Prevention of Human Papillomavirus

Chapter 7

Abstract

V 0.18, χ<sup>2</sup>

Kazakhstan

and Elnara Ismagulova

screening, risk factors, Kazakhstan

1. Introduction

111

Results of a Survey Concerning

During 2014–2017, a survey concerning risk factors for cervical cancer involving

–23.1). Social profiles of HPV-infected and CaCx-diseased women differ

significantly and, mainly, by standard of living and occupational status. The likelihood of the CaCx onset in Western Kazakhstan decreased by 14 times at relatively high standard of living (OR 0.0713, p = 0.024) and by 3.3 times provided at least irregular participation in screening (OR 0.3384, p = 0.0304). Overall, the findings are quite able to contribute to an understanding why women become affected by CaCx. Low standard of living due to lack of education, low attendance of screening, and low awareness on preventive measures‑all these reasons are interacted and

constitute a set of universal triggers for vulnerability toward CaCx.

Keywords: cervical cancer, human papillomavirus, awareness, vaccination,

For cervical cancer (CaCx), the number of diagnoses could "rise by at least 25% to over 700,000 by 2030, mainly in low- and middle-income countries," said a statement from the Lancet [1]. Some sources mention areas of Western Asia as countries with the lowest CaCx rates [2], while just a few sources are available on the disease-related issues in borderline Central Asia, where Kazakhstan and some other post-Soviet states are located [3, 4]. Reportedly, the annual incidence rate of cervical cancer for Kazakhstan was calculated as 14.5 0.3 with 8.0 0.1 mortality

1166 clinically healthy women and 65 having CaCx was conducted in Western Kazakhstan. Only 34.7% of interviewees constantly participated in state-sponsored screening program, while 37.3% ignored screening in free state-sponsored clinics. Favorable attitude toward vaccination stated 22.9% of the respondents, whereas 38.8% knew nothing, and 33.6% could not clarify their position in this issue. Education is a key factor for better perception of preventive measures—69.2% of the respondents with higher education are aware of vaccination (p ≤ 0.00001, Cramer's

Cervical Cancer Risk Factors

among Women in Western

Saule Balmagambetova, Arip Koyshybaev,

Kanshaiym Sakiyeva, Olzhas Urazayev

### Chapter 7

## Results of a Survey Concerning Cervical Cancer Risk Factors among Women in Western Kazakhstan

Saule Balmagambetova, Arip Koyshybaev, Kanshaiym Sakiyeva, Olzhas Urazayev and Elnara Ismagulova

### Abstract

During 2014–2017, a survey concerning risk factors for cervical cancer involving 1166 clinically healthy women and 65 having CaCx was conducted in Western Kazakhstan. Only 34.7% of interviewees constantly participated in state-sponsored screening program, while 37.3% ignored screening in free state-sponsored clinics. Favorable attitude toward vaccination stated 22.9% of the respondents, whereas 38.8% knew nothing, and 33.6% could not clarify their position in this issue. Education is a key factor for better perception of preventive measures—69.2% of the respondents with higher education are aware of vaccination (p ≤ 0.00001, Cramer's V 0.18, χ<sup>2</sup> –23.1). Social profiles of HPV-infected and CaCx-diseased women differ significantly and, mainly, by standard of living and occupational status. The likelihood of the CaCx onset in Western Kazakhstan decreased by 14 times at relatively high standard of living (OR 0.0713, p = 0.024) and by 3.3 times provided at least irregular participation in screening (OR 0.3384, p = 0.0304). Overall, the findings are quite able to contribute to an understanding why women become affected by CaCx. Low standard of living due to lack of education, low attendance of screening, and low awareness on preventive measures‑all these reasons are interacted and constitute a set of universal triggers for vulnerability toward CaCx.

Keywords: cervical cancer, human papillomavirus, awareness, vaccination, screening, risk factors, Kazakhstan

### 1. Introduction

For cervical cancer (CaCx), the number of diagnoses could "rise by at least 25% to over 700,000 by 2030, mainly in low- and middle-income countries," said a statement from the Lancet [1]. Some sources mention areas of Western Asia as countries with the lowest CaCx rates [2], while just a few sources are available on the disease-related issues in borderline Central Asia, where Kazakhstan and some other post-Soviet states are located [3, 4]. Reportedly, the annual incidence rate of cervical cancer for Kazakhstan was calculated as 14.5 0.3 with 8.0 0.1 mortality for the period 1999–2008 [5]. Data of the International Agency for Research on Cancer (IARC) on cervical cancer incidence in 2012 for the global network resource Cancer Today (formerly Globocan) indicated the highest incidence of CaCx in the Republic of Kazakhstan among borderline countries—29.4 per 100,000 of the female population standardized by age, while the corresponding index for the Russian Federation was 15.3, for Uzbekistan 13.5, and 7.5 for China, respectively [6]. Despite definite progress achieved, issues of cervical cancer prevention have still remained tense in the country. According to data of the ICO Information Centre on HPV and Cancer (the Catalan Institute of Oncology HPV center) as of December 23, 2015, there were 6.72 million women aged 15 years and older at risk of developing cervical cancer, and estimates indicated that every year 2789 women were diagnosed with cervical cancer and 982 died from the disease [7]. Morbidity, according to the ICO experts, has been roughly estimated 32.8 per every 100,000 women standardized by age, i.e., increased several times as many for the period less than a decade. Meanwhile, cervical cancer is a real object for early detection because of its belonging to a number of visual forms and can be largely prevented by both effective screening and vaccination [8].

compulsory vaccination of adolescents. Successfully launched in Kazakhstan in 2013, a pilot vaccination program then was discontinued, largely due to the negative attitude of parents who were not yet ready to the challenges of modern world. However, further efforts are needed to overcome prejudices in primary prevention of cervical cancer. According to the estimates of specialists, stated in the press release of the Centers for Disease Control and Prevention (CDC), in the USA there was an impressive decrease in the prevalence of vaccine types of HPV by 56% in the group 14–19 years old for 7 years of the introduction of vaccination against cervical cancer in adolescent girls (2006–2013) [26]. Recommendations for vaccination are developed by the world's leading cancer institutes not only for girls but also for boys 11–12 years old. Effectiveness of vaccination now is convincingly proven and is no

Results of a Survey Concerning Cervical Cancer Risk Factors among Women…

DOI: http://dx.doi.org/10.5772/intechopen.81601

Thus, a wide circle of issues on the CaCx prevention is to be solved in Kazakhstan in the nearest time, and specific information of the relatively targeted audience of these efforts would serve as a basis for positive changes in

2. Risk factors for HPV infection and cervical cancer development

• Inaccessibility of the screening program or rare participation in it.

According to WHO and CDC, the following conditions are considered the risk

• States causing immunosuppression, such as HIV, high-dose steroid use, etc.

• Lower genital tract neoplasia irrespective of the area: vulvar, vaginal, and anal.

• Increasing the number of sexual partners (increases risk of HPV acquisition)

• Presence of sexually transmitted infections, such as C. trachomatis and possibly

• Tobacco smoking (current and, to a lesser extent, past tobacco smoking)

• The use of birth control pills: long-term use increases the risk of cervical

It is worthwhile to emphasize that the risk factors for HPV infection do not coincide in full with the risk factors for cervical cancer. Only persistent HPV infection constitutes fundamental condition for the CaCx development, while other

To our knowledge, the peak incidence of HPV infection occurs in 20-year-olds, the peak incidence and detection of CIN-III is characteristic for the age group of 30-year-olds, and the peak incidence of cervical cancer occurs at the age of

mentioned risk factors such as smoking play a supporting role [13, 28].

increases the risk of cervical squamous cell carcinoma.

longer questioned [27].

factors for the cervical cancer development:

along with early age of sexual debut.

• More than three full-term pregnancies.

herpes simplex virus (HSV).

squamous cell carcinoma.

113

• Persistent HPV infection.

this direction.

A system of the cervical cancer screening has been implementing in our country since 2008, and in frames of this nationwide program, all women aged 30–70 years are subjected to mass cytological examination every 4 years. Age of women has been increased from 60 to 70 years, and the interval has been diminished from 4 to 5 years according to the latest regulation no. 995 as of December 25, 2017. With that, screening coverage (attendance), which had been about 72% for the first years upon implementation [3], i.e., in line with the WHO recommendations, then began to decline, reaching about 50% by the present time, as leading scientists of KazIOR (Kazakh Research Institute of Oncology and Radiology) recorded.

Furthermore, the other large problem is related to the CaCx screening routine in the country. To date, the majority of specialists in management of women with atypical cytological results are guided by the joint recommendations of the ACS (American Cancer Society), ASCCP (American Society for Colposcopy and Cervical Pathology), USPSTF (US Preventive Services Task Forces), and other leading institutions [9]. Regrettably, these recommendations still have not been adopted by the health policymakers in our country, despite the existing HTA (Health Technology Assessment) reports and leading experts' opinions confirming advantages of HPVbased screening in a co-testing way, i.e., collectively with cytology [10–14].

To implement worldwide-accepted screening in a co-testing way, any countries should first create their nationwide maps of HPV prevalence and type distribution, as HPV is an apparent causative factor for the CaCx development, and its various types differ by carcinogenic potential [15–19]. And meanwhile, data on HPV leading types across Kazakhstan still are limited with a few publications, and far not all the regions have been studied [20–23]. Currently, 14 types are referred to as the types of highly carcinogenic risk (HR-HPV) [24]. Listed researches on HPV prevalence reported high dissemination of HR-HPV types, within 25–28.3% across examined regions.

According to world's leading experts' opinion, only implementation of universal HPV vaccination with enhanced screening would maximally reduce the burden of cervical cancer in post-Soviet countries, albeit options for reducing the HPV-related disease burden are resource-dependent [4].

Revised in Melbourne (2014), the WHO tactics on the CaCx prevention has confirmed that HPV vaccination of girls aged 9–13 years still remains the primary principle of prevention [25].

High rates of cervical cancer along with wide dissemination of HR-HPV types in Kazakhstan entail the need to renew the state-scale program of universal

Results of a Survey Concerning Cervical Cancer Risk Factors among Women… DOI: http://dx.doi.org/10.5772/intechopen.81601

compulsory vaccination of adolescents. Successfully launched in Kazakhstan in 2013, a pilot vaccination program then was discontinued, largely due to the negative attitude of parents who were not yet ready to the challenges of modern world. However, further efforts are needed to overcome prejudices in primary prevention of cervical cancer. According to the estimates of specialists, stated in the press release of the Centers for Disease Control and Prevention (CDC), in the USA there was an impressive decrease in the prevalence of vaccine types of HPV by 56% in the group 14–19 years old for 7 years of the introduction of vaccination against cervical cancer in adolescent girls (2006–2013) [26]. Recommendations for vaccination are developed by the world's leading cancer institutes not only for girls but also for boys 11–12 years old. Effectiveness of vaccination now is convincingly proven and is no longer questioned [27].

Thus, a wide circle of issues on the CaCx prevention is to be solved in Kazakhstan in the nearest time, and specific information of the relatively targeted audience of these efforts would serve as a basis for positive changes in this direction.

