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An assessment of excess mortality during the COVID-19 pandemic, a retrospective post-mortem surveillance in 12 districts – Zambia, 2020–2022
BMC Public Health volume 24, Article number: 2625 (2024)
Abstract
Background
The number of COVID-19 deaths reported in Zambia (N = 4069) is most likely an underestimate due to limited testing, incomplete death registration and inability to account for indirect deaths due to socioeconomic disruption during the pandemic. We sought to assess excess mortality during the COVID-19 pandemic in Zambia.
Methods
We conducted a retrospective analysis of monthly-death-counts (2017–2022) and individual-daily-deaths (2020–2022) of all reported health facility and community deaths at district referral health facility mortuaries in 12 districts in Zambia. We defined COVID-19 wave periods based on a sustained nationally reported SARS-CoV-2 test positivity of greater than 5%. Excess mortality was calculated as the difference between observed monthly death counts during the pandemic (2020–2022) and the median monthly death counts from the pre-pandemic period (2017–2019), which served as the expected number of deaths. This calculation was conducted using a Microsoft Excel-based tool. We compared median daily death counts, median age at death, and the proportion of deaths by place of death (health facility vs. community) by wave period using the Mann-Whitney-U test and chi-square test respectively in R.
Results
A total of 112,768 deaths were reported in the 12 districts between 2020 and 2022, of which 17,111 (15.2%) were excess. Wave periods had higher median daily death counts than non-wave periods (median [IQR], 107 [95–126] versus 96 [85–107], p < 0.001). The median age at death during wave periods was older than non-wave periods (44.0 [25.0–67.0] versus 41.0 [22.0–63.0] years, p < 0.001). Approximately half of all reported deaths occurred in the community, with an even greater proportion during wave periods (50.6% versus 53.1%, p < 0.001), respectively.
Conclusion
There was excess mortality during the COVID-19 pandemic in Zambia, with more deaths occurring within the community during wave periods. This analysis suggests more COVID-19 deaths likely occurred in Zambia than suggested by officially reported numbers. Mortality surveillance can provide important information to monitor population health and inform public health programming during pandemics.
Background
Since the first cases of SARS-CoV-2 were reported in Zambia in March 2020 through to October 12, 2023, 349,287 cases and 4,069 COVID-19-related deaths were reported [1]. During this period, several phylogenetically distinct strains of SARS-CoV-2 were identified in Zambia, each associated with varying case fatality rates across different wave periods [2,3,4,5].
The number of cases and deaths reported in Zambia likely underestimates the true impact of the pandemic. A nationwide SARS-CoV-2 prevalence survey, using nasal specimens for PCR testing, revealed that for every reported SARS-CoV-2 infection in Zambia, approximately 92 infections went unreported [6]. A systematic postmortem prevalence study among deaths that occurred at a tertiary hospital in Lusaka showed a high SARS-CoV-2 PCR prevalence among deceased persons from January 2021 to June 2021, with greater per cent positivity during peak COVID-19 transmission periods [7]. However, it should be noted that while SARS-CoV-2 was detected among the deceased individuals in this study, it was not determined whether the virus directly caused their deaths or if its presence was merely incidental. Among those with a positive SARS-CoV-2 diagnosis postmortem, only a minority had a COVID-19 diagnosis antemortem. As such, officially reported COVID-19 deaths in Zambia may underestimate the total number of COVID-19 deaths that occurred during the pandemic.
During a public health emergency such as the COVID-19 pandemic, monitoring all-cause mortality trends may help assess the severity and impact of the emergency on the population affected [8]. Deaths among confirmed COVID-19 patients do not capture the full extent of the COVID-19 burden. In contrast, deaths from all causes can be used to estimate excess mortality and provide a more complete picture of the impact of the COVID-19 pandemic [9, 10]. For many countries, reporting statistics on COVID-19 mortality has been a challenge due to variations in access to testing, differential diagnostic capacity, the inconsistent and sub-optimal certification of COVID-19 as the immediate cause of death, and the nonspecific clinical presentation of COVID-19 (including in fatal cases) [11]. Additionally, the pandemic led to an increase in deaths due to other causes, because of disruptions to routine health services and loss of livelihoods due to the stringent non-pharmacological interventions put in place to mitigate the pandemic [12]. Therefore, the World Health Organization (WHO) recommends the surveillance of confirmed COVID-19 mortality and all-cause mortality during the COVID-19 pandemic [13].
