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Factors associated with full COVID-19 vaccination among persons living with diabetes mellitus in Uganda–A cross-sectional study

BMC Public Health volume 24, Article number: 2422 (2024) Cite this article

Abstract

Background

Diabetes mellitus (DM) is associated with severe outcomes of coronavirus disease (COVID-19), including death. COVID-19 vaccination is crucial for preventing infection and severe disease in the general population, but most importantly, among high-risk populations such as persons with DM. However, while COVID-19 vaccination uptake in the general population is regularly tracked, information on vaccination behavior specific to persons with DM is scarce. This study aimed to identify factors associated with the uptake of full COVID-19 vaccination among persons living with DM at Kiruddu National Referral Hospital (KRH).

Methods

We employed a cross-sectional study design and administered a structured questionnaire on a systematically selected random sample of 340 people with DM attending Kiruddu National Referral Hospital from March 08 to May 25, 2023. We used a Modified Poisson Regression model to identify the factors associated with full COVID-19 vaccination and present adjusted prevalence ratios, along with their 95% confidence intervals. Full COVID-19 vaccination in this study was defined as having completed the last dose in the primary series of a COVID-19 vaccine.

Results

We administered the questionnaire to 340 participants, with 75% (255 of 340) being female. The mean age of the participants was 52 years (± 12 years) and their median duration with diabetes mellitus was 5 years (± 7.3 years). Overall, 195 out of 340 participants (57.35%, 95% CI: 52-63%) completed the last dose in the primary series of a COVID-19 vaccine. The likelihood of receiving full vaccination was higher when a health provider advised one to receive a vaccine (aPR = 1.91, 95% CI: 1.20–3.02), when one reported having a comorbidity (aPR = 1.26, 95% CI: 1.06–1.53), and when one had a strong perceived benefit of vaccination (aPR = 1.76, 95% CI: 1.23–2.53). However, having a strong perceived barrier to vaccination was negatively associated with the likelihood of being fully vaccinated (aPR = 0.71, 95% CI: 0.60–0.84).

Conclusion

The uptake of COVID-19 vaccines among persons with DM at KRH is low, with only 57% having a full COVID-19 vaccination status. This underscores the progress in meeting the WHO recommendation of having a 100% COVID-19 vaccination uptake among people with underlying health conditions, including diabetes mellitus. At the policy level, the Ugandan Ministry of Health (MoH) may implement a provider-initiated vaccination strategy where healthcare providers who attend to DM patients during their routine clinic visits initiate the idea of vaccinating, sensitize, and spearhead myth-bursting around COVID-19 vaccines.

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Background

COVID-19 remains a significant global health threat, with more than 9 million cases and 174,286 deaths attributable to the virus occurring in the African region [1]. In Uganda, the SARS-CoV-2 virus which causes COVID-19 has resulted in more than 170,000 cases and 3,600 deaths within the general population as of December 31, 2023 [1], exacerbating the strain on an already challenged healthcare system. Persons with underlying health conditions, such as diabetes mellitus (DM) face an amplified risk of severe outcomes from COVID-19 [2]. While over 463 million people are living with DM globally and yet this number is expected to increase to 700 million by 2045 [3], people with DM are particularly susceptible to severe complications from COVID-19 [4] and face an estimated twofold higher risk of death compared to those without DM [5,6,7,8]. This heightened risk of severe COVID-19 outcomes is associated with factors such as poor glycemic control and obesity [9, 10]. Given this heightened vulnerability, prioritizing persons with DM for vaccination is strongly recommended [11]. Moreover, the World Health Organization (WHO) has advocated for 100% vaccination uptake among all people with underlying health conditions [12] emphasizing the critical importance of vaccinating this high-risk cohort to mitigate the impact of COVID-19 on their health outcomes.

