Women’s awareness of breast cancer symptoms: a national cross-sectional study from Palestine

This study was a national cross-sectional study conducted from July 2019 to March 2020. The study population was Palestinian women aged 18 years and over. Recruitment of participants was done from among female visitors to Palestinian governmental hospitals, primary healthcare centers and public spaces, including malls, markets, gardens, restaurants, churches, mosques, and transportation stations. Recruitment took place in the two main geographical areas of Palestine, the Gaza Strip and the WBJ. Excluded from taking part in the study were women with a citizenship other than Palestinian, women working or studying in the field of health, healthcare and medicine, as well as those visiting oncology departments or clinics.

Convenience sampling was used to recruit eligible women from the designated data collection sites, governmental hospitals, primary healthcare centers, and public spaces located in 11 governorates across Palestine. This was intended to represent the diversity of the Palestinian community in the study cohort. In 2019, the estimated female population (≥ 15 years) was 947,100 females in the WBJ and 587,271 females in the Gaza Strip [13]. With a confidence level of 95.0% and a margin of error of 3.0%, a total minimum sample size of 2132 was needed (1066 for each of the WBJ and the Gaza Strip).

A modified version of the Breast Cancer Awareness Measure (BCAM) was used to collect data. The BCAM is a validated tool that was designed to measure the public awareness of BC [14]. The original BCAM was first translated into Arabic by two bilingual experts and then back-translated into English by another two different bilingual experts. The Arabic version of the BCAM was evaluated for clinical relevance and accuracy of translation by five experts in the field of BC, public health, and survey design. This was followed by running a pilot study (n = 35) to assess the clarity of questions in the Arabic version of the BCAM. The internal consistency of the Arabic BCAM was tested using Cronbach’s Alpha that reached an acceptable value of 0.753.

The questionnaire included two sections. The first section described the sociodemographic factors of study participants including age, menarche, parity, highest level of education, occupation, monthly income, marital status, place of residency, having a chronic disease, and knowing someone with cancer. The second section evaluated the participant’s awareness of 13 BC symptoms. Of the 13 BC symptoms, 11 were adopted from the original BCAM [14] and ‘extreme generalized fatigue’ as well as ‘unexplained weight loss’ have been added to the questionnaire since they were included in other forms of Cancer Awareness Measure [15‐18], and it was thought that it would be helpful to include them in the context of BC. To minimize the possibility of participants answering questions randomly, the original questions evaluating the recognition of BC symptoms with yes/no/do not know responses were modified into a 5-point Likert scale (1 = strongly disagree, 5 = strongly agree). Meanwhile, the participants’ responses were subsequently converted to correct/incorrect responses similar to what was done in previous studies [19‐24].

For data collection, an electronic tool ‘Kobo Toolbox’ was used [14]. This secure tool can be used offline and online through smart phones. Participants were invited to complete the questionnaire in a face-to-face interview. Female data collectors with a medical background received a special training on how to use Kobo Toolbox and how to approach potential participants in the waiting areas at hospitals, primary healthcare centers, and public spaces on a daily basis. The inclusion of female data collectors was intended to minimize the possibility of women feeling embarrassed to answer some sensitive questions. Securing privacy was part of the training received and was carefully considered, where recruited women were interviewed in private at the designated place. In addition, all interviews were completed with the presence of the interviewer only.

The age of 40 is when women are first invited to undergo BC screening in Palestine [10]. Therefore, the continuous variable of age was categorized into two distinct groups using this cutoff: 18–39 years and ≥ 40 years. Menarche was categorized into three categories: early (≤ 11 years), normal (11–15 years), and late (≥ 16 years) [25]. Parity was also categorized into three categories: nulliparity, low multiparity [2‐4], and grand multiparity (≥ 5) [26]. The minimum wage in the Palestinian community is 1450 NIS (about $450) [27]. As a result, this was selected as a cutoff to categorize the monthly income into two categories: < 1450 NIS and ≥ 1450 NIS.

