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Ebola outbreak in , 2014 -2016: Epidemic timeline, differential diagnoses, determining factors, and lessons for future response

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Contents lists available at ScienceDirect

Journal of Infection and Public Health

journa l homepage: http://www.elsevier.com/locate/jiph

Ebola outbreak in West Africa, 2014 – 2016: Epidemic timeline,

differential diagnoses, determining factors, and lessons for

future response

a,b c,∗

Ramat Toyin Kamorudeen , Kamoru Ademola Adedokun ,

d,e

Ayodeji Oluwadare Olarinmoye

a

Public Health Department, University of South Wales, Pontypridd, United Kingdom

b

Children Welfare Unit, Osun State Hospital Management Board, Asubiaro, Osogbo, Osun State, Nigeria

c

Department of Oral Pathology, King Saud University Medical City, Riyadh, Kingdom of Saudi Arabia

d

Engineer Abdullah Bugshan Research Chair for Dental and Oral Rehabilitation (DOR), King Saud University, Riyadh, Kingdom of Saudi Arabia

e

Centre for Control and Prevention of Zoonoses (CCPZ), University of Ibadan, Ibadan, Nigeria

a r t i c l e i n f o a b s t r a c t

Article history: The outbreak of Ebola virus disease (EVD) that raged between 2014 and 2016 in the West African sub-

Received 24 January 2020

region was one of the global epidemics that spiked international public health concern in the last decade.

Received in revised form 15 March 2020

Since the discovery of in 1976, the 2014-2016 epidemics have been the worst with significant

Accepted 17 March 2020

case fatality rates and socioeconomic impact in the affected countries. This review looks at important

health determinants that directly accounted for the spatial events of rapid spread and severity of EVD in

Keywords:

West Africa, with consequent high fatality rates. It also brings up a time-point health determinant model

Ebolavirus

to conceptualize understanding of this important outbreak with a view to enlightening the public and-

Epidemic

providing valuable recommendations that may be crucial to preventing or curtailing any future outbreak

Case fatality

of the disease.

Health determinant model

© 2020 The Author(s). Published by Elsevier Ltd on behalf of King Saud Bin Abdulaziz University for

West Africa

Health Sciences. This is an open access article under the CC BY-NC-ND license (http://creativecommons. org/licenses/by-nc-nd/4.0/).

Contents

Introduction ...... 00

Outbreaks of Ebolavirus in Africa: Epidemic Timeline and Impacts ...... 00

Ebola and Other Infectious Diseases: Differential Diagnoses ...... 00

The Key Health Determinants Associated with High Mortality Rate of 2014-2016 West African Ebola Epidemics ...... 00

Medical Attention and Government Policy: Combinatorial Effects ...... 00

Social factors ...... 00

Seasonal and Climatic Factor...... 00

Physical Environment ...... 00

Health Status and Human Biology ...... 00

Individual risk behaviour ...... 00

Conclusion ...... 00

Recommendations ...... 00

References ...... 00

Introduction

Ebola virus disease (EVD) also known as viral hemorrhagic fever

and hereinafter referred to as Ebola, is a rare but deadly illness

∗

which primarily occurs as a result of the transmission of a deadly

Corresponding author.

E-mail address: [email protected] (K.A. Adedokun). ebolavirus from wild animals particularly fruit bats, to human pop-

https://doi.org/10.1016/j.jiph.2020.03.014

1876-0341/© 2020 The Author(s). Published by Elsevier Ltd on behalf of King Saud Bin Abdulaziz University for Health Sciences. This is an open access article under the CC

BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Please cite this article in press as: Kamorudeen RT, et al. Ebola outbreak in West Africa, 2014 – 2016: Epidemic timeline, differential

diagnoses, determining factors, and lessons for future response. J Infect Public Health (2020), https://doi.org/10.1016/j.jiph.2020.03.014

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Table 1

Mortality and Morbidity Measures of Ebola Outbreak in West Africa from 2014 to 2016.