### 2. Risk factors for HPV infection and cervical cancer development

According to WHO and CDC, the following conditions are considered the risk factors for the cervical cancer development:


for the period 1999–2008 [5]. Data of the International Agency for Research on Cancer (IARC) on cervical cancer incidence in 2012 for the global network resource Cancer Today (formerly Globocan) indicated the highest incidence of CaCx in the Republic of Kazakhstan among borderline countries—29.4 per 100,000 of the female population standardized by age, while the corresponding index for the Russian Federation was 15.3, for Uzbekistan 13.5, and 7.5 for China, respectively [6]. Despite definite progress achieved, issues of cervical cancer prevention have still remained tense in the country. According to data of the ICO Information Centre on HPV and Cancer (the Catalan Institute of Oncology HPV center) as of December 23, 2015, there were 6.72 million women aged 15 years and older at risk of developing cervical cancer, and estimates indicated that every year 2789 women were diagnosed with cervical cancer and 982 died from the disease [7]. Morbidity, according to the ICO experts, has been roughly estimated 32.8 per every 100,000 women standardized by age, i.e., increased several times as many for the period less than a decade. Meanwhile, cervical cancer is a real object for early detection because of its belonging to a number of visual forms and can be largely prevented by both

A system of the cervical cancer screening has been implementing in our country since 2008, and in frames of this nationwide program, all women aged 30–70 years are subjected to mass cytological examination every 4 years. Age of women has been increased from 60 to 70 years, and the interval has been diminished from 4 to 5 years according to the latest regulation no. 995 as of December 25, 2017. With that, screening coverage (attendance), which had been about 72% for the first years upon implementation [3], i.e., in line with the WHO recommendations, then began to decline, reaching about 50% by the present time, as leading scientists of KazIOR

Furthermore, the other large problem is related to the CaCx screening routine in

To implement worldwide-accepted screening in a co-testing way, any countries should first create their nationwide maps of HPV prevalence and type distribution, as HPV is an apparent causative factor for the CaCx development, and its various types differ by carcinogenic potential [15–19]. And meanwhile, data on HPV leading types across Kazakhstan still are limited with a few publications, and far not all the regions have been studied [20–23]. Currently, 14 types are referred to as the types of highly carcinogenic risk (HR-HPV) [24]. Listed researches on HPV prevalence reported high dissemination of HR-HPV types, within 25–28.3% across exam-

According to world's leading experts' opinion, only implementation of universal HPV vaccination with enhanced screening would maximally reduce the burden of cervical cancer in post-Soviet countries, albeit options for reducing the HPV-related

Revised in Melbourne (2014), the WHO tactics on the CaCx prevention has confirmed that HPV vaccination of girls aged 9–13 years still remains the primary

Kazakhstan entail the need to renew the state-scale program of universal

High rates of cervical cancer along with wide dissemination of HR-HPV types in

the country. To date, the majority of specialists in management of women with atypical cytological results are guided by the joint recommendations of the ACS (American Cancer Society), ASCCP (American Society for Colposcopy and Cervical Pathology), USPSTF (US Preventive Services Task Forces), and other leading institutions [9]. Regrettably, these recommendations still have not been adopted by the health policymakers in our country, despite the existing HTA (Health Technology Assessment) reports and leading experts' opinions confirming advantages of HPVbased screening in a co-testing way, i.e., collectively with cytology [10–14].

(Kazakh Research Institute of Oncology and Radiology) recorded.

effective screening and vaccination [8].

Current Perspectives in Human Papillomavirus

ined regions.

112

disease burden are resource-dependent [4].

principle of prevention [25].


It is worthwhile to emphasize that the risk factors for HPV infection do not coincide in full with the risk factors for cervical cancer. Only persistent HPV infection constitutes fundamental condition for the CaCx development, while other mentioned risk factors such as smoking play a supporting role [13, 28].

To our knowledge, the peak incidence of HPV infection occurs in 20-year-olds, the peak incidence and detection of CIN-III is characteristic for the age group of 30-year-olds, and the peak incidence of cervical cancer occurs at the age of

40 years or more. According to estimates, cervical cancer can occur in about 3–5% of women with high-risk HPV infection unless secondary prevention (screening) implements [29].

the trial interview purposes is combined with the testing of its internal consistency

Cronbach's alpha calculation, the amount of items may be changed. For example, in CPC-28 53 initial items then were decreased to 28, and other researchers reported cutting down their items from 69 to 26 in order to reach optimal Cronbach's alpha within 0.7 and higher [43]. It should be noted that when evaluating the survey specific results, it is not appropriate to rely on Cronbach's alpha index solely. Reliability of the interviewees' responses does not depend on Cronbach's alpha directly. In listed researches the number of items varies from 12 [36] to 26–29

by Cronbach's alpha coefficient. During the trial interviews combined with

Results of a Survey Concerning Cervical Cancer Risk Factors among Women…

A separate domain of surveys concerning CaCx is presented by studies addressing the issues of quality of life (QoL), information needs, sexuality, and other problems in patients with cervical cancer or its precursor, who had undergone

4. The survey on cervical cancer risk factors conducted in Western

Findings of the survey presented below are quite indicative and to a definite extent may reflect the current situation with awareness of the CaCx preventive measures not only in Kazakhstan alone but, in a broad sense, in post-Soviet Central

General information about the country: the Republic of Kazakhstan is a leading state in Central Asia and refers to middle-income countries. The country ranks 9th in terms of territory in the world, 64th in terms of population, and 184th in terms of density (6.3 per sq. km). The population of the country as of January 1, 2016, is 17,417,673; the ratio of men and women is 48:52%. Share of the population aged 15–65 is 71%. The national composition of Kazakhs is 66.1%, Russians 21.5%, and other ethnic group. 12.4% (data are taken from the information source of the Agency of Statistics of the Republic of Kazakhstan). The western region is industrially developed and consists of four large provinces: Aktobe, West Kazakhstan, Mangystau, and Atyrau. All provinces are involved in oil industry, with the

During 2014–2017 a multipurpose scientific project on HPV infection and cervi-

The interview constituted a part of the mentioned research and aimed to determine qualitatively and quantitatively a group at risk for possible cervical cancer

• Identifying women of general female population who are infected with HPV in order to allocate those who are exposed to the CaCx development risk factors

diagnosed with cervical cancer by matching, to establish dominant risk factors

• Comparing women infected with HPV but not having CaCx and those

cal cancer issues was carried out across the region by the West Kazakhstan

development. Therefore, tasks of the survey were the following:

the most rational information sources for the targeted audience.

Kazakhstan: aims, methodology, and findings

presence of atomic industry in Mangystau.

University's research team.

in the region

115

4.1 Aims, materials, and methods of the research

Overall, creating an effective tool allows for obtaining a lot of valuable data for timely renewal of cervical cancer prevention strategies, including issues of selecting

[32, 40, 43] and up to 64–65 [41, 44].

DOI: http://dx.doi.org/10.5772/intechopen.81601

the treatment [45–49].

Asian states.

### 3. Survey as an instrument to get information

Survey, being the most cost-effective and quick tool to recognize needs, intentions, and perception of the targeted audience, serves for specific purposes, but its design depends not only on the aims claimed but often on standard of living and concomitant features of the sample tested, such as educational level, availability and quality of healthcare, etc. One may observe quite noticeable differences in designing the surveys depending on economic status of the countries where those tools applied. Mostly, in high-income countries, more detailed surveys designed to reveal more complex context are used, due to relatively long practicing. For example, in Italy, surveys aimed for obtaining baseline data on risk factors have been widely practiced for at least 30 years [30]. Besides, in high-income countries, web-based survey, or computer-aided self-administered interviewing (CASI), appears to be frequently used, as well as applying mail and telephone surveys, due to providing better confidentiality for an individual, despite relatively low response rate (65% considered acceptable) [31–33]. Personal interviews usually are conducted upon facing "difficult cases," i.e., where obtaining complex information is needed. Direct interviewing provides opportunities for best control, surveillance, and on-site verification. Meanwhile, direct interviewing, being a relatively expensive and time-consuming way to obtain data, nonetheless, applies more frequently in low-/middle-income countries, where there are many illiterate or low-educated people or in sites where sociocultural customs, different from western lifestyle, are practiced [34–36]. Overall, all these generalizations are quite arbitrary, as specialists choose a way of operating mostly based on purposes and capabilities of their research.

As to the models for questionnaire development, the two most cited and used approaches seem to be most popular, according to literature sources.

One of these approaches constitutes a conception of the Theory of Planned Behavior (TPB) as applied to the behavioral researches on cervical cancer issues [32, 37, 38]. According to the theory, the author Ajzen I. stated, "a more favourable attitude makes a person more attentive toward a recommendation made by significant others" [39].

The second approach refers to the Health Belief Model, on the basis of which Robert DeVellis developed guidelines summarized in his book Scale Development. Based on these guidelines, a principally new questionnaire, CPC-28, has been developed by Maria Teresa Urrutia and R. Hall [40]. The questionnaire includes six domains: "the barriers to take a Pap test," "the cues to action," "the severity," "the need to have a Pap test," "the susceptibility to cervical cancer," and "the benefit" domain. CPC-28 has been used by many researchers as an example for development of their own questionnaires [41, 42].

These approaches suggest development of questionnaires aimed to reveal perception, intentions, beliefs, and possible attitudes of the individual tested. As applied toward HPV infection and cervical cancer issues, such models gave a lot to reveal prejudices relatively CaCx preventive measures—screening and vaccination—throughout almost all strata of the female population.

The following step in the questionnaire developing is testing for validation purposes, often including "pretest-test-retest" stages. Testing is the key factor for checking the tool's validation and reliability. Usually, outer experts are involved to check the questionnaire. Field-testing in specially selected representative groups for Results of a Survey Concerning Cervical Cancer Risk Factors among Women… DOI: http://dx.doi.org/10.5772/intechopen.81601

the trial interview purposes is combined with the testing of its internal consistency by Cronbach's alpha coefficient. During the trial interviews combined with Cronbach's alpha calculation, the amount of items may be changed. For example, in CPC-28 53 initial items then were decreased to 28, and other researchers reported cutting down their items from 69 to 26 in order to reach optimal Cronbach's alpha within 0.7 and higher [43]. It should be noted that when evaluating the survey specific results, it is not appropriate to rely on Cronbach's alpha index solely. Reliability of the interviewees' responses does not depend on Cronbach's alpha directly. In listed researches the number of items varies from 12 [36] to 26–29 [32, 40, 43] and up to 64–65 [41, 44].

A separate domain of surveys concerning CaCx is presented by studies addressing the issues of quality of life (QoL), information needs, sexuality, and other problems in patients with cervical cancer or its precursor, who had undergone the treatment [45–49].

Overall, creating an effective tool allows for obtaining a lot of valuable data for timely renewal of cervical cancer prevention strategies, including issues of selecting the most rational information sources for the targeted audience.

### 4. The survey on cervical cancer risk factors conducted in Western Kazakhstan: aims, methodology, and findings

Findings of the survey presented below are quite indicative and to a definite extent may reflect the current situation with awareness of the CaCx preventive measures not only in Kazakhstan alone but, in a broad sense, in post-Soviet Central Asian states.

General information about the country: the Republic of Kazakhstan is a leading state in Central Asia and refers to middle-income countries. The country ranks 9th in terms of territory in the world, 64th in terms of population, and 184th in terms of density (6.3 per sq. km). The population of the country as of January 1, 2016, is 17,417,673; the ratio of men and women is 48:52%. Share of the population aged 15–65 is 71%. The national composition of Kazakhs is 66.1%, Russians 21.5%, and other ethnic group. 12.4% (data are taken from the information source of the Agency of Statistics of the Republic of Kazakhstan). The western region is industrially developed and consists of four large provinces: Aktobe, West Kazakhstan, Mangystau, and Atyrau. All provinces are involved in oil industry, with the presence of atomic industry in Mangystau.

### 4.1 Aims, materials, and methods of the research

During 2014–2017 a multipurpose scientific project on HPV infection and cervical cancer issues was carried out across the region by the West Kazakhstan University's research team.