Continuous non-normally distributed variables were described using the median and interquartile range (IQR). Categorical variables were described using frequencies and percentages. Baseline comparisons between the Gaza Strip vs. the WBJ were performed using Pearson's Chi-square test if the variable was categorical or Kruskal–Wallis test if it was continuous.

For questions based on the 5-point Likert scale, ‘strongly agree’ and ‘agree’ were considered to be correct answers whereas ‘strongly disagree’, ‘disagree’, and ‘not sure’ were considered to be incorrect answers. BC symptoms were further categorized into three categories: breast symptoms, nipple symptoms, and other symptoms. Recognition of each of the BC symptoms was described using frequencies and percentages with comparisons made by Pearson's Chi-Square test. This was followed by running bivariable and multivariable logistic regression analyses. The model of the multivariable analyses adjusted for age-group, educational level, occupation, monthly income, residency, having a chronic disease, knowing someone with cancer, marital status, and site of data collection. This model was determined based on other previous studies [11, 28‐30]. Results of bivariable logistic regression analyses were provided in Additional file 1.

To evaluate the participants’ awareness level of BC symptoms, a previously used scoring system was also utilized in this study [19‐24]. For each correctly recognized BC symptom, the participant was given one point. The total score (ranging from 0 to 13) was calculated and categorized into three categories based on the number of BC symptoms recognized: poor (0 to 4), fair (5 to 9), and good (10 to 13). Comparisons in the awareness level between the Gaza Strip vs. the WBJ were performed using Pearson's Chi-Square test. Bi- and multi-variable logistic regression analyses were also used to test the association between participant characteristics with having a good awareness level.

Sensitivity analyses were performed and included women who were married, divorced, or widowed. Bi- and multi-variable logistic regression analyses were utilized to examine the association between participant characteristics and displaying good awareness. The multivariable models adjusted for the same factors included in the main analyses in addition to parity. Results of the sensitivity analyses were provided in Additional file 1.

Complete case analysis was used to handle missing data, which were completely at random. Data were analyzed using Stata software version 16.0 (StataCorp, College Station, Texas, United States).

Of the 6269 approached participants, 5434 participants completed the questionnaire (response rate = 86.7%). A total of 5257 questionnaires were included in the analysis (13 excluded and 164 had missing data): 2551 from the Gaza Strip and 2706 from the WBJ. The median age [IQR] for all participants was 31.0 years [24.0, 43.0] (Table 1). Participants living in the WBJ were more likely to be older, have higher monthly income, know someone with cancer, and suffer from more chronic diseases than participants living in the Gaza Strip.

A total of 2191 participants (41.7%) demonstrated good awareness of BC symptoms (Table 2). Participants from the Gaza Strip were more likely than participants from the WBJ to have good awareness (47.0.0% vs. 36.7%).

On the multivariable analysis, being 40 years or older, completing a post-secondary education, knowing someone with cancer, and visiting hospitals and primary healthcare centers were all associated with an increase in the likelihood of having a good awareness level of BC symptoms (Table 3). However, living in the WBJ was associated with a decrease in the likelihood of having good awareness.

Among all participants, breast symptoms were more often recognized than nipple symptoms. The most frequently identified BC symptom was ‘lump or thickening in the breast’ (n = 4887, 92.9%) followed by ‘lump or thickening under the armpit’ (n = 4394, 83.6%) (Table 4). These symptoms were also the most identified symptoms in both the Gaza Strip and the WBJ. The least frequently identified symptoms were ‘pulling in of the nipple’ (n = 2665, 50.7%) and ‘change in the position of the nipple’ (n = 2710, 51.6%). These symptoms were also the least identified symptoms in both the Gaza Strip and the WBJ.

On the multivariable analysis, women who had benefitted from post-secondary education were more likely to identify all breast symptoms (Table 5). Additionally, women recruited from hospitals or primary healthcare centers were more likely than women recruited from public spaces to recognize three out of the four breast symptoms. In contrast, women residing in the WBJ were less likely than women residing in the Gaza Strip to recognize three out of the four breast symptoms.

