COVID-19 surveillance in Democratic Republic of Congo, Nigeria, Senegal and Uganda: strengths, weaknesses and key Lessons

Introduction As part of efforts to rapidly identify and care for individuals with COVID-19, trace and quarantine contacts, and monitor disease trends over time, most African countries implemented interventions to strengthen their existing disease surveillance systems. This research describes the strengths, weaknesses and lessons learnt from the COVID-19 surveillance strategies implemented in four African countries to inform the enhancement of surveillance systems for future epidemics on the continent. Methods The four countries namely the Democratic Republic of Congo (DRC), Nigeria, Senegal, and Uganda, were selected based on their variability in COVID-19 response and representation of Francophone and Anglophone countries. A mixed-methods observational study was conducted including desk review and key informant interviews, to document best practices, gaps, and innovations in surveillance at the national, sub-national, health facilities, and community levels, and these learnings were synthesized across the countries. Results Surveillance approaches across countries included - case investigation, contact tracing, community-based, laboratory-based sentinel, serological, telephone hotlines, and genomic sequencing surveillance. As the COVID-19 pandemic progressed, the health systems moved from aggressive testing and contact tracing to detect virus and triage individual contacts into quarantine and confirmed cases, isolation and clinical care. Surveillance, including case definitions, changed from contact tracing of all contacts of confirmed cases to only symptomatic contacts and travelers. All countries reported inadequate staffing, staff capacity gaps and lack of full integration of data sources. All four countries under study improved data management and surveillance capacity by training health workers and increasing resources for laboratories, but the disease burden was under-detected. Decentralizing surveillance to enable swifter implementation of targeted public health measures at the subnational level was a challenge. There were also gaps in genomic and postmortem surveillance including community level sero-prevalence studies, as well as digital technologies to provide more timely and accurate surveillance data. Conclusion All the four countries demonstrated a prompt public health surveillance response and adopted similar approaches to surveillance with some adaptations as the pandemic progresses. There is need for investments to enhance surveillance approaches and systems including decentralizing surveillance to the subnational and community levels, strengthening capabilities for genomic surveillance and use of digital technologies, among others. Investing in health worker capacity, ensuring data quality and availability and improving ability to transmit surveillance data between and across multiple levels of the health care system is also critical. Countries need to take immediate action in strengthening their surveillance systems to better prepare for the next major disease outbreak and pandemic. Supplementary Information The online version contains supplementary material available at 10.1186/s12889-023-15708-6.