The interview constituted a part of the mentioned research and aimed to determine qualitatively and quantitatively a group at risk for possible cervical cancer development. Therefore, tasks of the survey were the following:


40 years or more. According to estimates, cervical cancer can occur in about 3–5% of women with high-risk HPV infection unless secondary prevention (screening)

Survey, being the most cost-effective and quick tool to recognize needs, intentions, and perception of the targeted audience, serves for specific purposes, but its design depends not only on the aims claimed but often on standard of living and concomitant features of the sample tested, such as educational level, availability and quality of healthcare, etc. One may observe quite noticeable differences in designing the surveys depending on economic status of the countries where those tools applied. Mostly, in high-income countries, more detailed surveys designed to reveal more complex context are used, due to relatively long practicing. For example, in Italy, surveys aimed for obtaining baseline data on risk factors have been widely practiced for at least 30 years [30]. Besides, in high-income countries, web-based survey, or computer-aided self-administered interviewing (CASI), appears to be frequently used, as well as applying mail and telephone surveys, due to providing better confidentiality for an individual, despite relatively low response rate (65% considered acceptable) [31–33]. Personal interviews usually are conducted upon facing "difficult cases," i.e., where obtaining complex information is needed. Direct interviewing provides opportunities for best control, surveillance, and on-site verification. Meanwhile, direct interviewing, being a relatively expensive and time-consuming way to obtain data, nonetheless, applies more frequently in low-/middle-income countries, where there are many illiterate or low-educated people or in sites where sociocultural customs, different from western lifestyle, are practiced [34–36]. Overall, all these generalizations are quite arbitrary, as specialists choose a way of operating

As to the models for questionnaire development, the two most cited and used

One of these approaches constitutes a conception of the Theory of Planned Behavior (TPB) as applied to the behavioral researches on cervical cancer issues [32, 37, 38]. According to the theory, the author Ajzen I. stated, "a more favourable attitude makes a person more attentive toward a recommendation made by signif-

The second approach refers to the Health Belief Model, on the basis of which Robert DeVellis developed guidelines summarized in his book Scale Development. Based on these guidelines, a principally new questionnaire, CPC-28, has been developed by Maria Teresa Urrutia and R. Hall [40]. The questionnaire includes six domains: "the barriers to take a Pap test," "the cues to action," "the severity," "the need to have a Pap test," "the susceptibility to cervical cancer," and "the benefit" domain. CPC-28 has been used by many researchers as an example for development

These approaches suggest development of questionnaires aimed to reveal per-

ception, intentions, beliefs, and possible attitudes of the individual tested. As applied toward HPV infection and cervical cancer issues, such models gave a lot to reveal prejudices relatively CaCx preventive measures—screening and vaccination—throughout almost all strata of the female population.

The following step in the questionnaire developing is testing for validation purposes, often including "pretest-test-retest" stages. Testing is the key factor for checking the tool's validation and reliability. Usually, outer experts are involved to check the questionnaire. Field-testing in specially selected representative groups for

3. Survey as an instrument to get information

Current Perspectives in Human Papillomavirus

mostly based on purposes and capabilities of their research.

approaches seem to be most popular, according to literature sources.

implements [29].

icant others" [39].

114

of their own questionnaires [41, 42].

Design and protocol of the study were approved by the University's Institutional Review Board (October 9, 2014). The work was carried out in accordance with the Helsinki Declaration principles. All participants who signed the informed consent form were fully informed on the objectives of this analysis.

Qualitative detection and quantification of human papillomavirus were performed in both samples by PCR real-time method based on the Russian test systems and equipment ("DNA-Technology" LLC, Russian Federation). Production

SPSS Statistics 20 software (IBM, Armonk, NY, USA) and the program Statistica 10 (Dell software, USA) were applied for calculations. For all tests a two-side type I error of p = 0.05 or less at 95% CI was assumed statistically significant. Nonparametric operational tests were used due to a priori missing a normal distribution. To identify the dominant risk factors for CaCx development, appropriate statistical tests were carried out: an analysis of the Pearson χ2 contingency tables to identify significant links (with the definition of the Cramer's V criterion), analysis of the quantitative variables in two independent samples (Mann-Whitney test), and

The questionnaire was developed in two languages, Kazakh and Russian (optional), in a semi-structured manner, with questions, mostly closed, to collect data reflecting a role of the most known risk factors in the development of CaCx. Overall, the questionnaire included three conditional domains: the first one for collecting social/demographic information, such as age, ethnicity, education, occupation, and family (per capita) income of women who were being interviewed. This domain also included issues related to the number of pregnancies and the presence of cervical cancer in close relatives irrespective to the time period, at present or in the past (not in terms of hereditary, but to assess differences in perception). The conditional second part of the questionnaire concerned behavioral/social settings: attitude toward smoking, the number of sexual partners

during life, age of sexual activity onset, and the method of contraception

currently used, with focus on the birth control pills (BCPs). The third conditional domain included questions devoted to perception of the CaCx preventive measures: attendance of municipal PHC clinics (in terms of availability of state-sponsored free healthcare), screening activities, and attitude toward vaccination against cervical cancer. This part consisted of closed questions, to reveal the women's perception of nationwide measures, given a mentioned decreasing of the screening coverage and discontinuation of the pilot vaccination program in adolescents, started in 2013. As previously stated, adolescents' parents perceived the program

As to the content of the questionnaire, models described in the literature were not applied when designing, since all available examples were intended for relatively homogeneous audience, whereas in this questionnaire, the list of questions was identical both for women from the general sample (i.e., clinically healthy) and women who were diagnosed with CaCx. Besides, another consideration was

mattered. Such a study was the first in its kind in medical practice of the region and the country, and its response rate was unknown. So, it was decided to develop a light version of the tool consisting of 14 most important items. Eventually, this number of questions did not burden the participants and allowed the stated objec-

of the company "DNA-Technology" was certified (ISO 13485: 2012).

Results of a Survey Concerning Cervical Cancer Risk Factors among Women…

logistic regression analysis with odds ratio calculation (OR).

4.2 Questionnaire designing and survey conducting

4.1.3 Statistical processing

DOI: http://dx.doi.org/10.5772/intechopen.81601

4.2.1 Questionnaire designing

mostly negatively.

117

tives of the survey to be solved.

### 4.1.1 General sample (clinically healthy women)

In determining the sample size for general female population, the following points mattered:


In total, N according to calculations (two-side type I error of p ≤ 0.05, 95% CI) was counted 1152, of which 417 in Aktobe, 253 in Uralsk (West Kazakhstan), 237 in Atyrau, and 245 in Mangystau.

Data were collected in medical settings in cities of regional importance, including the nearest vicinities. To reach maximally possible scope of female population and avoid possible bias, all kinds of outpatient clinics were involved: statesponsored, insurance, and private ones. Enrollment of women was held either during their routine visit to the gynecologist, by ads placed in the clinics lobby, or by the invitation of sentinel specialists. Inclusion criteria for general sample were the following: age 18–60+ years, resident of Western Kazakhstan of any ethnicity, and no vaccination history.

The exclusion criteria are nonresidents of Kazakhstan and vaccination history. HIV status and pregnancy of the first trimester were not exclusion criteria.

### 4.1.2 Cervical cancer sample

As to the sample size of the patients with CaCx first time diagnosed, the number of adult (18+) female population of the republic along with the incidence of cervical cancer in Kazakhstan equaled to 4.8% (data of the Agency on Statistics as of 2013) was applied in the formula:

$$\text{IN} = \frac{p \times q \times Z\_{\infty}^2 \times N}{\Delta^2 \times N + p \times q \times Z\_{\infty}^2} \tag{1}$$

where Z\_ (α) = 1.96 is the critical values of the normal standard distribution for a given α = 0.05, N is the number of female population of the republic (6,700,000), p = 0.048 is the incidence of cervical cancer, q = 1–p = 0.952, and Δ = 0.05 is the sampling error.

According to calculations, the needed sample size was within 67–80.

All consonants to participate in the study were selected among women with first-time-diagnosed cancer across all regional oncology centers.

Inclusion criteria are any age, any stage of the cancer process, and histological verification of the diagnosis.

Exclusion criteria are nonresidents of the Western Kazakhstan and presence of the previous medical intervention—radiotherapy, chemotherapy, and surgical treatment.

Results of a Survey Concerning Cervical Cancer Risk Factors among Women… DOI: http://dx.doi.org/10.5772/intechopen.81601

Qualitative detection and quantification of human papillomavirus were performed in both samples by PCR real-time method based on the Russian test systems and equipment ("DNA-Technology" LLC, Russian Federation). Production of the company "DNA-Technology" was certified (ISO 13485: 2012).

### 4.1.3 Statistical processing

Design and protocol of the study were approved by the University's Institutional Review Board (October 9, 2014). The work was carried out in accordance with the Helsinki Declaration principles. All participants who signed the informed consent

In determining the sample size for general female population, the following

• According to a pilot study of the West Kazakhstan University on HPV as of 2014, N for HPV genotyping was 1098 with valid statistical results at the

• Statistical data on the number of urban female population living in western

In total, N according to calculations (two-side type I error of p ≤ 0.05, 95% CI) was counted 1152, of which 417 in Aktobe, 253 in Uralsk (West Kazakhstan), 237 in

Data were collected in medical settings in cities of regional importance, including the nearest vicinities. To reach maximally possible scope of female population and avoid possible bias, all kinds of outpatient clinics were involved: statesponsored, insurance, and private ones. Enrollment of women was held either during their routine visit to the gynecologist, by ads placed in the clinics lobby, or by the invitation of sentinel specialists. Inclusion criteria for general sample were the following: age 18–60+ years, resident of Western Kazakhstan of any ethnicity,

The exclusion criteria are nonresidents of Kazakhstan and vaccination history. HIV status and pregnancy of the first trimester were not exclusion criteria.

As to the sample size of the patients with CaCx first time diagnosed, the number of adult (18+) female population of the republic along with the incidence of cervical cancer in Kazakhstan equaled to 4.8% (data of the Agency on Statistics as of 2013)

<sup>Δ</sup><sup>2</sup> � <sup>N</sup> <sup>þ</sup> <sup>p</sup> � <sup>q</sup> � <sup>Z</sup><sup>2</sup>

where Z\_ (α) = 1.96 is the critical values of the normal standard distribution for a given α = 0.05, N is the number of female population of the republic (6,700,000), p = 0.048 is the incidence of cervical cancer, q = 1–p = 0.952, and Δ = 0.05 is the

<sup>∝</sup> � N

∝

(1)

<sup>N</sup> <sup>=</sup> <sup>p</sup> � <sup>q</sup> � <sup>Z</sup><sup>2</sup>

According to calculations, the needed sample size was within 67–80.

first-time-diagnosed cancer across all regional oncology centers.

All consonants to participate in the study were selected among women with

Inclusion criteria are any age, any stage of the cancer process, and histological

Exclusion criteria are nonresidents of the Western Kazakhstan and presence of the previous medical intervention—radiotherapy, chemotherapy, and surgical

form were fully informed on the objectives of this analysis.

prevalence HR-HPV 26.04% (p ≤ 0.043) [21].

cities of regional importance and suburbs.

Atyrau, and 245 in Mangystau.

and no vaccination history.

4.1.2 Cervical cancer sample

was applied in the formula:

verification of the diagnosis.

sampling error.

treatment.

116

4.1.1 General sample (clinically healthy women)

Current Perspectives in Human Papillomavirus

points mattered:

SPSS Statistics 20 software (IBM, Armonk, NY, USA) and the program Statistica 10 (Dell software, USA) were applied for calculations. For all tests a two-side type I error of p = 0.05 or less at 95% CI was assumed statistically significant. Nonparametric operational tests were used due to a priori missing a normal distribution. To identify the dominant risk factors for CaCx development, appropriate statistical tests were carried out: an analysis of the Pearson χ2 contingency tables to identify significant links (with the definition of the Cramer's V criterion), analysis of the quantitative variables in two independent samples (Mann-Whitney test), and logistic regression analysis with odds ratio calculation (OR).

### 4.2 Questionnaire designing and survey conducting

### 4.2.1 Questionnaire designing

The questionnaire was developed in two languages, Kazakh and Russian (optional), in a semi-structured manner, with questions, mostly closed, to collect data reflecting a role of the most known risk factors in the development of CaCx.

Overall, the questionnaire included three conditional domains: the first one for collecting social/demographic information, such as age, ethnicity, education, occupation, and family (per capita) income of women who were being interviewed. This domain also included issues related to the number of pregnancies and the presence of cervical cancer in close relatives irrespective to the time period, at present or in the past (not in terms of hereditary, but to assess differences in perception). The conditional second part of the questionnaire concerned behavioral/social settings: attitude toward smoking, the number of sexual partners during life, age of sexual activity onset, and the method of contraception currently used, with focus on the birth control pills (BCPs). The third conditional domain included questions devoted to perception of the CaCx preventive measures: attendance of municipal PHC clinics (in terms of availability of state-sponsored free healthcare), screening activities, and attitude toward vaccination against cervical cancer. This part consisted of closed questions, to reveal the women's perception of nationwide measures, given a mentioned decreasing of the screening coverage and discontinuation of the pilot vaccination program in adolescents, started in 2013. As previously stated, adolescents' parents perceived the program mostly negatively.

