Epidemiological, Clinical, and Pathological Characteristics of Invasive Breast Cancer in Bedouin and Jewish Women in southern Israel: A Retrospective Comparative Study

doi:10.21203/rs.3.rs-2820426/v1

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Epidemiological, Clinical, and Pathological Characteristics of Invasive Breast Cancer in Bedouin and Jewish Women in southern Israel: A Retrospective Comparative Study

https://doi.org/10.21203/rs.3.rs-2820426/v1

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Background: Invasive Breast Cancer (IBC) is a leading cause of cancer-related death among women in Israel, regardless of ethnicity. This study compared IBC epidemiological, clinical, and pathological characteristics in Bedouin and Jewish patients in southern Israel.

Methods: Medical records of 1514 Jewish and 191 Bedouin women with IBC treated at Soroka Medical Center between 2014-2021 were analyzed retrospectively. Baseline measures and tumor characteristics were compared between groups. Overall survival (OS) was analyzed using log-rank test. Multivariate analysis was performed using Cox proportional hazard model.

Results: Bedouins were diagnosed at a significantly younger age (median 48vs62 years, p<0.001), had a significantly larger tumor (median 2.5vs2.13cm, p<0.001), and significantly higher rate of metastasis (18.8%vs12.7%, p = 0.03). Interestingly, Bedouins had a lower death rate compared to Jews (20%vs30.9%, p = 0.029), but median OS showed no difference between groups. When comparing treatment options, both surgery (124.5vs29.6months, p<0.001) and radiation therapy were associated with better OS (109.5vs59.6months, p<0.001), while chemotherapy was associated with worse OS (95.5vs109.5months, p=0.001). In a multivariate analysis, Surgery and radiation therapy remained significant, while age, tumor size, triple negative status, and metastasis were associated with worse OS.

Discussion: Despite a previous study showing worse OS for Bedouins than Jewish patients, we did not find a similar trend. This is likely due to improved cancer screening and prevention in Bedouin patients as a direct result of increased number of community clinics in Bedouin settlements. Moreover, Bedouins' access to healthcare improved as their lifestyle transformed from semi-nomadic to more modernized.

Breast Neoplasm

Bedouin

Mortality

Prevention

Invasive Breast Cancer (IBC) is the most frequently diagnosed cancer in women in North America, Australia, Northern and Western Europe, and Israel. Moreover, it is second among the causes of cancer-related deaths in women regardless of ethnic origin [1–3]. In Israel, age-adjusted IBC incidence rates vary among different ethnic groups and are known to be highest among Jewish women of European origin, lower among Jewish women of North African and Asian origin, and lowest among Arab women [4].

The Bedouins are part of the Israeli-Arab population and reside in the Negev, a desert in southern Israel. The Bedouin population accounts for approximately 22% of the 1.3 million population of the Negev, while most Israeli Arabs living in the Negev are Bedouins. They accounted for approximately 4% of the population of Israel in 2021[5].

IBC accounted for about a third of all invasive tumors in women in Israel according to 2018 data:33% among Jewish and others and 35% among Arab women, with a total of 4,235 Jewish women (90% of patients) and 507 Arab women (10% of patients) diagnosed that year. The population distribution in 2018 was 79% Jewish and other and 21% Arab; however, the age-adjusted incidence rates per 100,000 of IBC were 88.7 in Jewish and others and 69.5 in Arab women. Moreover, observation of the incidence of IBC in Israeli Arabs during 1996–2017 showed an annual increase of 1.7% compared to a decrease of 0.7% in Jewish women each year [6]. A study published in 2014 examined the epidemiology of IBC in Bedouin and Jewish women. The study found that Bedouin women have a worse prognosis compared with Jewish women[1].