Introduction
The Coronavirus disease of 2019 (COVID- 19) was first reported in Wuhan city of the Hubei Province in China around late December 2019 [1]. On 30th of January 2020, the World Health Organisation (WHO) declared COVID-19 a Public Health Emergency of International Concern [2]. COVID-19 was declared a pandemic on 11th of March 2020 and by the 23rd of February, 2023, it had caused over 757 million confirmed cases and over 6.8 million deaths globally [3].
Nigeria was one of the first countries in Africa to report a case of COVID-19 on 27th of February, 2020 [4]. A few days later, on 2nd of March, Senegal reported its first case in a traveler arriving from France [5]. Uganda and the Democratic Republic of Congo (DRC) also reported cases in March 2020 [6]. Like many other African countries, these four countries experienced a relatively mild first wave of the pandemic (through July 2020) reporting a total of 17998, 35511, 87564, and 19140 for DRC, Uganda, Nigeria and Senegal, respectively [7]. The period for subsequent waves of infection differed slightly between countries. A second wave of cases and deaths followed between November 2020 and February 2021, except in the DRC where the reported burden remained low. In early June 2021, Senegal had the most reported cases and death per capita. By the middle of June through July 2021, Uganda had already overtaken Senegal and peaked in a third wave while Senegal was already experiencing a trough.
Surveillance is one of the most critical features of disease outbreak detection and pandemic response [8,9]. The objectives of COVID-19 surveillance are to: enable the rapid detection, isolation, and management of suspected and probable cases including detecting and containing the clusters and outbreaks, especially among vulnerable populations [10]. Furthermore, surveillance is key to identifying, following up with, and quarantining contacts of confirmed COVID-19 cases at the beginning of the pandemic and providing requisite data to guide the implementation and adjustment of targeted control measures [10].
Compared with the rest of the world, COVID-19 has not been as severe in Africa. Although the African continent is home to about 14 per cent of the world's population, the region has accounted for only about 2 per cent of reported cases and deaths as at 10th November, 2020 [11]. Low case detection rates and reporting gaps exist in COVID-19 cases and deaths across the world, and these are particularly acute in sub-Saharan Africa (SSA) [12] due to weakeness of infectious disease and mortality surveillance systems. Disease reporting gaps could partially explain the relatively lower COVID-19 burden in SSA [13,14]. Test positivity, or the proportion of COVID-19 tests that are positive, can be used as a marker of how widespread the infection is and whether sufficient testing is being done. WHO suggests that a positivity rate of less than 5 percent is one indicator that a country has the spread of COVID-19 under control [15]. During some phases of the pandemic, especially during the second wave between November 2020 and February 2021, the test-positivity rates in all four countries were greater than 10 percent, much higher than the WHO benchmark of 5 percent, [16] suggesting a substantial undetected burden of COVID-19 by the surveillance systems.
To inform the development of sustainable and resilient surveillance systems for current COVID-19 response efforts and future disease preparedness in the region and globally, this study aimed to analyse and document the surveillance strategies in response to the COVID-19 pandemic adopted by four countries in SSA namely, the DRC, Nigeria, Senegal and Uganda. to enable swifter implementation of targeted public health measures at the subnational level was a challenge. There were also gaps in genomic and postmortem surveillance including community level sero-prevalence studies, as well as digital technologies to provide more timely and accurate surveillance data. Conclusion All the four countries demonstrated a prompt public health surveillance response and adopted similar approaches to surveillance with some adaptations as the pandemic progresses. There is need for investments to enhance surveillance approaches and systems including decentralizing surveillance to the subnational and community levels, strengthening capabilities for genomic surveillance and use of digital technologies, among others. Investing in health worker capacity, ensuring data quality and availability and improving ability to transmit surveillance data between and across multiple levels of the health care system is also critical. Countries need to take immediate action in strengthening their surveillance systems to better prepare for the next major disease outbreak and pandemic.

Study setting
The study was conducted in the DRC, Nigeria, Senegal and Uganda. These four countries were selected for the following reasons: 1. Variation in their COVID-19 responses, in terms of the scope and intensity of non-pharmaceutical interventions and their intended outcomes [17]. 2. Historical experience in managing epidemics of global concern, such as yellow fever, Ebola virus disease, and Marburg virus disease [18][19][20]. 3. Existing partnerships between local research institutions and government departments for ease of implementation and translation of research findings to evidence-based policy and practices. 4. Mixture of Francophone (the DRC and Senegal) and Anglophone (Nigeria and Uganda) [21] countries to enhance South-to-South cross-learning.

Study design
This study used a mixed-methods observational approach based on the surveillance and public health action framework (Fig. 1). The mixed-methods consisted of; 1) a desk review of the literature and relevant documents, and 2) key informant interviews (KIIs). First, the study undertook reviews of each country's guidelines and response plans, response reports, websites, presentations, and analysis of the COVID-19 epidemic curve. Second, researchers from the four countries conducted KIIs to further explore the issues identified in the desk reviews. Promising practices, innovations, and challenges with key recommendations for moving forward were documented and presented in this paper. The surveillance and public health action framework has the following five (5) domains each having at least two components: Response Strategy, Testing, Surveillance and Data Analysis, Public Health Action and Coordination, (Fig. 1).First, the Response Strategy domain includes setting testing and surveillance procedures and goals, partly informed by the ''pre-pandemic context, including exposure to prior epidemics [21]. Second, the Testing domain has one component titled use of diagnostic tests (e.g., RT-PCR) to identify COVID-19 cases which has several sub-components namely production and sourcing, test delivery, sample collection and test demand, sample delivery, laboratory analysis, and result communication [21]. Third, the Surveillance and Data Analysis domain constitutes of the following two components, namely collection, analysis and use of data to identify and understand trends in the outbreak (e.g., identification of case clusters) and use of different surveillance modalities (e.g.,, serological surveys, mortality surveillance). Then the Public Health Action domain constitutes four components namely setting new priorities and policies for response, case management for known and suspected cases, establishing guidelines for contact tracing and quarantine, and investigation and control measures. Finally, the Coordination domain constitutes two components which are establishing task forces groups and committees to manage aspects of direct surveillance and testing activities, and establishing regulatory practices [21]. This study focuses on only the surveillance and does not explore aspects of testing which is being addressed in another publication [21]. The study also explores how other components such as response strategy, public health action and coordination influence surveillance and data analysis.