As to the content of the questionnaire, models described in the literature were not applied when designing, since all available examples were intended for relatively homogeneous audience, whereas in this questionnaire, the list of questions was identical both for women from the general sample (i.e., clinically healthy) and women who were diagnosed with CaCx. Besides, another consideration was mattered. Such a study was the first in its kind in medical practice of the region and the country, and its response rate was unknown. So, it was decided to develop a light version of the tool consisting of 14 most important items. Eventually, this number of questions did not burden the participants and allowed the stated objectives of the survey to be solved.

### 4.2.2 Validation of the questionnaire

Validation of the questionnaire was performed through Cronbach's alpha (α) calculation, and findings were summarized in Table 1.

4.2.3 Allocation of interviewees according to the "per capita income"

Results of a Survey Concerning Cervical Cancer Risk Factors among Women…

500–1000 USD as a threshold of a conditional "well-off income."

USD (according to a currency rate).

DOI: http://dx.doi.org/10.5772/intechopen.81601

4.2.4 Survey conducting

4.3 Results and discussion

cervical cancer [7]:

present survey)

119

descriptive statistics, is presented in Table 2.

(20.8 in the present survey)

Data for the "per capita income" item were taken from the website of the Statistics Committee of the Ministry of National Economy for the fourth quarter of 2014 (data on the standard of living, www.statgov.kz). The amount of the subsistence minimum determining the poverty line was within or slightly more than 100

Overall, three grades were allocated: from less than 100 USD per month up to 200 USD per capita (category of "poor"), from 200 USD up to 500 USD per capita (category of "satisfactory income"), and from 500 to 1000 USD and higher (the category of "relatively well-off people"). Allocation of the respondents in this questionnaire ("poor," "satisfactory income," "well-off") was made based on statistical publications on the standard of living formed on the basis of a sample survey of households and posted on the website of the Statistics Agency of the Republic of Kazakhstan ("Monitoring of incomes and living standards of the population in the Republic of Kazakhstan". Analytical notes of the Agency of the Republic of Kazakhstan on Statistics of the Department of Labor and Living Standards. Astana, 2011–2013). Based on the above information, it was decided to calculate per capita income within the twofold subsistence minimum amounting to 200 US dollars, as a threshold of a relatively satisfactory income, and revenue of

Direct interviews have been held on site by the research team without participation of the local staff for providing a better confidentiality of the information obtained. To motivate a better veracity, researchers allowed not to indicate a real name and provided relevant explanations on filling in the most "problematic" items—smoking, number of sexual partners, and income. At the same time, active assistance to interviewees when filling in the questionnaire was not permitted.

A total of 1166 clinically healthy and 65 having CaCx women were interviewed

Some obtained data have been cross-checked through the available sources. Information on such indicators as the age of sexual debut, number of pregnancies, specific gravity of smokers, and number of women who use BCPs has been

presented in the mentioned report on Kazakhstan by the ICO group on monitoring

• Average age of sexual debut in women in the Republic of Kazakhstan—20.7

• Average number of pregnancies—2.7 (3.0 in the present survey)

• Total number of women applying birth control pills—7.1% (4.8% in the

• Total number of smoking women—9.5% (10.8% in the present survey)

across the region. A set of data on the survey across both samples, including

The item "contraceptive use" knocked down the total row due to negative r (0.06). When removing the item, a total Cronbach's α increased from 0.53 (bad) to 0.58, i.e., eventually was recognized "doubtful." Despite the fact that reliability properties of the questionnaire did not meet accepted requirements (α 0.07 and higher), it was decided not to modify the tool for increasing its internal consistency due to considerations described above. Preliminary testing and retest also were not performed.


#### Table 1.

Results of Cronbach's α calculation.

Results of a Survey Concerning Cervical Cancer Risk Factors among Women… DOI: http://dx.doi.org/10.5772/intechopen.81601

### 4.2.3 Allocation of interviewees according to the "per capita income"

Data for the "per capita income" item were taken from the website of the Statistics Committee of the Ministry of National Economy for the fourth quarter of 2014 (data on the standard of living, www.statgov.kz). The amount of the subsistence minimum determining the poverty line was within or slightly more than 100 USD (according to a currency rate).

Overall, three grades were allocated: from less than 100 USD per month up to 200 USD per capita (category of "poor"), from 200 USD up to 500 USD per capita (category of "satisfactory income"), and from 500 to 1000 USD and higher (the category of "relatively well-off people"). Allocation of the respondents in this questionnaire ("poor," "satisfactory income," "well-off") was made based on statistical publications on the standard of living formed on the basis of a sample survey of households and posted on the website of the Statistics Agency of the Republic of Kazakhstan ("Monitoring of incomes and living standards of the population in the Republic of Kazakhstan". Analytical notes of the Agency of the Republic of Kazakhstan on Statistics of the Department of Labor and Living Standards. Astana, 2011–2013). Based on the above information, it was decided to calculate per capita income within the twofold subsistence minimum amounting to 200 US dollars, as a threshold of a relatively satisfactory income, and revenue of 500–1000 USD as a threshold of a conditional "well-off income."

### 4.2.4 Survey conducting

4.2.2 Validation of the questionnaire

Current Perspectives in Human Papillomavirus

performed.

Number of pregnancies

life

Close relatives with CaCx

Duration of sexual

Number of sexual partners

State PHC facilities attendance

CaCx screening attendance

Results of Cronbach's α calculation.

Vaccination awareness

Table 1.

118

calculation, and findings were summarized in Table 1.

Validation of the questionnaire was performed through Cronbach's alpha (α)

The item "contraceptive use" knocked down the total row due to negative r (0.06). When removing the item, a total Cronbach's α increased from 0.53 (bad) to 0.58, i.e., eventually was recognized "doubtful." Despite the fact that reliability properties of the questionnaire did not meet accepted requirements (α 0.07 and higher), it was decided not to modify the tool for increasing its internal consistency due to considerations described above. Preliminary testing and retest also were not

Initial calculation for all items Calculation upon deleting the item

Result for the scale, mean = 21.2652 Result for the scale, averaged = 19.7543

Mean interposition correlation, 0.080197 Mean interposition correlation, 0.096674

Age 0.171210 0.430272 Age 0.254605 0.541922 Ethnicity 0.148982 0.441428 Ethnicity 0.146472 0.561391 Education 0.351550 0.376869 Education 0.364908 0.511785 Employment 0.370232 0.346615 Employment 0.396442 0.497283 Income 0.374762 0.378943 Income 0.420856 0.502972

pregnancies

with CaCx

life

partners

facilities attendance

attendance

awareness

α upon removal

0.018588 0.464434 Number of

0.075294 0.451611 Close relatives

0.227343 0.415536 Duration of sexual

0.263014 0.414043 Number of sexual

0.281290 0.407147 State PHC

0.015578 0.471991 CaCx screening

0.161580 0.437350 Vaccination

Contraceptive use 0.064162 0.568096 Contraceptive use — — Smoking 0.155715 0.443014 Smoking 0.161773 0.561118

Std. dev. = 4.07863 Std. dev. = 3,85,041

Alpha Cronbach, 0.452699 Alpha Cronbach, 0.567090 Standardized alpha, 0.525177 Standardized alpha, 0.578369

N items, 14 N items, 13

correl (r)

Items General position

"contraception methods"

Items General position

correl (r)

0.021628 0.585372

0.087969 0.567689

0.301034 0.529433

0.290278 0.536063

0.292777 0.533949

0.020295 0.595756

0.162059 0.558797

α upon removal

Direct interviews have been held on site by the research team without participation of the local staff for providing a better confidentiality of the information obtained. To motivate a better veracity, researchers allowed not to indicate a real name and provided relevant explanations on filling in the most "problematic" items—smoking, number of sexual partners, and income. At the same time, active assistance to interviewees when filling in the questionnaire was not permitted.

### 4.3 Results and discussion

A total of 1166 clinically healthy and 65 having CaCx women were interviewed across the region. A set of data on the survey across both samples, including descriptive statistics, is presented in Table 2.

Some obtained data have been cross-checked through the available sources. Information on such indicators as the age of sexual debut, number of pregnancies, specific gravity of smokers, and number of women who use BCPs has been presented in the mentioned report on Kazakhstan by the ICO group on monitoring cervical cancer [7]:



Parameters (the questionnaire items)

Presence of close relatives with CaCx

General sample\*: 20.8 3.4 Range 13.0–45.0

General sample: 13.5 9.2; range 1.0–45.0 М 12.0 (6.0–20.0)

Number of sexual partners during life

General sample:

Attitude toward smoking\*

Attendance of municipal PHC facilities (outpatient clinics at the place of residence)

Participation in the nationwide screening program for cervical cancer (in statesponsored clinics)

121

Current application of contraceptive methods (at the time of interview)\*

Age of onset of sexual activity

Average lasting of sexual life

М 20.0 (18.0–22.0 by 25/75 quartile)

Average number of sexual partners during life

2.2 2.9 (1.9;2.7, CI 95%); range 1–30

Cronbach's α for each item

DOI: http://dx.doi.org/10.5772/intechopen.81601

Results of a Survey Concerning Cervical Cancer Risk Factors among Women…

Detailing General

Lasting of sexual life 0.53 0–10 years 47.2% 3.1% Regardless the

CaCx sample:

M 22.0 (7.0–59.0)

pills\*

IUD (intrauterine device)

Other (tubal ligation, calendar method, coitus interruptus)

(smoked)

I visit sometimes, irregularly

I do not visit, as I attend only private clinics

constantly

I participate irregularly (missed the last/

0.53 I visit constantly 40.7% 31.3%

0.56 I smoke

0.60 I participate

sample, N 1166

0.57 Yes 5.1% 9.4% Irrespective to the

CaCx sample, N 65

present or in the past No 94.9% 90.6%

CaCx sample: 20.3 2.3 (19.4;20.8, 95% CI) Range 19.0–21.0 M 20.0 (15.0–27.0, 25/75 quartile)

relationship lasting <sup>11</sup>–20 years 29.9% 31.3%

relationship lasting <sup>2</sup>–5 partners 28.2% 28.1%

old was considered Birth control

4.8% —

12.4% 4.7%

16.1% —

46.3% 39.0%

13.0% 29.7%

28.0% 15.6%

3.0 3.4 (2.1;3.9, CI 95%); range 1–15

10.8% 9.4% Regardless of the

34.7% 39.0% Age category <

20+ years 22.9% 65.6%

0.54 1 partner 64.7% 60.9% Regardless of the

CaCx sample:

6 and more 7.1% 10.8%

— I do not apply 43.8% 89.0% Only the age

Condoms 23.0% 6.3%

I do not smoke 89.2% 90.6%

26.5 10.8 (23.3;29.7, CI 95%)

Notes

time period: at

marriage or

category ≤49 years

smoking lasting

30 years old was not considered as not included in the screening routine


### Results of a Survey Concerning Cervical Cancer Risk Factors among Women… DOI: http://dx.doi.org/10.5772/intechopen.81601

Parameters (the questionnaire items)

General sample:

Range 16.0–63.0

Monthly income per

Total number of pregnancies

General sample\*: 3.0 2.2; range 0–16; М 3.0 (2.8–4.4 by 25/75 quartile)

120

Average number of pregnancies in the history

capita

Average age of the interviewees

34.5 9.9 (31.2;36.1, 95% CI)

М 33.0 (27.0–41.0 by 25/75 quartile)

Cronbach's α for each item

Current Perspectives in Human Papillomavirus

Age categories 0.54 18–29 37.7% 1.5%

Detailing General

Ethnicity 0.56 "Asian" 85.3% 79.7% Representatives of

Other (mostly Caucasus ethnic groups)

> Professional college

Higher education (university)

Employment 0.50 Not occupied 33.6% 48.4% Unemployed,

Medium-sized proficiency sector

> Highly-skilled occupations

100 USD and up to 200 USD

From 200 USD up to 500 USD

From 500 to 1000 USD and >

0.50 From less than

Low-skilled labor 13.7% 26.5%

Education level 0.51 School education 31.4% 65.6%

sample, N 1166

30–39 34.0% 21.9% 40–49 17.8% 34.4% 50–60+ 10.5% 42.2%

CaCx sample, N 65

CaCx sample: 49.0 12.4 (45.9;52.1, 95% CI) Range 28.0–80.0 M 47.5 (40.0–58.5 by 25/75 quartile)

"European" 13.6% 20.3% Representatives of

22.9% 17.2%

45.7% 17.2%

20.7% 9.4%

32.0% 15.6%

0.59 None 10.7% 3.1% This refers to

3 and more 53.2% 71.9%

1.1% — Azerbaijanis,

40.1% 50.0% Category of "poor"

39.4% 46.9% Category of

20.5% 3.1% Category of

ectopic pregnancy <sup>1</sup>–2 36.1% 25.0%

CaCx sample: 4.5 3.3; range 0–14; M 4.0 (2.0–6.0 by 25/75 quartile) Notes

Turkic-speaking people

the Slavic diasporas, Germans

Dagestanis, Koreans, etc.

housewives, retired

people

"satisfactory income"

relatively well-off people

childbirth, abortion,


\*An asterisk indicates some indicators of general sample, for which there are republic-wide data from other sources.

