Workforce capacity assessment for public health emergencies, disaster preparedness and response in the Economic Community of West African States (ECOWAS) region, April - July, 2018

Virgil Lokossou¹, Kofi Mensah Nyarko², Emma Edinam Kploanyi³, Delia Akosua Bandoh⁴, Patrick Nguku⁵, Bernard Sawadogo⁶, Simon Nyovuura Antara⁷, Ernest Kenu⁴

 

¹ECOWAS Regional Center for Disease Surveillance and Control, Abuja, Nigeria, ²University of Environment and Sustainable Development, Somanya, Ghana, ³University of Ghana School of Public Health, Legon Accra, Ghana, ⁴Ghana Field Epidemiology and Laboratory Training Programme, University of Ghana School of Public Health, Accra, Ghana, ⁵African Field Epidemiology Network Nigeria, Abuja Nigeria, ⁶Burkina Field Epidemilogy and Laboratiory Training Programme, Ouagaduogu, Burkina Faso, ⁷African Field Epidemiology Network, Kampala, Uganda

 

 

^&Corresponding author
Prof Kofi Mensah Nyarko, University of Environment and Sustainable Development, Somanya, Ghana

 

 

 

 

Epidemics of infectious diseases such as cholera, meningococcal meningitis, yellow fever and viral hemorrhagic diseases particularly Ebola virus disease (EVD) and Lassa fever continue to occur in West Africa [1-6]. The attendant devastating consequences have been detrimental to development and stability in the sub-region. The EVD outbreak from 2014 to 2016 affected six countries in the Economic Community of West African States (ECOWAS) region (Guinea, Liberia, Mali, Nigeria, Senegal, and Sierra Leone). This crisis exposed the limited regional response capacities to outbreaks in terms of disease surveillance, preparedness and rapid response strategies; this has been blamed on the lack of a well-trained health workforce, late detection and wide geographic spread of the epidemic [7,8].

 

Workforce development which includes field epidemiology and related training is one of the major core capacities of the International Health Regulations (IHR) to detect, assess, report, notify and respond to public health events and emergencies of national and international concern. This is also one of the technical areas of the Joint External Evaluation (JEE) which most countries in the West African sub-region identified as a major gap and thus planned to improve it as outlined in their respective NAPHS [9-11]. This highlights the Global Health Security Agenda call for “sufficient field epidemiologic capacity in every country to rapidly detect, respond to, and contain public health emergencies, thereby ensuring global health security”[12].

 

In the wake of the EVD outbreak in the sub-region, the 47th ECOWAS Authority of Heads of State in May 2015 endorsed the establishment of the Regional Centre for Surveillance and Disease Control (ECOWAS/RCSDC), mandating the West African Health Organisation (WAHO) to support its operationalization [13,14]. Consequently, WAHO developed the ECOWAS Regional Strategic Preparedness and Response Plan for Public Health Emergencies to build epidemiologic capacity for rapid response to epidemics and other public health emergencies.

 

Building workforce capacity in disease surveillance and rapid response strategies requires that training goes beyond the traditional approaches that emphasize only on knowledge acquisition to embrace experiential training for competency acquisition [15]. In many countries, Field Epidemiology Training Programs (FETPs) have proven to be successful models for building skilled public health workforce capacity [16]. The three-tiered approach of FELTP (advanced, intermediate and frontline) has been implemented in the region since 2007. The 2-year advanced-level program trains residents to work at national surveillance and disease control programs. Currently, there are three advanced FELTP programs in West Africa situated in Ghana, Burkina Faso, and Nigeria. The frontline-level training was intensified after the EVD outbreak in 2014 as the healthcare workforce was depleted in affected countries through the many deaths that occurred in the initial months of the outbreak [17-19]. The frontline workforce comprises the veterinarians, physicians, clinical officers, nurses, and other public health workers at primary healthcare facilities who are usually the first point of call during public health emergencies. However, they usually have minimal field epidemiology skills but if they are well trained, they can detect threats early and respond rapidly to public health emergencies [20].