Bedouin women in Israel face many barriers to healthcare access, including socio-cultural factors such as gender inequality and marginalization within their community and practical barriers such as a lack of transportation and difficulty communicating with healthcare providers [7, 8]. However, recent studies indicate that the accessibility of healthcare for Bedouin women has improved due to linguistic adaptation of the healthcare system and the increased availability of early cancer diagnosis and treatment in Bedouin settlements and adjacent regions [9, 10]. Moreover, recent publications have shown that the Bedouin population has experienced a marked shift from a semi-nomadic, traditional lifestyle to a more sedentary and urbanized one[11]. Nevertheless, tribal endogamy and intra-familial consanguinity are strongly favored among Bedouins [12, 13]. Therefore, numerous hereditary disorders are common in the Bedouin population of the Negev[8] making the Bedouin population highly interesting for studying IBC.

The following study examined the epidemiology of IBC among Jewish and Bedouin women. Since prior studies assessed similar cancer characteristics among the Jewish and Bedouin population [1, 10], we aimed to assess the most current data available on the epidemiology of IBC among Jewish and Bedouin women treated at Soroka medical center. We hypothesized that due to the significant investments of healthcare funds in the southern of Israel[14, 15] and the transition of the Bedouin population to a more urbanized lifestyle[16], the prognosis of IBC among Bedouin women would be better than described in the past[1].

Eligibility Criteria

The data in this study were retrospectively collected from Soroka University Medical Center’s (SUMC) electronical medical record system. We included records from breast cancer patients treated at the hospital between 2014 to 2021. The data collection was performed by manual surveillance of patient’s computerized files. We gathered information on patient demographics, baseline tumor characteristics, treatment modality and survival outcome. Specifically for survival analysis, we included follow-up duration, tumor recurrence, and survival time. This study was approved by SUMC institutional Helsinki board.

Statistical Analysis

All statistical analysis from this study was done with RStudio 3.3.0+. Descriptive statistics presented demographic and clinical parameters. Continuous variables such as age and tumor size were summarized using mean and standard deviation. Categorical variables were summarized using percentages. Wilcox rank test was used to compare continuous variables (i.e., age and tumor size) between groups. Fisher’s exact test was used to compare frequency of categorical variables (i.e., recurrence and death rate) between groups. Overall survival (OS) was defined as the time from diagnosis to the time of death from any cause. Log rank test was used to compare Kaplan-Meier OS curve between groups. Statistically significant variables in the univariate analyses were included along with ethnicity in the multivariate Cox’s analyses. All statistical tests were two-sided, and statistical significance was defined at a level p less than 0.05.

A total of 1705 patients were retrospectively analyzed in this study, including 191 Bedouin patients and 1514 Jewish patients. Table 1 summarizes the baseline demographic and tumor characteristics between these two groups. Bedouin patients were significantly younger at the age of diagnosis compared to Jewish patients (49.6 vs 60.8 years, p < 0.001, Figure S1A). Bedouin patients also had a significantly larger tumor size (2.5 vs 2.13 cm, p < 0.001, Figure S1B), significantly more lymph nodes involvement (node positive 49.8% vs 38.4%, p < 0.001), and significantly more distal metastasis (18.8% vs 12.7%, p = 0.03). Interestingly, Bedouin patients had a significantly higher rate of solely PR positive tumors compared to Jewish patients (77% vs 69.9%, p = 0.02).

Table 1. Baseline patient demographics and tumor characteristics. SD, standard deviation; IDC, intraductal carcinoma; ILC, intralobular carcinoma; ER, estrogen receptor; PR, progesterone receptor; Her 2, human epidermal growth factor receptor 2.

