Racial/ethnic and socioeconomic disparities in colorectal cancer screening in a large organization with universal insurance before and during the coronavirus disease 2019 pandemic

Abstract

Objectives

Israel is regarded as a country with a developed economy and a moderate income inequality index. In this population-based study, we aimed to measure the inequalities in colorectal cancer screening within Clalit Health, an organization with universal insurance, before and during the coronavirus disease 2019 pandemic.

Setting

Retrospective analysis within Clalit Health Services, Israel.

Methods

We evaluated the rate of being up to date with screening (having a colonoscopy within 10 years or a fecal occult blood test within 1 year) and the colonoscopy completion rate (having a colonoscopy within 6 months of a positive fecal occult blood test) among subjects aged 50–75 in 2019–2021.

Results

In 2019, out of 918,135 subjects, 61.3% were up to date with screening; high socioeconomic status: 65.9% (referent), medium-socioeconomic status: 60.1% (odds ratio 0.81, 95% confidence interval 0.80–0.82), low-socioeconomic status: 59.0% (odds ratio 0.75, 95% confidence interval 0.74–0.75); Jews: 61.9% (referent), Arabs: 59.7% (odds ratio 0.91, 95% confidence interval 0.90–0.92), Ultraorthodox-Jews: 51.7% (odds ratio 0.77, 95% confidence interval 0.75–0.78). Out of 21,308 with a positive fecal occult blood test, the colonoscopy completion rate was 51.8%; high-socioeconomic status: 59.8% (referent), medium-socioeconomic status: 54.1% (odds ratio 0.79, 95% confidence interval 0.73–0.86), low-socioeconomic status: 45.5% (odds ratio 0.60, 95% confidence interval 0.56–0.65); Jews: 54.7% (referent), Ultraorthodox-Jews: 51.4% (odds ratio 0.91, 95% confidence interval 0.90–0.92), Arabs: 44.7% (odds ratio 0.77, 95% confidence interval 0.75–0.78). In 2020–2021, there was a slight drop in the rate of being up to date with screening, while most of the discrepancies were kept or slightly increased with time.

Conclusions

We report significant inequalities in colorectal cancer screening before and during the coronavirus disease 2019 pandemic in Israel, despite a declared policy of equality and universal insurance.

Keywords

Racial ethnic socioeconomic disparities colorectal cancer screening insurance coronavirus disease 2019

Introduction

Israel is ranked as a country with a developed economy (per capita gross domestic product in 2022: 44000 USD) and a moderate income inequality index (Gini coefficient in 2019: 0.342).¹ Healthcare in Israel is universal as all residents are entitled to healthcare by law.² The Israeli healthcare law is based on principles of equality, as subjects with low income are exempted from insurance payment.^2,3 The coronavirus disease 2019 (COVID-19) pandemic has exacerbated health inequalities, resulting in higher mortality and morbidity rates among the most socially disadvantaged.⁴ The International Agency for Research on Cancer (IARC) stated that social inequalities in cancer can be measured and monitored using absolute and relative measures.⁵ Although the measurement of longitudinal participation of individuals over time might be challenging,^6,7 data suggest that the implantation of colorectal cancer (CRC) screening programs by accepted quality measures (i.e., the participation rate of the eligible population) is highly variable and is lower among subjects with low socioeconomic status (SES) and minorities.^8–18 Subjects with low SES and racial or ethnic minorities are at increased risk of advanced CRC and cancer-related mortality,^10,12 attributed to greater exposure to risk factors, educational gaps, limited access to CRC screening, lack of follow-up of abnormal test results, and lack of insurance, even before the COVID-19 pandemic.^9–13,19 During the COVID-19 crisis, many preventive health services were suspended worldwide, as well as in Israel, and many diagnostic colonoscopies were canceled due to reduced healthcare system capacity and the perceived risk of infection.^20–28 There are data accumulating to suggest that the effect of the COVID-19 pandemic has been more pronounced among subjects with low SES, minorities, and those in rural areas in many countries.^{15,23,27,29–39} However, little is known about the impact of inequalities and the pandemic on CRC screening within an organization with universal health insurance.

