Review of Uganda´s high-risk Ebola preparedness activities enabling prompt control of imported Ebola Virus Outbreak from the Democratic Republic of Congo, June 2019

Sandra Nabatanzi^1,&, Allan Niyonzima Muruta², Issa Makumbi^2,3, Alex Riolexus Ario^1,2, Benon Kwesiga¹, Atek Atwiine Kagirita^2,4, Lilian Bulage¹, Bernard Lubwama², Doreen Nsiimire Gonahasa¹, Paul Mbaka^2,5, Innocent Komakech⁵, Maureen Nabatanzi¹, Felix Ocom^3,5, Jaco Homsy⁶, Vance Brown⁶, Joseph Ojwang⁶, David Matseketse⁷, Ida Marie Ameda⁷, Simon Kyazze³, Allan Mpairwe⁵, Julie Harris⁶, Henry Gatyanga Mwebesa², Miriam Nanyunja⁵

 

¹Uganda Public Health Fellowship Program, Ministry of Health, Kampala, Uganda, ²Ministry of Health, Kampala, Uganda, ³Public Health Emergency Operations Center, Ministry of Health, Kampala, Uganda, ⁴Uganda National Health Laboratory Services, Ministry of Health, Kampala, Uganda, ⁵World Health Organization, Kampala, Uganda, ⁶US Centers for Disease Control and Prevention, Kampala, Uganda, ⁷United Nations Children's Fund, Kampala, Uganda

 

 

^&Corresponding author
Sandra Nabatanzi, Uganda Public Health Fellowship Program, Ministry of Health, Kampala, Uganda.

 

 

 

 

Ebola Virus Disease (EVD) is a viral hemorrhagic fever (VHF) that affects humans and other primates, as well as bats, porcupines, and other mammals. The causative agent, the Ebola virus, is transmitted from wildlife to humans and then spreads from human to human through direct contact with blood, secretions, or bodily fluids from infected persons and contaminated materials [1]. Signs and symptoms of EVD include fever, fatigue, muscle pain, headache, sore throat, vomiting, diarrhea, rash and bleeding (internal and external) [2]. EVD is highly fatal, with a case fatality rate (CFR) ranging from 25-90%, depending on the strain [1].

 

Between 2000 and 2018, Uganda experienced five EVD outbreaks [3]. On 1 August 2018, the neighbouring Democratic Republic of Congo (DRC) declared its tenth EVD outbreak [4]. This became the largest EVD outbreak ever recorded in the DRC and the second largest EVD outbreak ever recorded anywhere, lasting for two years and resulting in nearly 3,500 confirmed cases and nearly 2,300 deaths between 2018 and 2020 [5]. The epicenter of the DRC outbreak was in North Kivu, approximately 100 kilometers (km) from the Uganda border. For socioeconomic and healthcare-seeking reasons, people frequently moved between the epicenter area and neighboring Ugandan districts, crossing through the designated and non-designated points of entry. Given these movements, the risk of EVD introduction into Uganda was considered very high, and Uganda embarked on an intensive EVD preparedness planning and extensive heightened preparedness activities to enhance readiness for a potential EVD spillover from DRC.

 

On 10 June 2019, a 5-year-old patient presented at Kagando Hospital, Kasese District. Health workers at this facility had undergone refresher training only weeks before on health facility-based surveillance for EVD and had also participated in a simulation exercise as part of preparedness efforts. Based on symptoms, staff immediately suspected EVD in the patient and referred him to the nearby Ebola Treatment Unit (ETU) that was set up during the preparedness period. On 11 June 2019, upon receiving laboratory confirmation of the case by PCR testing at the Uganda Virus Research Institute (UVRI) in Entebbe, 425 km away from the ETU, the Uganda Ministry of Health (MOH) declared the sixth EVD outbreak in the country. We describe the extensive preparedness activities and how they enabled prompt detection and control of imported EVD without further spread within Uganda.

