Syrian mothers, why to accept or to refuse HPV vaccine for their teen girls

Background: Cervical cancer (CC) ranks the eighth most frequent cancer among Syrian women with crude incidence rates 1.4 per 100, 000 populations per year. This study aimed to test the acceptance of the human papillomavirus (HPV) vaccine among mothers of schoolgirls in sixth-grade class. Methods: A cross-sectional survey was conducted through a structured and self-administrated questionnaire. A total of 400 Syrian mothers of schoolgirls were selected randomly by the cluster sampling method in Aleppo city, Syria, in 2011. Significant variables from univariate analysis were included in an enter technique multiple logistic regression analysis. Results: The response rate was 86%. If the vaccine was free, 282 (81.7%) mothers would accept the vaccine for themselves and 236 (68.4%) for their daughters, respectively. However, the acceptance rate grossly decreased to 24.6% and 15.1%, respectively, if the vaccine was not provided free. The high cost of the HPV vaccine and lack of knowledge were the significant barriers for mothers' acceptance of the HPV vaccine. Protection of daughters and the trust with health authority were the main encouraging reasons to accept the HPV vaccine. Findings from logistic regression analysis revealed that the employed mothers (odds ratio = 2.4; 95% CI: 1.3–4.4), with a positive history of gynecological examination (OR = 2.1; 95% CI: 1.6–2.9) and having sound knowledge (OR = 2.4; 95% CI: 1.0– 5.7) are independent factors related to the acceptance of the HPV vaccine for their daughters. Conclusion: The results from this study suggest that mothers from different cultural backgrounds, including Syrian mothers, are holding different beliefs on privacy and health that may affect their willingness to accept the HPV vaccine.

The crude incidence rates of CC related to HPV are 1.4 per 100 000 population of Syrian women per year compared to 6.2 in Tunisia, 4.5 in Sudan, 2.4 in Jordan, 2.1in Iraq, and 1.3 in both Egypt and Saudi Arabia [27]. Recently, the HPV vaccines ___________________________________________________ drsaadalezzi@gmail.com 2 Department of Public Health, Faculty of Medicine, Bezmialem Vakif University, Istanbul, Turkey Full list of author information is available at the end of the article have been licensed in over 120 countries, including some of the Arab world countries such as Egypt, Saudi Arabia, Kuwait, Bahrain, United Arab Emirates, and Morocco. However, in 2012 only six of low and middle-income countries (LMICs) were implementing national HPV vaccination program [28,29], that is why assessing of mother's acceptance of this vaccine before developing and implementing similar vaccination program is very important.

Study design and participants
This quantitative cross-sectional survey was conducted through a structured and self-administrated questionnaire at the primary schools in Aleppo Governorate, Syria. At the beginning of the year 2011, the Aleppo governorate was the largest city in the northeast part of Syria, with an estimated total population of 6,235,000. The purpose of the study was explained to all potential participants, and all those who agreed to take part gave written consent before participation.

Sampling technique
Between April and May 2011, a cluster sampling technique was recruited to collect a sample of 345 mothers of sixth-grade schoolgirls. In the first stage, twenty schools randomly selected in an average of four schools from each of the north, south, east, west, and central areas of Aleppo. In the second stage, one of the sixth-grade classes in each of these 20 schools randomly selected. All the schoolgirls (aged 12-13 years old) in the selected classes with their mothers were encouraged to participate in the study. Only female, primary, public schools in Aleppo city that function during the day time were included. Schools that only serve special needs students and evening schools were excluded.

Study instrument
The questionnaire was based on and virtually identical to previously published two studies in Belgium and Turkey, respectively [7,21]. With the help of two gynecologists and one family physician, minor modifications were made before and after a pilot trial (20 mothers) aimed at adapting the questionnaire to the Arabic population. The questionnaire contained a total of forty questions divided into three sections: socio-demographic and economics (part 1), knowledge of mothers about HPV infection and vaccination (part 2), and mother acceptance of the HPV vaccine for their daughters and reasons for acceptance and non-acceptance (part 3).