COVID-19 vaccination is the mainstay of prevention against infection in the general population, but, most importantly, among high-risk groups such as persons with DM. For instance, by the end of the first year of vaccination, COVID-19 vaccination had prevented 63% of global deaths [13]. In Uganda, the initiation of mass COVID-19 vaccination occurred in March 2021 with the deployment of 864,000 doses of the AstraZeneca vaccine. Subsequently, accelerated mass vaccination campaigns incorporated various vaccines, including Johnson & Johnson’s Janssen, Pfizer-BioNTech’s Pfizer, Inc., Oxford-AstraZeneca from Oxford University and AstraZeneca, and Sinopharm from China National Pharmaceutical Group Co., Ltd. and the Beijing Institute of Biological Products Co. [14]. The Ugandan MoH prioritized six high-risk groups at the launch of the first phase of mass COVID-19 vaccination, among which were persons with underlying health conditions aged below 50 years, estimated at 500,000 at the time [15]. Despite this prioritization, by November 21, 2022, a mere 10% of those with underlying health conditions had received a COVID-19 vaccine [16]. Unfortunately, specific data regarding the uptake of COVID-19 vaccination among persons with DM in Uganda remain unclear, highlighting a significant gap in the COVID-19 vaccination behavior among this particular high-risk subgroup.

The uptake of COVID-19 vaccination among persons with diabetes mellitus (DM), particularly in the sub-Saharan region, remains below optimal levels. Within the sub-Saharan region, only 6–14% of persons with DM have completed the primary series of a COVID-19 vaccine [17, 18]. In contrast, higher rates of full vaccination, approximately 25% and 55%, were observed among those with DM in China and Saudi Arabia, respectively, attributed to a higher perceived risk of infection, perceived safety of the vaccines, and higher income level [19,20,21]. This poor uptake among persons with DM is partly attributed to social-demographic factors and their perceptions regarding COVID-19 vaccines and the virus [17, 18, 20, 22,23,24]. Literature on the COVID-19 vaccination behavior among persons with DM is predominantly based on studies conducted in nations with greater access to COVID-19 vaccines, leaving a gap in understanding within low-income countries such as Uganda. Moreover, despite an estimated 10% uptake of COVID-19 vaccination among persons with comorbidities in Uganda [16], specific data regarding the full vaccination uptake among those with DM is scanty. Additionally, similar to many parts of the world, COVID-19 vaccination remains voluntary, placing the decision to be fully vaccinated solely on the individual. Given the high risk among persons with DM, the Ugandan Ministry of Health (MoH) and collaborating organizations must understand both their uptake of the vaccines and influencing factors to adapt vaccination sensitization campaigns for persons living with DM in Uganda. This study utilized Hochbaum and Rosenstock’s Health Belief Model (HBM) developed in 1952 to understand the vaccination behavior of persons living with DM at KRH. The HBM is a social behavior change model designed to explain and predict health behavior based on four major blocks: perceived risk, perceived severity, perceived benefits, and perceived barriers. The model also integrates the individual’s self-efficacy, that is, the self-belief in conducting the health behavior [25], and the cues to action – the triggers that prompt an individual to perform a health behavior that could either be internal or external [25, 26]. We set out to estimate the level of uptake of full COVID-19 vaccination among persons living with DM attending KRH and its correlates in Uganda.

Methods

Study design and setting

We used a cross-sectional study design to identify factors associated with receiving full COVID-19 vaccination among persons with DM attending the diabetes outpatient clinic of Kiruddu National Referral Hospital (KRH) from March 08 to May 25, 2023. KRH is located in Kiruddu on Buziga Hill in Makindye Division, Kampala district, Uganda. The hospital provides a range of clinical care services, including an outpatient diabetes care clinic that runs every Wednesday with an average clinic-day attendance of 200 adult clients. In addition to providing clinical care services, KRH serves as a teaching hospital for medical students at the Makerere University College of Health Sciences and provides an enabling environment for research.

Study population

The study population included all persons with a confirmed diagnosis of DM attending KRH for routine diabetic care from March 8 to May 25, 2023. We included clients aged 18 or more years who could speak Luganda or English, while clients with severe clinical or mental complications were excluded because they were potentially incapacitated from either providing written informed consent, or properly comprehending the interview questions. Luganda or English was part of the inclusion criteria because, whereas over 40 languages are spoken in Uganda, the study area was in Kampala, Central Uganda, where Luganda is the most spoken language. Therefore, the study tools were designed in English and Luganda, and administering the questionnaire in other native languages could have resulted in biased responses.

