key: cord-0773788-magjuu32
authors: Caspi, Gil; Dayan, Avshalom; Eshal, Yael; Liverant-Taub, Sigal; Twig, Gilad; Shalit, Uri; Lewis, Yair; Shina, Avi; Caspi, Oren
title: Socioeconomic disparities and COVID-19 vaccination acceptance: a nationwide ecologic study
date: 2021-06-07
journal: Clin Microbiol Infect
DOI: 10.1016/j.cmi.2021.05.030
sha: 92560ffde1180b2c4560c0bc0e66e474b47ad4ec
doc_id: 773788
cord_uid: magjuu32

OBJECTIVE: To analyze the correlation between COVID-19 vaccination percentage and socioeconomic status (SES). METHODS: A nationwide ecologic study based on open-sourced, anonymized, aggregated data provided by the Israel Ministry of Health. The correlations between municipal SES, vaccination percentage, and active COVID-19 cases during the vaccination campaign were analyzed by using weighted Pearson correlations. To assess the adequacy of first dose vaccination rollout relative to the municipality COVID-19 disease burden, a metric termed the vaccination need ratio was devised by dividing the total number of active cases (per 10,000 people) by the vaccination percentage of the population over 60 in each municipality, and its correlation with the SES was examined. RESULTS: 23 days after initiation of the vaccination campaign, 760,916 (56.8%) individuals over the age of 60 were vaccinated in Israel with the first dose of the BNT162b2 COVID-19 vaccine. A negative correlation was found between the COVID-19 active case burden and the vaccination percentage of the study population in each municipality (r=-0.47, 95% confidence interval [-0.59 to -0.30]). The vaccination percentage significantly correlated with the municipal SES (r=0.83, 95% confidence interval [0.79 to 0.87]). This finding persisted but was attenuated over a five-week period. A negative correlation between the vaccination need ratio and municipal SES (r=-0.80, 95% confidence interval [-0.88 to -0.66]) was found. CONCLUSION: Lower COVID-19 vaccination percentage was associated with lower SES and high active disease burden. Vaccination efforts should focus on areas with lower SES and high disease burden to assure equality of vaccine allocation and potentially provide a more diligent disease mitigation.

The coronavirus disease 2019 pandemic has resulted in the deaths of over 3 million people 63 worldwide by April 16, 2021 and has become a leading cause of mortality in adults. The rapid 64 development of COVID-19 vaccines provides new hopes regarding our ability to control the pandemic(1-65

3). However, while the availability of COVID-19 vaccinations is progressing globally, the pandemic is 66 overwhelming health care systems capabilities in some countries. Therefore, the limited roll-out of 67

vaccinations relative to the current COVID-19 burden mandates prioritization of the vaccination effort(4). 68

Currently, Israel, is one of the global leaders in vaccinating its population, making it a suitable case study 69 for other countries as they form their vaccination strategies(5). Many countries adopted strategies based 70 on prioritizing elderly people as they are at the greatest risk for severe COVID-19 related disease and 71 mortality. In Israel, people over the age of 60, along with healthcare personnel were the first to be offered 72 the vaccine(6). 73

Prior survey studies suggested that vaccination percentages may be reduced among demographically 74 defined groups of lower education and income levels(7). Also, municipalities with a lower socioeconomic 75 status (SES) may suffer from lower availability of healthcare resources, leading to poorer health and 76 lower acceptance of public healthcare measures such as vaccines by their residents(8). Concurrently, 77 some of these populations from municipalities of lower SES and of rural locations are more severely 78 affected by the COVID-19 pandemic worldwide (9-11). The overarching hypothesis of our research is 79 that population with a lower SES are subject to a double hit risk in the setting of the current pandemic, a 80 higher disease rates coupled with a lower vaccination acceptance.

Methods 84

The mandatory Israeli National Health Insurance Act provides health coverage through one of the four 86 national Health Maintenance Organizations (HMOs) to every Israeli resident. All HMOs use electronic 87 medical records and provide COVID-19 related data and vaccination information to the Israel Ministry of 88

Health. The national vaccination campaign was launched on December 19th, 2020 in Israel, actively 89 encouraging the population to receive the vaccine. All four national HMOs began to simultaneously 90 vaccinate medical staff and residents older than 60 with the BNT162b2 COVID-19 vaccine across the 91 country free of charge. 92

The study population consisted of the population of Israel. Included were nationally aggregated, 93 anonymized open-source data of the COVID-19 disease incidence by municipality in Israel as well as the 94 vaccinations given by age and municipality provided by the Israel Ministry of Health. In our database, 95 there were 9,070,297 subjects of which 1,466,664 were aged over 60, residing in 1,218 municipalities. 96