 

 

We conducted a descriptive study using desk reviews of all reports related to preparedness and response activities including situation reports, risk assessment reports, simulation exercise reports, and minutes from the national and district task force meetings. We synthesized and categorized information based on the themes below:

 

Response coordination mechanisms

 

In Uganda, “response coordination mechanisms” refer to the multi-sectoral and multidisciplinary teams and structures involved in response to a public health emergency. In the case of an infectious disease outbreak, these include all the partners and coordination structures of the multidisciplinary response teams involved in preventing, detecting, and responding to the outbreak at national and sub-national levels. The coordination structures are the National and District Task Forces. At the time of the outbreak, Uganda was divided into 128 districts.

 

On 4 August 2018, coordination mechanisms, comprising the National and District Task Forces (NTF and DTF), the Incident Management System, and the Emergency Operations Center (EOC) were activated at national and district levels to effectively coordinate EVD preparedness interventions in high-risk districts [5, 6]. In Uganda, the NTF and DTF provide technical oversight and guidance to the public health response at their respective levels. The Incident Management System comprises health professionals to plan, organize and oversee the training of key responders on the ground during preparedness, and coordinate all areas of the response phase, including planning, logistics, situational awareness, resource management, risk communication and community mobilization. Lastly, the EOC is activated at different levels to respond to emergencies from a central operational platform and provide the human and physical resources to support the response through. Both the IMS and EOC report to the NTF which is chaired by Uganda MOH´s top leadership. On 11 June 2019, these mechanisms were quickly repurposed to coordinate the response to the EVD outbreak.

 

Risk mapping and readiness assessments

 

When the 2018 EVD outbreak in DRC began, Uganda conducted risk mapping and readiness assessment using the WHO EVD checklist [7]. Uganda received a readiness score of 50% on the initial (baseline) assessment. This prompted immediate action to heighten preparedness and improve readiness for an EVD response, starting with developing a holistic preparedness plan. The plan included strategies to: a) enhance surveillance in high-risk districts including border points, health facility and community levels in order to enable early detection of any imported EVD case through training of immigration and border patrol officers, health workers and village health teams as well as setting up sanitation check points at border crossings, b) train laboratory personnel on safety procedures and Infection Prevention and Control (IPC) for specimen collection, packaging, labelling, referral and transportation to UVRI, c) train and equip district contact tracing teams, d) establish treatment centers for EVD cases, e) broaden and deepen community engagement and public and health worker awareness about EVD and the necessary actions to detect timely any imported case and prevent its transmission, f) protect health workers against EVD through the full implementation of IPC measures and preventive Ebola vaccination, g) build logistics capacity to quantify, procure, pre-position, and manage stock of equipment and supplies required for preparedness and response to EVD, h) improve IPC practices at all health facility levels and in the community, and i) strengthen local capacity for case management, including physical and mental health care, and psychosocial support [8].

 

EVD response plan

 

In June 2019, after the detection of the first EVD case in Uganda, the preparedness plan was quickly transitioned into a response plan through a consultative, multisectoral and multidisciplinary development process. Planned activities were structured around twelve preparedness and response intervention areas (coordination, epidemiological surveillance, laboratory, points of entry, emergency response, contact tracing, IPC, case management, safe and dignified burials, risk communication and community engagement, vaccination, and logistics), Risk categorizations were re-evaluated, and these interventions were implemented in 24 high-risk districts.

 

Monitoring and accountability of the National Preparedness Plan

 

The Uganda MOH adopted the WHO operational readiness checklist [7], which included the minimum requirements per intervention area for a country or district to be ready to handle an EVD outbreak. From August 2018 to March 2019, the country's EVD operational readiness was monitored regularly using this checklist that was administered to district task forces in high-risk districts and at the national level during meetings. Later, in May 2019, the WHO key performance indicators were also adopted by the MOH to monitor the implementation of key activities under different intervention areas at the sub-national level [9].

