INTRODUCTION
The recent Ebola outbreak has been proved to be devastating to vulnerable populations in West Africa. Because the primary focus had been on adults and children, apparently the casualties among the elderly were left unnoticed and rarely reported.1 Previous report showed that participation in traditional funeral rites during the outbreak increased the risk of acquiring Ebola virus disease (EVD).2 Traditional funerals are a kind of social happenings which interconnected to many other aspects of social life, including the logic of parenthood, the concept of authority, and care of sickness.3
In Africa, especially in Guinea, elderly people are the key members in any funeral activities and their roles include, but not limited to, leading mourning ceremonies, providing important information to attendees, and performing rituals and burial.4 At the time of outbreak, traditional funeral was made one of the main topics by media coverage related to Ebola transmission.3 Attending a funeral ceremony was perceived to facilitate and expose adults and the elderly to the risk of contracting EVD.5 It has been suggested that this situation contributed to the spread of the disease and hindered outbreak control efforts. Unfortunately, there is no comprehensive analysis of EVD in this key population (the elderly) to understand their potential role(s) in transmission and high fatality. Therefore, we sought to identify the predictors of EVD mortality during the 2014 outbreak in Guinea.
MATERIALS AND METHODS
Ethics statement.
This study was approved by the National Ethics Committee for Healthcare Research Board (No: 071/CNERS/15) with a waiver of informed consent for the collection and analysis of anonymized data.
Patients and study design.
It was a retrospective and analytical study, which included patients of 20 years or older admitted during January 2014 to December 2015 (2 years) in the Guinean Ebola Treatment Centers (ETCs) and confirmed positive for EVD by real-time polymerase chain reaction using blood or swab samples. All patients were managed using the World Health Organization (WHO) standardized EVD care path, improving consistency in clinical, laboratory, treatment, and outcome data.6 The patient’s care path included documentation of symptoms, examination findings, and laboratory parameters.
Case definitions.
We used the case definition developed by WHO for EVD surveillance, which classified EVD cases into suspected, probable, or laboratory-confirmed cases.6,7 Elderly is a descriptive term referring to people past midlife and in old age. At the moment, there is no universal standardized numerical criterion; therefore, we classified elderly patients based on the United Nations recommended cut-off for older population.8 In this study, patients aged 60 years and older according to the previously mentioned definition were considered as “elderly,” whereas patients between 20 and 59 years old were defined as “adults.”
Data collection.
The data originally designed for an Ebola outbreak containment purpose were retrieved from the database of National EVD Committee of Ministry of Health and Public Hygiene, which is the public body responsible for retaining EVD outbreak-related data in Guinea. The data were collected from 29,742 EVD suspected or probable cases previously recorded on WHO standardized forms during admission at the ETCs. Among them, information of 2,313 confirmed EVD patients was extracted by a medically trained research assistant and analyzed after appropriate data cleaning. The detailed flow diagram of the study is shown in Figure 1.
Flow diagram of this retrospective study.
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0372
Flow diagram of this retrospective study.
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0372
Flow diagram of this retrospective study.
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0372
Data analysis.
Baseline characteristics and outcomes were compared between adult (20–59 years old) and elderly (60 years and older) patients. Descriptive analyses were presented as frequency with percentage and median with interquartile range (IQR). Chi-square test or Fisher’s exact test was used to compare dichotomous variables, and Mann–Whitney U test was used for continuous variables, as appropriate. The association between different variables and EVD mortality was assessed using univariate logistic regression to obtain unadjusted odds ratios (ORs) and their 95% confidence intervals (CIs). Variables with a P value < 0.05 in the univariate analysis were combined and included in a stepwise fashion in a multivariate logistic regression model. The Kaplan–Meier method was used to measure the fraction of EVD patients living for a certain amount of time after admission to ETCs. The effect of age as a predictor was investigated by Cox regression. Statistical significance for all tests was set at a probability value < 0.05. All statistical analyses were performed using SPSS version 22 (IBM, SPSS Inc., Chicago, IL).
RESULTS
In the cohort of 2,313 laboratory-confirmed EVD patients, 2,004 were adults and 309 were elderly (Figure 1). The median age (IQR) was 35 years (23–44) and 65 years (60–70) for adults and elderly people, respectively. The proportion of males was 49.2% and 45.8% in the adult and elderly groups, respectively. Most of the patients were from Macenta Prefecture (20.9% adults and 23.2% elderly); however, there was no significant difference between the proportion of adult and elderly in any location including Macenta. The most frequent profession in both groups was housewife (19.1% adult and 22.4% elderly) followed by farmers (9.0% and 8.8%).