 

Globally, FETPs supported by US Centers for Disease Control and Prevention (CDC) have deployed their residents to respond to over 3,300 outbreaks since 2005[21]. These practical experiences, although mostly local, have equipped trainees to respond to both national and international public health emergencies [21]. For instance, during the Ebola epidemic (2014-2016) in West Africa, FETP trainees from over nine (9) African countries actively participated in investigation and response activities; they functioned as epidemiologists, laboratory scientists, surveillance officers among others[22]. In particular, the residents and graduates of the Nigeria Field Epidemiology and Laboratory Training Program (FELTP) supported contact tracing that prevented a major EVD epidemic in the country contrary to the rapid spread in neighboring countries without FETPs [23,24]. The rapid response strategies employed to address the outbreak of EVD in Lagos, Nigeria is a clear example of how a competent public health workforce could control an epidemic even in such a densely populated city in the region [24]. Also, control of the EVD outbreak in various counties in Liberia is partly attributable to the efforts of FETP graduates. It is evident that such training when expanded would develop stronger health systems that are capable of responding to epidemics of such magnitude in the near future [22].

 

In this study, we assessed the field epidemiology workforce capacity in the 15 Member States as against the global standard of 5 epidemiologists per million population.

 

 

Study design

 

A cross-sectional study was conducted across all 15 Member States of the ECOWAS region. Information was gathered from desk reviews on workforce development in relation to Public Health Emergency Preparedness, response, and recovery. Also, interviews with stakeholders in health in each country were conducted during field visits and or through teleconference from April to July 2018.

 

Study population

 

The Ministries of Health and other relevant public health agencies in each country were involved in the assessment. Representatives from each organization were interviewed.

 

Data collection tools

 

The data collection tools used in this study included a data review tool, a structured questionnaire, and an interview guide. These tools were developed based on the WHO International Health Regulation (IHR) core capacities [9]. Workforce capacity was assessed in relation to four of the sixteen (16) major areas of the WHO IHR core capacities including Rapid Response Capacity, Clinical Case Management, Availability of Epidemiology/ Surveillance and Related Capacity (Institutional Capacity), and Health Sector Workforce Development Plan. Specifically, epidemiology workforce capacity was assessed in relation to number of field epidemiologists, level of training from FETP and public health-related programs, and skill/functionality. Although functionality was not directly measured, it was assumed that the completion of the competency training served as a proxy for functionality because all FETP trainees had experience in field practice as part of the training and pre-requisite to graduation: they should have participated in at least one outbreak investigation and analysed at least one surveillance data set. This is because the role of field epidemiologists in the health system is cross-cutting in all four functions assessed. They are mostly used in West African context to strengthen surveillance, rapid response, and provide clinical case management where needed.

 

These tools were pre-tested and validated by WAHO and Ministers of Health in West Africa. Policy documents were verified where necessary during data collection.

 

Data collection

 

Data were collected from April to August 2018 in two phases. The first phase comprised the desk review of each country´s IHR capacity scores, Joint External Evaluation (JEE) report and actions implemented after JEE. Desk reviews of the national surveillance and response documents (policies, systems, plans, structures, coordination mechanisms, documents on simulation exercises, responsibilities, procedures, guidelines, and available assessment reports) were carried out at the regional and country-level.

 

Face to face interviews were conducted in the second phase using a structured questionnaire to assess the status of each country´s surveillance and response capacity as well as their respective roles in health emergency preparedness and response. Key informant interviews were conducted with country representatives from each Member State. All relevant data on the policies, plans, guidelines, and literature available on public health emergencies were assessed during data collection.

 

Data analysis

 

Data gathered from key informant interviews were transcribed and analyzed under major themes based on the WHO IHR core capacities. Data generated from desk reviews and document verification were also analyzed under these themes and triangulated with the interviews.

 

For the purposes of this study, the “field epidemiology workforce” was defined as any person working in an applied or field epidemiology role or acute public health responder role”[25]. The required number of field epidemiologists for each country was calculated using the country´s population as against the global standard of 5 epidemiologists per million population [10]. For the ECOWAS region, the population size used was 400 million at the time of assessment. This was calculated for the three FETP tiers. The estimation for the frontline FETP trained healthcare workers was based on sub-national units (districts/Local Government Areas) and depending on the country´s administrative unit´s size the requirement for frontline graduates was more than 1 graduate, preferably one in human health, animal in animal and one in environmental health per district/LGA cutting across human health, animal and environment in the all-hazard/one health approach. There were over 2000 districts/LGA in the region across the 15 countries, with a population range of 150,000 - 250,000 per district/LGA. The gaps in the number of trainees from the three tiers were quantified for each Member State. Spot maps were also drawn using the QGIS software to show the density of trained field epidemiologists by location in the region.