Study population
Study participants were selected based on their role in the COVID-19 response. They typical include policy makers and members of the national and regional emergency operations centres for COVID-19 response. Informants were identified and selected from national public health institutes, Nigeria centre for disease control, state ministry of health and local/district health authority. Research assistants visited the offices offices of the informants at their convenient time to conduct the KIIs. The study conducted (KIIs) with 30 informants per country, including policy makers, epidemic focal persons, and health managers.

Study instrument
Two data collection instruments were used (Supplementary Materials). The first instrument was a literature abstraction form (Additional file 1) used to gather information across the four countries on testing modalities, changes in testing criteria, modalities of implementing contact tracing, isolation, screening and the surveillance modalities for COVID-19. The second instrument was a KII guide (Additional file 2) which was used to obtain information on the strengths and weaknesses of the surveillance strategies in the four countries. The KII themes under which information was gathered were past experience with epidemics, health system preparedness (specifically about funding), response to the COVID-19 pandemic in Africa and the outcomes in terms of nonpharmaceutical COVID-19 control strategies, including strategies to ensure continuity of essential non-COVID services.

Data collection
The data extraction form was developed and piloted in the excel format but was also applied in the word document format to extract data, depending on preference by country teams. The sections relevant to surveillance extracted data on strategies including; modalities of contact tracing, modality of implementing isolation, modalities of screening, and surveillance data. For each strategy, data on key strengths, weaknesses, challenges and gaps were also extracted where reported. Investigators conducted search and extracted data on different sections independently.
In each country, data collection was facilitated by skilled research assistants with proficiency in qualitative research. The research assistants received additional training on data collection strategies and use of the guide. Between February and March, 2021, 30 KII were conducted in English (Nigeria and Uganda) and French (the DRC and Senegal) among policy makers, program managers, and epidemic response and health system implementers and managers to further explore the issues identified in the desk research.
Prior to conducting the KIIs, the research team conducted a desk research. The mixed-methods observational approach was utilized to facilitate the triangulation of information to enable a wide-ranging documentation of the strengths, weaknesses, gaps and innovations in surveillance at the national, sub-national, health facilities, implementing partners and community levels. Key learnings both similar and unique to a specific country context were synthesized across the countries.

Data management
The data from the literature review were synthesized thematically. All KIIs were audio-recorded on mobile phones and voice recorders. Codes were assigned to each key informant to ensure the confidentiality of the participants. The recorded data were transcribed, cleaned and coded. Thematic analysis was done using Excel and Atlas Ti software packages. The recordings and notebooks were securely stored in locked cabinets and password protected.

Ethical considerations
Each country research team obtained ethical clearance from relevant national and Institutional Review Boards. Clearance was obtained as such DRC-No d' Approbation: ESP/CE/198/2020; Nigeria-NHREC/01/01/2007; Senegal-000279/MSAS/DPRS/DR 03/03/2021; and Uganda-UNCST HS 1121ES/HDREC 903. The study was conducted in accordance with the Declaration of Helsinki. The permission of the gatekeepers' was obtained to allow access to the facilities. Before conducting interviews, the purpose of the study was explained to the participants who provided written or verbal (for respondents who desired more anonymity) informed consent depending on the country. Importantly, participants were reassured of confidentiality of their responses and anonymity.