A study of mortality trends among community deaths at the University Teaching Hospital (UTH) in Lusaka from April 2020 to December 2020 showed 1,139 excess deaths from all causes during the study period compared to the pre-pandemic baseline (2017–2019) [14]. Whilst excess mortality during the COVID-19 pandemic has been established in Lusaka [14, 15], the country’s predominantly urban capital, it remains unclear whether other regions within the country with different socio-demographic factors had comparable or worse outcomes. We, therefore, conducted this study to assess excess mortality across 12 districts of Zambia during the COVID-19 pandemic.
Methods
We conducted a mixed methods retrospective analysis of mortality records in Zambia by triangulating data from two different sources (health facility and community death mortuary records) between January 2017 and December 2022. These records were obtained from the mortuaries of the main district referral health facilities in the selected districts. Typically, the most life-threatening medical cases are referred to these referral health facilities from other health facilities within the district and deaths occurring within the communities outside health facilities are brought to these district hospital morgues.
We purposively selected 12 districts of Zambia (Chingola, Kabwe, Kitwe, Livingstone, Luanshya, Lusaka, Kasama, Mansa, Chipata, Mongu, Solwezi and Ndola) primarily based on the known availability of mortuary records over the study period, to ensure an adequate mix of urban and rural districts and to ensure adequate geographic representation from across the country. Combined, the selected districts are home to an estimated 6,882,437 (37.4% of the total projected 2021 population) Zambians [16].
Monthly counts of all health facility deaths and all reported community deaths between 2017 and 2019 were collected to estimate baseline all-cause mortality before the COVID-19 pandemic and monthly counts from 2020 to 2022 to estimate excess deaths during the COVID-19 pandemic. A COVID-19 wave period was defined as a sustained increase in the SARS-CoV-2 national test positivity of greater than five per cent, and between January 2020 and December 2022 days were dichotomized as wave or non-wave days. Additionally, wave days were further classified as the first wave (1 Jun 2020 to 1 Oct 2020), second wave (3rd Jan 2021 to 17th March 2021), third wave (29th May 2021 to 20th Aug 2021), fourth wave (12th Dec 2021 to 9th May 2022) and fifth wave (24th Dec 2022 to 31st Dec 2022), all other dates during the study period were non-wave days. Additionally, from January 2020 through to December 2022, daily individual records of all inpatient deaths and all reported community deaths by age and sex disaggregation were collected to analyse changes in the sex and age distribution of deaths between COVID-19 wave periods and non-COVID-19 wave periods. A categorical variable, age group, was recoded from the continuous variable age.
For the all-cause excess mortality analysis, the district-specific monthly counts of all deaths from 2017 to 2019 were used as the COVID-19 pre-pandemic baseline to compare with the period of the COVID-19 pandemic (2020–2022) using a Microsoft Excel-based tool developed by Resolve to Save Lives/Prevent Epidemics to calculate monthly medians and 95% confidence intervals for historic deaths [17]. This tool is recommended by an expert panel for Rapid Mortality Surveillance during COVID-19 [18]. We quantified the availability of death records by calculating the percentage of months with complete monthly count information over the total number of months within the study period (January 2017 to December 2022) for each district. To address missing monthly death counts at the district level, mean imputation was applied to the districts with missing data (Ndola, Solwezi, and Livingstone), as the monthly death counts at the district level were normally distributed.
Excess mortality was defined as the difference between the all-cause pandemic monthly death counts (2020–2022) (Observed events) and the median pre-pandemic all-cause monthly death counts and the 95% confidence interval (2017–2019) in the 12 districts (The previous step yields baseline mortality and a “normal” range of variability around that baseline). The 95% confidence interval for the median historical monthly count was calculated separately for each month using the sample standard deviations. Excess mortality was present if the observed count was greater than the 95% confidence limit of the historic number of deaths. District-specific excess mortality was calculated separately among community deaths and health facility deaths and then summed to get monthly and yearly excess mortality counts for each district.
To estimate overall excess mortality in Zambia, we assumed that there was sufficient heterogeneity in factors contributing to excess deaths in the 12 selected districts to be representative of the entire population of Zambia and that the excess mortality rate was only a function of the population. Based on these assumptions, we extrapolated the median excess mortality rate from the 12 districts to the entire country to estimate the total excess deaths in Zambia. We then compared this national estimate of excess deaths to the number of officially reported COVID-19 deaths in Zambia to calculate the ratio of reported COVID-19 deaths to excess deaths during the pandemic.