 

Ethical considerations

 

The Ministries of Health of all West African countries in ECOWAS gave their approval through WAHO for this assessment. Interviews were only conducted after participants gave their approval based on the explanation of the purpose of the assessment. Participants and countries had the liberty to withdraw from the assessment at any point and they were assured it would not affect them in any way as a nation.

 

 

Country-Specific Analysis for Field Epidemiologists

 

Trained workforce by FETP Tiers in Member States

 

The workforce country-specific analysis presented in Table 1 indicated a total of 358(18.4%) field epidemiologists with Advanced/Intermediate training in the ECOWAS region whereas there were 2,437(22.2%) with frontline training as of October 2018. The assessment found only 5 Member States out of the 15 that had at least one-fifth of the required number of field epidemiologists. They include Nigeria (22.7%), The Gambia (26.7%), Sierra Leone (40.0%), Ghana (45.0%), and Liberia (72.0%) which recorded the highest. The distribution of these trained field epidemiologists by country are shown in Figure 1. About half of the Member States in the region had over 20% frontline graduates. Nigeria (22%), Benin (25.0%), Liberia (32.9%), Ghana (34.9%), Sierra Leone (40.5%), Togo (47.3%), Guinea-Bissau (63.1%) and The Gambia (66%) constituted these 7 countries Table 1.

 

The gap in workforce development

 

The assessment estimated that approximately 1,950 field epidemiologists and 11,000 frontline graduates were required to meet the global standard. Although there were trained field epidemiologists identified in almost all Member States, there was still a wide gap of 1,592(81.6%) to make up for the required 2000 graduates Table 2. Also, 8,563(77.9%) frontline graduates were required to satisfy the 11,000 target. No Member State satisfied the required number of field epidemiologists. Moreover, Cabo Verde was the only Member State that did not record any trainees from either of the three FELTP tiers. Guinea-Bissau had no Advanced/Intermediate trained epidemiologists whereas Niger recorded no frontline graduates at the time of assessment. The six Member States in the region (Guinea, Liberia, Mali, Nigeria, Senegal, and Sierra Leone) where Ebola outbreaks had occurred had inadequate numbers of field epidemiologists required to respond to epidemics and health emergencies. No country had recorded half of the required number of advanced/intermediate or frontline trainees except Liberia that had 72.0% of the required number of trained field epidemiologists. There was only 32.9% of the required number of frontline graduates at the time of assessment. The gaps in the workforce for each Member State are shown in Figure 1 and Figure 2. It was observed that countries with the lowest density of field epidemiologists were farther away from those that had higher densities which clustered together.

 

For all countries assessed, there were inadequate numbers of public health personnel especially field epidemiologists, to implement IHR core capacity requirements. Apart from Ghana, none of the assessed countries had a full complement of all three FETP (basic, intermediate, and advanced). Poor in-country coordination of activities among the available personnel in the containment of epidemics and health emergencies was also identified.

 

 

The assessment revealed that there was an inadequate number of trained field epidemiologists in all Member States as a wide gap was identified measuring against the required number of frontline and advanced/intermediate trainees for each state. Liberia recorded the highest number of epidemiologists. Apart from Ghana, none of the assessed countries had a full complement of all three tiers of field epidemiology training.