Literature review
All four countries are committed to the Global Health Security Agenda (GHSA), and the International Health Regulations 2005. Furthermore, they all are implementing the Integrated Disease Surveillance and Response [21] system [22]. Table 1 shows the pre-pandemic health context in the four countries. Nigeria is the most populous of the four countries (215 million) compared to Senegal's 17 million. On the other hand, Senegal had the highest life-expectancy of 68.5 years while Nigeria has the lowest at 54.3 years. Uganda has the best universal health care coverage index of 53 compared to the + DRCs 45 [23,24]. Prior to the COVID-19 pandemic, WHO and MOH collaborative evalutions found that all four countries had very limited capacity in the following technical area across all levels of the epidemic preparedness of the health system namely detection, response and control of public health threats (WHO JEE reports: DRC-2018; Nigeria-2017; Senegal-2016; Uganda-2017). The COVID-19 epidemic underscored the critical role of surveillance in protecting individual nations and the global community.
Surveillance for COVID-19 was risk-based across all four countries and the prevention, control and mitigation strategies implemented had many similarities. Initially, the priority groups for contact tracing were all contacts of confirmed cases, travelers originating from countries that had reported COVID-19 cases, and health care workers exposed to confirmed cases, but as the pandemic progressed the prioritization was revised to include only symptomatic contacts and travelers. To implement contact tracing, additional human resources were engaged either through recruitment of volunteers or contract staff. Initially, contact tracing was centrally coordinated and targeted all contacts, but as the epidemic progressed to widespread community transmission and the cases increased, the activity was decentralized and tracing targeted individuals at higher risk of severe disease. Effectiveness of contact tracing during early phases was generally good, with over 90% of contacts reportedly traced in all the countries [25]. Table 2 shows data from literature on the morbidity and mortality patterns due to COVID-19 in the four countries under study. As at April 2022, Senegal had the highest number of cases and deaths per million and the DRC had the least (5000 and 114.27 versus 939.05 and 14.47 per million respectively).

Synthesis of literature review and key informant interviews Surveillance methods and Systems
Across the study sites and contexts, a networked and combination of different surveillance methods were used to get a holistic picture of the spread of the COVID-19 disease and behavior of the populations served by ministries of health and donors. The examples of methods used across the four countries can be classified into active and passive surveillance. The active surveillance included case investigation, contact tracing, communitybased surveillance, sentinel site surveillance, serological survey, event-based surveillance, telephone hotlines, genomic sequencing and pathogen surveillance and environmental surveillance. The passive surveillance included surveillance at the primary care level, laboratory-based surveillance, hospital/facility-based surveillance, point of entry surveillance, work-based surveillance, mortality and postmortem surveillance. These surveillance systems have been linked to electronic data collection  and reporting systems e.g. District Health Information Sysytem (DHIS-2) and Surveillance Outnreak Response Managaement and Analysis System (SORMAS) for real time access. Findings from the KIIs also buttressed the adoption and use of these various methods. Active case findings were adopted in community based surveillance across countries such as Nigeria, Uganda and DRC. Community health workers and village health teams collaborated with community members in some instances for community ownership of the tracing process. One key informant noted that:  2. Capacity enhancement.All the four participating countries strengthened surveillance capacity at subnational level by training rapid response teams at district/regional/provincial/state levels, with support from development partners [30]. Sub-national teams were pivotal in supporting lower-level structures including community health workers to conduct contact tracing. Training, dissemination of policies and tools (i.e., data collection forms, case definitions, and reporting tools) to support surveillance occurred in a timely manner. However, all four countries reported staffing shortages especially for dedicated surveillance officers at the local levels of the operation of the surveillance systems. ''Not only Village Health Teams (VHTs) but we also brought the community leaders on board to do surveillance, and that is working for us very well…the community is leading the surveillance rather than for us [31] owning the activity"(District Surveillance Focal Person, Uganda) "In Uganda the use of community health workers to implement COVID-19 surveillance was a strength, while in DRC, the use of Early Warning, Alert and Response System (EWARS) (Early Warning, Alert and Response System) was a strength" (Surveillance officer, DRC) 3. Data management reporting and use: All the four countries had established databases with capacity to report on key indicators on the status of the response to COVID-19. These countries built the reporting of COVID-19 indicators on existing data management systems for collecting, collating, analysis and reporting on the performance of these indicators. All countries adopted electronic systems to improve timeliness of reporting. The reporting systems were linked to the current (DHIS-2) system which enhanced storage, retrieval, analysis, and presentation as well as interpolation with existing data. Data was shared through dashboards [32], bulletins, situation reports and was accessible to key decision makers to support the response. The availability of scientifically sound data contributed to the regular review and update of surveillance policies and strategies. The use of digital platforms, short text messages and telephone calls was reported by all countries for sharing results with decision-makers and for improving the health of the population in their jurisdiction. However, interoperability and data quality were still key challenges. "To the best of my knowledge I will say [SORMAS] is near perfect…because we are not using the outdated paperbased surveillance system, we are using the e-format… which is like 'real time' , because as soon as the result is received from the lab, the data manager inputs the results electronically, and at that point everybody who is a stakeholder sees it and can respond" (Capacity Building  Trainer, NC, Nigeria).

