Low case fatality during 2017 cholera outbreak in Borno State, North Eastern Nigeria.

Background: Cholera is endemic in sub-Saharan Africa, especially in areas affected by natural disaster and human conflict. Northeastern Nigeria is experiencing a health crisis due to the destruction of essential amenities such as health infrastructure, sanitation facilities, water supplies, and human resources by Boko Haram insurgents. In 2017, a cholera outbreak occurred in five local government areas (LGAs) hosting internally displaced persons. The Nigeria Center for Disease Control, World Health Organization, Mĕdecins Sans Frontiĕres International, and several other organizations supported disease containment. An emergency operating center (EOC) established by the State Ministry of Health (SMoH) then coordinated the outbreak response.
Methods: We conducted a retrospective analysis of data extracted from the line list utilized by the SMoH to investigate outbreaks. We evaluated the outbreak by time, place, and person. Attack rate by LGA and age-specific case fatality rate (CFR) was calculated based on cases with complete records for age, sex, place of residence, date of symptom onset, and disease outcome.
Results: A total of 5889 cholera cases were reported from five LGAs with an overall attack rate of 395.3/100,000 population. Among 4956 cases with documented outcome, the overall CFR was 0.87%, with CFR ranging from 0% to 6.98% by LGA. The age-specific CFR was highest among those aged ≥60 years (1.92%) and least among those aged 20-29 years at 0.3%. The epidemiological curve revealed two peaks that coincided with periods of heavy rain and flooding.
Conclusion: This study reports on the largest ever documented cholera outbreak in five LGAs in Borno State. The outbreak was focused in LGA hit hardest by the destructive activities of insurgents and then spread to neighboring LGAs. The low CFR recorded in this cholera outbreak was achieved through timely detection, reporting, and response by the coordinated efforts of the EOC established by the SMoH that harmonized the outbreak response.

INTRODUCTION

Cholera, a diarrheal disease caused by Vibrio cholerae, occurs both as sporadic cases and as outbreaks. Globally, most reports of the disease emanate from tropical and subtropical countries where the disease is endemic, defined as detection of cholera cases in at least 3 of the preceding 5 years.[1] In endemic regions, lack of basic sanitation and health-care infrastructure, overcrowding, insufficient public health education, inadequate case tracking and surveillance, delayed case management, and lack of preventive measures are responsible for the persistence of the disease.[2] Outbreaks of cholera also occur in communities affected by natural disasters and conflicts due to disruption of sanitary and social amenities.[3] Unlike developed regions where cholera may occur as a point source epidemic due to damage to sanitary and sewage facilities, cholera outbreaks are common in Africa due to underdevelopment of sanitation and health-care infrastructure and are often associated with high mortality rates.[4] Unfortunately, mortality attributable to cholera is significantly underreported from African regions where it is common.[5] The high burden of cases and associated case-fatality may be attributed to delays in diagnosis and insufficient case surveillance and tracking, often resulting in enormous loss of human lives, overstretching of existing weak health infrastructure, and economic burden to the continent.[56]

In Nigeria, since the first reported case of cholera in 1971, multiple outbreaks have only occurred with an increase in frequency and case fatality reported in virtually all six geopolitical regions over time, with a particular increase in intensity in the Northern regions of the country.[7] Several factors such as lack of basic social amenities, dearth of sanitation facilities, and lack of education regarding health and hygiene are responsible for the persisting cholera outbreaks.[8] However, despite the huge public health impact of cholera, there is a dearth of information about this preventable disease in Northern Nigeria as most outbreaks are either underreported or not thoroughly investigated. The devastating activities of “Boko Haram” insurgents have resulted in health crises in Northeastern Nigeria. The senseless destruction of lives, means of livelihood, basic amenities, and health infrastructure by the insurgents is most intense in Borno State. This has resulted in an increase of epidemic-prone diseases such as cholera. A cholera outbreak was declared on the August 14, 2017, by the local government of Borno State, which then spread to four neighboring LGAs. We conducted a descriptive analysis of data from the outbreak to determine the epidemiological distribution, spatiotemporal characteristics, and case fatality rates (CFRs).