Statistical analysis
Data are presented as mean ± standard deviation (SD) or as numbers. All statistical analysis was carried out using the SPSS program, version 16 (SPSS Inc, Chicago, IL, USA). The bivariate analysis was done using the chi-square test. Multiple logistic regressions (Enter technique) were done to control for confounders and to obtain a predictive model of mother's acceptance of the HPV vaccine. All tests were two-sided, and a P-value of < 0.05 was considered statistically significant.

Descriptive analyses
Out of 400 questionnaires distributed to mothers, 345 of them returned the completed forms through their daughters, making the response rate of 86%. At baseline, the sample studied was mostly young, unemployed mothers with low education (secondary school or less) and low economic status. The mean age was 37±6.4 years old (Table 1).

Gynecological and vaccination outcomes
At the time of the study, most of the mothers reported a positive history of gynecological examination in the last five years with a positive family history of cancer in 35.9%. However, most of them had a negative history of cervical cancer screening and Pap smear tests. The highest percent 92.2% of schoolgirls in the sixth grade had received their all childhood vaccines, and few of them experienced some adverse effects after vaccination, such as rising in temperature or localized swelling ( Table 1).

Level of knowledge
A 14 item questionnaire tested mothers' knowledge in three areas; cervical cancer (4 questions), HPV infection (6 questions), and HPV vaccine (4 questions) [11]. The total knowledge score is the sum of all the knowledge questions and can range from 0 to 14. A score of 7 or more was considered good knowledge. The mean knowledge score was 2.67±2.3, and only 42 (27.8%) mothers had good knowledge (score seven or more) compared to 303 (72.2%) mother had poor knowledge (score six or less) ( Table 2). An internal consistency value of 0.8 Cronbach's Alpha was reported for all questions.

Mothers' acceptance of HPV vaccine
The vast majority of 282 (81.7%) of mothers had accepted the vaccine for themselves and 236 (68.4%) for their daughters. However, the acceptance rate grossly decreased to 24.6% for mothers and 15.1% for daughters, respectively, if the vaccine was not provided free of charge (Table 3).

Bivariate analysis
Seven factors are found to play a role in improving mothers' acceptance of the HPV vaccine for their daughters. These factors, including the employed mothers, with high family income, having a positive history of gynecological examinations, have undergone screening for CC, having a positive history of Pap smear test, with a positive attitude toward vaccination themselves and those with good knowledge (Table 5).  Table 6). The probability of mother to accept the HPV vaccine for her daughter is =1/1+e˗ᶻ, Z= (0.874*employment status) + (0.750*Gynecological examination) + (0.885*good knowledge level).  [27]. However, the number of unknown cervical cancer cases due to undiagnosed or unrecorded cases expected to be high. Moreover, the sensitivity of sexual issues in Arab societies increases the chances of denied cases of sexually transmitted diseases (STDs).
In the current study, out of 345 participated mothers, only 35 (10.1%) had undergone cervical cancer screening, and 50 (14.5%) have had an annual gynecological examination. Clearly, this study showed a low coverage rate of the cervical cancer screening program in Syria. The previous study from Turkey supports this finding indicated that around 38% of women (aged 17-80 years old) have had an annual gynecological examination [30].
Unfortunately, very few Syrian mothers (12, 3.5%) have correctly defined females (aged15-24 years old) as the age group at higher risk of HPV infection. This low-risk perception of HPV infection and poor knowledge levels may partly explain why they were more accepting of HPV vaccination for themselves (81.7%) than for their daughters (68.4%). Similarly, findings have seen among Turkish women (90% vs. 64%) [30]; however, the reverse has been reported in some other studies from United States [24][25][26] and Belgium [21].