 

This is worrying because field epidemiologists play the critical role of initiating the rapid response process to outbreaks through disease surveillance, contact tracing, determining how the infection is transmitted, and predicting where the outbreak is headed and its magnitude [26]. They generate data that inform decisions in outbreak management. The Ebola outbreak that occurred between 2014 and 2016 was the real test of regional preparedness and response for public health emergencies. Post-outbreak assessments implicated weak health systems as a major factor underlying the widespread and prolonged nature of the EVD outbreak [27]. This was influenced by the deficit in the health workforce that tackled the outbreak [28]. It was evident from this epidemic that the affected countries were caught off guard and unprepared [29] Two years post-outbreak, the six affected countries in the region still had inadequate numbers of field epidemiologists. It would have been expected that these countries would record far higher numbers drawing from their experience yet only one of them (Liberia) had over half of the required number of trained field epidemiologists. Generally, there were more frontline than advanced trainees in these countries. The gap identified by this assessment corroborates the need for long-term efforts to improve health systems especially in field epidemiological capacity in Member States towards a more rapid response to and management of future outbreaks [30]. Competency training in field epidemiology especially for health care workers who are at the frontline is crucial as the lack of it delayed an appropriate response during the outbreak with some of them leaving their post because of the fear of being infected [26,31,32]. It is not necessarily new response methods that are required, rather, an adequate workforce and coordination [33]. There is evidence of the poor coordination at the district level in managing the EVD control activities in Guinea [34]. Poor in-country coordination of activities among the few available personnel in the containment of epidemics and health emergencies was still a problem identified by this assessment. The workforce data should be regularly reviewed not only to assess the attainment of targets but to identify opportunities for refinement to serve the public health priorities of the country.

 

Until amended, the current IHR definition of a public health emergency of international concern (PHEIC) implies that outbreaks must necessarily overstep a national border before they warrant an international response [9,35]. Although the WHO has identified the need to transform organizational culture and delivery, that will not be sufficient to prevent and mitigate future outbreaks. This reiterates the need to build local capacity in preparation for imminent epidemics without overly relying on international interventions. This requires full political support from Member States for implementing the IHR core capacities for public health [36]. Such commitment to improving preparedness capability must reflect in fiscal budgetary changes and allocation as well as capacity building [37]. A failure in this regard only renders local economies of Member States vulnerable to a similar fate suffered by the high-transmission countries (Guinea, Liberia and Sierra Leone) who together lost over $2 billion due to the EVD outbreak in just two years [38] As at the time of assessment, there was no budgetary allocation for public health emergency preparedness.

 

The recent EVD epidemic has revealed that we are only as safe as the least prepared States [39] Findings from the assessment indicated that Cabo Verde was the only Member State that did not record any trainees from either of the three FELTP tiers. Guinea-Bissau had no Advanced/Intermediate trained epidemiologists whereas Niger recorded no frontline graduates. Although the Ebola outbreak did not occur in any of these countries, there are other epidemics that have occurred in previous years. Cabo Verde experienced a Zika virus outbreak in 2015 with unprecedented magnitude in Africa and it was the first to be associated with microcephaly in the continent. Earlier in 2009, there was also an unprecedented epidemic of dengue virus in the same island country. Although these were single outbreaks, they resulted in sequential epidemic waves due to the unique epidemiological setting in Cabo Verde thus accentuating the need for an improved and integrated surveillance system to address imminent outbreaks in the country [40,41] Such surveillance systems can only be implemented by skilled field epidemiologists. A chickenpox outbreak lasting for over 6 months was also reported in Guinea-Bissau [42] as well as a meningitis outbreak in Niger [43]. Two of these three countries: Cabo Verde and Niger, as well as the other Member States with lower densities of field epidemiologists were identified in this assessment to be farther away from those with higher densities which clustered together. Therefore, it is imperative that Member States support each other in improving epidemiological capacities as local and across border efforts are concerted in ensuring adequate preparedness [39].

 

The contribution of FETP trainees in mitigating the EVD outbreak in Nigeria and Liberia[22-24] shows the critical role being played by the three FETPs in the region. However, apart from Ghana, none of the assessed countries has a full complement of all three FETP tiers (basic/frontline, intermediate, and advanced). The competency training offered by FETPs combines veterinary and public health prediction-based surveillance to help identify zoonotic diseases before transmission to humans and their adequate management [44,45]. Also, frontline health workers are trained to be able to detect health threats early and respond rapidly to public health emergencies.[46] Moreover, programme ownership by ministries of health and local universities ensures the integration of graduates into the health system [18]. Another advantage of these programmes is that they are under a networking body (AFENET) that ensures coordination across countries in Africa hence fostering cross-border collaborations between trainees which can be harnessed in the event of a public health emergency. This highlights the need for more of these training programmes to be established in other Member States to widen coverage.