Sample size and sampling criteria

We used the Kish Leslie formula to calculate the sample size considering a categorical outcome for an infinite population [27]. Using the proportion of full COVID-19 vaccination among persons with DM (P) estimated at 27%, adopted from the uptake of full vaccination in the general population as of August 30, 2022, a Z value of 1.96 corresponding to a 95% confidence interval and \(\:\delta\:\) of 0.05, the estimated sample size for this study was 303. After including a 10% non-response rate adopted from a similar study [23], the minimum sample size for this study was 334. The estimated value of (P) used for this study’s sample size calculation was adopted from the general population instead of persons living with DM because the alternative estimates of P among persons with DM that were available in literature were either not representative of the public health context of Uganda, or were potentially biased because of how they were measured.

We used a systematic sampling technique to select 340 participants at an interval of 14 clients. The diabetes clinic of KRH runs 4 times a month (every Wednesday), and had approximately 4500 outpatient clients who had been actively attending it in the prior 12 months by the start of this study. Assuming that a person with diabetes was expected to see a physician at least once in 3 months [28], we estimated the average number of clinic visits per client at approximately 375 visits (4500/12) – where 12 here represents the 12 clinic days in three months. With an estimated sample size of 334 participants for this study, a maximum of 28 clients (334/12) were recruited on each clinic day at an interval of 14 clients (375/28). The participants were enrolled over 3 months on 12 clinic days. The first potential participant was selected randomly, using a list of the first 14 clients leaving the physician’s room as the sampling frame. Thereafter, an internet-based Research Randomizer tool (found at https://www.randomizer.org/) was used to sample the first participant and then every 14th potential participant leaving the consultation room was approached for the study.

Study variables and measurements

The outcome variable in this study was the uptake of full COVID-19 vaccination, and it was a binary variable with the categories; fully vaccinated and unvaccinated/ partially vaccinated. In this study, full vaccination was defined as having received the last dose in the primary series of a particular COVID-19 vaccine, while being unvaccinated/ partially vaccinated was defined as having received either no dose at all or fewer than the minimum doses (depending on the type of vaccine) in the primary series of a particular vaccine. Full vaccination was verified using the MOH’s online vaccination certification portal at https://epivac.health.go.ug/certificates/#/ or a vaccination card/ certificate.

The independent variables included demographic characteristics such as (1) age (in complete years), (2) gender (male/female), (3) highest educational level, (4) marital status, and (5) occupation. Other independent variables included (6) duration of DM (in complete months), (7) comorbidity with DM (Yes/No), (8) self-efficacy to vaccinate, (9) information from the media (yes/no), (10) vaccination status of close friends or family (yes/no), 11) prior diagnosis of COVID-19 (yes/no), 12) prior diagnosis of COVID-19 of close friends and family (yes/no) and 13) advice from a healthcare provider (yes/no). More explanatory variables were individual perceptions, that is; 14) perceived susceptibility, 15) perceived severity, 16) perceived benefit, and 17) perceived barrier to full COVID-19 vaccination.

We adopted questions assessing perceived susceptibility, perceived severity, perceived benefit, perceived barrier to full COVID-19 vaccination, and self-efficacy of receiving a full vaccination from similar studies [23, 29] and adapted them for this study. These variables were measured on a Likert scale of strongly disagree, disagree, agree, and strongly agree using the following questions: Perceived severity – “COVID-19 is a severe disease”, Perceived benefit – “Having a full vaccination reduces the risk of infection” and “Having a full vaccination reduces the risk of transmission to other people”, Perceived barrier – “As a person with diabetes, I worry about the safety of vaccination” and “I am worried about the side effects of vaccination”. The remaining part of the questionnaire (Annex 1) was developed for this study.

Data collection and management

We conducted face-to-face interviews to collect data using a structured questionnaire designed in Kobo toolbox, a secure open-source platform founded by Phuong Pham and Patrick Vinck (2005). In the questionnaire, we included data checks such as a maximum or a minimum digit for numerical questions, and compulsory responses for certain questions to minimize missing data and typing errors by the Research Assistant. The Research Assistant uploaded the completed questionnaires to a secure Kobo server at the end of each field day.