Year Country Population Cases Death Case Fatality Rate, CFR (%) Incidence Proportion Per 100,000

2014 *DR Congo 73,767,447 66 49 74.2 0.09

2014 Nigeria 176,404,902 20 8 40 0.01

2014–2015 Mali 16,934,214 8 6 75 0.04

2014–2016 * 7,328,834 14,124 3,956 28 192.7

* 4,243,000 10,675 4,809 45 251.6

* 11,738,441 3,811 2,543 66.7 32.5

Key: *Countries that experienced widespread transmission.

ulations [1]. Indeed, the predominant feature of an Ebola outbreak is Overall, no less than 20 Ebola outbreaks with about1, 743 reported

the involvement of human-to-human transmission. Ebolavirus is a human cases were recorded in Africa, between 1977 and 2014 [2].

genus of the virus family . Six species identified from the However, an outbreak which began in late 2013 (but spread widely

genus (ebolavirus) are- Zaire virus, Bundibugyo virus, Sudan virus, between 2014 and 2016) was the largest and first outbreak that

Taï Forest virus, and Bombali virus. Of these species, reached epidemic level and it involved a few West African countries

the Zaire virus or has been the most fatal and (see Table 1).This outbreak was the deadliest and it prompted inter-

most predominant in global outbreaks till date. Since1976, when national public health concern by August of 2014. It resulted in over

Ebola was first discovered in the Democratic Republic of Congo, 28,600 laboratory confirmed cases and nearly 11,300deaths within

not less than thirty-eight outbreaks have been reported across the a short period in the three worst affected countries - Guinea, Liberia,

globe. Although, some outbreaks are limited, in most cases Ebola and Sierra Leone –and an economic cost of about $4.3billion US

outbreaks are widespread [2]. Dollars[2,7]. Another report documented the death of many health

It is important to know that most Ebola outbreaks were success- workers in Guinea, Liberia and Sierra Leone [8]. It is important to

fully put under control in a short time. However, the 2014-2016 mention that apart from these epicenters of the disease, minor

Ebola outbreaks in West Africa matchlessly reached epidemic pro- outbreaks also occurred in other West African countries including

portions with more than 11,000 deaths recorded as a result of rapid Nigeria, Mali and Senegal.

spread, and involvement of several countries, among other factors Nigeria recorded the first case of Ebola in July 2014 when an

[2,3]. Indeed, the Ebola outbreaks across West Africa resulted in infected Liberian-American flew into , a highly populated city

significant human fatalities (till date the worst on record), and in the southwest region of the country. Following this, a nurse who

it had a huge impact on lives and livelihoods of residents of attended to the Liberian later died after contracting the disease [9].

countries such as Guinea, Liberia, and Sierra Leone, where major Ebola briefly spread to other cities before Nigeria undertook a fran-

outbreaks occurred. Those Ebola outbreaks led to the World Health tic effort to forestall further spread. Altogether, Nigeria recorded

Organization (WHO) declaration of a Public Health Emergency of 8 deaths out of 20 cases of Ebola. Four health workers (50% of

International Concern in 2014 that was later ended in 2016, albeit, all infected) were among those that succumbed to the infection.

with many cases subsequently recorded and attributed to flare-ups The effort at curtailing the spread of was regarded

[3–5]. as a spectacular success, according to the WHO’s representative

Although, many Ebola outbreaks preceded the massive 2014- who finally declared Nigeria Ebola free in October 2014, exactly

2016 epidemics across West Africa, in a spatiotemporal context, it 4 months after the first case was reported. Nigeria became the

is desirable to know what really triggered its rapid spread across first African nation to be officially confirmed Ebola free [10,11].

the sub-region, despite an awareness of what it took to successful Apart from Nigeria, Mali and Senegal also had a few cases, 8 and

halt its spread elsewhere on the continent [2].This review takes 1, respectively [2].

a critical look at some important health determinants that may Although, the 2014-2016 Ebola epidemics were initially

have facilitated the epidemic in contrast to previous outbreaks. believed to be caused by Zaire ebolavirus [12], investigations later

