Breast Cancer Screening and Socio-Demographic Factors in Kuwait: A Nationwide Study, 2014−2019

Abstract

Background: Breast cancer (BC) incidence is increasing worldwide, including in Kuwait, which established a national BC screening program in 2014. This study examines overall BC screening uptake in Kuwait and its variation by socio-demographic characteristics. Material and methods: We conducted a cross-sectional study using 2014−2019 BC screening records from the Kuwait National Mammography Screening Program (KNMSP) and population data of the target female population (age 40−69). Ever-screened uptakes were calculated separately for Kuwaitis and non-Kuwaitis. The six regions were grouped into high and low population density, indirectly reflecting accessibility to screening centers. A complete-case approach was used for the analyses by socio-demographics characteristics. Screening and population counts were modeled using a generalized linear model with a negative binomial distribution, stratified by population density. Results: The BC ever-screened uptake remained very low, at 1.6% and 0.05% among Kuwaiti and non-Kuwaiti women, respectively. The complete-case analysis (using 88% of records) did not reveal strong variations by socio-demographic characteristics. Uptake was highest (3.4%) among Kuwaitis living in high-density regions, aged 40−49, ever married and with the highest education. In the same regions, this uptake decreased to 0.4% in Kuwaiti women aged 60−69, single and with the lowest education. Uptakes were even lower in low-density regions or non-Kuwaitis. Including mammogram tests performed outside the KNMSP had little impact on the overall findings.Discussion: Although socio-demographic and geographic factors were associated with differences in BC screening uptake, the proportion of screened women remained overall too low to have any public health impact at population level. This suggests that barriers extend beyond socio-demographic factors and may involve program awareness and accessibility.Conclusion: Major changes are needed in the KNMSP to reduce the burden of BC in Kuwait. Targeted interventions addressing awareness, accessibility, and cultural barriers are necessary to improve early detection and reduce BC mortality.

Graphical abstract

Keywords

breast cancer / mass screening / socio-demographic factors / women / Gulf Cooperation Council countries / Kuwait / generalized linear model

Introduction

In 2020, female breast cancer (BC) was the cancer with the highest incidence, with more than two million new cases estimated (12% of all cases) worldwide, and the third leading cause of cancer death (7% of all cancer mortality)[1]. Even if BC incidence is increasing worldwide, rates remain three to ten times lower in Gulf Cooperation Council (GCC) Countries (i.e., Saudi Arabia, Kuwait, Bahrain, Qatar, UAE, and Oman) than in the West (e.g., USA, Australia, and the UK)[1–3]. However, both incidence and mortality of female BC are projected to roughly double in these countries between 2020 and 2040, up to over 13,000 new cases and 4,000 deaths per year, respectively[4]. In Kuwait, similar patterns and increases are projected, up to 1,600 new cases and over 700 deaths in 2040[4].

Mammography screening (MS) is a key component in the BC control strategy, early detection of BC enabling more effective treatment[2,5,6] and ultimately reducing morbidity and mortality from BC[7,8]. BC screening strategies vary amongst countries, from systematic invitation sent to every women identified within the target population for screening at each round, up to more opportunistic approach which depends on women’s decision to attend or clinicians’ decision to refer[9]. Nationwide screening programs usually use the invitation approach,[10] as in some European countries (e.g., Denmark, Finland, and the Netherlands) where BC screening uptake are above 80%[2,5,9,11]. In contrast, countries (e.g., South Korea and Japan) with more opportunistic screening strategy tend to have lower screening uptakes, below 60%[12–15]. Similarly, most GCC countries follow an opportunistic BC screening with an uptake ranging from 4.9% to 13.9%[16,17]. Kuwait National Mammography Screening Program (KNMSP) was rolled out nationwide in April 2014[18–21]. The KNMSP apply the international guidelines of the American College of Radiology (ACR) to detect BC at its early stages and to reduce the harm associated with screening by providing high-quality mammography[18,19,22]. The program passively invites (via mass media and social networks) all women aged 40−69 for screening annually at one of its five accredited BC screening centers[18,22,23]. In 2016, the first KNMSP report provided an estimated general attendance rate for BC screening in Kuwait at 4.2% among eligible Kuwaiti women[23].