After limiting our analysis to municipalities with a population of over 2,000 also excluding 1,036 97 municipalities (lack of COVID-19 active case data, SES ranking, vaccination data) 184 (182) 98 municipalities populated with 7,987,009 subjects were available for analysis. Of these, 1,338,751 subjects 99 were older than 60, with 467,257 accumulated cases of COVID-19. A total of 1,371,506 subjects were 100 vaccinated with the initial dose. Of these, 760,916 subjects were older than 60. 101

The socioeconomic status (SES) scoring was based on the Israeli Central Bureau of Statistics (ICBS) 105 scoring system. Accordingly, each place of residence, obtained from the Israeli Ministry of Interior, is 106 ranked from lowest to highest SES. The score stratifies all municipalities according to multiple variables 107 that might affect SES, such as age distribution, level of unemployment, and available work force, 108 education (the proportion of undergraduate students and those entitled to a high school diploma), average 109 income per capita, and the proportion that receives income support. The SES data were processed from 110 was taken from ICBS. Given that municipality's population was updated two years ago, in some extreme 114 cases the number of vaccinated persons over the age of 60 (currently counted) is higher than that found in 115 the municipality's population. 116

To assess whether the vaccination percentage were related to SES, we evaluated the correlation between 117 SES rank and vaccination rates in the at-risk population (aged over 60). 118

Data of active COVID-19 cases for each municipality was derived from the COVID-19 database of the 120 Israeli Ministry of Health (MOH) [https://data.gov.il/dataset/covid-19]. First dose vaccinations by 121 municipality and age group data were derived from a status report published by the Israeli MOH on the performed by replacing '<15' with the lower bound of 1. 127

The COVID-19 active cases and vaccination data were reported in 279 municipalities in Israel. SES was 128 reported in 196 out of the 279 municipalities. Vaccinations of people over the age of 60 were aggregated 129 out of 4 age groups ('60-69', '70-79', '80-89', '90+') . We filtered out the municipalities that had more 130 than 1 sub-group with missing data ('<15')and accordingly a total of 13 municipalities were omitted. 131

Hence, our analysis was performed using data of 183 municipalities in Israel. 132

To generate a national heat map, color coding of municipalities was conducted by ranking the relevant 133 metric according to percentiles. The lower 20 and upper 80 percentile were color-coded in red and green, 134 respectively. Color coding was spectrally determined according to the relevant percentile. 135

The vaccination need ratio 136

To characterize the association between the COVID-19 active case burden, and the vaccination 137 percentage of the population older than 60, we devised the vaccination need ratio (VNR). VNR is 138 calculated by dividing the total number of active cases (per 10,000 people) by the rate of vaccination of 139 the population over 60 in each municipality (m) 140

We examined the association between the municipal SES to the VNR. 141

Finally, we color-coded the municipalities according to the VNR metric where municipalities at top 20 142 percentiles of VNR were coded in red (e.g., high number of active cases per 10,000 people and low rates 143 of vaccination) and those in the bottom 20 percentiles were coded in green with range spectral coding of 144 all other municipalities, accordingly. We applied our findings to create a heatmap. 145 

Continuous variables are presented as median ± SD and categorical variables as numbers, percentages 153 median with interquartile (IQR) range where appropriate. The correlation was analyzed by using a 154

weighted Pearson correlation (according to the municipality population over 60 from the total population 155 over 60 from the evaluated municipalities) and the confidence interval (CI) was calculated using a 156 bootstrapping method with an alpha of 0.95. Basic arithmetic calculations were conducted using Python 157

Pandas and NumPy. Statistical analysis was done using Python SciPy. 158

At the time of analysis, the vaccination percentage of subjects over 60 in Israel was a median of 54.9% 160 (IQR 43.5-66.7) of subjects over 60 were vaccinated in Israel (760,916). The median of active cases per 161 municipality was 64.6 (IQR46.3-99.8)6 per 10,000 people. The ratio between the municipality's COVID-162 19 active disease burden, and the vaccination's percentage of 60+ population, was calculated to assess the 163 vaccination need termed vaccination need ratio (VNR). The median VNR was 1.2 (IQR 0.76-2.41). 164

Vaccination percentages strongly correlated with municipal SES (r=0.83, 95% CI [0.79 to 0.87]) as 165 shown in Figure 1A . This correlation persisted but was ablated over 5 weeks to r=0.72, 95% CI [0.60 to 166 0.81] (Video S1). The vaccination percentage of the population over 60 negatively correlated with the 167 95% CI [-0.59 to -0.30] as depicted in Figure 1B . 169

We identified a significant negative correlation between municipal SES and the VNR, (r=-0.80, 95% 170 confidence interval [-0.88 to -0.66]). To assess the geographical dispersion of the VNR across the 171 country, a color-coded heatmap was generated portraying the VNR ranges between different 172 municipalities ( Figure 2 ). The generated map demonstrated high VNR in northern Israel, the seam zones, 173 and municipalities heavily populated with minorities. 174