 

Study limitations

 

The assessment did not cover the utilization /deployment of FETP trainees within the systems. Also, interviews were only conducted at the national level hence we could not provide a detailed description from training institutions and FETP trainees of the underlying factors related to the deficiencies in epidemiology workforce capacity. These could be considered in future assessments of epidemiologic capacity.

 

 

The assessment revealed that there was an inadequate number of trained field epidemiologists in all Member States as a wide gap was identified measuring against the required number of frontline and advanced/intermediate trainees for each State. This is an indication that more resources should be invested into building local epidemiological capacity to enhance preparedness for and response to public health emergencies.

 

We recommend that the ECOWAS/RCSDC and other multinational public health workforce organizations that support FETPs worldwide engage relevant stakeholders, such as country representatives, regional public health organizations, and other funding institutions, to discuss ways of attaining the field epidemiology workforce targets through collaborative efforts.

 

 

Authors declare no competing interest.

 

 

VL, DAB, KMN, BS, EK participated in the Conceptualisation, data collection, report writing, drafting the manuscript, and finalizing manuscript writing. EEK AND SNA participated in drafting and finalizing manuscript writing. All authors read and approve the final version of the manuscript.

 

 

We would like to acknowledge all countries and institutions who participated and assisted us through the data collection process.

 

 

Table 1: Country Specific Analysis for Field Epidemiologists

Table 2: Country Specific Analysis for Field Epidemiologists

Figure 1: Map Showing the Gap and Available advanced FELTPs

Figure 2: Map showing the Gap and available frontline FELTPs

 

 

1. Greenwood B. 100 years of epidemic meningitis in West Africa-has anything changed? Trop Med Int Heal. 2006; 11(6):773-80.https://doi.org/10.1111/j.1365-3156.2006.01639.x . Google Scholar


2. Ehichioya DU, Hass M, Olschläger S, Becker-Ziaja B, Onyebuchi Chukwu CO, Coker J, Nasidi A, Ogugua OO, Günther S, Omilabu SA. Lassa fever, Nigeria, 2005-2008. Emerg Infect Dis. 2010 Jun; 16(6):1040-1.https://doi.org/10.3201/eid1606.100080 PubMed | Google Scholar


3. Franco L, Di Caro A, Carletti F, Vapalahti O, Renaudat C, Zeller H, Tenorio A. Recent expansion of dengue virus serotype 3 in West Africa. Eurosurveillance. 2010; 15(7):19490.https://doi.org/10.2807/ese.15.07.19490-en . Google Scholar


4. Anyamba A, Chretien JP, Small J, Tucker CJ, Formenty PB, Richardson JH, Britch SC, Schnabel DC, Erickson RL, Linthicum KJ. Prediction of a Rift Valley fever outbreak. Proc Natl Acad Sci. 2009; 106(3):955-9.https://doi.org/10.1073/pnas.0806490106 . Google Scholar


5. Monath TP, Vasconcelos PFC. Yellow fever. J Clin Virol. 2015; 64:160-73.https://doi.org/10.1016/j.jcv.2014.08.030 . Google Scholar


6. Baize S, Pannetier D, Oestereich L, Rieger T, Koivogui L, Magassouba N, Soropogui B, Sow MS, Keïta S, De Clerck H, Tiffany A, Dominguez G, Loua M, Traoré A, Kolié M, Malano ER, Heleze E, Bocquin A, Mély S, Raoul H, Caro V, Cadar D, Gabriel M, Pahlmann M, Tappe D, Schmidt-Chanasit J, Impouma B, Diallo AK, Formenty P, Van Herp M, Günther S. Emergence of Zaire Ebola virus disease in Guinea. N Engl J Med. 2014; 371(15):1418-25.https://doi.org/10.1056/nejmoa1404505 Google Scholar


7. Gostin LO, Friedman EA. Ebola: a crisis in global health leadership. Lancet. 2014;384(9951):1323-5.https://doi.org/10.1016/S0140-6736(14)61791-8 . Google Scholar


8. Ameme DK. West African Ebola epidemic: lessons and a call to action. Pan Afr Med J. 2015 Oct 10;22 Suppl 1(Suppl 1):2. https://doi.org/10.11694/pamj.supp.2015.22.1.6040 PubMed | Google Scholar


9. World Health Organization (WHO). International health regulations (2005). World Health Organization. 2008. Accessed Oct 2022.