Kuwait is a small (less than 20,000 km²) high-income country (HIC) of nearly 4.5 million people, of which roughly one third are Kuwaiti (nearly 1.5 million) and two thirds are non-Kuwaiti (nearly 3 million)[24]. The country has a population distributed across six governorates of vastly different sizes and populations, with almost 60% living in the area surrounding the capital[25]. The health system has national coverage and is fully funded by the Kuwaiti government: it provides services free of charge for Kuwaiti citizens, while non-Kuwaiti pay subsidized fees. KNMSP provides screening mammography free of charge for Kuwaiti women only. Non-Kuwaiti women can access screening mammography in the Ministry of Health (MoH) hospital network for a fee (50−105 GBP).

Population density is often used in epidemiological and health studies as a surrogate variable to assess the provision of and accessibility to healthcare as well as population characteristics[26,27]. Population density can be used here as a contextual factor to understand barriers and facilitators to BC screening access[26,28]. Additionally, population density can help identify areas where interventions are needed most, such as targeting resources for increasing BC screening uptake in underserved areas with high population density. However, other factors, such as socioeconomic status (SES), cultural beliefs and attitudes towards screening, and availability of transportation, should also be considered when estimating the proportion of BC screening uptake[26–28]. Furthermore, several factors influence screening uptake in GCC countries: inadequate knowledge of BC risk and screening practice, stigma and fatalistic beliefs, and social determinants of health, such as SES associated with educational level, and marital status, are linked with variable awareness and effective promotion of BC screening[2,3,17,29–31]. Therefore, a comprehensive approach incorporating multiple variables is necessary to accurately estimate the BC screening uptake and develop effective interventions to improve screening rates[26].

The aim of this study was to estimate the BC ever-screened uptake proportion in Kuwait between 2014 and 2019, as well as examine the association between women’s screening status, which considered as the dependent variable, and their socio-demographic characteristics.

Materials and methods

Data

To estimate the proportion of females undergoing screening uptake, individual-level data were aggregated from KNMSP registry and compared to the female general population data, stratifying both datasets by common socio-demographic factors such as age, nationality, marital status, educational level, and region for the period 2014−2019. The screening and general population datasets were extracted electronically from the KNMSP registry of Kuwait MoH and Public Authority for Civil Information (PACI), respectively. PACI is a databank known to be the most reliable source responsible for providing and maintaining civil information for citizens and residents of Kuwait, including Bedoon (i.e., without nationality). It runs as a Kuwaiti government agency. We restricted data extraction and linkage to women eligible for BC screening, i.e. aged 40 to 69. For each calendar year (2014−2019), socio-demographic information common to both datasets and of interest for this research were extracted and grouped as follows: three age categories (40−49, 50−59, and 60−69), education (illiterate or/and read and write, primary and/or secondary, high school and/or diploma, and bachelor and/or postgraduate), and marital status (single vs. ever-married which included widow or married). We created two variables of interest: population density (defined as the number of resident per km²) from governorate of residence by grouping into low population density < 1,000 individuals/km² (Al-Ahmadi and Al-Jahra) vs. high population density > 1,000 individuals/km² (Capital, Hawalli, Al-Farwaniya, and Mubarak Al-Kabeer), and nationality (Kuwaiti vs. non-Kuwaiti including Bedoon). This classification is based on the concentration of the five national screening centers within urban hubs, hence the use of density as a surrogate for geographic accessibility.

KNMSP includes all women who had ever participated in (planned or opportunistic) BC screening. Estimates of the Kuwait population are annually updated. The data in this study were accessed and collected during the period from July 2021 to June 2022.