The individual-level death information from 2020 to 2022 was used to calculate daily death counts among community deaths and health facility deaths. Decedents with missing age or sex variables were dropped from subsequent analyses involving age or sex variables but included in the time series graphs of daily deaths and daily death count analysis. Shapiro-Wilk test was used to test the normality assumption for the distribution of the daily death counts and age variables. All reported daily deaths were plotted as a 14-day rolling average time series disaggregated by place of death (community versus facility), district and age groups. To detect any difference in the median number of reported daily deaths between wave periods and non-wave period days, we used the Mann-Whitney u test. We then used the Kruskal-Wallis rank sum test to determine whether there was a statistically significant difference between the median daily number of deaths across the six identified wave periods (non-wave period, first wave, second wave, third wave, fourth wave, fifth wave). To identify which median daily death counts varied significantly by wave period, pairwise comparisons of median daily death count by wave period were conducted using the Wilcoxon rank sum test with continuity correction. The Benjamini & Hochberg p-value adjustment method was employed for multiple comparisons.
Furthermore, we compared disparities in the distribution of the median age at death, the proportion of individuals above 65 at the time of death, as well as sex, place of death (facility or community), and district of death between wave periods and non-wave periods. These comparisons were conducted using the Wilcoxon rank sum test for median age and Pearson’s Chi-squared test for categorical variables. All statistical analyses were performed using R version 4.2.1 statistical software.
Results
Between 2017 and 2022, there were 217 140 deaths reported in the 12 districts (range 32786 [2018] to 41613 [2021]) (Fig. 1). In the baseline period (2017–2019), October had the highest average death count (3071.3, 95% CI: 2984.8-3157.8) while May had one of the lowest (2710.0, 95% CI: 2528.1-2891.9) (Table 1).
Districts contributed from 2.4% (Mongu) to 41.0% (Lusaka) of the reported deaths. A total of 112,768 deaths were reported in the 12 districts between 2020 and 2022 of these 17,111 (15.2%) were excess (Fig. 1). The median district excess mortality rate was 237.5 (Interquartile range (IQR) [170.5-282.5]) per 100,000 population (Table 2). There was district-by-district variation in the number of excess deaths with the highest excess deaths reported in Chingola (449.5 per 100,000 population) and the lowest excess deaths reported in Mongu (101.1 per 100,000 population) (Fig. 2; Table 2). Most excess deaths were observed in 2021 (n = 8992, 52.6%). By extrapolation from these 12 districts, we estimate the median excess deaths across all three years of the COVID-19 pandemic in Zambia to be 43,701 (IQR, 31372-51,982). Compared to officially reported COVID-19 deaths [1], for every reported COVID-19 death, there was a median of 11 (IQR, 8–13) excess deaths during the COVID-19 pandemic in Zambia.
We analysed 112,768 individual death records across the 12 districts between January 2020 to December 2022. Overall, only 2.4% of all deaths had a variable missing (age or sex). Over the entire study period, on average, there were more deaths per day during wave periods than during non-wave periods (median [IQR]: 107 [95–126] versus, 96 [85–107]) respectively, < 0.001) (Table 3). The second (median [IQR]: 124 [113–138]), third (median IQR: 140 [116–168]) and fourth (median [IQR]: 102 [92–109]) waves had more deaths per day than non-wave periods (median [IQR]: 96 [85–107], p < 0.001), but no difference was seen between the first and fifth waves (Fig. 3; Table 4).
During wave periods, there was an increase in the daily number of deaths across all districts with a return to baseline after the wave periods (Fig. 4). When disaggregated by place of death, more deaths during the third wave were reported as having occurred within the community than in health facilities (Fig. 5). During non-wave periods approximately half of all reported deaths across all 12 districts occurred in the community (50.6%), and this proportion increased during wave periods (53.1%, p < 0.001) (Table 3). There was district-by-district variation in the baseline number of deaths per day, with Lusaka accounting for the highest proportion of all deaths (33.49%) and Mongu the least (2.96%). During wave periods, there was an increase in the proportion of all deaths from Lusaka (45.39%, p < 0.001) (Table 3).
In both wave and non-wave periods, more males died (58.7%, non-wave period versus 58.6%), However, the difference in proportions of men who died between the two periods was not statistically significant (p = 0.860). There was an increase in the median age at death during wave periods with a return to baseline median age at death after the wave period (41.0 years, IQR [22.0–63.0] versus 44.0 years, IQR [25.0–67.0], p < 0.001) (Table 3, supplementary Figs. 1 and 2). There was a corresponding increase in the proportion of individuals aged 65 and over who died during wave periods than those that died during non-wave periods (12886 [23.4%] non-wave period versus 11721 [27.7%] wave periods, p < 0.001) (Table 3, supplementary Fig. 1). When the time series of daily deaths was plotted by age group, the most noticeable change from baseline rates was in the 60 and over age group, which showed an increased number of deaths in this age category across the first, second, third and fourth waves (Fig. 6).