METHODS

We conducted a retrospective analysis of data extracted from the line list utilized by the State Ministry of Health (SMoH) to investigate the cholera outbreak in the five LGAs. A total of 5889 cholera cases were analyzed in this descriptive study [Figure 1]. Information abstracted from the mainline list include age, sex, residence (LGA), and date of symptom onset. The LGAs that reported the outbreak include Dikwa, Jere, Mafa, Maiduguri MMC, and Monguno [Figure 2]. A cholera case was defined as any patient with acute watery diarrhea, with or without vomiting, during the period of the outbreak, based on the case definition provided in the National Technical Guidelines of the Integrated Diseases Surveillance and Response.[9]

Figure 1

Organogram of cholera cases

Figure 2

Map of Borno state showing local government areas affected by the cholera outbreak

Patients aged <5 years were also included in our analysis consistent with previous outbreak studies.[101112] We evaluated and stratified data by time, place, and person using Epi Info (Version 3.5.3; CDC, Atlanta, GA, USA). Attack rate (AR: cases/100,000 population) was calculated based on the reported number of cases and projected population data based on the 2006 census [Table 1].[13] CFR and age-specific CFR were calculated using cases with complete clinical information, which we defined as any patient with data on age, sex, state, and outcome [Figure 1]. The numerator for the age-specific CFR is the number of deaths in the specific age group, while the denominator is the number of cases in the specific age group with complete clinical information. All cases with incomplete information were excluded from the determination of CFR. We defined the first epidemiological week of the year as the week that ends on the first Saturday of January, as long as it falls at least 4 days into the month. Subsequently, each epidemiological week begins on a Sunday and ends on a Saturday.

Table 1

Stratification of cholera attack rate based on local government, Borno State, Nigeria

Local government	Cases	Population	Attack rate/100,000 population
Dikwa	827	147,958	558.94
Jere	3180	295,058	1077.75
Mafa	2	144,618	1.38
Maiduguri MMC	50	748,539	6.68
Monguno	1830	153,465	1192.45
Total	5889	1,489,638	395.33

Ethical approval to conduct this study was obtained from the ethical committee of Borno SMoH. The information collected in the dataset (age, sex, date of onset of illness, local government area [LGA], and outcome) was safeguarded within the database of the Ministry of Health, Borno State.

RESULTS

A total of 5889 cholera cases among a total population of 1,489,638 in five LGAs were identified based on the case definition of cholera. The total attack rate/100,000 population was 395.3, which was highest in Monguno followed by Jere LGA as depicted in Table 1. The cases consisted of 3088 females and 2801 males spread across 22 wards of the five LGAs as shown in Figure 3. The median age (interquartile range [IQR]) of the studied population was 9 years (IQR, 5–27 years), with ages ranging from 0 to 95 years. The median age for females was 10 (IQR, 7–28) years, which was significantly higher than the median age for males of 7.5 (IQR, 4–25) years.

Figure 3

Cholera cases stratified by sex in wards of local government areas

All five LGAs in which cholera cases occurred were adversely affected by insurgency attacks. Representative samples from each of the LGAs were tested using rapid diagnostic tests, stool culture, and serotype detection. The entire sample was identified as O1 serogroup, serotype Ogawa. The first cases were documented in Jere LGA on the August 14, 2017, followed by spread to 13 wards of the LGA. Subsequent cases were then reported in four neighboring LGAs. The epidemic curve peaked during weeks 36, 37, and 38 with 1624, 1230, and 1389 cases, respectively [Figure 4]. One out of every two cases of cholera occurred in a child ≤9 years of age, and the majority of cases were aged <40 years. The cumulative percentage of cases by age group is presented in Figure 5. Of the 4956 cholera cases with documented outcome in the line list, 43 deaths were recorded, resulting in a CFR of 0.9% [Table 2]. Stratified by LGA, Maiduguri MMC had the highest CFR of 7.0%. Age-specific CFR was highest (2.0%) among patients 60 years of age or older, as shown in Table 3.

Figure 4

Daily epidemic curve of cholera cases in five local government areas, Borno State

Figure 5

Cholera cases by age group and percentage contribution

Table 2

Case fatality rates of cholera cases, stratified by local government areas Borno, Nigeria

LGA	Cases with documented outcome	Outcomes		Case fatality rates (%)
		Alive	dead
Dikwa	738	729	09	1.22
Jere	2530	2503	27	1.06
Mafa	02	02	00	0.00
Maiduguri MMC	43	40	03	6.98
Monguno	1643	1639	04	0.24
Total	4956	4913	43	0.87

LGA=Local government areas

Table 3

Age-specific case fatality rates of cholera cases, Borno, Nigeria

Age group (years)	Cases with documented outcome	Outcomes		Age-specific case fatality rates (%)
		Alive	Dead
0-4	1477	1464	13	0.9
5-9	1104	1091	13	1.3
10-19	727	724	03	0.4
20-29	592	590	02	0.3
30-39	421	417	05	1.2
40-49	230	228	01	0.4
50-59	176	174	02	1.1
≥60	209	205	04	1.9
Unknown	20	20	00	-
Total	4956	4913	43