The proportion of elderly people participating in the funeral was significantly higher than in the adult group (P = 0.039). However, we did not observe any difference between adult and elderly groups in the history of contact with confirmed or suspected EVD patients. In addition, the two groups were not different in terms of history of traveling to the hot spot of transmission during the outbreak (Table 1).
Comparison of demographic and clinical features of EVD in adult and elderly patients in Guinea
| Variables | Number of patients | Adults (N = 2,004) | Elderly (N = 309) | P value |
|---|---|---|---|---|
| Sociodemographics | ||||
| Median age, years (IQR) | – | 35 (23–44) | 65 (60–70) | < 0.001* |
| Gender (male), n (%) | 1,128 | 986 (49.2) | 142 (45.8) | 0.14 |
| Residence, n (%) | ||||
| Macenta | 490 | 418 (20.9) | 72 (23.2) | – |
| Conakry | 390 | 360 (18.0) | 30 (9.7) | – |
| Forecariah | 270 | 231 (11.5) | 39 (12.6) | – |
| Gueckedou | 179 | 156 (7.8) | 23 (7.4) | – |
| Coyah | 150 | 128 (6.4) | 22 (7.1) | – |
| N’Zerekore | 145 | 121 (6.0) | 24 (7.7) | – |
| Kerouane | 113 | 100 (5.0) | 13 (4.2) | – |
| Kissidougou | 53 | 40 (2.0) | 13 (4.2) | – |
| Kindia | 52 | 45 (2.2) | 7 (2.3) | – |
| Profession, n (%) | ||||
| Housewife | 309 | 253 (19.1) | 56 (22.4) | 0.13 |
| Farmer | 141 | 119 (9.0) | 22 (8.8) | 0.51 |
| Health-care worker | 98 | 88 (6.6) | 10 (4.0) | 0.69 |
| Business person | 45 | 43 (3.2) | 2 (0.8) | 0.01 |
| Religious leader | 2 | 2 (0.2) | 0 (0) | 0.70 |
| Transporter | 20 | 19 (1.4) | 1 (0.4) | 0.14 |
| Traditional healer | 2 | 2 (0.6) | 0 (0) | 0.25 |
| Risk factor for exposure to EVD, n (%) | ||||
| History of contact with suspected or confirmed cases | 513 | 457 (79.5) | 56 (86.2) | 0.13 |
| History of traveling to hot spot areas | 104 | 96 (19.7) | 8 (14.5) | 0.23 |
| History of attending funeral | 213 | 184 (37.8) | 29 (50.9) | 0.039 |
| Symptoms, n (%) | ||||
| Fever | 1,302 | 1,152 (92.2) | 150 (91.5) | 0.41 |
| Fatigue | 1,233 | 1,077 (91.1) | 156 (94.5) | 0.08 |
| Anorexia | 1,099 | 804 (81.7) | 93 (80.9) | 0.45 |
| Vomiting | 835 | 751 (78.4) | 84 (73.7) | 0.15 |
| Diarrhea | 793 | 701 (77.0) | 92 (76.0) | 0.44 |
| Muscle pain | 897 | 503 (61.5) | 71 (68.9) | 0.86 |
| Joint pain | 800 | 403 (56.0) | 45 (56.3) | 0.53 |
| Headache | 448 | 658 (74.8) | 76 (74.5) | 0.51 |
| Hiccups | 140 | 129 (23.6) | 11 (18.6) | 0.24 |
| Abdominal pain | 507 | 452 (59.9) | 55 (59.1) | 0.48 |
| Difficulty in swallowing | 49 | 43 (16.3) | 6 (13.3) | 0.09 |
| Chest pain | 138 | 124 (36.9) | 14 (29.8) | 0.21 |
| Cough | 124 | 107 (32.6) | 17 (34.0) | 0.48 |
| Difficulty in breathing | 86 | 78 (25.2) | 8 (16.7) | 0.13 |
| Sore throat | 81 | 74 (24.9) | 7 (14.9) | 0.40 |
| Unexplained bleeding | 190 | 167 (25.9) | 23 (29.5) | 0.28 |
| Gum bleeding | 6 | 6 (1.5) | 0 (0.0) | 0.54 |
| Hematemesis | 11 | 11 (2.7) | 0 (0.0) | 0.30 |
| Jaundice | 17 | 16 (9.6) | 1 (4.2) | 0.33 |
| Conjunctivitis | 88 | 85 (28.9) | 3 (7.9) | 0.03 |
| Comorbodity: malaria, n (%) | 116 | 98 (25.2) | 18 (30) | 0.36 |
| Case fatality rate, n (%) | 1,574 | 1,324 (66.1) | 250 (80.6) | < 0.001 |
| Other parameters, median in days (IQR) | ||||
| Time between onset and admission | 4 (3–6) | 5 (3–7) | < 0.001* | |
| Length of hospitalization | 8 (4–13) | 6 (3–11) | < 0.001* | |
| Survival time | 11 (7–16) | 9 (6–15) | 0.007* |
EVD = Ebola virus disease; IQR = interquartile range; N = the number of patients in each comparison group; n = the number of patients having a specific demographic or clinical feature.