Patient and Tumor Characteristics	All N = 1705	Jews N = 1514	Bedouin N = 191	p value
Age, yrs, mean (SD)	59.5 (14.6)	60.8 (14.3)	49.6 (13.8)	< 0.001
Tumor type, n (%) IDC ILC Others	1489 (87.3%) 149 (8.8 %) 67 (3.9%)	1322 (87.3%) 136 (9%) 56 (3.7%)	167 (87.4%) 13 (6.8%) 11 (5.8%)	0.26
ER positive, n (%)	1375 (80.6%)	1221 (80.6%)	154 (80.6%)	1
PR positive, n (%)	1205 (70.7%)	1058 (69.9%)	147 (77%)	0.04
HER 2 positive, n (%)	367 (21.5%)	317 (20.9%)	50 (26.2%)	0.11
Triple Negative	175 (10.3%)	161 (10.6%)	14 (7.3%)	0.17
Tumor Stage, n (%) T1 T2 T3 T4	865 (52.3%) 486 (29.4%) 74 (4.5%) 228 (13.8%)	769 (52%) 433 (30%) 72 (6%) 193 (12%)	96 (51%) 53 (29%) 2 (1%) 35 (19%)	0.02
Tumor Size (cm)	2.17 (1.51)	2.13 (1.49)	2.50 (1.60)	< 0.001
N Stage, n (%) 0 1-3 >3	193 (91.5%) 17 (8.1%) 1 (0.5%)	836 (55.2%) 581 (38.4%) 0 (0%)	85 (44.5%) 92 (48.2%) 3 (1.6%)	< 0.001
Metastasis	229 (13.4%)	193 (12.7%)	36 (18.8%)	0.03

Next, Table 2 summarizes treatment modality and prognostic outcomes. The median follow-up period for the whole cohort was 55.1 months. The median follow-up time was similar between the two groups (Bedouin 57.5 months vs Jewish 54.8 months, p = 0.11). Bedouin patients had a higher rate of receiving chemotherapy and neoadjuvant therapy than Jewish patients (62.8% vs 42.8%, p < 0.001; 49.7% vs 22.9% p < 0.001, respectively). However, there was no difference in the proportion that undergone surgery, radiotherapy, or hormonal therapy. Interestingly, Bedouin patients had a slightly higher cancer recurrence rate (20.4% vs 16%, p = 0.12) but lower death rate (20% vs 30.9%, p = 0.029) than Jewish patients.

Table 2

Treatment modality and prognostic outcome between Jew and Bedouin patients. SD, standard deviation.
	All N = 1705	Jews N = 1514	Bedouin N = 191	p value
Median follow-up, months (SD)	55.1 (34)	54.8 (34.5)	57.5 (30.3)	0.11
Surgery, n (%)	1462 (85.7%)	1296 (85.6%)	166 (86.9%)	0.74
Chemo, n (%)	768 (45%)	648 (42.8%)	120 (62.8%)	< 0.001
Neoadjuvant, n (%)	442 (25.9%)	347 (22.9%)	95 (49.7%)	< 0.001
Radiotherapy, n (%)	1240 (72.7%)	1089 (71.9%)	151 (79.1%)	0.056
Hormonal, n (%)	1245 (73%)	1101 (72.7%)	144 (75.4%)	0.49
Recurrence, n (%)	281 (16.5%)	242 (16%)	39 (20.4%)	0.12
Death, n (%)	512 (30.9%)	468 (30.9%)	44 (20%)	0.029

Furthermore, there was no difference in OS between Jewish and Bedouin patients (109 vs. 119 months, p = 0.08, Fig. 1). The 5-year survival rate was 80% in Bedouin patients compared to 74.5% in Jewish patients. While surgery and radiotherapy were associated with better OS (surgery 124.5 vs. 29.6 months, p < 0.001, Fig. 2A; radiotherapy 109.5 vs. 59.7 months, p < 0.001, Fig. 2B), chemotherapy was associated with worse OS (95.9 vs. 109.5 months, p < 0.001, Fig. 2C) and neoadjuvant therapy was not associated with OS (110 vs 110 months, p = 0.28, Fig. 2D). Importantly, patients with a triple-negative tumor or distant metastasis had reduced OS compared to those with other tumor markers (triple negative OS 124 vs 110 months, p < 0.001, survival curved crossed around 110 months, Figure S2A; metastasis OS 42.2 vs. 126.8 months, p < 0.001, Figure S2B). Additionally, advanced age (greater than 70 years) at diagnosis was associated with worse OS (Figure S3). OS was similar in Bedouin and Jews for patients less than 70 years old but in the group older than 70 years Bedouins had worse OS (Figure S4). Lastly, in a multivariate model that included patients’ demographics, treatment modality, and tumor characteristics, surgery and radiotherapy were associated with better OS while age at diagnosis, tumor size, triple negative status, and distal metastasis were associated with worse OS (Fig. 3).