In this population-based study, we aimed to measure the inequalities in CRC screening within Clalit Health Services, a large organization with universal healthcare insurance.

Methods

CRC screening program and measurements

This is a retrospective analysis of the rate of being up to date with screening and the colonoscopy completion rate (CCR) among subjects aged 50–75 within Clalit Health Services in 2019–2021. Clalit Health is the largest of four integrated healthcare organizations in Israel, with 4.7 million members (53% of the population).⁴⁰ Clalit Health has adopted an organized outreach, fecal occult blood test (FOBT)-based CRC screening program since 2007 for all subjects aged 50–75.^41,42 According to our quality measures program, being up to date with screening is defined as the percentage of the eligible population, aged 50–75, who had undergone a colonoscopy within 10 years or an FOBT within 1 year, and the CCR is defined as the percentage of subjects with a positive FOBT who had a follow-up colonoscopy within 6 months.⁴³

We extracted data about all insured subjects within Clalit Health aged 50–75 without a prior diagnosis of CRC. Age, sex, ethnicity (Jews, Arabs, Ultraorthodox Jews), and SES were extracted from the central database. The SES classification (high, medium, low) is based on multiple social and demographic factors defined by the Central Bureau of Statistics in Israel according to the last known address.⁴² FOBT results were categorized as either negative or positive.⁴⁴ We extracted data about colonoscopies from the administrative database. This database includes all colonoscopy procedures performed within the secondary and tertiary centers of Clalit Health, including all semiprivate procedures financed by the complimentary Clalit Health insurance and the completely private procedures reported in patients’ files by the primary care physicians.^43,44 The ethics committee of Clalit Health approved this study (No. 118, updated on September 5, 2019).

Statistical analysis

Both the rate of being up to date with screening and the CCR are expressed as percentages and are continuously calculated by months, stratified by SES (low, medium, high), population sector (Jewish, Jewish Ultraorthodox, Arab), and sex. To evaluate the social and ethnic disparities and trends over time, we calculated the net difference in the rate of both measures. We used logistic regression analysis, including SES, sector, and year to yield odds ratios (ORs) and confidence intervals (CIs) using the SAS v9.3 software (Cary, NC, USA).

Results

The total number of subjects aged 50–75 without a prior diagnosis of CRC in 2019 was 918,135; 53.0% were females, 69.4% belonged to the general Jewish sector, while 27.4% belonged to the Arab sector and 3.9%, were Ultraorthodox Jews; 47.4% were low-SES, 40.0% medium-SES, and 22.5% high-SES. Compared to 2019, during 2020 and 2021, the eligible population increased by 0.9% and 1.4%, respectively, while the proportion of social/ethnic characteristics remained stable, Table 1.

Table 1.

Subjects aged 50–75 within clalit health eligible for colorectal cancer screening.

		2019		2020		2021
		N	(%)	N	(%)	N	(%)
Total		918,135	(100%)	926,357	(100%)	931,010	(100%)
Sex	Female	486,754	(53.0%)	491,102	(53.0%)	493,240	(53.0%)
	Male	431,381	(47.0%)	435,255	(47.0%)	437,770	(47.0%)
Sector	Jew	718,999	(78.3%)	720,860	(77.8%)	719,518	(77.3%)
	Arab	162,675	(17.7%)	168,738	(18.2%)	174,894	(18.8%)
	Ultraorthodox Jew	35,910	(3.9%)	36,220	(3.9%)	36,245	(3.9%)
Socioeconomic status (SES)	High	206,037	(22.4%)	207,514	(22.4%)	207,457	(22.3%)
	Medium	374,224	(40.8%)	374,213	(40.4%)	372,437	(40.0%)
	Low	336,479	(36.6%)	340,757	(36.8%)	344,000	(36.9%)