Key strengths of the surveillance approaches employed
"

Insufficient space for quarantine and isolation
-In all four countries, there was insufficient accommodation space for quarantine and isolation. For example, at the beginning of the COVID-19 response in Nigeria, quarantine and isolation was carried out in government approved hotels, and in some instances all confirmed cases where hospitalized irrespective of disease severity. Initially the governments paid for hotel accommodation and general upkeep, however, later incoming travelers were required to pay their hotel fees. These deficiencies made contact tracing and surveillance more challenging, especially with increasing case volume. Across all study countries, as the pandemic gained momentum and funds became depleted, the institutional quarantine and isolation strategies were changed to home based quarantine and isolation. Compliance with self-isolation and self-quarantine became a challenge in the drive to prevent and control the epidemic resulting in increased community transmission of the virus [35]. 6. Weak surveillance infrastructure -The health infrastructure in all countries was weak and not adequately situated to manage a global pandemic. There was inadequate health manpower and funds designated for COVID-19 surveillance (Table 4). Surveillance tools and logistics were also not readily available in the early stages of the pandemic. The decentralized and community surveillance structures had varying degrees of performance and required additional support especially in data analysis and use, postmortem surveillance and tracking of excess deaths across the study countries.

Summary of findings
Disease surveillance systems are developed for the monitoring of the health status of populations and most importantly for early detection of infectious diseases outbreaks and prompt intervention. Surveillance is a top priority in management and control of any pandemic.
Countries' responses to emergent health crises depend mainly on the strength of the surveillance systems they establish [36]. This study aimed to document the COVID-19 surveillance strategies adopted by DRC, Nigeria, Senegal and Uganda in response to the COVID-19 pandemic as well as to describe the strengths, weaknesses, and lessons learnt about the existing surveillance approaches adopted during the epidemic. Furthermore, the aim of the study was to gather evidence on functionality of the adopted surveillance so as to inform the enhancement of surveillance systems to facilitate preparedness for future epidemics in Africa. Surveillance for COVID-19 cases was risk-based across all four countries and involved a combination and networking of several surveillance methods. It was found that all countries had previous experiences with managing surveillance systems in an epidemic situation such as Ebola disease and were therefore, able to respond promptly to the pandemic but insufficiently due to resource constraints. For example, the national Emergency Operation Centre (EOC) in Nigeria had been in existence and had ample experiences in polio as well as in Ebola outbreak surveillance and response. The key strengths across the studied countries included leveraging on these previous outbreak experiences and preexisting functional surveillance systems, strengthened surveillance capacity at sub-national levels by training rapid response teams at subnational levels; establishment of databases with capacity to report on key indicators on COVID-19 response, including electronic systems linked to DHIS-2 which contributed to regular review and update of surveillance policies and strategies. Developed countries on the other hand have standardized surveillance response system with skilled technical staff.
All four countries adopted realtime and active contact tracing as one of the essential surveillance approaches so as to control the disease through empowering decision makers with information on the health-related behaviors of their communities and the spread of the COVID-19 disease in the community. This enables the governments of the study countries to intervene quickly to stop the spread of disease. The priority groups for contact tracing included high-risk persons such as contacts of confirmed cases, and travelers from countries with reported COVID-19 cases, but prioritization was revised to include only symptomatic contacts and travelers, as the pandemic progressed. Furthermore, contact tracing was decentralized at a later time to target individuals at higher risk of severe disease.
The key challenges and gaps included; inadequate human resources for surveillance activities especially at lower levels; insufficient space for institutional quarantine and isolation; low case detection rates; limited capacity for routine genomic sequencing of variants; weak decentralized surveillance capacity; insufficient infrastructural capacity for quarantine and isolation; weak health care infrastructure including inadequate funds and tools for surveillance activities; misinformation and poor public perception about COVID-19, especially on social media. For example, inadequate human resources limited the optimal performance of surveillance systems. This was corroborated by the overwhelming load of contact tracing workload for healthcare workers reported in other studies where Uganda had 186/100,000 population and Nigeria had 111 per each state with populations in millions [25]. There was also humanitarian assistance from donors such as WHO, UN baskets, non-govermental organizations and the Nigerian indigenous Coalition against COVID-19. The world bank provided funds for contact tracing and Africa Centres for Disease Control and Prevention funded active case search.