Discussion
There was excess mortality in all 12 districts included in the study between January 2020-December 2022, with the most excess deaths (52.6%) in 2021. These results suggest that the impact of the COVID-19 pandemic in Zambia was more widespread than official statistics indicate, and not only restricted to urban centres such as Lusaka [7, 15, 19, 20]. Similar findings of excess mortality in other sub-Saharan countries during the COVID-19 pandemic have been observed [21, 22]. Globally, the World Health Organisation estimates excess mortality is 2.74 times higher than reported COVID-19 deaths [22].
Modelled estimates of excess mortality during the COVID-19 pandemic in Zambia vary widely (74.3 credible interval (CI) [2.5-147.6] [23] vs. 228.2 [165.9-322.8] per 100,000 population [24]). Due to the unavailability of publicly available population-level mortality data, these current estimates of excess mortality in Zambia used statistical models to directly predict excess mortality for Zambia [24] or used mathematical models to generate historical and current mortality data and then calculated the excess mortality rate [23].
Our national estimate of the excess mortality rate (median 237.5 [(IQR)170.5-282.5] per 100,000 population), which lies within the range of modelled estimates for Zambia, is most likely an underestimate as not all deaths that occur within communities are reported at health facilities, and therefore were not included in this analysis. Our study demonstrates the value of applying mortality surveillance to understand the impact of a major public health event. If done in real-time, it could have also helped inform public health messaging and policymaking in response to the COVID-19 pandemic in Zambia. Further studies need to be conducted to understand the characteristics and explore surveillance strategies to detect and report these otherwise undocumented community deaths.
The observed variation in excess mortality rates across districts may be attributed to district-specific differences in geospatial factors influencing COVID-19 transmission dynamics, variations in healthcare quality and its utilization by the community, and the proportion of deaths occurring within the community that are reported to health facilities. Consequently, there is a degree of underreporting of community deaths at health facilities, the extent of which is unknown but tends to be higher in rural areas compared to urban areas. Evidence suggests that rural-urban residence significantly impacts the location of deaths in Zambia [25]. Additionally, differences in geographical factors between different regions have been shown to affect the spread of COVID-19 [26, 27]. Further studies are required to identify these factors and their impact on the spread of COVID-19 in Zambia.
Most of the observed excess deaths were likely due to COVID-19 or due to the socioeconomic disruption due to the pandemic. We observed an increase in the daily number of deaths during COVID-19 wave periods compared to non-COVID-19 wave periods. To our knowledge, there were no other reported widespread public health emergencies during the study period that could explain the abrupt increase in the number of deaths during the specific wave periods and across all 12 districts almost simultaneously [1]. Additionally, when we analysed the different wave periods, we noted that the relative increase in daily deaths during wave periods was associated with the relative case fatality of the predominant strain of SARS-CoV-2 associated with that wave. The predominant strain during Zambia’s third wave, which had the highest median daily death count, was the delta variant, a finding consistent with numerous other countries [7, 19, 28]. Further, after an increase in the daily number of deaths during a COVID-19 wave period, we observed a return to baseline pre-pandemic mortality rates between waves and this was consistent across all 12 districts visited and across the different age groups.
COVID-19 mortality has been shown to disproportionately affect the elderly [29,30,31,32]. We observed an increase in the overall median age at death (44 years vs. 41 years, p < 0.001) and in the proportion of deceased persons aged 65 years and older (27.7 per cent vs. 23.4 per cent, p < 0.001) during COVID-19 wave periods with a return to baseline between wave periods respectively. However, the exact proportion of these excess deaths that were directly attributable to COVID-19 remains unknown because of limitations in antemortem and postmortem SARS-CoV-2 testing and limited death registration and certification across the country.
There were more community deaths than facility deaths in both wave periods and non-wave periods. Community deaths increased during wave periods, suggesting potential gaps in health services brought on by the COVID-19 pandemic. As not all deaths that occur within the community are brought to health facilities before burial, the actual proportion of total deaths that occur within the community may even be higher. An analysis of places of death in Zambia among adults 15–59 years between 2010 and 2012 showed that slightly less than half of the adult deaths occurred in the home, factors associated with dying in a health facility included higher educational attainment, urban versus rural residence, and being of female gender [25]. The observed increase in the proportion of deaths in the community during COVID-19 waves could be due to barriers to access to health facilities as some facilities were repurposed to serve as specialised COVID-19 treatment centres whilst other facilities scaled down services offered by only offering essential health services or attending to only emergencies [33,34,35]. This could have compromised the quality of outpatient care that chronically ill patients received. Additionally, the myths and misconceptions around COVID-19 could have prevented those in most need of care from seeking health care [36]. We recommend risk communication and engagement strategies tailored to increasing demand within the community for seeking health services during public health emergencies. Additionally, surge capacity plans should be developed by the Ministry of Health and implemented during public health emergencies. These could help ensure the continued provision of essential health services as well as provide additional capacity to respond to the public health emergency.