In the present study, we examined the epidemiology of breast cancer among Jewish and Bedouin women based on data from SUMC between 2014–2021. Our study found an interesting pattern of IBC in Bedouin women, that is significantly different from IBC among the Jewish population. While the incidence is higher among the Jewish population, Bedouin women diagnosed with IBC presented at a younger age with a larger tumor, a more advanced stage, and more metastases. A greater incidence of PR was observed in Bedouin women but not for ER and HER2 subtypes. The mortality rates were higher among Jewish women, while no significant differences in OS and DFS were found.

First, our study showed a significant difference in the age at diagnosis. Bedouin women’s mean age at diagnosis was 11 years younger than Jewish patients. Previous studies in Israel, Saudi Arabia, United Arab Emirates, and others have shown a similar young onset, around age 50, among Arab-origin women [17–19]. Possible reasons for this finding may be due to differences in disease biology between the two populations, rapid growth of the younger Bedouin population, and potential under-diagnosis or incomplete registration of IBC in the elderly, leading to the under-representation of IBC cases in this group. Health policy is equal for both populations, as they are entitled to the same health services under Israeli National Health Insurance Law[20]. Additionally, Israel's Central Bureau of Statistics reports no difference in mammography screening adherence between Jewish and Bedouin women since 2011 [21]. Previous studies have highlighted challenges in accessing healthcare for the Bedouin population due to transportation, language, and socio-cultural barriers[22, 23]. However, under-diagnosis or lack of registration is difficult to determine as healthcare accessibility has improved with linguistic adaptation of the healthcare system and increased availability of early cancer diagnosis and treatment in Bedouin settlements and surrounding areas.[9, 10].

Second, we found that Bedouin women are diagnosed at a more advanced stage than Jewish women. As described, the Bedouin population is a minority group in Israel that counts for approximately 4% of the population. Previous works showed a similar trend in the Bedouin population[1] and in different minority groups [24, 25]. Biologic and minority characteristics might explain such differences. The observed overexpression of PR in the Bedouin population's biology could provide a supporting factor for the disparity in the diagnosis stage. While studies did not find a connection between PR overexpression as a single risk factor for worse prognosis [26] and wide-genome analysis of PR have shown minor variable genes in ER- and ER + tumors[27], others found aggressive phenotypes that were associated with poor prognosis[28]. Since the SUMC labs did not analyze data for subtypes of PR receptors, we could not recheck it. Nevertheless, multiple studies still question the need for PR analysis since its minor effect as a single predictor on stage at diagnosis [29, 30]. Hence, further evaluation might be needed to determine whether other biological factors might explain this difference. As described, although the Bedouin population is a minority group experiencing challenges accessing health services, the screening programs didn’t show any difference in adherence and accessibility for IBC screening since 2011, making it a less plausible explanation.