### Table 2.

Total data for both samples across the region with inclusion of descriptive statistics.

In another authoritative source [50], published in the framework of the UNICEF international research and summarizing data of the Republic of Kazakhstan on many medical and social indicators, the share of women 15–24 years old who had sexual intercourses with the "unofficial partner/partners" (promiscuity) during the last year was 16.6%, while the proportion of smoking women aged 15–49 years—8.4%.

Overall, data from these authoritative sources in fact coincided with those obtained in the present work, which to a definite extent might indicate reliability of the information provided by participants of the interview.

their history. These women constitute a group at risk for further development of the process, i.e., persistent infection and possible invasive cancer. Increasing awareness of CaCx prevention among young women should rank first in making policy

4.3.2 Relationship between the level of education and perception of CaCx preventive

Further analysis has been performed with the aim of clarifying the relationship between the level of education and perception of preventive measures for cervical cancer. As mentioned before, attendance of state (municipal) PHC facilities implies accessibility and sufficiency of a national free healthcare. In a broad sense, opportunity to attend state-sponsored free outpatient clinics is also to be considered as a

concerning CaCx issues.

№. Parameter or potential risk factor

DOI: http://dx.doi.org/10.5772/intechopen.81601

5 Level of per capita income

6 Number of pregnancies

7 Presence of close relatives with CaCx

9 Number of sexual partners

10 Application of birth control pills

12 Municipal outpatient clinic attendance

13 Participation in screening program

14 Awareness of vaccination

Table 3.

123

8 Sexual life duration/age of onset of sexual activity

Achieved level of significance, pvalue (≤0.05)

1 Age 0.062 0.09 — 2 Ethnicity 0.78 0.03 — 3 Education 0.4 0.05 — 4 Employment 0.002 0.11 χ<sup>2</sup>

Results of a Survey Concerning Cervical Cancer Risk Factors among Women…

Cramer's V value

0.00007 0.13 χ<sup>2</sup>

<0.00001 0.14 χ<sup>2</sup>

0.52 0.02 —

0.062 0.07 —

<0.00001 0.16 χ<sup>2</sup>

0.00096

0.46 0.02 —

0.19 0.05 —

0.54 0.03 —

0.33 Phi

11 Smoking 0.47 0.02 —

Analysis of the links between HPV infection and social/behavioral parameters.

Maximum contribution to the final statistics, Pearson's χ<sup>2</sup>

—18.03 9.1% out of 25.0% HPV-infected are representatives of highly skilled occupations

—19.1 12.1% out of 25.0%—a group with an income of 200–500 USD per month per capita ("satisfactory income")

—24.0 11.2% out of 25.0% had three and more pregnancies

—30.7 23.5% out of 25.0% had up to five partners

—

prevention of socially significant diseases.

measures

### 4.3.1 Social profile of women infected with HPV in the western region of Kazakhstan

A total of 25% of women from the general sample in frames of the present research appeared to be infected either with HR-HPV types or with non-HR types (22.3; 27.7 CI 95%, p = 0.05), N 291. One of the tasks of the present study was to compare those infected with HPV with those who are not infected in order to identify links between the risk for HPV infection and social/behavioral parameters. Results of the analysis are presented in Table 3.

This analysis made it possible to outline the social profile of women infected with HPV in the western region of the country. These are women with satisfactory financial status (monthly per capita income 200–500 USD), occupied with highly skilled work, who had up to five sexual partners and more than three pregnancies in


Results of a Survey Concerning Cervical Cancer Risk Factors among Women… DOI: http://dx.doi.org/10.5772/intechopen.81601

### Table 3.

In another authoritative source [50], published in the framework of the UNICEF international research and summarizing data of the Republic of Kazakhstan on many medical and social indicators, the share of women 15–24 years old who had sexual intercourses with the "unofficial partner/partners" (promiscuity) during the last year was 16.6%, while the proportion of smoking women aged

Total data for both samples across the region with inclusion of descriptive statistics.

Overall, data from these authoritative sources in fact coincided with those obtained in the present work, which to a definite extent might indicate reliability of

4.3.1 Social profile of women infected with HPV in the western region of Kazakhstan

A total of 25% of women from the general sample in frames of the present research appeared to be infected either with HR-HPV types or with non-HR types (22.3; 27.7 CI 95%, p = 0.05), N 291. One of the tasks of the present study was to compare those infected with HPV with those who are not infected in order to identify links between the risk for HPV infection and social/behavioral parameters.

This analysis made it possible to outline the social profile of women infected with HPV in the western region of the country. These are women with satisfactory financial status (monthly per capita income 200–500 USD), occupied with highly skilled work, who had up to five sexual partners and more than three pregnancies in

the information provided by participants of the interview.

Results of the analysis are presented in Table 3.

15–49 years—8.4%.

Table 2.

122

Parameters (the questionnaire items)

Awareness of vaccination against cervical cancer

Cronbach's α for each item

Current Perspectives in Human Papillomavirus

Detailing General

previous examination) I do not participate (ignore, as I attend gynecologists in private clinics only

0.58 I know nothing

about vaccination

I have heard about vaccination, but do not know how to percept

I welcome vaccination against cervical cancer

I am set against vaccination/I consider it unnecessary/ dangerous

\*An asterisk indicates some indicators of general sample, for which there are republic-wide data from other sources.

sample, N 1166

37.3% 45.3%

38.8% 60.9%

33.6% 25.0%

22.9% 10.9%

4.7% 3.1%

CaCx sample, N 65

Notes

Analysis of the links between HPV infection and social/behavioral parameters.

their history. These women constitute a group at risk for further development of the process, i.e., persistent infection and possible invasive cancer. Increasing awareness of CaCx prevention among young women should rank first in making policy concerning CaCx issues.

### 4.3.2 Relationship between the level of education and perception of CaCx preventive measures

Further analysis has been performed with the aim of clarifying the relationship between the level of education and perception of preventive measures for cervical cancer. As mentioned before, attendance of state (municipal) PHC facilities implies accessibility and sufficiency of a national free healthcare. In a broad sense, opportunity to attend state-sponsored free outpatient clinics is also to be considered as a prevention of socially significant diseases.

In the general sample (Table 1), only 13% of respondents indicated that they do not visit state-sponsored clinics at the place of residence, while among respondents with higher education, this indicator has increased up to 35.1% (p ≤ 0.00001; Cramer's V 0.14; χ<sup>2</sup> –23.1). Only 62.7% of interviewees (34.7% constantly and 28.0% sometimes) respond to an invitation to visit free screening in state (municipal) facilities, and 37.3% of respondents do not attend free screening program at all, preferring either opportunistic screening in private physicians or not undergoing Pap test at all. Among the educated subjects, this indicator has increased up to 51.3% (p = 0.002, Cramer's V 0.1, χ<sup>2</sup> –18.1). Among respondents in the general sample, 40.7% regularly visit the state PHC facilities, but only 34.7% of all interviewees treat toward screening activities responsibly.

showing to them more favorable attitude (close relatives, etc.), might be traced in findings of the present survey. A group of interviewees which collided with cervical cancer in their families were analyzed in order to compare their awareness with a baseline level in general sample. Among relatives of women who fell ill or died from cervical cancer, the awareness of vaccination has reached 76.8% (p = 0.01, phi 0.1,

Results of a Survey Concerning Cervical Cancer Risk Factors among Women…

–6.0), i.е., even higher than in the stratum of highly educated interviewees (69.2%), which implied that a part of them purposefully had sought information regarding prevention/treatment of CaCx. These findings involve the issues on information sources. According to the mentioned survey conducted across the country's households [50], a share of women aged 15–24 which use the Internet (social networks, messengers) is 94.6%, while the proportion of women aged 15–49 years, at least once a week consuming mass media (newspapers, magazines, radio, TV), is only 16.1%. Results of this research concerning preferences in information seeking in young women would be worth to arrange CaCx prevention

4.4 Cervical cancer-diseased women in the western region of Kazakhstan:

A total of 65 women aged in average 49.0 12.4 diseased with CaCx (just diagnosed and not yet undergoing treatment) have been interviewed during a survey. Overall description of this sample has been summarized in Table 1. What is the most inherent to them comparing to the general sample: most of them (65.6%) have just school education (compulsory for all population in Kazakhstan) vs. 31.4% in the general sample, the share of the employed in highly skilled occupations is 15.4 vs. 32% in the general sample, only 3.1% of them refer to a "relatively well-off" in terms of income, a part of them never visited municipal PHC facilities (31.3%) vs. 13% in the general sample, and they never heard about vaccination (60.9%) vs.

In order to reveal the dominant risk factors for cervical cancer and select a control group, matching was conducted among those infected with HPV but not affected with cervical cancer and those having CaCx. Matching was carried out in proportion 1:1 (65 vs. 65), i.e., for each case of the disease, there was one case from the control group. Selection of the control group for matching was made according to the age criterion and also with the help of the random number generator, i.e., each HPV-infected had equal chances to get into the control group. Thus, 65 respondents from HPV-infected group were randomly selected for analysis to iden-

An analysis of the Pearson χ<sup>2</sup> contingency tables to identify significant links

Table 5 presents results of the Mann-Whitney test, detailing the analysis of

To assess the likelihood of the disease onset, a logistic regression model was developed. As a "positive effect," the onset of the disease was accepted, and as a "negative effect"—the absence of cervical cancer. The logistic regression was performed by the "forward" method, provided that the variables were introduced, if p < 0.05, and removed, if p > 0.1. The sample size was 130 cases, where 65 (50%)

Thus, social profile of women with CaCx was defined: they are mostly aged 50– 60 + years old, in overwhelming majority infected with HPV 16, poorly educated, unemployed, mostly living within the poverty line, with lasting of sexual life over 20 years, not participating in the screening program, and not aware of the cervical cancer prevention measures (vaccination). A large number of pregnancies and high

awareness campaign via the Internet across the country.

likelihood of the disease onset

DOI: http://dx.doi.org/10.5772/intechopen.81601

38.8% of clinically healthy women, respectively.

(including the Cramer's V criterion) is shown in Table 4.

level of viral load also mattered in their profile.

tify risk factors.

125

quantitative variables.

χ2

More than two-thirds (69.2%) of subjects with higher education are aware of vaccination against cervical cancer (p ≤ 0.00001, Cramer's V 0.18, χ<sup>2</sup> –23.1), whereas in the total sample, this figure amounted to 56.5% (33.6% have heard, but cannot clarify their attitude—positive or negative, 22.9% are aware and welcome).

Ideally, close to 100% of educated subjects of this research had to welcome mass screening and nationwide immunization program against cervical cancer. For example, according to a large-scale survey conducted in Brazil (n = 54,000), a high correlation was found between the level of education/standard of living and the attendance of mammography and cytology (Pap test): up to 70–80% of educated interviewees constantly visited screening events—r = 0.52 and r = 0.66, respectively [51]. In general, Kazakhstan belongs to a group of countries with high Human Development Index (HDI). According to the results of HDI evaluation in 2016 [52] when these data were collected, our country ranked 56th in the international rating between Belarus and Malaysia.