 

On 11-12 April 2019, MOH, Uganda conducted a full-scale Ebola virus simulation exercise. This was conducted at national, district, and community levels to assess operational readiness in the event of an Ebola outbreak. The exercise simulated 3 suspected cases of Ebola virus infection at 2 points of entry (Mpondwe, Kasese district and Entebbe International Airport) and Kasindi village, Kasese. The exercise was coordinated by the national EOC and was organized and executed over a period of 6 weeks (Figure 1). Strengths identified included 1) proper coordination by the EOC and real-time information sharing, 2) high level of risk perception at Mpondwe border, Entebbe airport and in the community, 3) proper isolation of suspect at Mpondwe and Entebbe, 4) Bwera treatment unit was in place with prepositioned logistics to manage patients, 5) samples were quickly collected and 6) proper screening at the points of entry. Areas that were identified for strengthening included 1) communication between the community and district level, 2) alert management, 3) sample transportation, 4) IPC measures in the community, at points of entry and health facilities as there was improper donning and doffing procedures observed and poor hand hygiene, 5) stigma in the community, and 6) inadequate knowledge on patient management.

 

Recommendations were to 1) conduct continuous drills on patient management and enhancing IPC measures at all levels, 2) provide IPC mentorship and conduct continuous drills, 3) train and deploy psychosocial staff in high-risk districts, 4) conduct drills on alert management, 5) print and disseminate information, education and communication materials and 6) provide stand by vehicles to support VHF sample transportation. Immediately after the exercise, the districts embarked on corrective measures and filling in the gaps. On 29 May 2019, an accountability forum was held at the national level to assess achievements and resources mobilized against the MOH national plan by the different stakeholders.

 

Capacities built during preparedness

 

Multiple actions were taken to build local and national capacities during preparedness activities. These activities are shown in (Figure 2).

 

Availability of data and materials

 

The data supporting our write-up belong to the Ministry of Health Uganda. For confidentiality reasons, the data is not publicly available. However, upon reasonable request to the corresponding author and with permission from the Ministry of Health Uganda, the data can be availed.

 

Ethical consideration

 

The Ebola preparedness, investigation and response activities were directed by Uganda´s MOH in response to a public health event and MOH directed and approved all the methods and procedures of this investigation. The IRB of CDC´s Center for Global Health in Atlanta determined that this activity was not human subject research, and that its primary intent was public health practice as an epidemic disease control activity. Verbal informed consent was sought from respondents supporting the response in Kasese district and at national level. They were informed that their participation was voluntary, and their refusal would not result in any negative consequences. Unique identifiers were used instead of real names to protect the confidentiality of the respondents and no names or personal identifiers of any respondents were disclosed in any verbal or written dissemination of the reports or investigations concerning this outbreak. Uganda´s MOH, CDC and Uganda´s Public Fellowship Program are aware of, approve and support the dissemination of the results of this investigation in any peer-reviewed journal.

 

 

Preparedness

 

The enhanced surveillance system designed to strengthen VHF alerts detected 655 alerts between 1 August 2018 and 11 June 2019. All samples were tested at UVRI, of which 23 tested positive for Viral Hemorrhagic Fevers (VHF): eight for Rift Valley Fever, 14 for Crimean Congo Hemorrhagic Fever, and one for Ebola Zaire. As a result of the preparedness activities, the preparedness score for the country increased from 50% in June 2018 to 84% in June 2019. The accountability forum identified the following gaps: weak coordination of partners resulting in fragmentation and duplication of efforts in some pillars, weak framework for monitoring preparedness efforts, insufficient mentorship in some districts, delayed reporting of alerts from the community to the national level, inadequate quality of isolation facilities as most were temporary structures, as well as weak IPC practices in districts where trainings were conducted. The stakeholders began addressing several of the identified gaps to enhance readiness.