10. World Health Organization. Joint external evaluation tool: International Health Regulations (2005) .[Internet] 2nd ed. Geneva: World Health Organization. 2018. Accessed May 2022.


11. WHO. National Action Plan for Health Security. Accessed May 2022.


12. Nsubuga P, Nwanyanwu O, Nkengasong JN, Mukanga D, Trostle M. Strengthening public health surveillance and response using the health systems strengthening agenda in developing countries. BMC Public Health. 2010 Dec 3;10 Suppl 1(Suppl 1):S5.https://doi.org/10.1186/1471-2458-10-S1-S5 PubMed | Google Scholar


13. ECOWAS Commission. ECOWAS Revised Treaty. Abuja: ECOWAS Commisision. 1993. Accessed Oct 2022.


14. West African Health Organization (WAHO). Strategic Plan 2016-2020. Bobo-Dioulasso. WAHO. 2016. Accessed Oct 2022.


15. Koo D, Thacker SB. In Snow´s footsteps: commentary on shoe-leather and applied epidemiology. Am J Epidemiol. 2010; 172(6):737-9.https://doi.org/10.1093/aje/kwq252 . PubMed | Google Scholar


16. Schneider D, Evering-Watley M, Walke H, Bloland PB. Training the global public health workforce through applied epidemiology training programs: CDC´s experience, 1951-2011. Public Health Rev. 2011; 33(1):190.https://doi.org/10.1007/BF03391627 . Google Scholar


17. World Health Organization (WHO). Health worker Ebola infections in Guinea, Liberia and Sierra Leone: a preliminary report 21 May 2015. World Health Organization. 2015. Accessed Oct 2022.


18. Mukanga D, Namusisi O, Gitta SN, Pariyo G, Tshimanga M, Weaver A, Trostle M. Field Epidemiology Training Programmes in Africa - Where are the Graduates? Hum Resour Health. 2010 Aug 9; 8(1):18https://doi.org/10.1186/1478-4491-8-18 PubMed | Google Scholar


19. Nsubuga P, Johnson K, Tetteh C, Oundo J, Weathers A, Vaughan J, Elbon S, Tshimanga M, Ndugulile F, Ohuabunwo C, Evering-Watley M, Mosha F, Oleribe O, Nguku P, Davis L, Preacely N, Luce R, Antara S, Imara H, Ndjakani Y, Doyle T, Espinosa Y, Kazambu D, Delissaint D, Ngulefac J, Njenga K. Field Epidemiology and Laboratory Training Programs in sub-Saharan Africa from 2004 to 2010: need, the process, and prospects. Pan Afr Med J. 2011;10:24.https://doi.org/10.4314/pamj.v10i0.72235 PubMed | Google Scholar


20. Roka ZG, Githuku J, Obonyo M, Boru W, Galgalo T, Amwayi S, Kioko J, Njoroge D, Ransom JA. Strengthening health systems in Africa: a case study of the Kenya field epidemiology training program for local frontline health workers. Public Health Rev. 2017 Oct 24; 38:23.https://doi.org/10.1186/s40985-017-0070-7 PubMed | Google Scholar


21. Jones DS, Dicker RC, Fontaine RE, Boore AL, Omolo JO, Ashgar RJ, Baggett HC. Building Global Epidemiology and Response Capacity with Field Epidemiology Training Programs. Emerg Infect Dis. 2017 Dec; 23(13):S158-65.https://doi.org/10.3201/eid2313.170509 PubMed | Google Scholar


22. Lubogo M, Donewell B, Godbless L, Shabani S, Maeda J, Temba H, Malibiche TC, Berhanu N. Ebola virus disease outbreak; the role of field epidemiology training programme in the fight against the epidemic, Liberia, 2014. Pan Afr Med J. 2015 Oct 10; 22 Suppl 1(Suppl 1):5. https://doi.org/10.11694/pamj.supp.2015.22.1.6053 PubMed | Google Scholar