Given the relatively high HDI of the country with a large stratum of enlightened women, the findings suggest that measures for primary (vaccination) and secondary (screening) prevention of cervical cancer are insufficient and do not meet the needs of population, especially of its educated part. The same applies to situation with municipal PHC facility attendance (35.1% of educated subjects avoid visit and 51.3% of them avoid free screening there). In this context, relatively low attendance found in the present survey in educated population can be indicative of unsatisfactory quality of services, which eventually may result in bringing down a prestige of the national healthcare.

### 4.3.3 Overall awareness of CaCx preventive measures: role of information sources

Overall awareness of the broad circle of the issues on CaCx prevention varies depending on the countries, age groups, and education level. Though 71–78% adults aged 50–70 in England knew that the main aim of the screening programs was to catch cancer early, but only 18% of them were aware that cervical screening is primarily preventive [53]. The low level of Pap screening awareness was found among the students in South Korea [32], about 65% female Saudi teachers were considered less-knowledgeable about CaCx risk factors [33], only 13% of interviewed Uyghur women heard about vaccine against CaCx [34], and 30.1% of female students in Poland were unaware of vaccination as a prevention method [44]. In the present research, the obtained data on awareness of vaccination in general sample are approximately similar with the mentioned: 38.8% knew nothing about vaccines against cervical cancer, while 33.6% heard, but could not decide how to percept it. These findings evidence a deficit of information apprehensible for a majority of female population.

A trend, to a definite extent confirming the mentioned TPV model, according to which most of people in issues of health are guided by opinion of significant others

Results of a Survey Concerning Cervical Cancer Risk Factors among Women… DOI: http://dx.doi.org/10.5772/intechopen.81601

showing to them more favorable attitude (close relatives, etc.), might be traced in findings of the present survey. A group of interviewees which collided with cervical cancer in their families were analyzed in order to compare their awareness with a baseline level in general sample. Among relatives of women who fell ill or died from cervical cancer, the awareness of vaccination has reached 76.8% (p = 0.01, phi 0.1, χ2 –6.0), i.е., even higher than in the stratum of highly educated interviewees (69.2%), which implied that a part of them purposefully had sought information regarding prevention/treatment of CaCx. These findings involve the issues on information sources. According to the mentioned survey conducted across the country's households [50], a share of women aged 15–24 which use the Internet (social networks, messengers) is 94.6%, while the proportion of women aged 15–49 years, at least once a week consuming mass media (newspapers, magazines, radio, TV), is only 16.1%. Results of this research concerning preferences in information seeking in young women would be worth to arrange CaCx prevention awareness campaign via the Internet across the country.

### 4.4 Cervical cancer-diseased women in the western region of Kazakhstan: likelihood of the disease onset

A total of 65 women aged in average 49.0 12.4 diseased with CaCx (just diagnosed and not yet undergoing treatment) have been interviewed during a survey. Overall description of this sample has been summarized in Table 1. What is the most inherent to them comparing to the general sample: most of them (65.6%) have just school education (compulsory for all population in Kazakhstan) vs. 31.4% in the general sample, the share of the employed in highly skilled occupations is 15.4 vs. 32% in the general sample, only 3.1% of them refer to a "relatively well-off" in terms of income, a part of them never visited municipal PHC facilities (31.3%) vs. 13% in the general sample, and they never heard about vaccination (60.9%) vs. 38.8% of clinically healthy women, respectively.

In order to reveal the dominant risk factors for cervical cancer and select a control group, matching was conducted among those infected with HPV but not affected with cervical cancer and those having CaCx. Matching was carried out in proportion 1:1 (65 vs. 65), i.e., for each case of the disease, there was one case from the control group. Selection of the control group for matching was made according to the age criterion and also with the help of the random number generator, i.e., each HPV-infected had equal chances to get into the control group. Thus, 65 respondents from HPV-infected group were randomly selected for analysis to identify risk factors.

An analysis of the Pearson χ<sup>2</sup> contingency tables to identify significant links (including the Cramer's V criterion) is shown in Table 4.

Table 5 presents results of the Mann-Whitney test, detailing the analysis of quantitative variables.

Thus, social profile of women with CaCx was defined: they are mostly aged 50– 60 + years old, in overwhelming majority infected with HPV 16, poorly educated, unemployed, mostly living within the poverty line, with lasting of sexual life over 20 years, not participating in the screening program, and not aware of the cervical cancer prevention measures (vaccination). A large number of pregnancies and high level of viral load also mattered in their profile.

To assess the likelihood of the disease onset, a logistic regression model was developed. As a "positive effect," the onset of the disease was accepted, and as a "negative effect"—the absence of cervical cancer. The logistic regression was performed by the "forward" method, provided that the variables were introduced, if p < 0.05, and removed, if p > 0.1. The sample size was 130 cases, where 65 (50%)

In the general sample (Table 1), only 13% of respondents indicated that they do not visit state-sponsored clinics at the place of residence, while among respondents with higher education, this indicator has increased up to 35.1% (p ≤ 0.00001;

sometimes) respond to an invitation to visit free screening in state (municipal) facilities, and 37.3% of respondents do not attend free screening program at all, preferring either opportunistic screening in private physicians or not undergoing Pap test at all. Among the educated subjects, this indicator has increased up to 51.3%

40.7% regularly visit the state PHC facilities, but only 34.7% of all interviewees

vaccination against cervical cancer (p ≤ 0.00001, Cramer's V 0.18, χ<sup>2</sup>

More than two-thirds (69.2%) of subjects with higher education are aware of

whereas in the total sample, this figure amounted to 56.5% (33.6% have heard, but cannot clarify their attitude—positive or negative, 22.9% are aware and welcome). Ideally, close to 100% of educated subjects of this research had to welcome mass

Given the relatively high HDI of the country with a large stratum of enlightened women, the findings suggest that measures for primary (vaccination) and secondary (screening) prevention of cervical cancer are insufficient and do not meet the needs of population, especially of its educated part. The same applies to situation with municipal PHC facility attendance (35.1% of educated subjects avoid visit and 51.3% of them avoid free screening there). In this context, relatively low attendance found in the present survey in educated population can be indicative of unsatisfactory quality of services, which eventually may result in bringing down a prestige of

4.3.3 Overall awareness of CaCx preventive measures: role of information sources

Overall awareness of the broad circle of the issues on CaCx prevention varies depending on the countries, age groups, and education level. Though 71–78% adults aged 50–70 in England knew that the main aim of the screening programs was to catch cancer early, but only 18% of them were aware that cervical screening is primarily preventive [53]. The low level of Pap screening awareness was found among the students in South Korea [32], about 65% female Saudi teachers were considered less-knowledgeable about CaCx risk factors [33], only 13% of

interviewed Uyghur women heard about vaccine against CaCx [34], and 30.1% of female students in Poland were unaware of vaccination as a prevention method [44]. In the present research, the obtained data on awareness of vaccination in general sample are approximately similar with the mentioned: 38.8% knew nothing about vaccines against cervical cancer, while 33.6% heard, but could not decide how to percept it. These findings evidence a deficit of information apprehensible for a

A trend, to a definite extent confirming the mentioned TPV model, according to which most of people in issues of health are guided by opinion of significant others

screening and nationwide immunization program against cervical cancer. For example, according to a large-scale survey conducted in Brazil (n = 54,000), a high correlation was found between the level of education/standard of living and the attendance of mammography and cytology (Pap test): up to 70–80% of educated interviewees constantly visited screening events—r = 0.52 and r = 0.66, respectively [51]. In general, Kazakhstan belongs to a group of countries with high Human Development Index (HDI). According to the results of HDI evaluation in 2016 [52] when these data were collected, our country ranked 56th in the international rating

–23.1). Only 62.7% of interviewees (34.7% constantly and 28.0%

–18.1). Among respondents in the general sample,

–23.1),

Cramer's V 0.14; χ<sup>2</sup>

(p = 0.002, Cramer's V 0.1, χ<sup>2</sup>

between Belarus and Malaysia.

the national healthcare.

majority of female population.

124

treat toward screening activities responsibly.

Current Perspectives in Human Papillomavirus


\* For other genotypes of HPV p-value 0.05 has not been revealed.

### Table 4.

Results of contingency table analysis.

were positive and 65 (50%) were negative ones. The logistic regression model was evaluated through the Nagelkerke R2 (0.3881, p < 0.0001) and recognized "working." Coefficients, standard errors, and a chance, including the odds ratio (OR), have been calculated by commonly accepted methods, and the risk group for CaCx begins at a value >40. Results are summarized in Table 6.

Thus, likelihood of the disease onset:


Variables

127

U

Criteria are significant

> Summary rank CaCx

4931.5 3845.0 4049.5 4955.0 4595.0 4785.0

3453.5 4540.0 4335.5 3430.0 3790.0 3600.0

1455.0

 2.94174

 0.003264

 2.94231

 0.003258

 0.003057

Results of a Survey Concerning Cervical Cancer Risk Factors among Women…

1645.0

 2.04674

 0.040685

 2.06837

 0.038606

 0.040401

1285.0

 3.74254

 0.000182

 3.74551

 0.000180

 0.000148

1969.5

0.51816

 0.604346

1765.0

1.48147

 0.138482

Age Age of onset of sexual activity

Number of partners

Duration of sexual life (exposure)

Number of pregnancies

Viral load level

Table 5. Results of the

Mann-Whitney

 test.

 Summary rank control

 U 1308.5

 3.63184

 0.000281

 3.63469 1.49867

0.56433

 0.572531

 0.603861

DOI: http://dx.doi.org/10.5772/intechopen.81601

 0.133960

 0.138856

 0.000278

 0.000233

 Z

 p-Level

 Z correct.

 p-Level

 Two-sided

 exact p

Mann-Whitney

 at the level of p <

 test .05000

Calculation of the morbidity prognosis based on OR in both groups (HPVinfected but not affected with CaCx and having CaCx) was performed.


Table 5.

Results of the Mann-Whitney test.

### Results of a Survey Concerning Cervical Cancer Risk Factors among Women… DOI: http://dx.doi.org/10.5772/intechopen.81601

were positive and 65 (50%) were negative ones. The logistic regression model was evaluated through the Nagelkerke R2 (0.3881, p < 0.0001) and recognized "working." Coefficients, standard errors, and a chance, including the odds ratio (OR), have been calculated by commonly accepted methods, and the risk group for

14 Awareness of vaccination 0.026 0.27 9.2—not aware of vaccination 15 Type of HPV\* 0.00007 0.35—phi 15.9–72.6% of women with CaCx

• Decreases by 14 times at a per capita income level of 500–1000 USD

• Increases by 0.9 times with the lasting of sexual life over 20 years

• Increases by 0.16 times provided lack of attendance in the state (municipal)

• Decreases by 3.3 times provided at least irregular participation in screening for

Calculation of the morbidity prognosis based on OR in both groups (HPV-

infected but not affected with CaCx and having CaCx) was performed.

CaCx begins at a value >40. Results are summarized in Table 6.

Thus, likelihood of the disease onset:

\* For other genotypes of HPV p-value 0.05 has not been revealed.

№. Qualitative parameter or potential risk factor

Current Perspectives in Human Papillomavirus

4 Employment

5 The level of per capita income

7 Presence of close relatives with CaCx

9 Number of sexual partners

12 Attendance of the state clinics

13 Participation in screening program

Results of contingency table analysis.