It utilizes a health determinant model (HDM) consisting of both linked this outbreak with two viruses, Sudan and Zaire

micro-determinants (such as religious rites, health provider com- [1]. In addition, far from West Africa, cases of Reston ebolavirus

petency and nearness to forest) and macro-determinants (such were linked with monkeys imported to the United States from

as culture and tradition, health quality system, and port of entry the Philippines [1]. Even though, the 2014-2016 Ebola epidemics

security), to further enhance the conceptual understanding of this appears to have fully put under control, yet since 2016, cases of

important epidemic. Most importantly and based on lessons learnt Zaire ebolavirus have not ceased to occur. In 2017, 8 cases and 4

from previous Ebola outbreaks, it offers useful recommendations deaths of Ebola were reported in Likati town, D.R Congo. Again, in

through adequate barriers, early and accurate diagnosis, improved 201854 cases and 33 deaths were recorded in Bikoro, another town

strategic response management, and preventive measures against in D.R Congo. Worse still, during 2019, Ebola cases were still being

its recurrence through adequate follow-ups of survivors. reported in both D.R Congo and Uganda despite several interven-

tions by international aid agencies [2].

Outbreaks of Ebolavirus in Africa: Epidemic Timeline and

Impacts Ebola and Other Infectious Diseases: Differential Diagnoses

Ebola virus was first documented in 1976, with two concurrent Ebola is commonly associated with high death risk which is

outbreaks in Nzara town, South Sudan () and Yam- largely due to the severity of body fluid loss and dehydration, lead-

buku town, the neighborhood of a river called in D.R ing to hypovolemic shock on account of low blood pressure. It is

Congo(Zaire ebolavirus). Following these cases, within some weeks noteworthy that low blood pressure is generally associated with

of the first incidence, about 318 Ebola cases were reported with a clinical symptoms such as diarrhea and vomiting in other infec-

fatality rate of 88% [6]. In 1994, another 52 cases of Zaire ebolavirus tious diseases, like cholera [12]. Other symptoms of Ebola include

were reported in Mekouka town, Gabon, with 31 deaths recorded. fever, sore throat, muscular pain, and headaches and these are all

In the same year, one case of new specie (Taï Forest ebolavirus) was common early signs and symptoms of Ebola (from first few days up

recorded in Côte d’Ivoire, although it was later successfully treated. to first three weeks after ebolavirus infection) but are also common

Please cite this article in press as: Kamorudeen RT, et al. Ebola outbreak in West Africa, 2014 – 2016: Epidemic timeline, differential

diagnoses, determining factors, and lessons for future response. J Infect Public Health (2020), https://doi.org/10.1016/j.jiph.2020.03.014

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with other health conditions. Hence, it is important to note that water, among others [15].It was indeed an aftermath of the Ebola

body rash and internal and external bleedings (haemorrhages) are threat that predisposed many Nigerians to hypertension, cardiac

important symptoms of EBOV that help to differentiate it clinically challenges, and kidney problems, and worsened the plight of those

from other infectious diseases, such as meningitis, malaria, typhoid that were on dialysis. Furthermore, many Nigerians, particularly

fever, and cholera [12]. Confirmatory diagnosis of early infection those residents in the rural areas, failed to adhere to government

with ebolavirus may involve testing for viral RNA and assays for and expert recommendations against contracting the disease, even

Ebola-specific immune antibodies, to urgently save the patient and though public campaigns were intense.

the public from the spread of the disease. In contrast to the health systems in Nigeria, those in some

other western African countries including Sierra Leone, Liberia

and Guinea, were inadequate and the few functional health sys-

The Key Health Determinants Associated with High

tems that were crucial to preventing the spread of Ebola failed to

Mortality Rate of 2014-2016 West African Ebola Epidemics

perform optimally. Health workers, particularly the skilled ones,

were also insufficient in number [16]. Government infrastructure,

Generally speaking, a number of factors could determine the

government-enforced quarantine, health record, and drug supply

rapid spread of Ebola in several African populations. These factors

were practically inadequate [16]. In addition, government response

may include social and economic factors, poverty, malnutrition,

which was expected to be central to reducing the rate of transmis-

poor sanitation, intercurrent diseases, individual health status,

sion and preventing the spread of Ebola, was weak in many West

health literacy, and other education-related factors, among others.