The data flowchart is detailed in Figure 1. Briefly, 935,573 women, eligible for BC screening in Kuwait between 2014 and 2019 because of their age, were used to calculate the overall BC screening uptake. After exclusion due to missing socio-demographic information, 830,454 (89%) women eligible for BC screening were included in the more detailed analysis. The KNMSP identified 22,429 records of BC screening in women eligible for BC screening, of which 50 were excluded because of missing sociodemographic information.

As BC screening is recommended every year in Kuwait, women can be screened several times during the study period. We used a unique identification code (UIC) provided by KNMSP to identify any women who had repeated MS during the study period (N = 23,120) and remove duplicated UIC records (n = 7,076). Overall, 15,303 women were screening at least once between 2014 and 2019 (ever-screened women).

Observations with missing information excluded for the analysis represented less than 1% of the data, except for the variable reporting level of education (8.2% in the population data; Figure 1).

Statistical analysis

The individual BC screening data were grouped to match the population count data defined by calendar year, age, education, marital status, governorate, and nationality.

The ever-screened proportions were estimated using the number of screening participants (excluding second and subsequent screening records) divided by the whole population. Further analyses by socio-demographic factor and year were based on a complete-case approach. The population counts were assumed to be full person-years, except in 2014 where we accounted for the fact that BC screening started only in April 2014. We modelled ever-screened counts using a generalized linear model (GLM) with a negative binomial distribution to account for the overdispersion of the observed ever-screened counts, instead of the more conventional Poisson distribution[32]. The population counts being used to weight the ever-screened counts in order to derive the ever-screened proportions according to socio-demographic characteristics. The denominators for these proportions were constructed based on annual person-years of the target female population (ages 40−69) extracted from PACI data. This construction justifies the use of adjusted Incidence Rate Ratios (IRR) as the measure of association, representing the relative likelihood of screening participation across different socio-demographic strata. Calendar year and governorate were examined as potential confounders were examined as well as potential effect modifiers. While age and education level were treated as primary independent variables. We checked for the absence of multicollinearity between independent explanatory variables using the variance inflation factor. We stratified the analyses by nationality and by governorate, according to their density (more or less than 1000 individuals/km²), as a surrogate measure of the rurality which is associated with differential access to health services. Independent and significant socio-demographic factors (p < 0.01) related to the outcome variable were retained in the final model.

Adjusted incidence rate ratio and their 95% confidence interval (CI) were derived from the final multivariable GLMs. All analyses were conducted using Stata 17[33].

Results

Table 1 describes the target population for BC screening and their screening proportions by socio-demographic characteristics in Kuwait. The target population was larger in Hawalli region and, in the Capital for Kuwaiti and Al-Farwaniya for non-Kuwaiti. Compared to the Kuwaiti target population, the non-Kuwaiti women were younger (66% vs. 46% in age 40−49) and with a lower level of education (46% vs. 10% in illiterate/read and write). The “single” category of marital status was small in both nationality groups, even if higher in non-Kuwaiti women (19% vs. 7%).

The overall screening uptake among Kuwaiti women were constant between 2014 and 2019 at around 1.8%, ranging between 1.4% (2019) and 2.3% (2015). The uptakes remained clearly below 1% among the non-Kuwaiti women over the entire study period. Because of this, we did not perform further analysis among non-Kuwaiti women as uptake hardly varied by socio-demographic factors.

Among Kuwaiti women, the BC screening uptakes varied marginally according to socio-demographic characteristics. This is confirmed by the univariable analyses stratified by regions, grouped according to the population density of the governorates: Hawalli, Al-Farwaniya, Mubarak Al-Kabeer and the Capital with over 1000 individuals/km² and Al-Ahmadi and Al-Jahra with less than 1000 individuals/km² (Table 2). In both groups of regions, unadjusted ever-screened proportion rate ratios decreased with increasing age, were higher among ever-married women, and increased with level of education. Estimates based on the multivariable models (Table 2) did not change dramatically, except that age was a less important factor in the lower-density region. We predicted the BC ever-screening uptakes from the multivariable models in a few groups of interest, in order to contrast the uptake proportions, according to extreme (i.e., the lowest and the highest) age categories, marital statuses, and education levels (Figure 2). Among Kuwaiti women living in low-density population regions, the BC ever-screening uptake varied between 0.2% [95% CI: 0.15−0.26] in women aged 60−69, single, and lowest education and 1.3% [95% CI: 1.16−1.38] in women aged 40−49, ever married, with highest education. In high-density population regions, the corresponding uptakes were at 0.4% [95% CI: 0.33−0.45], and 3.4% [95% CI: 3.3−3.5], respectively.