(occupation)

Achieved level of p-value (≤0.05)

6 Number of pregnancies 0.23 0.15 2.9

8 Sexual life duration 0.007 0.28 9.9—over 20 years

10 Methods of contraception 0.32 0.007 0.0009 11 Smoking 0.97 0.002 0.0007

1 Age 0.003 0.29 11.3—age 50–60+ 2 Ethnicity 0.5 0.09 1.19

3 Education 0.00075 0.33 14.4—poorly educated

Cramer's V criterion

0.00053 0.37 17.6—not employed

0.001 0.33 13.6—low income

0.13 0.13—phi 2.2

0.19 0.16 3.3

0.09 0.19 4.8

0.006 0.28 10.2—not participating in

Maximum contribution to the summary statistics, Pearson's χ<sup>2</sup>

> (unemployed, housewives, retired)

> > screening program

are infected with typ. 16

+ (category of relatively well-off)

clinics

126

Table 4.

cervical cancer


cancer prevention measures (vaccination). A large number of pregnancies and high

Findings obtained in this first survey arranged in Kazakhstan are quite general-

Elaboration and implementation of a new program should focus on a significant increase of awareness in female population on cervical cancer consequences and a

This research has been performed in frames of the scientific project "Epidemio-

logical analysis of Human Papillomavirus in Western Kazakhstan in relation to HPV-attributable cervical pathology - social, clinical and genetic aspects," funded by the Committee of Science of the Ministry of Education and Science of the Republic of Kazakhstan (Grant №. 2230/GF4, State Registration No. 0115РК01224). The study has been registered in ISRCTN registry, No. ISRCTN71514910

All authors declare that they have no competing interests.

izable for post-Soviet Central Asian states and, to a lesser extent, for the overwhelming majority of Asian developing countries with high incidence of CaCx. These findings are quite able to contribute to an understanding why women become diseased with CaCx. Low standard of living due to lack of education, low attendance of screening, and low awareness on preventive measures, all these reasons, are interacted and constitute a set of universal triggers for vulnerability toward CaCx. Kazakhstan is not an exclusion within a wide range of middle-income countries, which need drastic changes in approach to prevent cervical cancer and in revision of a set of applied measures. Population-based surveys, being a very effective tool for studying needs of the targeted audience, should serve as the first step toward diagnostically optimal and cost-effective updated nationwide program for the CaCx

The likelihood of the CaCx onset under conditions of Western Kazakhstan decreases by 14 times at relatively high standard of living, income not less 500 USD per capita (OR 0.0713, p = 0.024) and decreases by 3.3 times provided at least irregular participation in screening for cervical cancer (OR 0.3384, p = 0.0304). Overall, the findings suggest that measures for primary (vaccination) and secondary (screening) prevention of cervical cancer are insufficient and do not meet

level of HPV viral load also mattered in their profile.

DOI: http://dx.doi.org/10.5772/intechopen.81601

Results of a Survey Concerning Cervical Cancer Risk Factors among Women…

the needs of the population, especially of its educated part.

5. General conclusion

prevention.

(01.02.2018).

129

Conflict of interest

Acknowledgements

role of HPV infection as a causative factor.

### Table 6.

Calculation of a chance and OR for the disease onset.

Overall, prognosis is justified for 73.9% infected with HPV, but not affected by cervical cancer and for 70.3% for women having CaCx (correctly predicted cases— 72.09%, at a cutoff value of p = 0.5).

### 4.5 What was learned from a survey on cervical cancer risk factors in Western Kazakhstan

Based on the data collected in 1166 clinically healthy women, of them 291 (25%) infected with HPV, and 65 women having cervical cancer, one may conclude that the main reason for a chance of the CaCx onset is a low understanding on what are the measures of preventing CaCx.

Only 34.7% of interviewees constantly participate in nationwide screening program, while 37.3% fully ignore nationwide screening in free state-sponsored PHC facilities. Favorable attitude toward vaccination against cervical cancer stated 22.9% of respondents, whereas 38.8% knew nothing, and the rest 33.6% could not clarify their position in this issue.

Education is a key factor for better perception of preventive measures—more than two-thirds of respondents with higher education are aware of vaccination against cervical cancer (p ≤ 0.00001, Cramer's V 0.18, χ<sup>2</sup> –23.1).

And meanwhile, the same stratum of educated women mostly negatively treats to state-sponsored PHC facilities, avoiding visit (35.1 vs. 13.0% in the general sample, p ≤ 0.00001, Cramer's V 0.14, χ<sup>2</sup> –23.1). Moreover, 51.3% of educated women avoid nationwide free screening in state PHC facilities (p = 0.002; Cramer's V 0.1; χ<sup>2</sup> –18.1). This fact evidences insufficient quality of medical care in statesponsored clinics.

Lack of relevant information on the CaCx in interviewees who had close relatives with CaCx made them seek and eventually reach a higher awareness level concerning preventive measures—76.8% vs. 56.5 in the general sample (p = 0.01, phi 0.1, χ<sup>2</sup> –6.0). These findings evidence a deficit of information apprehensible for a majority of the female population.

Though a more number of sexual partners contributed to the risk of being infected with HPV (p ≤ 0.00001, Cramer's V 0.16, χ<sup>2</sup> –30.7), but this factor played no role in the risk of CaCx development. Overall, social profiles of HPV-infected and CaCx-affected women differ significantly and, mainly, by standard of living and occupational status.

Social profile of women having CaCx is mostly aged 50–60 + years old, in overwhelming majority infected with HPV 16 (72.6% of them), poorly educated, unemployed, mostly living within the poverty line, with the sexual life lasting over 20 years, not participating in the screening program, and not aware of the cervical

Results of a Survey Concerning Cervical Cancer Risk Factors among Women… DOI: http://dx.doi.org/10.5772/intechopen.81601

cancer prevention measures (vaccination). A large number of pregnancies and high level of HPV viral load also mattered in their profile.

The likelihood of the CaCx onset under conditions of Western Kazakhstan decreases by 14 times at relatively high standard of living, income not less 500 USD per capita (OR 0.0713, p = 0.024) and decreases by 3.3 times provided at least irregular participation in screening for cervical cancer (OR 0.3384, p = 0.0304).

Overall, the findings suggest that measures for primary (vaccination) and secondary (screening) prevention of cervical cancer are insufficient and do not meet the needs of the population, especially of its educated part.

### 5. General conclusion

Overall, prognosis is justified for 73.9% infected with HPV, but not affected by cervical cancer and for 70.3% for women having CaCx (correctly predicted cases—

Constant 1.69108 0.58494 8.3581 0.0038

Variables Coefficient Std. error Wald p ОR 95% CI

Sexual life lasting >20 years (3) 0.083917 0.023797 12.4349 0.0004 1.0875 1.0380–1.1395

2.64144 0.86882 9.2432 0.0024 0.0713 0.0130–0.3912

1.80433 0.63020 8.1974 0.0042 6.0759 1.7667–20.8954

1.08362 0.50041 4.6892 0.0304 0.3384 0.1269–0.9023

4.5 What was learned from a survey on cervical cancer risk factors in Western

Based on the data collected in 1166 clinically healthy women, of them 291 (25%) infected with HPV, and 65 women having cervical cancer, one may conclude that the main reason for a chance of the CaCx onset is a low understanding on what are

Only 34.7% of interviewees constantly participate in nationwide screening program, while 37.3% fully ignore nationwide screening in free state-sponsored PHC facilities. Favorable attitude toward vaccination against cervical cancer stated 22.9% of respondents, whereas 38.8% knew nothing, and the rest 33.6% could not clarify

Education is a key factor for better perception of preventive measures—more than two-thirds of respondents with higher education are aware of vaccination

And meanwhile, the same stratum of educated women mostly negatively treats

women avoid nationwide free screening in state PHC facilities (p = 0.002; Cramer's

Lack of relevant information on the CaCx in interviewees who had close relatives with CaCx made them seek and eventually reach a higher awareness level concerning preventive measures—76.8% vs. 56.5 in the general sample (p = 0.01,

Though a more number of sexual partners contributed to the risk of being

no role in the risk of CaCx development. Overall, social profiles of HPV-infected and CaCx-affected women differ significantly and, mainly, by standard of living

Social profile of women having CaCx is mostly aged 50–60 + years old, in overwhelming majority infected with HPV 16 (72.6% of them), poorly educated, unemployed, mostly living within the poverty line, with the sexual life lasting over 20 years, not participating in the screening program, and not aware of the cervical

–18.1). This fact evidences insufficient quality of medical care in state-

–6.0). These findings evidence a deficit of information apprehensible for

to state-sponsored PHC facilities, avoiding visit (35.1 vs. 13.0% in the general

–23.1).

–23.1). Moreover, 51.3% of educated

–30.7), but this factor played

against cervical cancer (p ≤ 0.00001, Cramer's V 0.18, χ<sup>2</sup>

infected with HPV (p ≤ 0.00001, Cramer's V 0.16, χ<sup>2</sup>

sample, p ≤ 0.00001, Cramer's V 0.14, χ<sup>2</sup>

a majority of the female population.

and occupational status.

72.09%, at a cutoff value of p = 0.5).

Calculation of a chance and OR for the disease onset.

Current Perspectives in Human Papillomavirus

Income per capita 500–1000

Attendance of state clinics (lack of attendance) (3)

Participation in screening

USD + (3)

(irregular) (2)

Table 6.

the measures of preventing CaCx.

their position in this issue.

V 0.1; χ<sup>2</sup>

phi 0.1, χ<sup>2</sup>

128

sponsored clinics.

Kazakhstan

Findings obtained in this first survey arranged in Kazakhstan are quite generalizable for post-Soviet Central Asian states and, to a lesser extent, for the overwhelming majority of Asian developing countries with high incidence of CaCx. These findings are quite able to contribute to an understanding why women become diseased with CaCx. Low standard of living due to lack of education, low attendance of screening, and low awareness on preventive measures, all these reasons, are interacted and constitute a set of universal triggers for vulnerability toward CaCx.

Kazakhstan is not an exclusion within a wide range of middle-income countries, which need drastic changes in approach to prevent cervical cancer and in revision of a set of applied measures. Population-based surveys, being a very effective tool for studying needs of the targeted audience, should serve as the first step toward diagnostically optimal and cost-effective updated nationwide program for the CaCx prevention.

Elaboration and implementation of a new program should focus on a significant increase of awareness in female population on cervical cancer consequences and a role of HPV infection as a causative factor.

### Acknowledgements

This research has been performed in frames of the scientific project "Epidemiological analysis of Human Papillomavirus in Western Kazakhstan in relation to HPV-attributable cervical pathology - social, clinical and genetic aspects," funded by the Committee of Science of the Ministry of Education and Science of the Republic of Kazakhstan (Grant №. 2230/GF4, State Registration No. 0115РК01224).

The study has been registered in ISRCTN registry, No. ISRCTN71514910 (01.02.2018).

### Conflict of interest

All authors declare that they have no competing interests.

Current Perspectives in Human Papillomavirus

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(16)31392-7

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### Author details

Saule Balmagambetova\*, Arip Koyshybaev, Kanshaiym Sakiyeva, Olzhas Urazayev and Elnara Ismagulova West Kazakhstan Marat Ospanov State Medical University, Aktobe, Kazakhstan

\*Address all correspondence to: sau3567@gmail.com

© 2018 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Results of a Survey Concerning Cervical Cancer Risk Factors among Women… DOI: http://dx.doi.org/10.5772/intechopen.81601

### References

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[2] Shrestha AD, Neupane D, Vedsted P, Kallestrup P. Cervical cancer prevalence, incidence and mortality in low and middle income countries: A systematic review. Asian Pacific Journal of Cancer Prevention. 2018;19(2): 319-324. DOI: 10.22034/ APJCP.2018.19.2.319

[3] Rogovskaya SI, Shabalova IP, Mikheeva IV, Minkina GN, et al. Human papillomavirus prevalence and typedistribution, cervical cancer screening practices and current status of vaccination in Russian Federation, the Western countries of the former Soviet Union, Caucasus Region and Central Asia. Vaccine. 2013;31(7):H46-H58. DOI: 10.1016/j.vaccine.2013.06.043

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Author details

130

and Elnara Ismagulova

Saule Balmagambetova\*, Arip Koyshybaev, Kanshaiym Sakiyeva, Olzhas Urazayev

West Kazakhstan Marat Ospanov State Medical University, Aktobe, Kazakhstan

© 2018 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/ by/3.0), which permits unrestricted use, distribution, and reproduction in any medium,

\*Address all correspondence to: sau3567@gmail.com

provided the original work is properly cited.