 

Outbreak detection and response, and international collaboration

 

On 27 May 2019, a funeral was held in DRC for a man who died of EVD. On June 9, the DRC Minister of Health notified the Uganda Minister of Health of the possibility of high-risk contacts from the funeral potentially crossing into Uganda. On 10 June 2019, all the 12 high-risk contacts tried crossing the border into Kasese District, Uganda. However, when they noticed ongoing entry screening on the Uganda side at Mpondwe, they turned back to remain in DRC. The DRC national hygiene program traced and isolated them at a transitional isolation unit at Kasindi Hospital in DRC, where blood samples were collected to test for EVD. Later that same day on 10 June 2019, before results were available, six members of this group, including a 5-year-old boy and five of his family members left Kasindi Hospital and crossed into Uganda through an undesignated border crossing near Mpondwe, Kasese District (Figure 3).

 

As the 5-year-old child was unwell, his mother brought him to Kagando Hospital in Uganda (27 km from the border crossing) on the evening of 10 June 2019 where he presented with bloody diarrhoea, muscle pain, headache, vomiting blood, fatigue, and abdominal pain. Prior to the EVD outbreak, Kagando Hospital staff had been trained and re-oriented on health facility-based surveillance to be able to quickly identify EVD suspects, basic management and IPC. Hospital staff had also received the Ebola vaccine in November 2018. In addition, Kagando Hospital participated in the functional district-level simulation exercise in April 2019. When the boy was admitted, Kagando Hospital health workers suspected EVD and referred him to an Ebola Treatment Unit (ETU) at Bwera Hospital that had been set up during the preparedness phase (Figure 3). There, a blood sample was collected for PCR testing and EVD was confirmed within 48 hours of collection by the Uganda Virus Research Institute (UVRI) VHF Laboratory in Entebbe (425 kms from Bwera Hospital).

 

On 11 June 2019, two of the boy´s five accompanying relatives also developed symptoms, sought care at Bwera Hospital, and were referred to the ETU where blood samples were collected for PCR testing at UVRI. EVD was confirmed in two of the boy´s relatives, including the boy´s mother, while the other three tested negative (Figure 4).

 

A high-level ministerial cross-border meeting between DRC and Uganda held in Kasese District on 11 June 2019 agreed on the repatriation of cases and family members, which occurred the next morning. In addition, the meeting participants prepared a bilateral Memorandum of Understanding on cross-border collaboration and established formal information-sharing mechanisms, including situation reports. As Uganda was still processing the importation of the EVD vaccine, DRC agreed to share 100 doses of vaccine to immunize high-risk contacts of the EVD patients. In total, 78 of the 114 contacts were vaccinated against EVD using the rVSV-ZEBOV vaccine (Figure 5). All healthcare workers who had exposure to the patients had already been vaccinated during the preparedness period except one who received the vaccine within five days of exposure.

 

All three EVD patients who crossed into Uganda died; the index and second case died and were buried in Uganda while the third case died in DRC during the process of repatriation. The three surviving family members were repatriated to DRC. In Kasese District, an emergency response team comprising national and local responders trained during preparedness identified and listed 114 contacts of the 3 EVD patients and followed them up with a 100% follow-up reporting rate for 21 days.

 

None of the contacts developed EVD symptoms after 21 days of observation. The outbreak was thus contained, with no transmission within the community in Kasese District, and declared over after 42 days on 28 October 2019 [10] (representing two incubation periods after the index cases exited Uganda). The outbreak response was district-led with support from the National Task Force and partners.

 

The response and preparedness plan was costed at USD 17.2 million by the Uganda MOH, of which USD 10 million (59%) was raised for its implementation by the partners.

 

Post-outbreak activities

 

Risk mapping was repeated on 12 June 2019, after confirmation of the outbreak, and districts were reclassified into 3 categories based on the level of risk (Figure 6): Category 1 (district with ongoing outbreak: Kasese District); Category 2 (10 high-risk districts bordering Kasese and/or with direct routes to/from DRC´s EVD outbreak epicenters), and Category 3 (13 moderate-risk districts that required enhanced preparedness due to population movements and/or refugee hosting).