DISCUSSION

Cholera, an acute diarrheal disease due to V. cholerae thither to a global threat to public health, is currently largely restricted to developing countries in the tropic and subtropics. Lack of resources, infrastructure and weak or nonexistence of disease outbreak preparedness, and response system are responsible for the disproportionately high cholera burden in developing countries.[1214] In endemic areas, outbreaks are usually due to inadequate personal hygiene, poor sewage, and sanitary conditions. Other drivers of cholera outbreaks include natural disasters such as flooding and human conflicts such as war or civil unrest that disrupts public sanitation services. In Nigeria, since the first reported series of cholera cases from 1970 to 1990, it remained endemic with frequent and large outbreaks, especially in Northern Nigeria. Despite this long experience with cholera and its public health challenges in Nigeria, comprehensive data on the disease epidemiology, factors facilitating its persistence and commensurate rapid response to contain outbreak is lacking. Available information on cholera is based on aggregate data even in Northern part that is worse hit by cholera, most often in large epidemic proportion. In this descriptive analysis study, the cholera outbreak started in the middle of the month of August 2017. The outbreak coincides with period of heavy rain and flooding in Jere LGA and rapidly spread to four other neighboring LGAs. In agreement with the current report, the trend in the incidence in cholera in Northern Nigeria appears to peak in raining season.[15] This is in contrast to report from Southern Nigeria where most cases are seen during dry season from possible sources such as estuarine waters, fishery products, small streams, and rivers.[16] The devastating activities of “Boko Haram” insurgents have resulted in health crisis in northeastern Nigeria. The senseless destruction of lives, means of livelihood, basic amenities, and health infrastructure by the insurgents was more intense in Borno State. This has resulted in increase of epidemic-prone diseases including cholera. Cholera outbreak is associated with significant breach in water, sanitation, and hygiene infrastructure. Previous reports had established a direct link between cholera outbreak with sanitation and water supply.[1718] Furthermore, hand dug wells and contaminated ponds are common sources of water for both human and domestic animals in Northern Nigeria. During the rainy season, it is not uncommon for rainwater to result in run-off of sewage from shallow pit latrines and blocked drainages into open wells and ponds. Fecal matter from open defecation can also be washed into source of water for drinking and other household needs. This poor sewage and sanitation make the communities vulnerable to cholera and other enteric infections.

Despite ongoing displacement and violence caused by Bokon Haram, the CFR during this large cholera outbreak in northeastern Nigeria was 0.9%, within the World Health Organization (WHO) recommended threshold of 1%.[19] High mortality rates are often associated with limited health infrastructure and expertise, lack of education on proper sanitation and hygiene, and weak or nonexistent surveillance systems to trigger a prompt response. Previous studies from Nigeria have shown higher CFR. However, a downward trend in case fatalities has been observed from 7.40% in 2001 to 4.2% in 2010.[720] In a study from Nigeria, prompt early alert surveillance and case management was shown to achieve CFR of <1%.[7] Leveraging the support from implementing partners such as WHO, Mĕdecins Sans Frontiĕres, UNICEFś water, sanitation and hygiene strategy, and other partners to combat the ongoing health crisis, Borno State has a robust early warning and alert system (EWARS) in place. The outbreak was, therefore, promptly detected and cholera treatment centers were established in health centers. This emergency preparedness and response lead to low CFR despite a high attack rate.

Age-specific case fatality was highest among patients 60 years of age and older, in agreement with an earlier report,[8] but in sharp contrast to studies that indicate highest age-specific mortality among patients aged ≤5 years.[1112] Neglect of the elderly, most often as they rely on relatives for care or due to associated comorbidity may be responsible for higher mortality among the older age group observed in this outbreak.[8] In this report, more females were affected than males. Our finding is similar to previous studies that reported higher attack rates among females.[18] The studies suggested that more females may become infected because they care for the sick, thereby increasing the chance of contracting the bacteria from patients.[718]

Limitations

Many cases had incomplete information and thus were excluded from the analysis.

CONCLUSION

We report a cholera outbreak that started in Jere, a LGA within the state capital, then quickly spread to four neighboring LGAs. The outbreak occurred in an area decimated and displaced by activities of Boko Haram insurgents. The EWARS and support from implementing partners assisted in containing and restricting the spread of the disease and minimizing mortality.

Recommendations

Emergency preparedness and response system should be instituted in areas that are prone to cholera outbreaks. Provision of basic amenities and sanitary facilities is necessary to avoid fecal contamination.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.