African countries [17,18].

In the 2014-2016 West African epidemics, some of these factors

An important micro-determinant of the rapid and extensive

were peculiar and occurred concurrently with others that are well

spread of Ebola in West Africa was the occurrence of the infection

established, to determine the transmission, spread, and outcomes

in medical settings. Such infections otherwise termed nosocomial

such as degree of morbidity and mortality rates. These factors can be

infections were largely due to failures in established procedures of

categorized as micro- and macro-determinants and modeled into a

infection control and breach of standard barrier precautions[19,20],

conceptual prism to indicate how they interconnect, for a better

attributable to poor safety orientation, inexperience and lack of

understanding of the epidemic (see fig.1). Critical health deter-

skilled workers, and poor financing of healthcare systems and

minants, which militated against the control of 2014-2016 Ebola

infrastructure. These inadequacies may be attributed to poor gov-

outbreaks, are discussed below;

ernment policies, poor medical attention, and weak economic state

of almost all of the affected countries (Fig. 1).

Medical Attention and Government Policy: Combinatorial Effects

Social factors

Ebola is an emergency that requires quick and urgent reactions.

It was in reverse that many western African countries where the Social factors, such as culture, tradition, and occupational hazard

epidemics of Ebola struck really lacked rapid response and were also played significant roles in the spread of 2014-2016 Ebola out-

aback from the use of adequate resources to combat the emergency. breaks in West Africa. According to a report, many people through

In addition, majority of these countries had relaxed immigration attendance of funerals in Sierra Leone contracted the disease and

policies which worsened the spread across the regional boundaries, helped in the spread to their families and friends [21]. Similarly, in

apart from common vector-agent migration [2,13]. Guinea, traditional burial method which is a common practice in

Nigeria, though abundant in vector agents of Ebola never experi- which dead bodies are washed and touched unprotected or some-

enced any case between 1976 and 2014 when there were consistent times unsuitably protected, resulted in the spread of Ebola and the

records in the neighboring West African countries [14].The disease high death rates recorded[22]. The modern practice of embalm-

was eventually imported by an infected individual who traveled ment of corpses could also have contributed to the spread of Ebola

from Liberia, without any evidence of adequate screening of his in parts of West African countries [23]. Occupational risks also con-

health status at the port of entry in Lagos. However, the public tributed to the increased Ebola mortality rate and was the main risk

health system involving Emergency Operations Center, National of transmission of the virus to healthcare workers who attended to

Public Health Institute and Incident Management System had been Ebola patients [23].The imported case of Ebola in Nigeria was first

in place two years before the epidemic of Ebola struck. Nigeria transmitted by the attending nurse who later died [11]. It is believed

had earlier declared public health state of emergency against polio, that some occupations are more contributory to the transmission

another viral disease, and the structures and mechanisms that were than the other. Although, the risk becomes higher when proper

in place already were promptly activated in mitigating the spread of use of the protective, such as gloves, masks, and eye-protection is

Ebola within the country [6,13].In other words, rapid health inter- disregarded, as was the situation in many of the African countries

ventions, healthcare quality, political commitment, operational where the disease struck [24]. In other words, one may conclude

and strategic changes helped Nigerian public health system with that social factors including occupational hazard and safety failures

Emergency Operation Centers and Incident Management System, involving the use of personal protective equipment were instru-

among others, and greatly contributed to the rapid response to mental to the rapid and widespread transmission of Ebola in West

Ebola and its effectiveness. This limited the epidemic to twenty Africa, 2014-2016 (Fig. 1).

cases, as established from the laboratory results of confirmatory

tests performed on the suspected victims (Table 1). In addition, it Seasonal and Climatic Factor

restricted the increase and spread of the virus due to stable pub-

lic health institutions, apart from the rapid interventional method It has been reported that the annual dry season, which runs