Continuous variables.
Among the elderly group, fever (91.5%), fatigue (94.5%), vomiting (80.9%), and diarrhea (84%) were the most common clinical features; however, bleeding signs were present in only 29% patients. There was no difference in symptom manifestation between adult and elderly groups (Table 1). The median time (in days) between the onset of symptoms and admission was significantly longer in the elderly (P < 0.001), which indicates delayed hospital presentation. In contrast, both the median length of hospitalization and median survival time (in days) were significantly shorter in the elderly group (P < 0.001). The survival analysis using Kaplan–Meier curves showed that the median survival period was significantly different between adults and elderly groups (Cox regression χ2 = 20.82; P < 0.001) (Figure 2).
The Kaplan–Meier curves of laboratory-confirmed Ebola virus disease in adult and elderly patients in Guinea. The Cox regression test yielded a χ2 value of 20.82 at 3 degree of freedom (P < 0.001). This figure appears in color at www.ajtmh.org.
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0372
The Kaplan–Meier curves of laboratory-confirmed Ebola virus disease in adult and elderly patients in Guinea. The Cox regression test yielded a χ2 value of 20.82 at 3 degree of freedom (P < 0.001). This figure appears in color at www.ajtmh.org.
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0372
The Kaplan–Meier curves of laboratory-confirmed Ebola virus disease in adult and elderly patients in Guinea. The Cox regression test yielded a χ2 value of 20.82 at 3 degree of freedom (P < 0.001). This figure appears in color at www.ajtmh.org.
Citation: The American Journal of Tropical Medicine and Hygiene 98, 1; 10.4269/ajtmh.17-0372
Case fatality rate (CFR) of EVD was also significantly higher in the elderly group (80.6%) (P < 0.001). In multivariable analysis, there was a significant association between increasing age and risk of death with EVD in the elderly group (OR [95% CI] = 1.05 [1.003–1.098]; P = 0.036) (Table 2). However, no clinical symptom was found to be predictive of the poor outcome in EVD among elderly people. Cox regression analysis showed that age was the only factor that could influence the EVD outcome. Therefore, age was considered as an independent factor that predicts EVD death in the elderly group.
Logistic regression analysis of factors associated with death in the elderly patients (N = 309) with EVD in Guinea
| Univariate | Multivariate | |||
|---|---|---|---|---|
| OR (95% CI) | P value | OR (95% CI) | P value | |
| Age (years)* | 1.05 (1.003–1.098) | 0.036 | 1.05 (1.003–1.098) | 0.036 |
| Gender | 1.12 (0.64–1.98) | 0.691 | – | – |
| History of contact with suspected or confirmed cases | 2.009 (0.0–3.38) | 0.99 | – | – |
| History of traveling to hot spot areas | 1.03 (0.18–5.79) | 0.975 | – | – |
| History of attending funeral | 1.4 (0.97–1.96) | 0.077 | – | – |
| Fever | 0.70 (0.19–2.64) | 0.600 | – | – |
| Unexplained bleeding | 1.47 (0.42–5.11) | 0.544 | – | – |
| Vomiting | 0.94 (0.38–2.47) | 0.940 | – | – |
| Diarrhea | 1.00 (0.36–2.81) | 0.997 | – | – |
| Fatigue | 0.75 (0.15–3.76) | 0.727 | – | – |
| Anorexia | 0.68 (0.21–2.20) | 0.516 | – | – |
| Abdominal pain | 1.05 (0.41–2.69) | 0.926 | – | – |
| Joint pain | 0.92 (0.32–2.59) | 0.869 | – | – |
| Muscle pain | 0.55 (0.20–1.53) | 0.252 | – | – |
| Headache | 1.54 (0.57–4.16) | 0.392 | – | – |
| Cough | 1.04 (0.23–4.78) | 0.963 | – | – |
| Hiccups | 1.04 (0.19–5.66) | 0.965 | – | – |
| Difficulty in swallowing | 0.44 (0.06–2.87) | 0.390 | – | – |
| Comorbidity: malaria | 0.85 (0.38–1.88) | 0.687 | – | – |
| Time between onset and admission | 0.95 (0.89–1.02) | 0.199 | – | – |
CI = confidence interval; EVD = Ebola virus disease; OR = odds ratio.
