and medical students uptake among outpatients. Outpatients who had high family income (OR 1.80) and a positive family history of cancer (OR 1.99) were more likely to perform Pap smear. While husband's level of education, income more than 1,000 OMR/Month, and a positive family history of cancer were not significantly influenced the practice of Pap smear among staff Table 5.

Discussion
Several studies suggested that adequate knowledge  (Mutyaba et al., 2006, Al-Shaikh et al., 2014. We also found that there was a lack of knowledge about warning signs and risk factors of cervical cancer among outpatients and students. As such, more than half of females did not knew HPV infection as a risk factor which could be explained by poor knowledge about HPV infection and HPV vaccine especially in Gulf countries (Al-Darwish et al., 2014;Ortashi et al., 2013). In contrast, high awareness about HPV and its vaccine was found in other Islamic countries like Turkey   (Donders et al., 2008). This might be due to conservative society in Gulf countries and lack of public program for sexual and reproductive education. It was observed that countries that provide good sexual and reproductive education program like Australia showed high levels of knowledge (80.0-90.0%) (Giles and Garland., 2006). We found that knowledge of HPV as etiological factor of cervical cancer was high among our medical staff (72.9%), in contrast to data from Jordan which showed almost half of health professionals did not knew about HPV infection as a risk factor (Obeidat et al., 2012).
We assessed the influence of some independent variables on knowledge level of cervical cancer and Pap smear. Educational level and family income were significant independent predictors of knowledge level among outpatients, comparable to previous studies     (Barghouti et al., 2008;Al Sairafi and Mohamed, 2009;Al-Meer at al., 2011). Also, outpatients with higher family income had better cancer knowledge scores as confirmed by other series (Strohl et al., 2015). High level of income might have influenced cancer knowledge level directly and indirectly by providing more chances for receiving better education and highly standard healthcare where health professionals have more time to raise the knowledge level regarding important health issues. It is noteworthy that, educational level and family income of medical staff did not influence their level of knowledge. This finding is in line with other similar studies (Obeidat et al., 2012;Mutyaba et al., 2006). Health care providers and all of the medical staff are expected to be adequately knowledgeable about all the aspects related to cervical cancer and Pap smear because they play an active role in the provision of appropriate information about the warning signs, risk factors and importance of screening test to their patients and the public.
Most of students had inadequately knowledge about cervical cancer and screening. Similar finding was found in a study conducted on medical students in Saudi Arabia

Characteristics
Outpatients ( (Al-Shaikh et al., 2014). Our data suggests that this subgroup as a future new generation needs to be highly educated about important health issues and screening programs. Marital status influenced significantly the level of knowledge among outpatients. This result was similar to a study conducted in Michigan (Holcomb et al., 2004). However, age and husband education were not associated with the knowledge score among females participated in the study, consistent with other similar study (Su., 2011). In addition, the findings of this study show that parity and abortion were not associated with knowledge scores among the outpatients, staff and students, in disagreement with other studies (Al-Meer et al., 2011;Su, 2011).
Among outpatients, 36.8% had undergone a Pap smear test. This, in consistent with other studies, suggests a low uptake among females possibly due to lack of national preventive health-screening program, lack of encouragement by health professionals (Barghouti et al., 2008;Al-Meer at al., 2011;Ranabhat et al., 2014) as only 32.4% of females were recommended by health professionals to do Pap smear. In contrary, in Jordan, most of the Pap smear testing among female outpatients was encouraged by health providers (Obeidat et al., 2012).
Outpatients were more likely to perform Pap smear if they were older than 30 years, had a family income > 1,000 OMR/Month, and had a positive family history of cancer. This finding is in line with other similar studies (Barghouti et al., 2008;Al-Meer at al., 2011). This might be due to more access to health care facilities and performing regular check-ups.
As such, female outpatients who are married to a husband with secondary education or below were less likely to perform Pap smear. Although this finding is in disagreement other study (Su, 2011), education is considered as an important predictor of performance and  knowledge of Pap smear (Barghouti et al., 2008;Su, 2011). Married female staff were more likely to perform Pap smear test than single females. This would be explained that married females are more likely to have multiple visits to gynecology clinic for their contraceptive and obstetric consultation. Unlike other study conducted among nurses (Tay et al., 2015), the present study showed that husband education is not an influencing factor on the practice of Pap smear among female staff. While, many of the demographic factors such as age, family income, family history of cancer, parity, and abortion were found to correlate positively with uptake of Pap smear test among the medical staff in previous study (Ackerson and Gretebeck, 2007), this correlation was not recorded in the present study.
In conclusion, the findings of this study showed inadequate knowledge of cervical cancer and poor uptake of Pap smear test among outpatients, staff, and medical students. As a recommendation, culturally appropriate educational health programs and interventions that focus on improving the level of knowledge are needed to maximize screening uptake with Pap smear testing.