[13]. between December to May (longest period of the year) is a breeding

Notwithstanding, the epidemic itself was not without any season for fruit bats, a reservoir of ebolavirus with high poten-

consequence. Despite the apparent quality health and rapid inter- tial to replicate and thus enhances transmission [25].An increase

vention, apprehension of Ebola led to misconceptions in some parts in the number of bats (species) is said to influence viral load and

of the country. The fear of Ebola and poor health education resulted interspecies fighting which may both enhance viral transmission.

in various health problems and challenges, down to self-prescribed It is believed that a favourable climate indirectly leads to more

preventive measures such as the drinking and bathing with salty spillovers from swarming Ebola reservoirs and may also force inter-

Please cite this article in press as: Kamorudeen RT, et al. Ebola outbreak in West Africa, 2014 – 2016: Epidemic timeline, differential

diagnoses, determining factors, and lessons for future response. J Infect Public Health (2020), https://doi.org/10.1016/j.jiph.2020.03.014

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Fig. 1. A Model of Eight Cardinal Health Determinants Associated with Epidemic of Ebola Outbreak in West Africa from 2014 to 2016. (A: Determinant categories; B:

Macro-determinants; C: Micro-determinants).

Fig. 2. Effect of Climatic Changes and Human Activities on Ebolavirus Transmission.

Please cite this article in press as: Kamorudeen RT, et al. Ebola outbreak in West Africa, 2014 – 2016: Epidemic timeline, differential

diagnoses, determining factors, and lessons for future response. J Infect Public Health (2020), https://doi.org/10.1016/j.jiph.2020.03.014

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action of the bats with other wildlife species, especially under high cases [32,33]. Sexual exploitative relationship is a common basic

forage and wildlife distributions [25]. Ebola is mainly found within means of survival among many people including the refugees for

◦

10 equator where the climatic condition in conjunction with other a long period of time, and it involves many agency staff like NGO’s

factors, favoured the intensity of spread of the virus from 2014 to workers. This is grossly attributed to poverty, and lack of livelihood

2016[26]. Another factor is human activities such as, deforestation. option to survive. According to a report through a sexually exploited

Habitat destruction through human activities such as tree felling, woman in Guinea, indiscriminate sexual involvement has no ugly

bush clearing and burning, could lead to the wider dispersion of meaning. Likewise in Liberia, another place with rampant spread of

wildlife reservoirs of Ebola. This coupled with the usual practice of Ebola, sex-for-money activities are common practices [32]. Strong

hunting of wildlife animals(Fig. 2). association between Ebola transmission and sexual behaviour has

been reported [33,34]. Therefore, there is indication that persistent

Physical Environment recurrence of Ebola in some of these notable West African countries

could be as a result of viral persistence and sexual risk behaviour.

Physical environment is an important determining factor in the

spread of ebolavirus. It may include closeness of residential sites

Conclusion

to the harbouring forest where wildlife with potential influence of

transmission are located. Aside from location as a determinant of

It is very obvious that many factors mitigated against the control

Ebola transmission, residential quality is a possible enabling deter-

of 2014-2016 Ebola epidemic, involving poverty, failed government

minant for the spread of ebolavirus (Fig. 1). It is reported that poor

policies, individual risk behaviours, poor health system, among oth-

structural housing quality, poor access to safe water, overcrowding,

ers. In the hardest hit countries, the situation went downheartedly

sanitation, and insecure residential status, among other infrastruc-

evoking economic impacts in spite of many international aids for

tural inadequacies are favourable stimuli for transmission of Ebola.

logistic supplies and other response activities. Unfortunately, today

Again, data shows that outbreaks of Ebola took place in rural and

Ebola outbreak remains unabated in some of these affected coun-

among the geographically isolated populations riddled in poor res-

tries, although with limited cases. Importantly, evidences show

idential quality [27].