 

Discussion

 

Sustained preparedness activities assessed by the simulation exercise in high-risk areas of Uganda may have enabled the containment of an Ebola outbreak at its importation site without further spread. This underscores the importance of investment in preparedness and a focus on operational readiness in high-risk areas. Implementing effective preparedness activities during the West Africa Ebola outbreak in the African region and countries with direct travel links could have significantly reduced the risk of global importation [11]. Additionally, prior vaccine administration for frontline health workers may have protected health workers in Kagando Hospital who had close contact with the confirmed cases [12, 13].

 

Readiness at the hospital and community levels requires substantial effort and investment that may have prevented a much more widespread and costly EVD outbreak involving high morbidity and mortality [12].

 

Uganda experienced Ebola outbreaks in the past, which compelled the nation to improve its preparedness and response strategies to manage health crises [13]. Steps undertaken to bolster Ebola preparedness: 1) strengthened surveillance systems to ensure early detection of outbreaks including enhancing information systems and laboratory specimen referral networks for real-time reporting, 2) training health workers, 3) establishment of Public Health Emergency Operations Centres to coordinate and support for outbreak response activities 4) building trust and educating local communities to participate in surveillance and reporting, as well as understanding preventive measures. 5) Uganda works with international bodies such as WHO and CDC to improve its regulatory framework for managing infectious diseases and to access resources and expertise that aid in preparedness and response. 6) Uganda has learned the importance of allocating resources to prepare for health emergencies, which include both financial investment and human resources [13, 6].

 

While Uganda's efforts significantly improved its readiness to confront Ebola from a score of 50% in June 2018 to 84% in June 2019, maintaining and updating these health systems is crucial, especially considering evolving threats and the challenges posed by other concurrent health crises [14].Preparation is also about building resilient health systems that not only respond to outbreaks but also ensure the continuity of essential health services during crises [14].

 

Many of the lessons learned during the West Africa Ebola outbreak have been translated into improved preparedness measures: like capacity building for health workers, engaging local communities in surveillance, reporting and public health measures, establishing and equipping treatment centres, and improving the overall health infrastructure to manage potential outbreaks. Lessons include enhanced disease surveillance and availability of rapid response systems to quickly identify and isolate cases, trace contacts, and limit the spread of the virus. Advocating for financial and technical support from international and local organizations to support response efforts and vaccine stockpiling are also critical in Ebola preparedness [14, 15].

 

Despite the lessons West African countries learnt, they continue to face challenges in maintaining sustained funding, coordination, and political will to keep public health systems ready for Ebola and other infectious diseases. A continuous commitment to international cooperation and investment in healthcare infrastructure is necessary to maintain and further enhance preparedness levels [15, 16].

 

Wolicki also emphasizes strengthening cross border collaborations and information sharing to prevent infectious diseases spreading across boundaries [17]. Cross border collaboration between Uganda and DRC was a significant benefit in the quick detection of Ebola cases in Uganda following communication and information sharing from DRC. This was facilitated by prior cross border engagements between DRC, Uganda and other at-risk countries in October 2018 when a ministerial meeting was held to formalize cross border collaboration and information sharing. This was followed by a second bilateral meeting held in December 2018 that focussed on drafting a memorandum of understanding on information sharing and cross border collaboration between Uganda and DRC and formation of surveillance zones between the two countries [6].

