https://orcid.org/0000-0002-0550-0077
ABSTRACT
The potential future burden of COVID-19 is determined by the level of susceptibility of the population to infection. The protective effect provided by those previously infected diminishes over several months, while individuals with mixed immunity have the highest degree and persistence of protection. This study aimed to clarify the vaccination status of COVID-19 patients with hypertension and to analyze the characteristics and risk factors of non-vaccinated patients to protect this vulnerable population in the future. The study ultimately enrolled 4576 hypertensive patients with Omicron infection from April 6, 2022, to May 15, 2022. Among them, 3556 patients (77.7%) had received at least one dose of vaccine, and 2058 patients (45.0%) received a booster dose. In the multivariate logistic analysis, male (OR 1.328, 95% CI 1.138–1.550, p < .001), age (60–69 years vs.18–49 years) (OR 0.348, 95% CI 0.270–0.448, p < .001), age (≥70 years vs.18–49 years) (OR 0.130, 95% CI 0.100–0.169, p < .001), diabetes mellitus (OR 0.553, 95% CI 0.463–0.661, p < .001), chronic pulmonary diseases (OR 0.474, 95% CI 0.260–0.863, p = .015), chronic kidney disease (OR 0.177, 95% CI 0.076–0.410, p < .001), and cancer (OR 0.225, 95% CI 0.094–0.535, p = .001) were associated with vaccinated status. The vaccine coverage rate, especially the booster vaccine, was low for hypertensive patients with Omicron infection. Females, increasing age, and coexisting chronic diseases were associated with more inadequate vaccine coverage in hypertensive COVID-19 patients. Targeted interventions are required to address the under-vaccination of diverse hypertensive populations.
Introduction
Coronavirus Disease 2019 (COVID-19) has been a global public health concern since December 2019.Citation1,Citation2 Severe acute pulmonary syndrome coronavirus 2 (SARS-CoV-2) evolves through random mutations, and new mutations can potentially increase or decrease infectiousness and virulence. Prevention and control of the spread of COVID-19 have become more difficult due to the emerging mutations in the SARS-CoV-2 variant. The Omicron variant of SARS-CoV-2 has spread rapidly since its emergence in South Africa in 2021, and it has quickly become the dominant variant worldwide.Citation3,Citation4 This pandemic is putting enormous pressure on health systems. There was a significant difference in the severity of COVID-19 between vaccinated and non-vaccinated populations. In this context, an effective vaccine is essential to prevent further morbidity and mortality.Citation5,Citation6 From December 2020, vaccination is being rolled out globally to protect at-risk groups, such as older people and people with chronic diseases.Citation7–9
However, Omicron’s pathogenicity differs from the previous strains.Citation3,Citation10,Citation11 Omicron variants may evade immunity from previous vaccines or infections.Citation12–14 Many countries have experienced several waves of infection with the SARS-CoV-2 Omicron variant.Citation15,Citation16 Individuals previously infected with any SARS-CoV-2 variant have some protection against symptomatic reinfection, which is increased by vaccination.Citation17 People who have received two doses of the mRNA vaccine and have been previously infected with BA.1 are subsequently well protected against reinfection with BA.2 over a long period.Citation18 Previous SARS-CoV-2 BA.2 infection with booster vaccination (mixed immunity) provides excellent protection against reinfection.Citation19 However, the protective effect wanes fast over time.Citation19 The time since vaccination is a strong determinant in preventing infection, as is the status of previous infections and the number of vaccine shots.Citation20 In assessing the future disease burden of COVID-19, immunity from past infections should be weighed against the protection offered by vaccination to guide booster vaccination after an infected individual.