After the data were collected, the corresponding author retrieved the complete dataset from the Kobo server and imported it into Microsoft Excel (Microsoft Corporation, Redmond, Washington, USA) for data cleaning and preparation for analysis. The data were further cleaned in STATA version 14.0 (StataCorp, College Station, TX, USA) using summary statistics such as the minimum and maximum values, frequency counts, and valid percentages to identify entry errors. For missing information, we used litwise deletion as it minimizes the potential bias of the parameters [30].

Statistical analysis

We analyzed the data in STATA version 14 (StataCorp, College Station, TX, USA). We summarized the numerical variables using measures of central tendency, that is, the mean with its standard deviation for normally distributed variables, and the median along with its interquartile range for non-normally distributed variables. Likewise, we used percentages and frequencies for the categorical variables. Furthermore, we used the modified Poisson regression model with robust variances for analysis at both the bivariable and multivariable levels. The modified Poisson technique with robust variances was used instead of logistic regression, a more popular technique for a binary outcome because the prevalence of the outcome in this study was high. Where the prevalence of the outcome is not rare, that is, above 10% [31], the odds ratios produced from a logistic regression model overestimate the effects of the covariates on the outcome [32]. However, the prevalence ratios produced from the modified Poisson regression model are a better alternative for approximating the risk ratio (Barros & Hirakata, 2003).

At the bivariable level, we considered variables associated with receiving a full COVID-19 vaccination with p-values less than 0.2 for inclusion in the multivariable analysis. These variables were tested for both minimum collinearity and overdispersion and neither was observed. We then used stepwise elimination to select variables suitable for the final model, and only variables with p < 0.1 were considered.

Results

Study subjects

From March 8, 2023, to May 25, 2023, an estimated 2371 clients attended the diabetes outpatient clinic of KRH, and of those, 361 clients were approached for the study. Of the 361 clients, 21 (5.8%) were not included in the study and of these 21 clients, 6 did not meet the study’s eligibility criteria (2 had a mental disability while 4 could not speak English or Luganda), while 15 declined to participate in the study. A total of 340 clients consented to and participated in the study, as shown below (Fig. 1).

Fig. 1
figure 1

Flow diagram showing the recruitment of clients into the study

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Demographic characteristics of the participants

A total of 340 clients with DM participated in the study. Of the 340, 255 (75%) participants were female, 178 (52.35%) had a primary level of education and 163 (47.94%) reported being married or in a steady relationship. The mean age of the study participants was 52 years (± 8 years) and they had spent a median duration of 5 years (IQR = 7.3 years) with DM. In addition to DM, 111 of the 340 participants (56.35%) had hypertension (Table 1).

Table 1 Socio-demographic characteristics of the study participants (n = 340)
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Perceptions of persons with DM of full COVID-19 infection and COVID-19 vaccination

Most of the participants reported being at risk of contracting COVID-19 (85%), that COVID-19 is severe (93.5%), and that vaccination was of benefit to them (73.4%). However, the perceived barrier to full vaccination was greater for most of the participants (61.5%) (Table 2).

Table 2 Perceptions of full COVID-19 and COVID-19 vaccination among people with DM
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The uptake of full COVID-19 vaccination among persons living with DM

The uptake of full COVID-19 vaccination among persons living with DM was 57.35% (n = 195) while 7.9% (n = 27) had incomplete vaccination. However, 34.7% (n = 118) were not vaccinated at all. The most common vaccine combination received among those who had at least one dose was Oxford-AstraZeneca alone (36.94%) (Table 3).

Table 3 Uptake of COVID-19 vaccination among persons living with diabetes mellitus
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Factors associated with full COVID-19 vaccination among persons living with DM

Four factors were associated with the likelihood of being fully vaccinated against COVID-19 (Table 4). These included: (1) the presence of comorbidity, (2) strong perceived benefit, (3) advice from a health provider, and (4) a strong perceived barrier to getting fully vaccinated.

Clients who reported having been advised to get vaccinated by a health provider were 91% more likely to get fully vaccinated than those who were never advised by a health provider to get vaccinated (aPR = 1.91, 95% CI: 1.2–3.02). Similarly, clients who reported at least one comorbidity with DM were 26% more likely to be fully vaccinated than those who did not have any comorbidity (aPR = 1.26, 95% CI: 1.06–1.53). Clients who strongly perceived that full vaccination was beneficial were 76% more likely to be fully vaccinated than those who weakly perceived that full vaccination was beneficial (aPR = 1.76, 95% CI: 1.23–2.53). Conversely, clients found to have a strong perceived barrier to full vaccination were 29% less likely to be fully vaccinated than those with a weak perceived barrier to full vaccination (aPR = 0.71, 95% CI: 0.6–0.84).