Women aged ≥ 40 years were more likely than younger women (18–39 years) to recognize ‘puckering or dimpling of the breast skin’ (OR = 1.52, 95% CI: 1.32–1.76) and ‘redness of the breast skin’ (OR = 1.47, 95% CI: 1.27–1.69). However, women aged ≥ 40 years were less likely to recognize ‘pain in one of the breasts or armpits’ (OR = 0.80, 95% CI: 0.69–0.92).

Women residing in the WBJ were less likely than women residing in the Gaza Strip to recognize all nipple symptoms (Table 6). On the contrary, women recruited from hospitals or primary healthcare centers were more likely than women recruited from public spaces to recognize all nipple symptoms. Additionally, women aged ≥ 40 years had a higher likelihood than younger women (18–39 years) to recognize all nipple symptoms.

Women residing in the WBJ were less likely than women residing in the Gaza Strip to recognize all other BC symptoms except ‘unexplained weight loss’ for which no difference was noticed (Table 7). In contrast, women recruited from hospitals and those with post-secondary education were more likely to recognize all other BC symptoms.

The low to moderate awareness of BC symptoms in this study is similar to the findings of Al-Mousa and colleagues among Jordanian women with 44.0% displaying good knowledge of BC symptoms [39]. Hassan and colleagues showed lower knowledge of BC in Egypt with 33.2% demonstrating good knowledge [40]. Other previous studies from non-Arab countries including China, Turkey, Nigeria, and Singapore also showed inadequate awareness of BC symptoms [29, 41‐43]. A study conducted in Lebanon found a higher awareness of BC symptoms than of BC treatment options and curability. The authors explained that could be due to the focus of public campaigns on the detection of BC through its symptoms not the potential to cure BC [44]. Negative beliefs and worry about a potential BC diagnosis were also found to be barriers to early diagnosis in other studies [11, 20, 45] Future educational interventions should focus more on clarifying the link between the recognition of BC symptoms and early diagnosis leading to higher chances of curability [20]. In concordance with this study, previous studies found that women recognized breast symptoms, especially those with lump, more often than nipple symptoms [12, 46‐48]. In fact, patients with non-lump symptoms were more likely to delay their medical visit [12]. This necessitates that the nature of BC symptoms should be included in the design of educational interventions aiming to raise the awareness of BC symptoms.

In comparison with another study looking at the awareness of cervical and ovarian cancer warning signs and symptoms among Palestinian women, good BC symptoms awareness in this study is relatively higher (41.7% vs. 27.4% and 17.4%, respectively) [21, 23]. This could be due to local awareness campaigns focusing on BC rather than other cancers. Quintanilha and colleagues demonstrated the efficiency of the ‘Pink October’ in increasing the interest of the Brazilian population in searching the internet about BC awareness [49]. Another contributing factor for the better awareness of BC symptoms could be the greater incidence of BC than other cancers, which may lead to higher chances that women could know someone with BC [1]. This may drive women to read more about BC.

In line with this study, previous studies showed that higher education was associated with higher awareness of BC symptoms [29, 43, 48, 50‐53]. This suggests that targeting women with curricula discussing health-related topics such as BC could be an effective strategy to raise their awareness [11]. In addition, similar to this study, a study conducted in Kuwait found that participants who knew someone diagnosed with cancer were more likely to recognize BC symptoms [54]. Knowing someone with cancer might make women feel more worried about having it themselves. This feeling may encourage women to search and ask about the BC symptoms, which will be reflected as a higher level of awareness about BC symptoms [21]. Further research is needed to explore the emotional and practical driving forces of women to learn more about BC symptoms and what sources they use to enrich their knowledge.

In this study, older women were more likely to have good awareness of BC symptoms. Older women have usually been more frequently exposed to healthcare professionals than younger women for maternity care as well as sexual and reproductive health purposes than younger women.