Individuals with chronic illnesses are at high risk of contracting SARS-Cov-2 and are more likely to develop serious complications leading to death.Citation21 Hypertension is a common comorbidity in hospitalized COVID-19 patients. Hypertension was present in 25% of the patients as a comorbid disease. The proportions of hypertension, cardia-cerebrovascular disease, and diabetes in patients with COVID-19 were 17.1%, 16.4%, and 9.7%, respectively. The most common comorbidities were hypertension (3026; 56.6%).Citation21–23 It significantly increases the risk of mortality, the severity of the disease, and the probability of admission to the intensive care unit.Citation22 Studies have shown low acceptance of vaccines among patients with chronic diseases.Citation24 We should focus on vulnerable populations prone to complications after infection. Knowing the vaccination status of hypertensive patients infected with COVID-19 helps us assess this population’s immune situation. In late February 2022, a wave of SARS-CoV-2 Omicron variant infections swiftly occurred in Shanghai, China. It was the first COVID-19 pandemic in Shanghai. Phylogenetic characterization of the viral genome suggested that the viral genomes of SARS-CoV-2 in patients were all clustered in the SARS-CoV-2 BA.2.2 sublineage. Considering that the protection from previous infections is limited and decreases over time,Citation25 we should still focus on the already infected and unvaccinated population to provide them with more robust immune protection in the future. This study aims to clarify the vaccination status of COVID-19 patients with hypertension and to analyze the characteristics and risk factors of non-vaccinated patients to protect this vulnerable population in the future.
Methods
Study design and participants
This retrospective cohort study enrolled hypertensive patients with a confirmed diagnosis of COVID-19 infection admitted to Shanghai Lingang Shelter Hospital in China. Hospital admission varied from April 6, 2022, to May 15, 2022. Patients who meet the following criteria were enrolled: 1) confirmed diagnosis of COVID-19 infection by nucleic acid real-time reverse transcriptase-polymerase chain reaction (RT-PCR) tests, 2) aged 18 years or older, 3) had a history of hypertension, 4) infected by the Omicron variant related to the recent outbreak in Shanghai. Patients were excluded if they had incomplete clinical data, including age, sex, vaccination status, and comorbidities. This study was approved by the Ethics Commission for Clinical Research of Zhongda Hospital, affiliated to Southeast University (approval number: 2022ZDSYLL170-P01). Informed consent was waived due to the nature of the study as a retrospective study. The study was conducted following the principles described in the Declaration of Helsinki, and the confidentiality of patients was guaranteed.
We divided the patients into two groups according to their vaccination status: the unvaccinated and vaccinated groups. The vaccinated group included patients who had received at least one dose of inactivated vaccine, while patients with no vaccination history were placed in the unvaccinated group. Patients in the vaccinated group were further grouped into three subgroups: partially vaccinated group, fully vaccinated group, and booster vaccinated group. The partially vaccinated group was defined as having one dose of the inactivated vaccine only, and fully vaccinated patients were referred to those who received two doses of the vaccine. The booster vaccinated group referred to patients who had already received three vaccine doses. We also analyzed patients into different groups based on age and gender.
Data collection
We collected health information from patients stored in the electronic medical record system. We gathered available clinical details, including age, sex, vaccination status, comorbidities, and nucleic acid test results. Comorbidities included diabetes mellitus, cardiovascular disease, chronic pulmonary disease (asthma, chronic obstructive pulmonary disease, or interstitial lung disease), chronic kidney disease, gastrointestinal/hepatic disease, autoimmune disease, and cancer.
Statistical analysis
Categorical variables were expressed as frequency and percentages (%) of the total and were compared between groups using the chi-square, Fisher’s exact tests, or Mann-Whitney U test as appropriate. Continuous variables were shown as the median (Quartile 25%-75%). The distribution of continuous variables was assessed using the Shapiro-Wilk test. We used the student’s t-test or Mann-Whitney U test as appropriate and compared continuous variables between different groups. The odds ratio (OR) and confidence interval (CI) from the univariate and multivariable logistic analysis was used to identify factors independently associated with vaccination status. All analyses were performed using SPSS 25.0 software (SPSS Inc, Chicago, IL). Two-tailed p values of < .05 were considered statistically significant.