Our study had several limitations. As we investigated excess deaths, we were unable to quantify the proportion of these excess deaths that were due to COVID-19, however, due to the timing and demographic composition of these deaths and the absence of other explanatory events, we believe that most of these deaths could have been due to COVID-19. Only community deaths that were reported at health facilities were analysed during this investigation, as such our findings underestimate the total number of deaths that occurred within these districts, as not all community deaths are reported at these facilities. While our study employed purposive sampling for site selection, which may have introduced selection bias and impacted the generalizability of our findings, the consistency observed across all selected districts—despite varying sociodemographic factors—suggests that our results are broadly reflective of the entire country. This consistent pattern across diverse districts supports the robustness of our findings and their applicability at a national level. Sampling additional districts was impossible because of resource limitations (data abstraction was time-consuming). Our method of determining excess mortality did not consider potential seasonal variations. However, due to the large size of the data set, the consistency of findings across the different districts, the consistency of our findings with current known epidemiological characteristics of COVID-19 and the consistency of our findings with other similar studies, we believe our findings are credible.
There was excess mortality in all 12 districts visited during the COVID-19 pandemic in Zambia with most of these deaths occurring within the community and among the elderly. These findings suggest the impact of the COVID-19 pandemic in Zambia was far greater than implied by reported COVID-19 deaths alone. Strengthening routine and continuous mortality surveillance systems with cause of death ascertainment especially among community deaths could help guide public health decision-making and strengthen risk communication and community engagement during public health emergencies.
Data availability
The data that support the findings of this study are available from the Permanent Secretary Technical Services of the Ministry of Health, but restrictions apply to the availability of these data, which were used under license for the current study, and so are not publicly available. Data are however available from the authors upon reasonable request and with permission of the Permanent Secretary of Technical Services of the Ministry of Health.
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Acknowledgements
Francis Swaba, Jane Nalwimba, Paul Linde, Micheal Mwamba, Patrick Kamfwa.
Funding
This work has been partly financially supported by the President’s Emergency Plan for AIDS Relief (PEPFAR) through the US Centers for Disease Control and Prevention (CDC) and the CDC Emergency Response to the COVID-19 pandemic through a cooperative agreement with the Zambia Ministry of Health (CoAg ID number: GH002234; CoAg funding period: 9/30/2020-9/29/2025).
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Stephen Longa Chanda, MBChB, MSc: Project conception, Protocol development and implementation, monitoring, data collection, management and analysis, manuscript writting. Nathan Kapata, MBChB, PhD, Nyambe Sinyange, MBChB, MSc, Muzala Kapina, MBChB, MPH, Amos Hamukale, MSc: Protocol development and implementation, data collection and manuscript writting. Luchenga Adam Mucheleng’anga, Fellow FP, MMed Path, MBChB, BScHB: Protocol development, data collection and management. Jonas Hines, MD Surveillance Team Lead: Protocol development, data collection and management manuscript writing. Warren Malambo, MPH Public Health Specialist: Project conception, Protocol development, monitoring, data analysis, manuscript writing. Roma Chilengi, MBChB, MSc, Director General Zambia National Public Health Institute: Protocol development, monitoring, data management and analysis and manuscript writing.
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Informed consent was waived by Excellence Research Ethics and Science (ERES) converge (Ref. No 2022-April-018) (IRB and Federal Wide Assurance (FWA) numbers, 00005948 and 00011697 respectively) and authority to conduct the study from the National Health Research Authority (NHR0000005/31/10/2022). The activity was reviewed by the US Centers for Disease Control and Prevention and was conducted consistent with applicable US federal law and CDC policy.
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Supplementary Figure 2: Trendline of median age at death and median daily count of deaths in 12 districts, Zambia 2020–2022
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Chanda, S.L., Hines, J.Z., Malambo, W. et al. An assessment of excess mortality during the COVID-19 pandemic, a retrospective post-mortem surveillance in 12 districts – Zambia, 2020–2022. BMC Public Health 24, 2625 (2024). https://doi.org/10.1186/s12889-024-20045-3
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DOI: https://doi.org/10.1186/s12889-024-20045-3