We did not detect any multicollinearity between the variables of interest. Our analyses focused on ever-screened women. Including the second and subsequent screening records in the analyses had no impact on our findings.

Discussion

BC screening uptake in Kuwait is known to be poor, as reported by recent reports and articles[18,23,34]. Our aim was to update the estimated BC screening uptake among Kuwaiti and non-Kuwaiti women, and to examine whether this uptake varied according to socio-demographic characteristics and access to health services through the population density of their region of residence. Our analysis confirmed the overall low uptake, both in Kuwaiti and non-Kuwaiti women, below 2%. Even among the groups with the highest BC screening uptake (aged 40−49, ever married, with high education and living in high-density regions), the proportion of ever-screened remained below 5% in Kuwaiti, and below 1% in non-Kuwaiti women. This difference may be explained by the provision of the KNMSP booking platform to Kuwaiti nationals only, whereas non-nationals must be referred by primary or secondary care to a general hospital where a fee is charged either for screening or diagnostic test.

Part of the screening tests may be done outside the national screening program. For example, asymptomatic patients can be referred to BC screening by their physicians and surgeons in their assigned outpatient clinics, either from the hospital or the primary care clinics. It was shown that physicians in Kuwait had a substantial influence in increasing women’s awareness of BC screening, especially among women aged 50 and above, because of their frequent visits to healthcare facilities related to the menopausal experience[29,30].

BC screening uptake can therefore be under-estimated because of these mammograms outside the BC screening program. For example, in France, nationwide databases were used to estimate the opportunistic and overall coverage of MS uptake between 2016 and 2017[35]. The overall coverage BC screening rate amongst women aged 40–84 was estimated at 47.8%, divided in 17.5% opportunistic screening and 30.3% of organized screening[35]. We conducted an analogous investigation in Kuwait by examining the mammograms performed in the radiology units of major hospitals outside the BC screening program. We gathered all these tests in each medical region for the same study period (2014−2019). The numbers of such additional mammograms by medical region were 6,010 (Al-Ahmadi), 3,853 (Al-Farwaniya), 3,166 (Al-Jahra), 3,856 (Al-Sabah), 5,096 (The Capital), and 7,250 (Hawalli), regardless of their medical indication. Even if all these tests were assumed to be only for screening and among Kuwaiti women, the total uptake among the Kuwaiti women will range between 4% and 7% in the different regions. It hardly modifies our conclusion about the low BC screening uptake.

The BC screening rates in various GCC countries, including Kuwait, UAE, Oman, and Saudi Arabia, are low[16]. Factors such as lower educational level and unmarried status are associated with decreased screening uptake among women aged 40−75 years[16,17]. To our knowledge, literature on national screening uptake in the GCC countries largely relies on annual reports from MoH (based on utilisation of screening services in the respective country) and national surveys. National screening uptake is limited in the region, with estimates varying, according to the sources, between 6.5% and 8% in Saudia Arabia,[36,37] not exceeding 25% in UAE,[38] or between 13% and 35% in Qatar amongst the eligible women[39,40]. Despite national programs and opportunistic tests, the BC screening uptake remains consistently low in the GCC countries.