Age includes patients from the elderly group only.
DISCUSSION
To the best of our knowledge, this is one of the few studies to systematically compare the risk factors of exposure, clinical characteristics, and outcomes of EVD between adult (20–59 years old) and elderly (60 years and older) cases with confirmed EVD in Guinea. In this study, the CFR was significantly higher in the elderly group than in the adult group. Although there is no report on CFR in the elderly group, previous reports showed higher CFR among the patients aged 45 years and older.9,10 Higher mortality rate in elderly patients might be attributable not only to the age-related fragility of the immune system, causing a high viral load at the time of admission that subsequently contributes to multiorgan failure in the EVD,11,12 but also to the longer duration between onset and presentation to ETCs and other preexisting morbidities.13,14 Apart from that, the lack of trained caregivers and equipment in the treatment facilities possibly contributed to high fatality15 in general (among both groups). Moreover, the limited access to health-care facilities probably due to a strong social resistance to outbreak control interventions16,17 would have delayed hospital admission in both groups. In this regard, the WHO also reported the challenges in community engagement in some affected prefectures of Guinea, with several reported incidents of violence against the Ebola fighters team.15
We found that the proportion of EVD patients participating in the funeral was significantly higher in the elderly group than in its adult counterpart. Although the elderly in our study were not asked directly about participation in preparation of funeral rituals, cultural practices suggest this is highly likely.18 Our finding also concords with a previous report which pointed out participation in traditional funeral rites as a major risk factor.18 Among these risk factors, caring practices before the moment of death (in the role of traditional health caregivers) and dead body preparation such as washing and cleaning (in the role funeral ceremony leader) were reported as a source of contamination in countries affected by EVD.17,18 These practices put the elderly at differing patterns of risk of contracting EVD compared with younger adults.5
In Guinea, although most of the elderly and adults had a history of contact with suspected or confirmed cases, no significant difference was observed. This observation demonstrates that the conditions required for EVD to spread from person to person were not specific to one age.
We found that delay in seeking treatment was significantly longer in the elderly group. In addition, the length of hospital stay and survival time were significantly shorter in the elderly group. This observation is similar to previous reports.19,20 Providing instruction to seek medical attention as soon as any symptom appears in the population could reduce this delayed admission and educating them could improve the awareness of this disease.
In this study, clinical features of EVD in elderly, characterized by nonspecific signs and symptoms such as fever, diarrhea, anorexia, abdominal pain, joint pain, and headache, were similar to those reported elsewhere.21 Bleeding, previously considered as a hallmark of EVD,19 was seen relatively in low numbers compared with other reports.19,21 This finding suggests that bleeding was not a major characteristic of this West African EVD outbreak.
The logistic regression analysis showed that age was significantly associated with death. In other words, elderly patients had a higher probability to die when infected with the Ebola virus than the adult group. This observation was also concordant with the earlier report.9
The retrospective design of the present analysis is the primary limitation, and as with other retrospective studies, caution must be exercised when interpreting the results because selection, information, and recall bias in the elderly cannot be totally excluded.
In summary, the present cohort study demonstrated that the CFR was significantly higher in the elderly group than in the adult group, and that participation in funeral was a risk factor for EVD. The duration between the onset of symptom and presentation to ETCs was significantly longer in the elderly group. In elderly people, age was found to be associated with death due to EVD. Based on our observations, the EVD control program should focus on educating the elderly and/or providing new strategies for behaviors and practices among those involved in handling the deceased. This information could be important for the management of future EVD outbreaks.
Acknowledgments:
We thank the Coordination Nationale de lutte contre la Maladie à Virus Ebola for the collaboration.
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