Inadequate human resources and other challenges moderated the gains that would have accrued from adapting already existing surveillance systems and experience in managing outbreaks. The UK support initiative and Clinton health access initiative supported state and local capacity building and ongoing vaccine development.
As the pandemic progressed, the resources available could not cope with upsurge in activities required to maintain standard operating procedures leading to modifications in surveillance strategies. The criteria for testing and contact tracing were streamlined to reduce the workload. Isolation and quarantine facilities were expanded to private facilities with the implication of poorer followup and monitoring. Furthermore, all countries reported gaps in data management and surveillance response at subnational levels. The importance of task shifting to community health workers, adopting technology based solutions, strong national leadership including enhancing multisectoral partnership to respond to the pandemic was adopted. The countries prioritized national-level coordination of the various surveillance approaches across sectors and stakeholders. Each country established or leveraged robust partnerships with non-governmental organizations, academics, and other global institutions. These countries improved data management and surveillance capacity rapidly by training health workers and increasing resources for laboratories, but the disease burden continued to be under-detected.

Results in context of the literature
A key objective of the World Health Organisation's COVID-19 surveillance is to guide the implementation and adjustments of COVID-19 control measures including isolation of cases, contact tracing and quarantine of contacts [37]. The experience of African countries in handling previous infectious disease outbreaks and the existing surveillance infrastructure were helpful and in part made Africa fare better in COVID-19 pandemic compared to the high-income countries [38]. The exising surveillance infrastructure was revitalized and repurposed for COVID-19 surveillance. The surveillance methods documented in this study was corroborated by a systematic review of COVID-19 surveillance systems in 13 other African countries which documented the similar surveillance methods reported in this study [21]. Some variations however, exist in the level of implementation of the surveillance strategies between the countries which determines to a large extent, the representativeness of the systems. South Africa with more comprehensive surveillance system reported more representative COVID-19 burden data compared to countries such as Tanzania and our four study countries where COVID-19 surveillance strategies were poorly developed [21]. The interpretation of the morbidity and mortality burden from COVID-19 is subject to the quality of the surveillance system adopted. The surveillance systems in the four African countries under study have been generally non-representative of the entire underlying population. The seroprevalence surveys conducted in these countries reported a much higher COVID-19 prevalence than would be expected by the number of cases reported.
Therefore, there is a need for these countries to utilize multiple surveillance approaches to understand the full picture of the disease burden. The risk based testing strategy adopted by the countries underestimated the burden of COVID-19 due to underreporting. Extending COVID-19 testing to all contacts of a confirmed case would give a better sense of the disease burden but this attracts high cost which the countries may not have the capacity to afford and sustain. Hence, additional sources of data may be needed for example from mortality surveillance, and community surveys which were not fully integrated. A study in Zambia found significant excess mortality due to COVID-19, with the majority of deaths occurring in the community that were undiagnosed, while many deaths at the facility were also un-tested prior to death [39]. Mortality surveillance and all-cause mortality tracking has generally not been widely practiced in many African countries. Uganda attempted to establish a mortality surveillance system and has been conducting post-mortem surveillance for hospital and community COVID-19 deaths, but this has remained weak due to challenges in mortality reporting in the health systems. In Nigeria, the serological surveys conducted confirmed much higher COVID-19 prevalence than reported through the regular surveillance system, thereby emphasizing the importance of using multiple surveillance methods.