Results
Clinical characteristics
4633 COVID-19 patients with hypertension met the inclusion criteria. Of these, 57 patients were excluded from the study due to incomplete clinical data. The study ultimately enrolled 4576 hypertensive patients with Omicron infection. shows the clinical characteristics of COVID-19 patients with hypertension. The median age of the patients was 58 years. Of these, 973 patients (21.3%) were 18–49 years old, 1565 (34.2%) were 50–59 years old, 1250 (27.3%) were 60–69 years old, and 788 (17.2%) were ≥70 years old. 2876 patients (62.8%) were male, and 1700 (37.2%) were female. Comorbidities other than hypertension were common in these patients. 999 patients (21.8%) had at least one comorbidity other than hypertension, including 825 patients (18.0%) with diabetes mellitus, 80 (1.7%) with cardiovascular disease, 54 (1.2%) with chronic pulmonary disease, 32 (0.7%) with gastrointestinal/hepatic disease, 25 (0.5%) with chronic kidney disease. 24 (0.5%) with autoimmune diseases, and 25 (0.5%) with cancer.
Table 1. Clinical characteristics of hypertensive COVID-19 patients infected by SARS-CoV-2 Omicron variant.
Comparison between the vaccinated group and unvaccinated group
Clinical data were compared according to whether or not the vaccine was administered. 1020 patients (22.3%) had no history of vaccination and were assigned to the unvaccinated group, and the vaccinated group consisted of 3556 patients (77.7%) who had received at least one dose of inactivated vaccine (vero cell). Compared with cases in the vaccinated group, patients were older [67(58,74) vs. 56(50,64), p < .001], and the proportion of women was higher (47.5% vs. 34.2%, p < .001) in the unvaccinated group. In addition, patients in the unvaccinated group were more likely to have another comorbidity(35.5% vs. 17.9%, p < .001). Increased frequency was noticed for other comorbidities such as diabetes mellitus (28.8% vs. 14.9%, p < .001), cardiovascular diseases (3.8% vs. 1.2%, p < .001), chronic pulmonary diseases (2.2% vs. 0.9%, p = .001), chronic kidney disease (1.3 vs. 0.3%, p < .001), and cancer (1.7% vs. 0.2%, p < .001) in unvaccinated patients.
By applying logistic regression analysis, we aimed to determine the factors associated with vaccination status in COVID-19 patients with hypertension. summarizes the results of the univariate analysis. Male (OR 1.738, 95% CI 1.509–2.001, p < .001), age (50–59 years vs.18–49 years) (OR 0.765, 95% CI 0.590–0.991, p = .043), age (60–69 years vs.18–49 years) (OR 0.297, 95% CI 0.232–0.379, p < .001), age (≥70 years vs.18–49 years) (OR 0.107, 95% CI 0.083–0.137, p < .001), diabetes mellitus (OR 0.433, 95% CI 0.368–0.511, p < .001), chronic pulmonary diseases (OR 0.412, 95% CI 0.238–0.712, p = .001), cardiovascular diseases (OR 0.293, 95% CI 0.188–0.457, p < .001), chronic kidney disease (OR 0.262, 95% CI 0.119–0.577, p = .001), and cancer (OR 0.133, 95% CI 0.057–0.309, p < .001) were associated with vaccinated status.
Figure 1. Univariate and multivariate analysis of factors associated with vaccination status in COVID-19 patients with hypertension.
Furthermore, multivariate logistic regression was then performed. Ultimately, male (OR 1.328, 95% CI 1.138–1.550, p < .001), age (60–69 years vs.18–49 years) (OR 0.348, 95% CI 0.270–0.448, p < .001), age (≥70 years vs.18–49 years) (OR 0.130, 95% CI 0.100–0.169, p < .001), diabetes mellitus (OR 0.553, 95% CI 0.463–0.661, p < .001), chronic pulmonary diseases (OR 0.474, 95% CI 0.260–0.863, p = .015), chronic kidney disease (OR 0.177, 95% CI 0.076–0.410, p < .001), and cancer (OR 0.225, 95% CI 0.094–0.535, p = .001) were associated with vaccinated status ().