Third, we found that more Bedouin women were treated with neoadjuvant and chemotherapy treatments than Jewish women. In contrast, no difference was found in surgery and radiation between the groups. The rates of disease stage at diagnosis can explain this difference. While in both groups, the rate of those diagnosed in Stages 1 and 2 was similar (82% Jewish women and 80% Bedouin women), a significant difference was found in Stages 3 and 4; 19% of Bedouin women were diagnosed at Stage 4 in the Bedouin group, only 12% were diagnosed at this stage in the Jewish group. Previous studies found similar treatment trends, while staging was dramatically different. Based on data from 2004–2012, Lazarev et al showed that 62% of Bedouin and 64% of Jewish women were diagnosed with stages 1 and 2. Bedouin women had a higher percentage of stage 3 diagnoses (39% vs. 19% for Jewish women), and a higher percentage of stage 4 diagnosis (8% vs. 7% for Jewish women) [1]. The main goals in treating nonmetastatic breast cancer are eliminating the tumor and preventing recurrence. Local therapy involves surgery and possibly radiation, while systemic treatment depends on the tumor subtype. Endocrine therapy is prescribed for all tumors with hormone receptor positivity (HR+), while HER2 + tumors receive trastuzumab-based antibody therapy and chemotherapy. Triple-negative breast cancer is treated with chemotherapy alone.[31, 32]. As described, no difference between groups regarding triple negative and HER2 + was found, so it is reasonable to assume there was no difference among groups based on this tumor characteristic. In metastatic breast cancer, therapy goals are to extend the life and alleviate symptoms. Hence, surgery and radiation are considered only in palliative settings. In most cases, the first line of therapy will be more radical, using chemotherapy and other treatments based on specific tumor characteristics[31, 32].

We did not find a significant association between ethnicity and OS nor for DFS. Furthermore, in the Bedouin stage 4 group, the OS was better than the Jewish stage 4 group, while age-sub analysis of OS did not differ. Lazarev et al has previously shown that Bedouin women had worse OS and DFS rates than Jewish women[1]. The possible differences between the past study and ours, in the context of OS and DFS, could be explained by the improvement in primary, secondary, and tertiary prevention of IBC[9, 33, 34]. Over the past decade, primary prevention efforts to raise awareness about the importance of Oncologic, and particularly IBC, screening have been successful in the Israeli population by implementing multilingual educational campaigns via television, newsletters, and other media outlets in Hebrew, Arab, Russian, English, and French languages[14, 35]. Moreover, a report published by the Israel Center for Disease Control, in 2008 described 51 women's and primary care clinics in the Bedouin community, which comprised at the time of approximately 184,000 residents[36, 37].

In addition, according to the 2013 State Comptroller's Report, the oncology department at Soroka had only 22 beds in 2012, responsible for more than a million residents, and was almost closed due to a lack of staff. However, the report stated that a governmental program to grant better access to healthcare in the southern periphery had been established and funded [38]. This historical lack of access to healthcare facilities and the cultural difference could have contributed to the lower survival rate in previous studies. A study examining a similar difference in the epidemiology of Colorectal Cancer between the Jewish and Bedouin populations on data from 1997–2013 showed a low response in the Bedouin population to screening tests and worse OS compared to the Jewish population [10]. It has been established that secondary prevention, leading to early diagnosis of breast cancer, is a crucial strategy for preventing its progression[9]. This is particularly important for populations that have limited access to healthcare facilities. In the case of Bedouin women in Israel, a report published by the Israeli government revealed that from 2008 to 2020, there was a rise of approximately 150% in the number of clinics operating in the Bedouin settlements. The report showed that over 70 clinics serving the Bedouin population, which at the time of the report consisted of approximately 270,000 residents [15]. To further improve access to IBC screenings, multiple interventions, such as a mobile mammography unit, started operating in the Israeli periphery in 2006. It aimed to increase adherence among women living in geographically and socially peripheral areas. Due to increased demand, another mobile unit was funded in 2011, making mammography examinations more accessible, causing a steady increase in compliance rates for IBC screenings among Bedouin women [14]. Previous works have shown that early treatment is crucial for improving the survival rate of breast cancer patients [38]. This highlights the importance of having access to healthcare facilities, particularly those with oncology departments, close to one's home to maintain tertiary prevention. In this context, opening the SUMC cancer center in 2018 might have significantly impacted the Bedouin population. It provides better access to oncologic and multidisciplinary care, including cancer screenings, diagnostic tests, and treatment options. SUMC cancer center allows patients to receive comprehensive care in one location rather than traveling long distances for different aspects of their treatment. This improves the patient's experience, prognosis, and quality of life[9]. In the study by Lazarev et al., the sample size was 265. However, we had a larger sample size (n = 1705), and no significant differences in OS and DFS were found between Bedouin and Jewish IBC patients. This discrepancy might reflect a non-accurate effect described. However, it is unlikely that Lazarev et al. work did not represent the larger population due to similar trends in other oncologic fields and the very significant p-value found.