Implications for epidemic preparedness and response
During the epidemic these countries made efforts to upgrade and upscale the health systems infrastructure so as to improve resilience and to enhance rapid response to infectious diseases emergencies.
Generally, all the four countries started planning early and had a fairly slow buildup of COVID-19 cases. The study revealed the existence of a emerging framework for surveillance structure and system in the four countries. At the onset of the pandemic, all four countries under study had in place limited existing surge capacities mainly in the areas of laboratory testing and trained epidemiologists with limited dedicated funds for outbreak response management such as contact tracing. Nigeria, Senegal and Uganda all reported having dedicated budgets for outbreak response which were available at the beginning of the outbreak for provision of personal protective equipment and limited contract tracing [35].
The existing surveillance systems in all the countries were built to respond to localised epidemics whereby the central level response team would support the decentralized rapid response team (RRT) at the outset of an outbreak. However, the subnational structures have never been activated into full preparedness response mode. At the same time the countries were never prepared for simultaneous country-wide outbreak response in multiple geographic locations. In the event of a widespread pandemic such as COVID-19, all countries experienced challenges in subnational responses including shortages in adequately trained surveillance officers, data analyst and contact tracers. Building the capacity of subnational epidemic response capacity requires substantial resources allocation including funding, training staff, and equipping the decentralized centers. Due to resource constraint, a strategy adopted by the countries was to prioritize the districts or regions at highest risk i.e., geographies with higher number of cases. For example, in the DRC, surveillance efforts were strongest in Kinshasa which was the epicentre of the epidemic and where mass testing centres and several diagnostics laboratories were established.
There was deliberate modification in the daily schedule of human resources in communities and at health facilities to reduce their work load and lessen the risk of contracting COVID-19 [12]. Furthermore, countries did not have the appropriate number of responders. For example, there was a lack of adequate contact tracers to match the pandemic demand across all countries. In addition, the study countries still have challenges with ensuring the availability of adequate and appropriately skilled human resource, a situation that preceded the pandemic and that will require strategic resourcing during and after the COVID-19 pandemic. The countries could rapidly train, repurpose, and deploy community-based voluntary health workers (VHW) and facility-based health workers, but these structures require additional strengthening for epidemic preparedness and rapid response.
Overall, analysis and use of surveillance data for action existed at the central/national level but was limited at the subnational levels in all the studied countries. Ensuring timely data availability and use of data is critical to public health decision making. During the pandemic crisis we observed the importance of having the right data which was routinely used for EOC guidance. Therefore, countries had strategies to report data daily, weekly and monthly. The study countries in various degrees adopted electronic systems from paper-based to improve efficiency of data transmission and data use for decision making. Availability of surveillance data contributed to regular review and update of the existing surveillance policies, strategies and standard operating procedures. However, there were notable gaps in data accuracy and consistency at non-sentinel sites than at sentinel sites. Furthermore, the data were not disaggregated by sociodemographic characteristics such as sex, location/ place of residence to show burden at the individual level characteristics. The establishment of databases linking surveillance with testing that were accessible to key stakeholders improved communication and efficiency. Data systems development and use require improvement at the subnational levels for more efficient response.
Technological innovations were deployed to enhance surveillance activities including contact tracing, monitoring persons in quarantine, reporting, data analysis, laboratory results return, with improved efficiency. For example, Senegal adopted and used digital communication innovations such as the "Alerte Santé Sénégal" app and "Sunucity" which is an incident reporting app for suspected COVID-19 cases from community that allows feedback from the authorities [12]. These need to be evaluated and replicated.
Strengthening partnerships is key for epidemic preparedness and response. The studied countries were able to source initial supplies with support from non-governmemtal organizations, philanthropists and international partners. The private sector provided funding for testing kits and built facilities for quarantine and isolation services as a surveillance measure. However, the countries need to optimize the public private partnerships in several areas including provision of health services and manufacture of health products. South-to-South COVID-19 response collaboration and technical support can be fostered as a result of the countries' differential experience. For example, Nigeria and Uganda with expertise in capacity building for epidemic preparedness among responders can be a resource in this area in the region.
Furthermore, there is a need for the improvement of the alert management systems for identification of COVID-19 cases or any other epidemic disease from the community. Senegal, Nigeria and Uganda, reported using call centers with toll free lines to support case identi. fication and contact tracing. However, these call centers were eventually overwhelmed and response became suboptimal as the pandemic progressed with widespread community transmission. Routine alerts could be supplemented with other active surveillance approaches such as systematic health facility surveillance, mortality surveillance and periodic surveys for better estimation of the burden of disease and disease outcomes.