Comparison between the fully vaccinated group and booster vaccinated group
Only 127 patients (2.8%) received one dose of the vaccine (partially vaccinated group), and 1371 patients (30.0%) got two doses (fully vaccinated group) (). 2058 patients (45.0%) received a third (booster) dose (booster vaccinated group) (). Compared with cases in the fully vaccinated group, patients were younger [55(49,61) vs. 59(50,66), p < .001], and the proportion of women was lower (30.1% vs. 40.3%, p < .001) in the booster vaccinated group. In comparison with the fully vaccinated group, the booster vaccinated group had a lower ratio of another comorbidity (15.4% vs. 21.1%, p < 0.001), which included diabetes mellitus (13.0% vs. 17.1%, p = .001), cardiovascular diseases (0.6% vs. 2.0%, p < .001) ().
Male (OR 1.572, 95% CI 1.362–1.814, p < .001), age (50–59 years vs.18–49 years) (OR 1.266, 95% CI 1.057–1.517, p = .011), age (60–69 years vs.18–49 years) (OR 0.642, 95% CI 0.530–0.778, p < .001), age (≥70 years vs.18–49 years) (OR 0.634, 95% CI 0.496–0.810, p < .001), diabetes mellitus (OR 0.724, 95% CI 0.598–0.875, p = .001), and cardiovascular diseases (OR 0.316, 95% CI 0.163–0.615, p = .001) were associated with booster vaccinated status in the univariate analysis().
Figure 2. Univariate and multivariate analysis of factors associated with booster vaccinated status in COVID-19 patients with hypertension.
In the multivariate analysis, male (OR 1.453, 95% CI 1.254–1.685, p < .001), age (50–59 years vs.18–49 years) (OR 1.318, 95% CI 1.098–1.581, p = .003) age (60–69 years vs.18–49 years) (OR 0.720, 95% CI 0.591–0.876, p = .001), age (≥70 years vs.18–49 years) (OR 0.746, 95% CI 0.579–0.961, p = .023), diabetes mellitus (OR 0.806, 95% CI 0.662–0.981, p < .031), and cardiovascular diseases (OR 0.429, 95% CI 0.218–0.846, p = .015) were associated with booster vaccinated status().
Factors associated with vaccination status in different age groups
Patients were further grouped into four age subgroups in more detailed analyses of the factors associated with vaccination status. In the multivariate analysis, only chronic kidney disease (OR 0.057, 95% CI 0.013–0.243, p < .001) was associated with vaccinated status in the age group of 18 to 49 (). In the age group of 50 to 59, male (OR 1.740, 95% CI 1.272–2.381, p = .001), diabetes mellitus (OR 0.363, 95% CI 0.252–0.524, p < .001), and chronic kidney disease (OR 0.192, 95% CI 0.041–0.906, p = .037) were associated with vaccinated status (). Diabetes mellitus (OR 0.568, 95% CI 0.427–0.755, p < .001), chronic pulmonary diseases (OR 0.214, 95% CI 0.073–0.629, p = .005), and cancer (OR 0.248, 95% CI 0.077–0.798, p = .019) were associated with vaccinated status in the age group of 60 to 69 (). In the ≥70 years age group, male (OR 1.354, 95% CI 1.018–1.799, p = .037) and diabetes mellitus (OR 0.721,95% CI 0.525–0.991, p = .044) were associated with vaccinated status ().
Figure 3. Multivariate analysis of factors associated with vaccination status in COVID-19 patients with hypertension in different age groups.
Factors associated with vaccination status in different gender groups
Moreover, we also analyzed patients in different groups based on gender. In the multivariate analysis, age (60–69 years vs.18–49 years) (OR 0.332, 95% CI 0.245–0.449, p < .001), age (≥70 years vs.18–49 years) (OR 0.141, 95% CI 0.102–0.195, p < .001), diabetes mellitus (OR 0.598, 95% CI 0.470–0.760, p < .001), chronic pulmonary diseases (OR 0.407, 95% CI 0.202–0.819, p = .012), cardiovascular diseases (OR 0.328, 95% CI 0.163–0.659, p = .002), and chronic kidney disease (OR 0.221, 95% CI 0.087–0.560, p = .001) were associated with vaccinated status in the male group().