In 2019, out of 918,135 subjects, the overall rate of the population being up to date with screening was 61.3%; 62.6% for females (referent) and 59.8% for males (OR 0.89–0.90); 61.9% for Jews (referent), 59.7% for Arabs (OR 0.91, 95%CI 0.90–0.92), and 51.7% for Ultraorthodox Jews (OR 0.77, 95%CI 0.75–0.78); 65.9% for high-SES (referent), 60.1% for medium-SES (OR 0.81, 95%CI 0.80–0.82), and 59.0% for low-SES (OR 0.75, 95%CI 0.74–0.75), Table 2. As compared to 2019, in 2020 and 2021, the overall rate of being up to date with screening was reduced by 1.6% and 1.8%, respectively, while the sex, ethnic, and socioeconomic disparities were further enlarged (P for interaction with time < 0.001 for both sector and SES), Figure 1.

Figure 1.

Rate of being up to date with colorectal cancer screening (defined as having had a colonoscopy within 10 years or a fecal occult blood test (FOBT) within 1 year) according to sex, ethnicity, and socioeconomic status.

Table 2.

Rate of being up to date with CRC screening (percentage of subjects having had a colonoscopy within 10 years or an FOBT within 1 year).

		2019			2020			2021
		Rate	Δ%	OR, 95%CI	Rate	Δ%	OR, 95%CI	Rate	Δ%	OR, 95%CI	P*
Total		61.3%			59.7%			59.5%
Sex	Female	62.6%	Referent	1.00	60.8%	Referent	1.00	60.6%	Referent	1.00	0.0009
	Male	59.8%	2.8%	0.89, 0.88–0.90	58.5%	2.3%	0.91, 0.90–0.92	58.2%	2.5%	0.90,0.90–0.91
Sector	Jew	61.9%	Referent	1.00	60.8%	Referent	1.00	60.1%	Referent	1.00	<0.0001
	Arab	59.7%	2.2%	O.91, 0.90–0.92	56.6%	4.2%	0.84, 0.83–0.85	58.7%	1.4%	0.94, 0.93–0.95
	Ultraorthodox Jew	55.4%	6.5%	0.77, 0.75–0.78	53.7%	7.1%	0.75, 0.73–0.76	51.7%	8.4%	0.71, 0.70–0.73
SES	High	65.9%	Referent	1.00	64.6%	Referent	1.00	63.8%	Referent	1.00	<0.0001
	Medium	60.9%	4.9%	0.81, 0.80–0.82	59.8%	4.8%	0.81, 0.80–0.82	59.3%	4.5%	0.82, 0.81–0.83
	Low	59.0%	6.9%	0.75, 0.74–0.75	56.8%	7.9%	0.72, 0.71–0.73	57.1%	6.7%	0.76, 0.75–0.76

CRC: colorectal cancer screening; FOBT: fecal occult blood test; SES: socioeconomic status; OR: odds ratio, CI: confidence interval; *P interaction with time.

Out of 918,135 eligible subjects in 2019, 258,135 subjects performed an FOBT (participation rate of 28.1%). Of these, 21,308 subjects had a positive result (positivity rate of 8.5%). About 69% were Jews, 28% Arabs, and 3% Ultraorthodox Jews; 15.7% belonged to the high-SES, 37.1% medium-SES, and 47.1% low-SES, Table 3. In 2020 and 2021, the participation rate was 26.0% and 25.3%, respectively, while the positivity rate increased to 9.5% and 10.7%. The proportions of the socioeconomic and demographic characteristics remained stable. In 2019, out of 21,308 with a positive FOBT, the CCR was 51.8%; 52.7% for females (referent) and 51.0% for males (OR 0.94, 0.89–0.99); 59.8% high-SES (referent), 54.1% medium-SES (OR 0.79, 95%CI, 0.73–0.86), and 45.5% low-SES (OR 0.60, 95%CI 0.56–0.65); 54.7% for Jews (referent), 51.4% for Ultraorthodox Jews (OR 0.91, 95%CI 0.90–0.92), and 44.7% for Arabs (OR 0.77, 95%CI 0.75–0.78), Table 4. Compared to 2019, in 2020 and 2021, the overall CCR was reduced by 1.3% and 0.9%, respectively, while the sex, ethnic, and socioeconomic disparities remained stable or further enlarged (P for interaction with time < .001 for the sector), Figure 2.