The current research identified a correlation between municipal vaccination percentages and SES. 176

Furthermore, the need for vaccinations in municipalities (measured as the VNR) inversely correlated with 177 the municipal SES. Finally, we generated a geographic heatmap highlighting areas of high VNR, allowing 178 us to outline the need for vaccination in a geographical context and assisting policymakers in avoiding 179 pockets of high COVID-19 morbidity and low immunity. 180

We found that municipalities with a lower SES suffer from a higher disease burden, yet their at-risk 181 population has not been vaccinated against COVID-19 in the targeted rates. In Israel, like other countries, 182 populations from lower SES and minorities suffer from lower accessibility and availability to healthcare 183 resources. This leads to a reduced willingness to actively partake in recommended public health measures 184 (social distancing, mask-wearing), putting these populations at an increased risk for COVID-19 infection. 185

The reduced acceptance of these measures may further be augmented when introducing a vaccine based 186 on novel technologies to the public potentially raising further objection and safety concerns. 187

The strengths of our study stem from the analysis of a nationwide, publicly available, aggregated dataset 188 of COVID-19 morbidity and vaccinations in an ethnically heterogenous population, making our findings 189 generalizable to other countries. Moreover, we were able to examine our findings over a five-week period 190 enabling tracking of the vaccination efforts across municipalities. Thirdly, the timeliness of our findings is 191 of temporal relevance to other countries. Moreover, our analysis was conducted prior to initiation of the 192 protective effects of the vaccines expected to further widen the differences between municipalities with 193 low and high SES. Fourth, a national diagnostic effort (a rate of over 12 tests/day per 1,000 people) 194 coupled with real-time monitoring of the vaccination percentage allow for an accurate and timely 195 derivation of the VNR metrics. Our analysis is updated on our website 196 (https://vaccinations.covid19maps.org/) enabling policymakers to track the effect of their actions. 197

Our study has limitations. SES is calculated differently in each country, though the national Israeli 198

Central Bureau of Statistics classification correlative with metabolic disease (12) making our findings 199 generalizable. Also, in this study, SES is used as an ecological variable and is not indicative of individual 200

health, yet this is a more appropriate representation of its implication on municipal vaccination. We did 201 not have available data regarding active disease burden of population over 60, or the disease severity of 202 active cases within municipalities. As data were aggregated, we did not have available personal data 203 regarding other COVID-19 risk factors, though older age is the most important risk factor for severe 204 COVID-19 (13). We were not able to remove the population aged over 60 who recovered or died from 205 COVID-19 from the vaccination potential population in each municipality. However, at the time of 206 analysis there were approximately 4,000 COVID-19 related deaths and 5% of the population recovered 207 from the disease in Israel. Finally, the analysis time point, three weeks following the initiation of 208 vaccinations in Israel, aimed to evaluate the vaccination, distribution and compliance but was not 209 intended to evaluate vaccination efficiency. 210

Of note, the vaccine availability in Israel through the HMOs was equal between different municipalities, 211 and vaccination is free to all residents. When faced with monetary and insurance barriers to healthcare 212 which may exist in other countries, the need to directly target socio-economically disadvantaged 213 populations is even more urgent. We confirm in a real-world setting, that prior concerns raised regarding 214 vaccination acceptance in lower SES were warranted and should be addressed accordingly. Based on our findings, the Israeli Ministry of Health focused its vacation effort on municipalities with lower SES, 216 resulting in improved vaccination acceptance in those population. 217

In conclusion, as the initial vaccine rollout is limited, case numbers are spiking and more infectious 218 COVID-19 strains are emerging, we urge policymakers to emphasize efforts of vaccination in 219 municipalities with lower SES while using the suggested novel, metric, the VNR, to target the vaccination 220 efforts. Geographic heatmap layering of the VNR can further assist in preventing pockets of regional 221 decreased immunity. and arrow B point to municipalities in Northern Israel and the seam zone, respectively. Those 296 municipalities have a VNR, which might be indicative of a forming geographical pocket of low 297

immunity. The Bubble size is indicative of the size of the population over the age of 60. 298 Video S1: Dynamic correlation between vaccination of at-risk population and Socioeconomic status. 300

A bubble chart animation depicting the dynamics of the association between the percentage of the 301 vaccinated population over the age of 60 in a municipality and the municipality socioeconomic status 302 (SES) over a period of 5 weeks since the initiation of the vaccination effort in Israel. Over that period, the 303 correlation persists. After prioritization of these low SES population by the Israel Ministry of Health the 304 correlation was attenuated. 305

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