Determinants of mothers to accept HPV vaccination for their daughters
Employment and family income are interrelated factors and differently affecting the acceptance of HPV vaccination. In the present study, employed mothers had a significantly higher acceptance rate towards the HPV vaccination for daughters (OR=2.4, 95%CI 1.3-4.4, p =0.005) compared to unemployed mothers. Moreover, about 76.5% of mothers who had higher family income (more than 15,000 Syrian lira /monthly ) accepted the HPV vaccination for daughters compared to 65% of mothers with either unknown or low family income (OR=1.7, 95% CI 1.01-3, p =0.037). Dursun et al. [30] found that the employed Turkish women were more accepting of the HPV vaccine than unemployed women (61% vs. 40%, P < 0.0001), however, there was no significant difference in the HPV vaccine acceptance rate according to family income and most of them (88%) were believed that the government should pay the cost of vaccination.
Contrary to our findings, conditions when the parents not gainfully employed [7] or at lower income were more likely to support the acceptance of HPV vaccination [5]. Although most respondents in this study, 303 (72.2%) lacked good knowledge concerning CC, HPV infection, and its vaccine, however mothers who had good knowledge accepted the HPV vaccine for their daughters more than mothers who had poor knowledge. Understandably, willingness and the intention to vaccinate associated with awareness and knowledge about HPV [7,12].
Medical counseling has a significant impact on family attitude and the final decision to vaccinate the daughters even prior to the sexual debut [22]. Moreover, the more trained caregivers were, the more likely to correctly classify illnesses and help mothers to make the right decision [31].
In this study, mothers who had a positive history of gynecological examination and positive history of cervical cancer screening were more likely to accept the HPV vaccine for their daughters than their counterparts. Moreover, among the participants, 54 (15.7%) mothers have experienced Pap smear tests, and only four cases were reported with abnormal history; however, these mothers are significantly more accepting of the HPV vaccine for their daughters than the others. Similar findings were reported among Turkish women [30].
Results from countries such as the USA [22,24], Canada [12] and the Netherlands [23] found that the younger mothers or parents are more likely to accept HPV vaccination than older women or parents. However, in this study, there was no significant relationship between the age of mothers and their decision to accept the HPV vaccine for their daughters. Surprisingly, families with higher education levels were associated with a decreased likelihood of having daughters receive the HPV vaccine [6,7,13]. In previous studies [5,9,11], maternal education was related to excellent knowledge of CC and HPV infection; however, in our study, there was no significant association between higher maternal education and the acceptance rate of the HPV vaccine.

Why mothers accept HPV vaccine for daughters
The majority of Syrian mothers who have accepted the HPV vaccine for their daughters have cited the protection and the trust in health authority approval as the most important reasons or additional reasons. Similar findings were reported in the USA [32] and Canada [6].
In most developed [5,9,15,17] and developing countries [14,19] including our study, the recommendations from the healthcare providers have indicated to be the most important influencing factor in deciding to get vaccinated. However, future research on health care providers' attitudes toward the vaccine could improve the interplay between health care providers and patients. Therefore information from health care providers could be important for successful vaccine uptake. Considerably, one-third of Syrian mothers accepted the HPV vaccine because they strongly believed in all vaccinations. The effectiveness of vaccine seven and the parents' belief in vaccines were other prominent factors [32].