Figure 4. Multivariate analysis of factors associated with vaccination status in COVID-19 patients with hypertension in different gender groups.
In the female group, age (50–59 years vs.18–49 years) (OR 0.603, 95% CI 0.367–0.992, p = .046), age (60–69 years vs.18–49 years) (OR 0.338, 95% CI 0.210–0.545, p < .001), age (≥70 years vs.18–49 years) (OR 0.108, 95% CI 0.067–0.175, p < .001), diabetes mellitus (OR 0.498,95% CI 0.381–0.650, p < .001), chronic kidney disease (OR 0.056, 95% CI 0.006–0.560, p = .014), and cancer (OR 0.155, 95% CI 0.053–0.455, p = .001) were associated with vaccinated status in the multivariate analysis ().
Discussion
The study ultimately included 4576 hypertensive patients with Omicron infection, while 1020 patients (22.3%) had no vaccination history, and 2058 patients (45.0%) received a booster dose. This vaccination rate is relatively low, considering the higher risk of infection in patients with chronic diseases. Undeniably, the low efficacy of current vaccines and the rapid mutation rate of viruses are preventing herd immunity from being achieved. Vaccination remains the most effective way to avoid COVID-19-related complications, including reducing the risk of progression to severe disease and death. Vaccination can also improve the quality of life.Citation26 Due to the massive and rapid epidemic of Omicron in China in 2022, herd resistance has been gained but maintained for a limited period. Challenges remain in the future after immunity has waned following infection. Moreover, anti-vaccine attitudes of previously infected individuals following a large-scale epidemic will continue to challenge the use of more effective vaccines in the future. We should focus on high-risk patients and provide them with immune protection.
There were significant gender differences in our study. Of the 4576 patients with hypertensive Omicron infection, 2876 patients (62.8%) were male, and 1700 (37.2%) were female. The reason for more males than females may be that hypertensive males have a higher level of social activity and are susceptible to Omicron infection. It was also found that male hypertensive patients had higher vaccination rates than females in this study, possibly because male patients had a higher risk of disease and were thus more willing to be vaccinated. Previous studies have also confirmed that gender affects COVID-19 vaccine acceptability, with men having higher vaccine acceptability and coverage.Citation27–30 Therefore, female hypertensive patients are a vulnerable group with low vaccine uptake. The age groups in which the effect of gender on vaccine coverage occurred in this study were 50–59 years and ≥70 years. Among hypertensive men with COVID-19 infection, vaccine coverage declined only when they were older than 60. In contrast, among women, a decline in vaccine coverage occurred when they reached the age of 50 years. There were also few gender differences in comorbidities other than hypertension that affected vaccine coverage. In the male group, diabetes mellitus, chronic pulmonary disease, cardiovascular disease, and chronic kidney disease were all associated with lower vaccination status. However, only diabetes mellitus, chronic kidney disease, and cancer were associated with inadequate vaccine coverage in the female group in our study.
Complications other than hypertension were common in our study. 999 patients (21.8%) had at least one comorbidity other than hypertension, including 825 patients (18.0%) with diabetes mellitus. Patients with multiple comorbidities were at greater risk of breakthrough infection or hospitalization than those without comorbidities.Citation31 Acceptance and coverage of the COVID-19 vaccine vary between patients with different chronic diseases. In this study, diabetes mellitus, chronic pulmonary disease, chronic kidney disease, and cancer were associated with inadequate vaccine coverage in COVID-19 patients with hypertension. Diabetes mellitus and cardiovascular disease are associated with lower coverage of booster vaccines in hypertensive patients with COVID-19 in multivariate analysis. The coexisting chronic condition was associated with COVID-19 vaccine uptake,Citation32 and poor health status was associated with lower vaccination rates.Citation30 In turn, COVID-19 reinfection and corresponding mortality would increase in patients with coexisting chronic conditions. Attitudinal barriers are related to the uptake of the COVID-19 vaccine in people with chronic diseases.Citation33 Interventions must address the attitudinal barriers of chronically ill patients who may be particularly concerned about conflicts between vaccines and ongoing medical care.Citation34 Measures are still needed to maintain immunity in patients with multiple chronic diseases.