Study limitations
A substantial part of this study relied on document review. At times the codified evidence in guidelines, policy documents and scientific publication may differ from the real world experience or may lag behind on what could be happening on the ground. Thus, the extent to which the documents reviewed reflected the true practice is uncertain. However, the study mitigated this potential bias by triangulation the literature review information with the qualitative interviews.
This study did not assess the relative performance or effectiveness of surveillance methods. Surveillance methods adopted in the countries studied were complementary. In the face of resource challenges, there is a need to adopt the most comprehensive and cost-effective methods. For example, the European Centre for Disease Preventiion and Control recommended for member countries no longer testing mild suspected cases of COVID-19 should integrate COVID-19 surveillance with sentinel surveillance of influenza-like illness or acute respiratory infection [40]. The swabs obtained at the sentinel sites would then be tested for SARS-CoV-2 in addition to influenza virus. This provides some cost saving by using existing resource framework.
The article showed that private sector contributed immensely to COVID-19 response such as surveillance and testing, treatment, risk communication, health promotion and maintenance of access to essential health services.

Conclusion
Following the COVID-19 outbreak on the African continent in February-March 2020, the DRC, Nigeria, Senegal and Uganda demonstrated a prompt public health response to the epidemic ass well as instituted national policies aligned to WHO guidance and modified these strategies along the phases of the local epidemic. The countries adopted similar approaches to surveillance, although at different levels and with slight modifications. All four stiudy countries seemingly performed well at the initial stages of preventing transmission through quarantine and isolation. However, as the number of COVID-19 cases began to increase the quarantine and isolation approach began to fault.Coordination of the COVID-19 response in all four study countries built on existing surveillance systems with establishment of central task teams. All countries noted capacity gaps for response at subnational level and adopted electronic systems for data management at varying levels; and they utilized webbased platforms for public data access and visualization. Across four countries, one common challenge was lack of human resource capacity for conducting contact tracing, data analysis, as well as public health expertise.
Recommended approaches such as (1) adopting more innovative technological solutions to improve efficiencies of their surveillance strategies, (2) having a central database across the response pillars to make surveillance more efficient and improve data use at the subnational level, can help stem the further spread of COVID-19, while enhancing readiness for future disease outbreaks. Other approaches include, (3) improvement of human resource surge capacity at subnational level, (4) decentralization of isolation centers and (5) enhancement of home/self-isolation with support from community structures. The private sector should be involved to support response activities, while ensuring proper regulation and quality assurance. Efforts to stem further spread of COVID-19 are critical including roll-out of COVID-19 vaccines, and implementation of targeted non-pharmaceutical interventions.
Supplementary Material 1