As in the GCC countries, knowledge about BC screening uptake in Middle East countries is mostly based on MoH annual reports and surveys, with often inconsistent estimates because of differential study designs. Furthermore, the methodology used to estimate the uptake was not always clearly defined. However, BC screening uptakes were consistently low, ranging between 2% in Palestine[41] and up to 17% in Jordan[42–44]. Contrasting with these low estimates, BC screening uptake in Lebanon was estimated, based on several surveys, to be between 29% in 2005 and up to 59% in the more recent years[45–47]. This higher screening uptake may reflect the successive screening campaigns implemented by the Lebanese Ministry of Public Health since 2002, during which mobile screening units, free of charge, were used[48]. In Kuwait, screening campaigns are usually limited to the BC Month in October. Nonetheless, none of the GCC countries, despite being all classified HICs, seems to reach the higher uptake observed in Lebanon[47].

Low income, poor education, and long distance to screening services, have been shown to be associated with lower BC screening uptake even in countries with overall much higher uptake than in the GCC countries, such as, for example, the UK, Canada or France.[11,49–55] Non-nationals represent high proportions of the populations of most GCC countries, and these non-national women often face cost barriers to screening services and cancer treatment, even when they hold a medical insurance, which is likely to discourage the use of BC screening.[56] Though individual economic data was unavailable, the free-for-service requirement for non-nationals poses an economic barrier. Further research is necessary to inform the effect of income from cultural factors and types of health insurance among this population. However, BC screening uptake remains very low even among national women of GCC countries, and even when screening is free of charge, at least since the establishment of national screening programs.

Other factors may play an important role. Some HICs such as the UK, Denmark and USA are well known for high BC screening uptake. The European Union Council consider 70% as an acceptable BC screening uptake level for the target population (50−69 years) and publishes recommendations to help reach this target[2,5,9]. One such recommendation is the invitation method to the targeted population, which is effective at increasing screening participation[9]. In Denmark and England, BC screening is organized for women aged 50 to under 71, through invitation, and uptake reached 84% and 71%, respectively[9,57,58]. Lack of information among women, cultural constraints and other contextual factors may explain some of the low uptake, in particular among nationals who generally have a free-of-charge access to screening program. However, participation rates are also very low for the few colorectal cancer screening programs implemented in the region (e.g., Kuwait and UAE)[59,60]. In contrast, the pro-active approach chosen by Lebanon proves that much higher breast cancer screening uptakes are achievable in the region. Apart from cancer, other screening programs in Kuwait have achieved higher participation rates, either because of their mandatory aspect (e.g., National Newborn Screening Program) or pro-active approach (e.g., Premarital Screening Program)[61,62].

Strengths and limitations

In this study, we were able, for the first time in Kuwait, to examine, at national level, the characteristics of both all women eligible for BC screening and all screened women, using the national population data and the national screening program data, respectively. Additionally, we contrasted our results to the number of mammograms performed in the major hospitals within each governorate, which further confirmed Kuwait’s BC screening uptake is very low and far from reaching the optimal goal of 70%. Our study in Kuwait measured the uptake of MS at population level, as opposed to national surveys which are subject to reporting bias and lack of representativeness.

The primary potential drawback is an underestimation of the proportion of opportunistic screening because all women identified to have screening or diagnostic mammography were seen in governmentally funded hospitals. However, in Kuwait, the private sector, which also offers BC screenings, represents less than 15% of health expenditure, the rest being paid for by the general government[63]. This study is a critical baseline for the implementation phase of the KNMSP. However, the study does not reflect the changes that have occurred after the year 2020, including the impact of the COVID-19 pandemic on the attendance rate at the screening events. Future longitudinal studies are needed to be conducted to reflect the data from the period 2020 to 2025 to assess program’s recovery and the effectiveness of the recent awareness campaign.

Conclusion

The BC uptake among the eligible women in Kuwait is found to be very low and remains constant even after considering the socio-demographic factors. Although the facilities for the screening events are concentrated in the high-density regions, indicating the presence of significant geographic barriers in the lower-density regions, the low attendance rates are not sufficient to bring about a significant impact on the mortality rates among the general Kuwaiti population. For better outcomes, a paradigm shift is required from the passive approach to a more systematic invitation-based approach. In addition, the expansion of the ongoing awareness campaign, geographic accessibility, and the removal of cost factors for non-national women need to be addressed.

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