23. Ohuabunwo C, Ameh C, Oduyebo O, Ahumibe A, Mutiu B, Olayinka A, Gbadamosi W, Garcia E, Nanclares C, Famiyesin W, Mohammed A, Nguku P, Koko RI, Obasanya J, Adebayo D, Gbadegesin Y, Idigbe O, Oguntimehin O, Nyanti S, Nzuki C, Abdus-Salam I, Adeyemi J, Onyekwere N, Musa E, Brett-Major D, Shuaib F, Nasidi A. Clinical profile and containment of the Ebola virus disease outbreak in two large West African cities, Nigeria, July-September 2014. Int J Infect Dis. 2016; 53:23-9.https://doi.org/10.1016/j.ijid.2016.08.011 . Google Scholar


24. Shuaib F, Gunnala R, Musa EO, Mahoney FJ, Oguntimehin O, Nguku PM, Nyanti SB, Knight N, Gwarzo NS, Idigbe O, Nasidi A, Vertefeuille JF; Centers for Disease Control and Prevention (CDC). Ebola virus disease outbreak - Nigeria, July-September 2014. MMWR Morb Mortal Wkly Rep. 2014 Oct 3; 63(39):867-72. PubMed | Google Scholar


25. Parry AE, Kirk MD, Durrheim DN, Olowokure B, Colquhoun SM, Housen T. Shaping applied epidemiology workforce training to strengthen emergency response: a global survey of applied epidemiologists, 2019-2020. Hum Resour Health. 2021; 19(1):58.https://doi.org/10.1186/s12960-021-00603-1 . PubMed | Google Scholar


26. Nsubuga P. The Ebola outbreak in West Africa: a story of related public health challenges and a pointer to solutions to mitigate the inevitable next outbreak. Pan Afr Med J. 2014 Sep 22;19:48.https://doi.org/10.11604/pamj.2014.19.48.5336 PubMed | Google Scholar


27. Kim JY, Farmer PE. What´s missing from the Ebola fight in West Africa. The Washington Post. 2014 Aug 31; 31.


28. Shoman H, Karafillakis E, Rawaf S. The link between the West African Ebola outbreak and health systems in Guinea, Liberia and Sierra Leone: a systematic review. Global Health. 2017 Jan 4;13:1.https://doi.org/10.1186/s12992-016-0224-2 PubMed | Google Scholar


29. Forrester JD, Pillai SK, Beer KD, Neatherlin J, Massaquoi M, Nyenswah TG, Montgomery JM, De Cock K; Centers for Disease Control and Prevention (CDC). Assessment of ebola virus disease, health care infrastructure, and preparedness - four counties,Southeastern Liberia, august 2014. MMWR Morb Mortal Wkly Rep. 2014 Oct 10; 63(40):891-3. PubMed | Google Scholar


30. Youde J. The ebola outbreak in guinea, liberia, and sierra leone [Internet]. E-International Relations. 2014 [cited 2022 Nov 3].


31. Pathmanathan I, O'Connor KA, Adams ML, Rao CY, Kilmarx PH, Park BJ, Mermin J, Kargbo B, Wurie AH, Clarke KR; Centers for Disease Control and Prevention (CDC). Rapid assessment of Ebola infection prevention and control needs--six districts, Sierra Leone, October 2014. MMWR Morb Mortal Wkly Rep. 2014 Dec 12; 63(49):1172-4. Google Scholar


32. Delamou A, Beavogui AH, Kondé MK, van Griensven J, De Brouwere V. Ebola: better protection needed for Guinean health-care workers. Lancet. 2015; 385(9967):503-4.https://doi.org/10.1016/S0140-6736(15)60193-3 . Google Scholar


33. Petherick A. Ebola in west Africa: Learning the lessons. Lancet. 2015; 385(9968):591-2.http://dx.doi.org/10.1016/S0140-6736(15)60075-7 . Google Scholar


34. Thiam S, Delamou A, Camara S, Carter J, Lama EK, Ndiaye B, Nyagero J, Nduba J, Ngom M. Challenges in controlling the Ebola outbreak in two prefectures in Guinea: why did communities continue to resist? Pan Afr Med J. 2015 Oct 11; 22 Suppl 1(Suppl 1):22.https://doi.org/10.11694/pamj.supp.2015.22.1.6626 PubMed | Google Scholar