Table 4 Analytical table of the factors associated with full COVID-19 vaccination
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Discussion

Overall, while approximately 65% of persons living with DM received at least one dose of a COVID-19 vaccine, only 57.3% had completed the final dose in the primary series of any COVID-19 vaccine. This highlights a significant challenge for the Ugandan Ministry of Health (MoH) in achieving the WHO-recommended 100% vaccination uptake among people with underlying health conditions [33]. However, the prevalence of full vaccination found in this study was over four times higher than that found in a similar cross-sectional study conducted among persons with DM in South Sudan [24] and over eight times greater than that found in another web-based survey conducted in sub-Saharan Africa [17]. The sharp differences may be attributed to the extensive sensitization campaigns on COVID-19 vaccination that have been conducted over time, especially in the Eastern and Central regions of Uganda [34].

We found that having a comorbidity with DM increased the likelihood of being fully vaccinated by 26% compared to not having any comorbidities. This finding is consistent with prior cross-sectional studies conducted among persons with DM in China that showed that patients with DM who had other chronic illnesses, such as hypertension, were more likely to be vaccinated against COVID-19 [20, 35]. Having a comorbidity potentially increases the perceived risk of severe COVID-19 outcomes among people with DM, making them less hesitant to accept COVID-19 vaccination [20, 36]. However, interestingly, this study revealed that more participants with a strongly perceived severity of COVID-19 were not fully vaccinated than were those with a weakly perceived severity of COVID-19 infection. This finding supports the notion that perceived severity is less likely to predict health behavior [26].

This study also found that a strong perceived benefit from full vaccination was associated with a greater likelihood of receiving full vaccination. Similarly, a Health Belief Model-backed study found that the belief that vaccination reduces the risk of infection increases the likelihood of vaccination among persons living with DM by over three times [22]. Conversely, we found that having a strong perceived barrier to full vaccination reduces the likelihood of full vaccination among persons with DM by 29%. This finding is consistent with other cross-sectional studies conducted in sub-Saharan Africa that showed that concerns about vaccine safety and side effects discouraged people living with DM from accepting the COVID-19 vaccines and were behind their low uptake of the vaccines [17, 18]. Our findings are also consistent with a meta-analysis on COVID-19 vaccination hesitancy among persons living with diabetes, which found that the primary reason for their vaccine hesitancy was their concern about the safety of COVID-19 vaccines [37].

Furthermore, we found that nine in every ten people with DM who received advice from a health worker were more likely to be fully vaccinated. This may be due to the ability of health professionals to explain the pros of COVID-19 vaccination and clear misconceptions to help patients make informed choices. Our findings concur with a recent survey on the COVID-19 vaccine uptake in the adult population of Uganda which revealed that having a health worker as a source of COVID-19-related information was positively associated with one’s likelihood of getting vaccinated against COVID-19 [38].

Interestingly, this study did not find a significant association between the perceived severity of COVID-19 infection among persons with DM and their likelihood of receiving full vaccination. This contradicts some literature on the vaccination behavior of persons with DM in China [20, 39], probably due to the different patterns of the pandemic between Uganda and China, with fewer reported COVID-19 cases and deaths in Uganda than in Eastern Asia [1].

The main strength of our study was in the objectivity of assessing full COVID-19 vaccination status. In this study, participants’ COVID-19 vaccination status was digitally verified through the MoH’s online vaccination certification portal at https://epivac.health.go.ug/certificates/#/ or through a vaccination card/certificate, which greatly minimized social desirability bias. However, the main limitation of this study was that it was overtaken by events as the dynamics of the COVID-19 pandemic in Uganda changed rapidly, potentially rendering the current perceptions of the virus and vaccination among persons living with DM inadequate at predicting their likelihood of receiving a full COVID-19 vaccination. Second, the study was potentially affected by a small degree of social desirability bias since the interviews were conducted in a hospital setting, potentially affecting the honesty of the responses during the interviews. However, we minimized this by constantly reminding participants that their responses were entirely for research purposes. Lastly, we only sampled from the DM outpatient clinic of KRH due to time and other resource constraints, and therefore, our findings may not be generalizable to other regions of the country.