 

The West Africa Ebola outbreak in 2014-2016 was costly and estimated that over $3.6 billion was spent by international donors and affected countries in response to the outbreak [18]. Response to an outbreak like Ebola can be vastly expensive due to the need for rapid mobilization of a large-scale, coordinated effort involving emergency medical care, deploying health workers, setting up isolation units and field hospitals, significant quantities of medical supplies and protective gear, logistical support, and public health interventions to control the spread. Additionally, there are indirect costs such as economic disruptions, trade restrictions, and decreased productivity [18]. While effective preparedness measures are much less costly; however, they require consistent investment and a long-term outlook [19]. Although the cost of preparedness is substantial, the economic impact of an uncontained Ebola outbreak could be far more severe, with long-term detrimental effects on the national economy and public health systems. While a cost benefit analysis for preparedness has not been undertaken in Uganda, proactive investment in Ebola preparedness is both a necessary and cost-saving measure over the long term.

 

Preparedness is more cost-effective in the long term, as it can prevent epidemics that are both humanly devastating and economically disastrous [20].

 

The Government of Uganda was able to mobilize preparedness resources in cash, and in kind from partners due to the existing collaboration and continuous accountability for transparency. International and nongovernment partnerships facilitate joint advocacy and resource mobilization, hence pooling resources for broader funding streams.

 

Repeated risk mapping is a proactive process to preparedness and control of Ebola. This prevents Ebola from becoming a worldwide threat by deploying targeted interventions for affected areas. It is also used for strategically guiding allocation of limited resources to prevent Ebola spread and control transmission.

 

Uganda conducted repeated risk mapping which was informed by the dynamics of the geographical distribution of Ebola in DRC. District categorization in the preparedness phase was informed by proximity to hot spots in DRC while the recategorization was based on declaration of an outbreak in Kasese district which was previously identified as a high-risk district and preparedness measures had been deployed [6, 20]. Lesson learnt was that risk mapping contributes to better understanding of the geospatial distribution and aides in anticipation and mitigation of future outbreaks hence should be conducted repeatedly as the outbreak evolves.

 

 

Investing in and maintaining epidemic preparedness during Ebola response, especially in high-risk areas with potential importation, is crucial. This proactive approach can lead to rapid detection and an effective response when faced with an imminent threat.

 

 

The authors declare no competing interests.

 

Funding

 

The EVD response activities were supported by the Ministry of Health, Uganda, Development Partners, and International Agencies. The findings and recommendations in this manuscript represent the opinions of the authors and do not represent the official positions of the funding agencies.

 

 

The Ministry of Health and partners responded to the EVD outbreak in Kasese District, Uganda. SN, ANM, IM, ARA, BK, AAK, LB, DNG, MN, PM, IK, FO, JH, JHo, VB, JO, DM, IMA, SK, and AM participated in data collection and management and manuscript writing and technical input. LB, AAR, JH, JHo, VB, HGM, and MN reviewed the manuscript for intellectual content. All authors contributed to writing and approval of the final manuscript.

 

 

We thank the Incident Management Team – National Task Force, Kasese District Local Government and all partners and bilateral donors that made it possible for the prompt containment of the EVD outbreak in Kasese District, Uganda, as well as the UVRI VHF Lab through its support from the Viral Special Pathogens Branch, Centers for Disease Control and Prevention, Atlanta, USA, for building capacity to detect, prevent and control EVD and other VHFs before and during this exercise.

 

 

Figure 1: Planning and execution of the full-scale simulation exercise at two points of entry (Mpondwe, Kasese and Entebbe International), Kisinga community in Kasese district and at the national level, Uganda, April 2019

Figure 2: Capacities built/trainings conducted in high-risk districts during the EVD preparedness phase, Uganda 2018-2019

Figure 3: Movement of Ebola cases from Beni, DRC into Kasese District, Uganda, through an undesignated crossing point at Mpondwe, June 2019

Figure 4: Timeline of Ebola outbreak from alert identification to death of last imported case from DRC, Uganda, June 2019

Figure 5: Number of persons vaccinated during the Ebola outbreak in Kasese District, Uganda, June 2019

Figure 6: Map of Uganda showing Ebola Virus Disease district risk classification, June 2019

 

 

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