35. Siedner MJ, Gostin LO, Cranmer HH, Kraemer JD. Strengthening the Detection of and Early Response to Public Health Emergencies: Lessons from the West African Ebola Epidemic. PLOS Med [Internet]. 2015 Mar 24;12(3):e1001804.https://dx.plos.org/10.1371/journal.pmed.1001804 . PubMed | Google Scholar


36. Coltart CE, Lindsey B, Ghinai I, Johnson AM, Heymann DL. The Ebola outbreak, 2013-2016: old lessons for new epidemics. Philos Trans R Soc Lond B Biol Sci. 2017 May 26; 372(1721):20160297.https://doi.org/10.1098/rstb.2016.0297 PubMed | Google Scholar


37. Mulinge I, Soyemi K. End of the Ebola virus outbreak: time to reinforce the African health system and improve preparedness capacity. Pan Afr Med J. 2016 Mar 24; 23:121.https://doi.org/10.11604/pamj.2016.23.121.8955 PubMed | Google Scholar


38. The World Bank. Update on the economic impact of the 2014 ebola epidemic on Liberia, Sierra Leone and Guinea. The World Bank. 2014. Accesessed Oct 2022.


39. Heymann DL, Chen L, Takemi K, Fidler DP, Tappero JW, Thomas MJ, Kenyon TA, Frieden TR, Yach D, Nishtar S, Kalache A, Olliaro PL, Horby P, Torreele E, Gostin LO, Ndomondo-Sigonda M, Carpenter D, Rushton S, Lillywhite L, Devkota B, Koser K, Yates R, Dhillon RS, Rannan-Eliya RP. Global health security: the wider lessons from the west African Ebola virus disease epidemic. Lancet. 2015 May 9; 385(9980):1884-901.https://doi.org/10.1016/S0140-6736(15)60858-3 PubMed | Google Scholar


40. Lourenço J, de Lourdes Monteiro M, Valdez T, Monteiro Rodrigues J, Pybus O, Rodrigues Faria N. Epidemiology of the Zika Virus Outbreak in the Cabo Verde Islands, West Africa. PLoS Curr. 2018 Mar 15; 10:ecurrents.outbreaks.19433b1e4d007451c691f138e1e67e8c. https://doi.org/10.1371/currents.outbreaks.19433b1e4d007451c691f138e1e67e8c PubMed | Google Scholar


41. World Health Organization. Dengue fever in Cape Verde. Wkly Epidemiol Rec. 2009;84(469).


42. Depledge DP, Gray ER, Kundu S, Cooray S, Poulsen A, Aaby P, Breuer J. Evolution of cocirculating varicella-zoster virus genotypes during a chickenpox outbreak in Guinea-Bissau. J Virol. 2014 Dec; 88(24):13936-46.https://doi.org/10.1128/JVI.02337-14 PubMed | Google Scholar


43. Burki T. Meningitis outbreak in Niger is an urgent warning. Lancet Infect Dis . 2015 Sep; 15(9):1011.http://dx.doi.org/10.1016/S1473-3099(15)00254-6 . Google Scholar


44. Becker KM, Ohuabunwo C, Ndjakani Y, Nguku P, Nsubuga P, Mukanga D, Wurapa F. Field Epidemiology and Laboratory Training Programs in West Africa as a model for sustainable partnerships in animal and human health. J Am Vet Med Assoc. 2012; 241(5):572-9.https://doi.org/10.2460/javma.241.5.572 . Google Scholar


45. Morse SS, Mazet JA, Woolhouse M, Parrish CR, Carroll D, Karesh WB, Zambrana-Torrelio C, Lipkin WI, Daszak P. Prediction and prevention of the next pandemic zoonosis. Lancet. 2012 Dec 1; 380(9857):1956-65.https://doi.org/10.1016/s0140-6736(12)61684-5 PubMed | Google Scholar


46. André AM, Lopez A, Perkins S, Lambert S, Chace L, Noudeke N, Fall A, Pedalino B. Frontline Field Epidemiology Training Programs as a Strategy to Improve Disease Surveillance and Response. Emerg Infect Dis. 2017 Dec; 23(13):S166-73.https://doi.org/10.3201/eid2313.170803 PubMed | Google Scholar