Such visits may help older women to accumulate more information about health-related topics including BC symptoms [21‐24]. To further investigate this, a sensitivity analysis was performed among married, divorced, or widowed women and found no association between parity and displaying good awareness of BC symptoms (supplementary table 1). However, the finding that women recruited from hospitals or primary healthcare centers were more likely to have good awareness of BC symptoms (both in the main and sensitivity analyses) indicates that the exposure to healthcare professionals and other sources of information in healthcare facilities seems to play a role in shaping women’s health literacy. Governmental hospitals and primary healthcare centers can be attended free of charge by anyone with public health insurance or at very low cost by those who do not choose to pay for the publicly available low-cost health insurance. Therefore, a broad section of the Palestinian population can be met at governmental hospitals and primary healthcare centers. Women recruited from hospitals or primary healthcare centers display health-seeking behavior by their attendance of healthcare facilities. This might reflect an interest in their health and a greater general awareness of issues around health when compared to the group of women recruited from public spaces [11]. Therefore, both, more chances to have benefitted from education by healthcare professionals as well as their own health-seeking behavior, might have provided older women and those women visiting healthcare facilities with more opportunities to enhance their awareness of BC symptoms. Thus, exposure to health education and information appears to increase BC awareness and might be an important factor to improve early detection of BC and, hence, outcomes for women suffering from BC [32‐34].

Women from the Gaza Strip were more likely than women from the WBJ to recognize BC symptoms. This could be explained by the lower exposure of women residing in the WBJ to healthcare professionals, therefore, they had lower chances to promote their health literacy [21]. The WBJ has checkpoints and restrictions on the internal movement, even between cities, leading to longer hours of delay to reach healthcare facilities accompanied with the fear and anxiety to come across checkpoints and settlements [55]. In addition, the WBJ has a wider geographical variation than the Gaza Strip and more women are living in rural areas in the WBJ than the Gaza Strip limiting their access to healthcare centers [56].

The results of this study highlight the substantial need to create sustainable educational interventions to raise Palestinian women’s awareness about BC symptoms. These interventions should adopt different strategies that aim to maximize the outreach especially to women living in underserved areas. This could be facilitated by running health education activities in coordination with the mobile healthcare clinics of the Palestinian Ministry of Health that are distributed across the WBJ [57]. Education programs should include the less known BC symptoms beyond the breast lump as well as the more positive outlook on prognosis with an early diagnosis in order to improve impact.

Involving healthcare professionals in these activities should also be considered [37]. This will necessitate training Palestinian healthcare professionals on how to deliver information about health topics, including BC, in a way that is appropriate to the health literacy of the public. In addition, a special training could be implemented to improve the communication skills of Palestinian healthcare professionals so that women would have more confidence to talk about their concerns if they recognized any possible BC symptoms. The diagnosis of BC could be stressful for women and training healthcare professionals on how to handle such situations could help reduce women’s stress especially that BC patients may rely on oncologists for their diagnosis-related emotional and social issues [58].

The major strengths of this study include the use of a translated version of the validated tool (BCAM) to assess women’s awareness of BC symptoms and the high response rate. In addition, the large sample size covering most geographical areas of Palestine may have generated the diversity of the Palestinian community in the study cohort. This study also has some limitations. The use of the convenience sampling may potentially limit the generalizability of the findings. However, the large number of study participants, the high response rate, and the diversity of geographical areas covered may mitigate this limitation. For example, the lower monthly income among women from the Gaza Strip than that of women from the WBJ mirrored the difference in the unemployment rates that are higher in the Gaza Strip than in the WBJ (47% vs. 16%) [27]. Moreover, the sociodemographics of the women included in this study were close to the demographics reported by other studies conducted in Palestine to assess awareness of various cancers [21‐24]. Another limitation could be that the study included participants who did not experience actual BC symptoms and looked at their perceived knowledge. Finally, the recognition of BC symptoms was assessed while it might have been helpful to assess the recall of these symptoms as well.