Figure 2.

Colonoscopy completion rate (defined as having had a follow-up colonoscopy within 6 months of a positive fecal occult blood test (FOBT)) according to sex, ethnicity, and socioeconomic status.

Table 3.

Subjects aged 50–75 within Clalit health with a positive FOBT who are eligible for a colonoscopy.

		2019		2020		2021
		N	(%)	N	(%)	N	(%)

Total		21,308	(100%)	22,798	(100%)	25,222	(100%)
Sex	Female	11,195	(52.5%)	11,722	(51.4%)	13,185	(52.3%)
	Male	10,113	(47.5%)	11,076	(48.6%)	12,037	(47.7%)
Sector	Jew	5959	(28.0%)	6027	(26.4%)	7583	(30.1%)
	Arab	648	(3.0%)	848	(3.7%)	813	(3.2%)
	Ultraorthodox Jew	14,701	(69.0%)	15,923	(69.8%)	16,824	(66.7%)
SES	High	10,036	(47.1%)	10,581	(46.4%)	12,203	(48.4%)
	Medium	7898	(37.1%)	8472	(37.2%)	9112	(36.1%)
	Low	3356	(15.7%)	3671	(16.1%)	3749	(14.9%)

FOBT: fecal occult blood test; SES: socioeconomic status.

Table 4.

Colonoscopy completion rate (percentage of subjects with a positive FOBT who had a follow-up colonoscopy within 6 months).

		2019			2020			2021
		Rate	Δ%	OR, 95%CI	Rate	Δ%	OR, 95%CI	Rate	Δ%	OR, 95%CI	P*
Total		51.8%			50.5%			50.9%
Sex	Female	52.7%	Referent	1.00	52.0%	Referent	1.00	52.3%	Referent	1.00	0.3926
	Male	51.0%	1.7%	0.94, 0.89–0.99	49.2%	2.8%	0.89, 0.85–0.94	49.6%	2.7%	0.90, 0.85–0.94
Sector	Jew	54.7%	Referent	1.00	53.5%	Referent	1.00	53.8%	Referent	1.00	0.0310
	Arab	44.7%	10.0%	0.67, 0.63–0.71	42.6%	10.9%	0.65, 0.61–0.69	44.8%	9.0%	0.70, 0.66–0.74
	Ultraorthodox Jew	51.4%	3.3%	0.88, 0.75–1.03	52.0%	1.5%	0.94, 0.82–1.08	46.3%	7.6%	0.74, 0.64–0.85
SES	High	59.8%	Referent	1.00	59.5%	Referent	1.00	59.9%	Referent	1.00	0.4261
	Medium	54.1%	5.6%	0.79, 0.73–0.86	53.0%	6.5%	0.77, 0.71–0.83	52.6%	7.4%	0.74, 0.69–0.80
	Low	47.3%	12.5%	0.60, 0.56–0.65	45.5%	14.0%	0.57, 0.53–0.61	46.7%	13.2%	0.59, 0.54–0.63

FOBT: fecal occult blood test; SES: socioeconomic status; OR: odds ratio, CI: confidence interval. *P interaction with time.