Conclusions

The uptake of full vaccination among persons with diabetes mellitus in Uganda remains low despite the accelerated mass vaccination campaigns. Approximately 43% of persons living with diabetes mellitus who attend the KRH diabetic clinic have either not received a single dose of any COVID-19 vaccine or have an incomplete vaccination. This low uptake justifies the need to prioritize persons living with DM in the ongoing vaccination campaigns in the country. Second, both positive and negative perceptions of full COVID-19 vaccination and the vaccines held by persons living with DM play a significant role in their decision to get fully vaccinated. Individuals who have a negative perception of full vaccination are less likely to accept it, whereas positive perceptions are likely to motivate them to receive full vaccination. Similarly, having comorbidity of diabetes mellitus with illnesses such as hypertension increases the likelihood of full COVID-19 vaccination among persons living with DM. Last but not least, receiving pro-vaccination advice from a healthcare provider is a crucial cue to action in the decision to get a full COVID-19 vaccination among persons living with DM.

To boost the uptake of full COVID-19 vaccination among persons with diabetes mellitus in Uganda, the Ugandan Ministry of Health (MoH) may utilize the neurology outpatient clinic days across public hospitals and health centers at all levels to target persons with DM who report for their routine physician assessments and medication refills with COVID-19 vaccination and sensitization. Additionally, the Ministry of Health may implement a provider-initiated vaccination strategy where healthcare providers who attend to patients with DM during their routine clinic visits initiate the idea of vaccinating. They can then sensitize and spearhead myth-busting around COVID-19 vaccines. The Ministry may also collaborate with NGOs that work with people with DM, such as the Uganda Diabetes Association (UDA), to utilize the latter’s resources in facilitating COVID-19 vaccine sensitization among people with DM. Last but not least, clinicians in public health facilities may identify and utilize persons with DM as peer leaders in COVID-19 vaccination and sensitization campaigns to boost the self-efficacy of receiving a COVID-19 vaccine among people with DM.

Data availability

The data used in this study will be available upon reasonable request to the corresponding author.

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Acknowledgements

We acknowledge the administration and clinical staff of KRH for providing a suitable environment for this study. We are also grateful to Ms. Rose Naigino and Ms. Hadija Nalubwama for their mentorship. Lastly, we are thankful to our Research Assistant, Ms. Viola Nakasumba, for her commitment to completing interviews with all the eligible participants.

Funding

No external financial assistance was received to conduct this study.

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Authors and Affiliations

  1. Department of Epidemiology and Biostatistics, School of Public Health, Makerere University, Kampala, Uganda

    Umar Senoga & David Guwatudde

  2. Department of Disease Control and Environmental Health, School of Public Health, Makerere University, Kampala, Uganda

    John Bosco Isunju

  3. Clinical Epidemiology Unit, School of Medicine, Makerere University College of Health Sciences, Kampala, Uganda

    Kevin Ouma Ojiambo

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  1. Umar Senoga
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  2. David Guwatudde
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Contributions

U.S conceived and drafted the idea, and also conducted the statistical analyses. DG, JBI, and KOO guided the refinement of the manuscript to meet acceptable scientific standards.

Corresponding author

Correspondence to Umar Senoga.

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Ethics approval and consent to participate

This study received approval from the Makerere University School of Public Health Research and Ethics Committee (Ref No. Mak-SPHREC-2023-147) and the administration of Kiruddu Referral Hospital. The study participants provided written informed consent while the illiterate participants were represented by an impartial witness who confirmed that the illiterate participant understood the study information and voluntarily agreed to participate in the study before the study interviews were conducted. The study interviews were only conducted after the participants received the intended service for their clinic visit.

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Not applicable.

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The authors declare no competing interests.

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Senoga, U., Guwatudde, D., Isunju, J.B. et al. Factors associated with full COVID-19 vaccination among persons living with diabetes mellitus in Uganda–A cross-sectional study. BMC Public Health 24, 2422 (2024). https://doi.org/10.1186/s12889-024-19869-w

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BMC Public Health

ISSN: 1471-2458

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