Our study found that COVID-19 vaccine coverage began to decline among hypertensive patients beyond 60 years. While aging is a high-risk factor for COVID-19 patients to become seriously ill. Increasing vaccine uptake among older people is essential to effectively reduce the number of deaths and avoid overburdening the healthcare system.Citation35 Therefore, it is imperative to maintain lasting immunity in elderly patients with hypertension. Patients who refused the vaccine were concerned about its negative impact on their treatment.Citation36 The extent to which chronic diseases affect vaccine coverage varies by age group. Only chronic kidney disease was associated with vaccination rate status in 18 to 49 years. In the age group of 50 to 59, diabetes mellitus and chronic kidney disease were associated with reduced vaccine coverage status. Meanwhile, the influencing factors were diabetes mellitus, chronic pulmonary disease, and cancer in the age group of 60 to 69. In the age group ≥70 years, only diabetes mellitus was associated with lower vaccination rates.
The potential future burden of COVID-19 is determined by the level of susceptibility of the population to infection. Immune gene variations were related to the COVID-19 severe respiratory symptoms.Citation37 Whereas vaccine coverage and its corresponding efficacy and the level of protection provided by those previously infected assess susceptibility. The protective effect provided by those previously infected diminishes over several months, while individuals with mixed immunity have the highest degree and persistence of protection.Citation38,Citation39 Vaccine coverage in individuals with prior SARS-CoV-2 infection protects against Omicron-related hospitalization.Citation40 The benefits of vaccination for people who have been previously infected have been well documented.Citation14 Previous infection and booster vaccination may each work independently of each other. Although high primary vaccine and booster dose coverage have been achieved in the overall population, vaccine coverage still needs further improvement in the hypertensive patient population. In patients with multiple chronic diseases, vaccine safety concerns have a different impact on acceptability. The focus should be on specific groups to inform them of the benefits of COVID-19 vaccination and to address safety concerns.
This study has several limitations. As a retrospective study, psychological factors have not been studied. Furthermore, psychological factors are associated with the intention to uptake COVID-19 vaccination.Citation41–44 In addition, we have not evaluated other factors such as education, economic level, and place of residence. We did not explore the period from the last dose. This study also did not follow up with patients to observe subsequent reinfection.
Conclusion
The vaccine coverage rate, especially the booster vaccine, was low for hypertensive patients with COVID-19 infection. Females, increasing age, and coexisting chronic diseases were associated with more inadequate vaccine coverage in hypertensive COVID-19 patients. Targeted interventions are required to address the under-vaccination of diverse hypertensive populations.
Author contributions
Kongbo Zhu, Genshan Ma and Yingzi Huang were involved in the conception and design. Kongbo Zhu, Shaolei Ma, Hui Chen, Jianfeng Xie and Dan Huang were involved in the analysis and interpretation of the data. Kongbo Zhu, Genshan Ma and Yingzi Huang were involved in the drafting of the paper, revising it critically for intellectual content, and the final approval of the version to be published. All authors agree to be accountable for all aspects of the work.
Ethical approval
This study was approved by the Ethics Commission for Clinical Research of Zhongda Hospital, affiliated to Southeast University (approval number: 2022ZDSYLL170-P01). Informed consent was waived due to the nature of the study as a retrospective study. The study was conducted following the principles described in the Declaration of Helsinki, and the confidentiality of patients was guaranteed.
Acknowledgments
We thank the medical staff for their hard work at Lingang shelter hospital. Additionally, we want to thank the heads of Lingang shelter hospital for their support.
Disclosure statement
No potential conflict of interest was reported by the authors.
Additional information
Funding
References
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