Why mothers refuse HPV vaccine for daughters
About one third (31.6%) of Syrian mothers did not accept the HPV vaccine for their daughters. The economic burden and testing the willingness to pay are essential considerations before introducing the vaccine. The acceptance rate came down to only 15.1% for daughters and 24.6% for Syrian mothers if the vaccine is chargeable. Similar findings are found among Swedish parents of children (aged 12-15 years old); 76% of them were willing to vaccinate their daughters if the vaccine is for free, and 63% were willing to pay for the vaccine [7].
In the current study, the average monthly income of the families was 21, 201 (SD 14, 495) Syrian lira. The HPV vaccine appears to be very costly for Syrian families. This high cost makes mothers hesitate to pay for the HPV vaccine and consequently could influence the vaccine uptake in all over Syria. Moreover, Syrian people have a high vaccine uptake in the national vaccination program (92.2% in this study). Except for the HPV vaccine, the national vaccination program offers free vaccinations through public health services. That is why some of the Syrian mothers might expect the HPV vaccine to be free as well. The financial situation and decision of the family is the prerogative of the husband in most Syrian families, which may also explain the tending of about 11.9% of mothers waiting for their husbands to make the final decision [20].
The lack of sufficient information negatively reflected in the opinion of about half (46.7%) of Syrian mothers. Mothers have hesitated and asked for more information about the HPV vaccine before accepting to pay for vaccination. This fact has also been reported by Onan et al. (2009) among Turkish women; 61.5% required more information about the vaccine before they could decide to get the vaccine [9]. Dempsey et al. (2009) found evidence that low-risk perception of HPV infection was one of the common reasons for refusing the vaccine [9]. As expected, among Syrian mothers who participated in this study, only 8.7% of them knew that both men and women could be affected by HPV infection and 96% of them either chose the incorrect age group at highest risk for acquiring HPV or they did not know the age-associated with this. Of the Syrian mothers surveyed, 10.4% were aware that HPV is transmitted via sexual intercourse. Moreover, the minority, only 8.4% of mothers, realized that HPV infection could lead to cancer.
A picture of low-risk perception about HPV infection appeared among Syrian mothers who refused the HPV vaccine because they thought that their daughters are not at risk of cervical cancer (13.8%); afraid of the possible unknown side effects of the vaccine (15.6%); thought that their daughters were too young to be vaccinated against sexually transmitted diseases (8.3%); thought that no enough research had been done on this new vaccine (6.4%) and the negative attitude towards vaccines in general (5.5%).
Such findings are supported by Dempsey et al. (2006), who found that parents concern about the lack of knowledge, safety, and the perception that their daughter was too young as factors associated with declining acceptance of the HPV vaccine [9]. In Canada, Ogilvie et al. [6] also found that the overall attitude to vaccines was predictive of parents having a daughter receive the HPV vaccine in a publicly funded school-based HPV vaccine program. The main reasons for not having a daughter receive the HPV vaccine were concerned about the HPV vaccine safety (29.2%), preference to wait until their daughters get older (15.6%).

Strength and limitations
We believe this study has made an essential contribution to the plan in the HPV vaccine implementation in Syria and Arabic countries. This study was clarified the reason behind mothers' acceptance in two ways. Directly, we asked Syrian mothers about the reasons for accepting or refusing the HPV vaccine. Statistically, we tried to found a significant relationship between mother acceptance and factors by performing the bivariate and multivariate analysis.
The study sample was collected from schools within the city of Aleppo and did not include the rural areas around Aleppo. For that, we can claim that the result of the study is representative of Syrian mothers' acceptance from the urban area but not rural areas. Because CC is a disease of women, we assumed that the acceptance of the mothers for the HPV vaccine is essential to the success of the vaccination program. Some previous studies were done among both parents, while this study was done among mothers only. Decision-making in some families may involve both the father and mother.

Conclusions
The results from this study suggest that the Syrian mothers who participated differ from other populations in terms of their reasons for accepting the HPV vaccine. Mothers from different cultural backgrounds hold differing beliefs on privacy and health that may affect their willingness to accept the vaccine that prevents STDs. The acceptance rate of the HPV vaccine is positively related to low cost or free of charge vaccine. Lack of knowledge was a significant barrier for mothers to accept the HPV vaccine. Protection of daughters and the trust with health authority were the main two reasons encouraging mothers to accept the HPV vaccine for their daughter. However, mothers who are working with a positive history of gynecological examination and good knowledge were the most influential factors affecting the acceptance of the HPV vaccine in logistic regression.
We recommend further studies to confirm the findings of this study. Cost-effectiveness studies to test the affordability of vaccines are critical. More effort must need to educate Syrian mothers through the media and educational campaign about sexually transmitted diseases (including HPV) and an association between HPV infection and CC.