Current Perspectives in Human Papillomavirus

screening based on cytology or HPV test. Geburtshilfe und Frauenheilkunde. 2016;76(10):1081-1085. DOI: 10.1055/s-0042-112457

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[14] Huh WK, Ault KA, Chelmow D, Davey DD, Goulart RA, et al. Use of primary high-risk human papillomavirus testing for cervical cancer screening: Interim clinical guidance. Obstetrics and Gynecology. 2015;125(2):330-337. DOI: 10.1097/ AOG.0000000000000669

[15] zur Hausen H. Papillomaviruses causing cancer: Evasion from host-cell control in early events in carcinogenesis. Journal of the National Cancer Institute. 2000;92(9):690-698. Available from: https://www.ncbi.nlm.nih.gov/ pubmed/10793105. PMID: 10793105

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[17] Bernard HU, Burk RD, Chen Z, van Doorslaer K, zur Hausen H, de Villiers EM. Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology. 2010;401(1):70-79. DOI: 10.1016/j.virol.2010.02.002

[18] Schiffman M, Clifford G, Buonaguro FM. Classification of weakly carcinogenic human papillomavirus types: Addressing the limits of epidemiology at the borderline. Infectious Agents and Cancer. 2009;4(8):17-29. DOI: 10.1186/ 1750-9378-4-8

[19] Bzhalava D, Guan P, Franceschi S, Dillner J, Clifford G. A systematic review of the prevalence of mucosal and cutaneous human papillomavirus types. Virology. 2013;445:224-231. DOI: 10.1016/j.virol.2013.07.015

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[36] Lataifeh I, Al Chalabi H, Faleh N, Yousef L, et al. A survey of knowledge and awareness of Jordanian female university students of human

papillomavirus infection and its vaccine. European Journal Of Gynaecological Oncology. 2016;6:796-799. DOI:

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[20] Kairbayev M, Chingissova Z, Shibanova A et al. Planning future cervical cancer prevention strategy in Kazakhstan. In: Proceedings of the 18th International Meeting of the European Society of Gynaecological Oncology (ESGO); 2013. International Journal of Gynecological Cancer 2013;8:1031

[21] Bekmukhambetov Y,

17(5):2667-2672

Balmagambetova S, et al. Distribution of high risk human papillomavirus types in Western Kazakhstan – Retrospective analysis of PCR data. Asian Pacific Journal of Cancer Prevention. 2016;

[22] Niyazmetova L, Aimagambetova G, Stambekova N, et al. Application of molecular genotyping to determine prevalence of HPV strains in Pap smears of Kazakhstan women. International Journal of Infectious Diseases. 2016;54: 85-88. DOI: 10.1016/j.ijid.2016.11.410

[23] Aimagambetova G, Azizan A. Epidemiology of HPV infection and HPV-related cancers in Kazakhstan: A review. Asian Pacific Journal of Cancer Prevention. 2018;19(5):1175-1180. DOI:

10.22034/APJCP.2018.19.5.1175

DOI: 10.1002/ijc.25396

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2014. 364 p. Available from:

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[13] Evantash E. The Critical Importance of HPV Co-Testing for Cervical Cancer Screening. Special Report. Available from: https://www.mlo-online. com/critical-importance-hpvco-testing-cervical-cancer-screening [Accessed: December 21, 2017]

[14] Huh WK, Ault KA, Chelmow D, Davey DD, Goulart RA, et al. Use of

papillomavirus testing for cervical cancer screening: Interim clinical guidance. Obstetrics and Gynecology. 2015;125(2):330-337. DOI: 10.1097/

[15] zur Hausen H. Papillomaviruses causing cancer: Evasion from host-cell control in early events in carcinogenesis. Journal of the National Cancer Institute. 2000;92(9):690-698. Available from: https://www.ncbi.nlm.nih.gov/ pubmed/10793105. PMID: 10793105

[16] Wheeler CM, Hunt WC, Schiffman M, Castle PE. Human papillomavirus genotypes and the cumulative 2-years risk of cervical precancer. The Journal of Infectious Diseases. 2006;194(9): 1291-1299. DOI: 10.1086/507909

[17] Bernard HU, Burk RD, Chen Z, van Doorslaer K, zur Hausen H, de Villiers EM. Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology. 2010;401(1):70-79. DOI: 10.1016/j.virol.2010.02.002

Buonaguro FM. Classification of weakly carcinogenic human papillomavirus types: Addressing the limits of epidemiology at the borderline. Infectious Agents and Cancer. 2009;4(8):17-29. DOI: 10.1186/

[18] Schiffman M, Clifford G,

1750-9378-4-8

132

primary high-risk human

AOG.0000000000000669

0042-112457

[26] USA CDC Press Release 19 June 2013: New study shows HPV vaccine helping lower HPV infection rates in teen girls. Available from: https://www. cdc.gov/vaccines/news/press-rel/ [Accessed: June 19, 2013]

[27] Saslow D, Andrews KS, Manassaram-Baptiste D, Loomer L, et al. On behalf of the American Cancer Society guideline development group: Human papillomavirus vaccination guideline update: American Cancer Society guideline endorsement. CA: A Cancer Journal for Clinicians. 2016; 66(5):375-385. DOI: 10.3322/caac.21355

[28] Risk Factors for Cervical Cancer Development. Available from: https:// www.cdc.gov/cancer/ knowledge/provider-education/ [Accessed: September 16, 2015]

[29] Cuzick J, Arbyn M,

Sankaranarayanan R, et al. Overview of human papillomavirus-based and other novel options for cervical cancer screening in developed and developing countries. Vaccine. 2008;26(10):29-41. DOI: 10.1016/j.vaccine.2008.06.019

[30] Donfrancesco C, Palmieri L, Lo Noce C, Vanuzzo D, et al. Challenges and opportunities in establishing an health examination survey. Epidemiology, Biostatistics and Public Health (EBPH). 2017;14(3). DOI: 10.2427/12726

[31] Mannocci A, Bontempi C, Colamesta V, Ferretti F, et al. Reliability of the telephone-administered International Physical Activity Questionnaire in an Italian pilot sample. Epidemiology, Biostatistics and Public Health (EBPH). 2014;11(1). DOI: 10.2427/8860

[32] Kim HW. Awareness of Pap testing and factors associated with intent to

undergo Pap testing by level of sexual experience in unmarried university students in Korea: Results from an online survey. BMC Women's Health. 2014;14:100. DOI: 10.1186/1472-6874- 14-100

[33] Salem MR, Amin TT, Alhulaybi AA, et al. Perceived risk of cervical cancer and barriers to screening among secondary school female teachers in Al Hassa, Saudi Arabia. Asian Pacific Journal of Cancer Prevention. 2017; 18(4):969-979. DOI: 10.22034/ APJCP.2017.18.4.969

[34] Abudukadeer A et al. Knowledge and attitude of Uyghur women in Xinjiang province of China related to the prevention and early detection of cervical cancer. World Journal of Surgical Oncology. 2015;13:110. DOI: 10.1186/s12957-015-0531-8

[35] Selmouni F, Zidouh A, Alvarez-Plaza C, El Rhazi K. Perception and satisfaction of cervical cancer screening by visual inspection with acetic acid (VIA) at Meknes-Tafilalet region, Morocco: A population-based cross-sectional study. BMC Women's Health. 2015;15:106. DOI: 10.1186/s12905-015-0268-0

[36] Lataifeh I, Al Chalabi H, Faleh N, Yousef L, et al. A survey of knowledge and awareness of Jordanian female university students of human papillomavirus infection and its vaccine. European Journal Of Gynaecological Oncology. 2016;6:796-799. DOI: 10.12892/ejgo3293.2016

[37] Duffett-Leger LA, Letourneau NL, Croll JC. Cervical cancer screening practices among university women. Journal of Obstetric, Gynecologic, and Neonatal Nursing. 2008;37(5):572-581. DOI: 10.1111/j.1552-6909.2008.00276.x

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[42] Szabóová V, Švihrová V, Švihra J Jr, Rišková L, Hudečková H. Validation of a new tool for identification of barriers to cervical cancer prevention in Slovakia. Ceská Gynekologie. 2018;83(1):30-35. PMID: 29510636

[43] Saulle R, Miccoli S, Unim B, et al. Validation of a questionnaire for young women to assess knowledge, attitudes and behaviors towards cervical screening and vaccination against HPV in Italy. Epidemiology, Biostatistics and Public Health (EBPH). 2014;11(2): 173-181. DOI: 10.2427/8913

[44] Kamzol W, Jaglarz K, Tomaszewski KA, Puskulluoglu M, et al. Assessment of knowledge about cervical cancer and its prevention among female students aged 17-26 years. European Journal of Obstetrics, Gynecology, and Reproductive Biology. 2013;166(2): 196-203. DOI: 10.1016/j.ejogrb. 2012.10.019

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Current Perspectives in Human Papillomavirus

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[46] Iyer NS, Osann K, Hsieh S, Tucker JA, Monk BJ, Nelson EL, et al. Health behaviors in cervical cancer survivors and associations with quality of life. Clinical Therapeutics. 2016;38: 467-475. DOI: 10.1016/j.clinthera.

[47] Zhou W, Yang X, Dai Y, Wu Q, He G, Yin G. Survey of cervical cancer survivors regarding quality of life and sexual function. Journal of Cancer Research and Therapeutics. 2016;12:938.

DOI: 10.4103/0973-1482.175427

and validation of the functional assessment of chronic illness therapy – Cervical dysplasia (FACIT-CD) questionnaire for Serbian women. European Journal of Obstetrics,

2018;226:7-14. DOI: 10.1016/j.

ejogrb.2018.05.009

[48] Kesic V, Sparic R, Watrowskic R, DotliC J, et al. Cross-cultural adaptation

Gynecology, and Reproductive Biology.

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org/dataset/kazakhstan-

May 16, 2018]

311X00073014

crt.2015.425

2016.02.006

[39] Ajzen I. The theory of planned behavior. Organizational Behavior and Human Decision Processes. 1991;50(2): 179-211. DOI: 10.1016/0749-5978(91)

[40] Urrutia MT, Hall R. Beliefs about cervical cancer and Pap test: A new Chilean questionnaire. Journal of Nursing Scholarship. 2013;45(2): 126-131. DOI: 10.1111/jnu.12009

[41] Jaglarz K, Tomaszewski KA, Kamzol W, Puskulluoglu M, et al. Creating and field-testing the questionnaire for the assessment of knowledge about cervical cancer and its prevention among schoolgirls and female students. Journal of Gynecologic Oncology. 2014;25(2): 81-89. DOI: 10.3802/jgo.2014.25.2.81

[42] Szabóová V, Švihrová V, Švihra J Jr, Rišková L, Hudečková H. Validation of a new tool for identification of barriers to cervical cancer prevention in Slovakia. Ceská Gynekologie. 2018;83(1):30-35.

[43] Saulle R, Miccoli S, Unim B, et al. Validation of a questionnaire for young women to assess knowledge, attitudes and behaviors towards cervical

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[44] Kamzol W, Jaglarz K, Tomaszewski KA, Puskulluoglu M, et al. Assessment of knowledge about cervical cancer and its prevention among female students aged 17-26 years. European Journal of

[45] Lee Y, Lim MC, Kim SI, Joo J, Lee DO, Park SY. Comparison of quality of

173-181. DOI: 10.2427/8913

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2012.10.019

134

PMID: 29510636

10.1037/0278-6133.25.5.604

90020-T

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### *Edited by Shailendra K. Saxena*

This book gives a comprehensive overview of recent advances in human papillomavirus (HPV) infection, as well as general concepts of infections, immunopathology, diagnosis, treatment, epidemiology, and etiology. It examines current clinical recommendations in the management of HPV, highlighting the ongoing issues, recent advances, and future directions in diagnostic approaches and therapeutic strategies. The book focuses on various aspects and properties of HPV, whose deep understanding is very important for safeguarding the human race from further loss of resources and economies due to HPV infection. I hope that this work will increase the interest in this field of research and that the readers will find it useful for their investigations, management, and clinical usage.

Published in London, UK © 2019 IntechOpen © Aunt\_Spray / iStock

Current Perspectives in Human Papillomavirus

IntechOpen Book Series

Infectious Diseases, Volume 2

Current Perspectives in

Human Papillomavirus

*Edited by Shailendra K. Saxena*