While studying the epidemiology of breast cancer in Jewish and Bedouin women, we should consider the significant societal changes the Bedouin community are undergoing. Traditionally, Bedouin society has been a semi-tribal, isolated minority emphasizing family, community, and cultural and traditional beliefs [38,39]. However, in recent times, Bedouin society is becoming more modern and urbanized, driven by improved access to education and employment, modern technology, media exposure, and urbanization [11].

Limitations:

Our study is a single-site retrospective cohort study that may have limitations due to its time frame for patient selection. However, the large sample size and similarities in screening characteristics between papulations suggest that the trends found in this study may hold in the future. It is well-established that multiple factors influence breast cancer, including genetics, reproductive factors, and lifestyle [9]. Limitations in the data gathered on factors such as parity, BMI, diabetes, and family history of IBC, prevented us from comparing the prevalence of these factors and may have led to a confounding bias. Moreover, the lack of data regarding the Ki-67 marker precluded the ability to analyze luminal A and B IBC subtypes. Despite not finding differences in OS and DFS, it is essential to note that other factors, such as age and stage of diagnosis, do differ. Therefore, it is crucial to continue researching the epidemiology of breast cancer in Jewish and Bedouin women to better understand the differences and similarities. Furthermore, since a similar difference of prognosis was seen in the Bedouin population in other oncological diseases, such as colorectal cancer[10], it is worthwhile to examine whether intervention prevention programs showed a similar trend in other diseases and other populations.

IBC in Bedouin women in southern Israel, is characterized by a lower incidence, a younger age at diagnosis, larger tumors, and a more advanced stage at diagnosis then Jewish women. A similar tendency of IBC recurrence and survival rates was observed. Further research with a more extensive database and exploration of molecular indicators of cancer for the two populations is needed to better understand the difference in IBC between Bedouin and Jewish women.

Ethics approval and consent to participate

The study was approved and informed consent was waived by the Ethical Review Board in Soroka University Medical Center (approval number: 0008-22 SOR). The research was performed in accordance with the Declaration of Helsinki and all methods were carried out in accordance with relevant guidelines and regulations.

Consent for publication

Not applicable

Availability of data and materials
The datasets generated and analyzed during the current study are not publicly available because we intend to use the database for future studies and analysis. However, the datasets are available from the corresponding author on reasonable request.

Competing interests

The authors of this paper report no competing interests.

Funding

No additional funding.

Authors' contributions
I.B.S- Writing – Conceptualization, Methodology, Investigation, Writing - original draft

A.W – Conceptualization, Formal Analysis, Writing – original draft

K.I– Investigation, Writing – review & editing

R.A- Resources

S.A.F – Investigation

J.V - Project administration, Supervision

Acknowledgements

Not applicable

Authors' information

Soroka University Medical Center, Faculty of Health Sciences, Ben-Gurion University of the Negev, Beer- Sheva, Israel.

Itamar Ben Shitrit, Ao Wang, Karny Ilan, Ravit Agassi, Safian abu Frech, Julie Vaynshtein

Clinical Research Center, Soroka University Medical Center, Faculty of Health Sciences, Ben-Gurion University of the Negev, Beer-Sheva, Israel

Itamar Ben Shitrit

Corresponding author to: [email protected] (I. Ben Shitrit)

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No competing interests reported.

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Epidemiological, Clinical, and Pathological Characteristics of Invasive Breast Cancer in Bedouin and Jewish Women in southern Israel: A Retrospective Comparative Study

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