that Ebola is a sexually transmitted disease and tend to persist

In addition, interaction or closeness with animals, such as;

long among the survivors, even after recovery, thus the chance of

animal petting and domestication are possible ways for animal-to-

re-transmission is still highly probable especially with indiscrim-

human transmission. Also, most times, different animals are found

inate sexual activities. It is therefore important for every country

in the farm feeding on agricultural products and transmit the virus

involved to focus inwards on some health determinants associated

on leftovers. Although, there is a debate whether ebolavirus can

with Ebola outbreak in other to eradicate the disease and to prevent

be transmitted through food, ebolavirus can spread through inges-

future recurrence.

tion of fruit already contaminated with ebolavirus-infected saliva

or faeces of the reservoirs. Thus, some habits of local food process-

Recommendations

ing or preservation such as open silos method or traditionally store

silage in the rural areas could be a potential route of transmission

From the previous lessons of outbreaks in West African coun-

(Fig. 1). In addition, fruit bat spillovers could also be a different route

tries, some health determining factors may need to be addressed,

in transmitting the virus to other wildlife species (such as duiker,

to finally put the continual outbreak of Ebola to rest.

nonhuman primates) or even humans [28].

Health Status and Human Biology I As a policy tool and an important check-up, screening of immi-

grant health status with detailed health condition should not

Human biology and nutritional status are two important deter- be taken for granted before visa approval, especially in an

minants that may determine the transmission of Ebola. It is Ebola-free zone, not even within the region where visa is

understood that ebolavirus may remain protected from host immu- abolished. It is believed that a detailed health screening plan

nity in the body by penetrating immune-priviledged sites. In this will prevent importation of deadly disease agents. Some viral

way, some organs including testicles, eyes, fetus, placenta, among diseases including Ebola, COVID-19, and others have become

others, are immune-protected, and thus referred to as immune- global health threats and causes for concern with high risk

privileged in the body. In other words, this means that they tolerate of morbidity and/or mortality rates through contact transmis-

any inflow of antigens without eliciting immune response. This sion. Thus, enforcing immigration regulation on detailed health

pathway is an opportunity for ebolavirus antigen to be free from screening policy will prevent case importation and forestall

host immunity and may be the reason why semen of male patients epidemic especially through the port of entry.

suffering from Ebola may subject them to high risk of transmission II Apart from enforcing immigration regulation, physical envi-

of the virus after recovery [29]. ronment favouring the transmission of Ebola in West African

In addition, report (after follow-up) from the 2014 Ebola epi- sub-regions is an important factor to handle properly. In

demic establishes that survivors who recover can harbour the viral many areas, where there are flocks of vector-agent reservoirs

RNA in their semen for minimum of 2.5 years, with high chance of in the neighbourhood, ecological interventions may be con-

transmitting the virus by sexual intercourse during that time[30]. sidered necessary to check and manage zoonotic pathogen

This brings Ebola to the limelight of sexually transmission diseases. spillovers. This may be achieved if the habitat is precondi-

Keita and coworkers [31] reported that in Guinea, many survivors tioned unfavourable for the reservoirs and by disconnecting

of Ebola were found with persistence of the viral RNA in semen the food chain, particularly against the fruit bats that are com-

(men) and breast milk (female) after several months. mon host for many viral pathogens, to prevent spillovers and

transmission to other wildlife species.

Individual risk behaviour III Also, to foster the degree of preparedness and prevention con-

trol, vaccination is an important measure that should be made

Unfortunately, sexual violence and exploitation are common available, especially in the prone areas where media campaign

habits that pose high risk of transmission in the three major coun- and other awareness programs may not totally prevent human

tries (Guinea, Liberia and Sierra Leone) with reported widespread risk behaviours. Likewise, funding of research on emerging

Please cite this article in press as: Kamorudeen RT, et al. Ebola outbreak in West Africa, 2014 – 2016: Epidemic timeline, differential

diagnoses, determining factors, and lessons for future response. J Infect Public Health (2020), https://doi.org/10.1016/j.jiph.2020.03.014

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