Discussion

In this population-based study, we provide solid data about the socioeconomic and racial disparities in CRC screening within an outreach-organized screening program in Israel, a country with a moderate Gini coefficient score and an intended policy of equality in health (universal health insurance with an exemption from any payment for subjects with low income). We report that subjects of low-SES and ethnic minorities (Israeli Arabs and Ultraorthodox Jews) are significantly prone to be not up to date with CRC screening nor to complete colonoscopy after a positive FOBT. We also report that during the COVID-19 pandemic the inequalities were kept or slightly increased.

In this context, it should be noted that the public expenditure per capita on healthcare in Israel is relatively low and stands at about 65% of the OECD average.¹ Even though public spending increased in 2020, due to the need to manage the COVID-19 pandemic, a similar increase occurred in other OECD countries. Therefore, Israel's relative position remained relatively low on this index.^1,3 The primary attention should be directed to recovery, as unequal recovery can widen the disparities unless an active program is issued.^45,46

In our current report, the measured CCR within 180 days of a positive FOBT was 51% (59.8% for high-SES, 47.3% for low-SES), a rate that is far from the target of ≥80%, as stated by the US Multi-Society Task Force on CRC.⁴⁷ Although it is challenging to compare adherence to screening between different screening programs,^6,48 a systematic review and meta-analysis of population screening program studies [18 studies (23 substudies/data sets); 342,555 patients with a positive FOBT] concluded that the compliance rate for any second procedure in patients with a positive FOBT was only 61.6% (95% CI 46.8–73.6).⁴⁹ An international survey of 32 screening programs worldwide stated that the mean reported CCR was 79% (standard deviation 16%), with somewhat higher rates in Europe (mean 86%, SD 13%) than in North America (mean 74%, SD 18%).⁵⁰ In the US alone, CCRs vary substantially across healthcare systems, from 85% in the organized outreach program of the Kaiser Permanente Northern California to much lower numbers within the safety-net population of the Southern California Federally Qualified Health Centers and the Medicade-insured population.^51–53

It should be noted that the data on participation rate were prepared by the Department of Quality Measures at the headquarters of Clalit Health and were based on multiple resources (claims data, International Classification of Diseases diagnosis, and reports of the primary care physicians). However, if some of the procedures done privately were not reported, the disparities would even widen. In general, the reasons for not completing a colonoscopy after a positive FOBT are attributed to both the patient and the provider.^54,55 A recent study from Israel reported that patient lack of comprehension regarding the test was the strongest predictor of non-adherence to follow-up. Arab ethnicity and lower SES significantly reduced adherence.⁵⁵

As stated earlier, substantial social and ethnic inequalities with regard to several other non-communicable diseases in Israel do exist.¹⁴ These might be attributed to both patient (i.e., general approach to health and fear of being examined by a male physician) and provider-system-related causes, and also the degree of access to semiprivate or private services.^20,21,23 The strength of our study is the large number of patients within a national population-based program of a large health maintenance organization with a diverse population, access to excellent electronic databases and monitoring tools, and the use of defined quality measures. Due to a short follow-up time since the COVID-19 pandemic, it has not yet been possible to assess the impact of the decrease in screening activity and increased subpopulation disparities on the cancer burden. Future studies are planned to evaluate cancer incidence, stage, and mortality outcomes among the sub-population sectors.

In conclusion, in Israel, a country with a developed economy and a moderate income inequality index, we report significant inequalities in CRC screening before and during the COVID-19 pandemic despite a declared policy of equality and universal insurance. The roots of the disparities reported here should be learned, targeted, and continuously monitored.

Footnotes

Data availability

The aggregated data of this study are available upon request.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

Specific author contributions

Conception and design were done by ZL and ADC; data extraction was done by DC and TB; analysis and interpretation of the data were done by ADC, AF, and OW; drafting of the article was done by ZL, AF, and SE; critical revision of the article for important intellectual content was done NAF, AF, and OW; final approval of the article was done by ZL. All authors included in the authorship list approved the article's final version.

ORCID iDs

Zohar Levi

Naim Abu-Frecha

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