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Background: Following the 2013-2016 West African Ebola outbreak, distinct, persistent health complaints were recognized in Ebola virus disease (EVD) survivors. Here we provide an in-depth characterization of post-Ebola syndrome >2.5 years after resolution of disease. Additionally, we report subphenotypes of post-Ebola syndrome with overlapping symptom clusters in survivors from Eastern Sierra Leone.
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Methods: Participants in Eastern Sierra Leone were identied by the Sierra Leone Association of Ebola survivors. Survivors and their contacts were administered a questionnaire assessing self-reported symptoms and a physical examination. Comparisons between survivors and contacts were conducted using conditional logistic regression. Symptom groupings were identified using hierarchical clustering approaches. Simplified presentation of incredibly complex evaluations (SPICE), correlation analysis, logistic regression, and principal component analysis (PCA) were performed to explore the relationships between symptom clusters.
Results: Three hundred seventy-five EVD survivors and 1040 contacts were enrolled into the study. At enrollment, EVD survivors reported signicantly more symptoms than their contacts in all categories (P < .001). Symptom clusters representing distinct organ systems were identified. Correlation and logistic regression analysis identified relationships between symptom clusters, including stronger relationships between clusters including musculoskeletal symptoms (r = 0.63, P < .001; and P < .001 for correlation and logistic regression, respectively). SPICE and PCA further highlighted subphenotypes with or without musculoskeletal symptoms.
Conclusions: This study presents an in-depth characterization of post-Ebola syndrome in Sierra Leonean survivors >2.5 years after disease. The interrelationship between symptom clusters indicates that post-Ebola syndrome is a heterogeneous disease. The distinct musculoskeletal and non-musculoskeletal phenotypes identified likely require targeted therapies to optimize long-term treatment for EVD survivors.
This study is the first to use an objective and standardized measurement to report hearing loss among EVD survivors in a clinically meaningful manner. In this study it was found that greater than 1/5th of EVD survivors develop hearing loss. The association between hearing impairment and symptoms affecting the eye and nervous system may indicate a similar mechanism of pathogenesis, which should be investigated further. Due to the quality of life and socioeconomic detriments associated with untreated hearing loss, a greater emphasis must be placed on understanding and mitigating hearing loss following survival to aid in economic recovery following infectious disease epidemics.
It is well known that individuals living in these environments suffer from higher rates of bacterial and viral meningitis and the neurologic sequelae associated with these infections [14, 15]. Hearing loss secondary to these infections is thought to occur due to overactivation of the immune system and direct toxicity causing damage to the cochlea [16,17,18]. However, the pathophysiology of hearing loss related to lesser understood tropical viruses remains poorly characterized.
The case control study described here sought to characterize Post-Ebola Syndrome hearing loss. Characterization of this and other sequelae may help elucidate the pathogenesis of Post-Ebola Syndrome, identify treatment and intervention options, and increase understanding of the full disease course of EVD. An increased understanding of this disease course will allow for improved ability to design interventions and treatments to mitigate and prevent the acute and chronic symptoms of EVD affecting these tropical and LMIC.
This study was conducted in eastern Sierra Leone from July 2018 to June 2019. Most participants were already enrolled in an ongoing longitudinal study of EVD survivors and household contacts in Sierra Leone [32]. EVD survivors of the West African Ebola outbreak were eligible for enrollment if they were seven years of age or older, if they were registered with the Sierra Leone Association of EVD survivors, and lived in the Eastern Province of Sierra Leone. Each EVD survivor was asked to recruit up to three additional individuals without a history of EBOV infection from their household or village. These additional individuals serve as the control population for the cohort of EVD survivors.
All individuals completed an extensive questionnaire concerning constitutional, psychiatric, neurologic, ocular, audiovestibular, respiratory, cardiac, gastrointestinal, urorenal, and reproductive or sexual symptoms experienced at the time of the audiometry testing. Additionally, all individuals were given a full physical exam completed by a government hospital physician and a two-step audiometry process.
Symptom surveys and physical exams were organized and grouped into aggregate variables according to the affected organ system (Fig. 2). When physical exam and symptom survey data are pooled and viewed together, EVD survivors were more likely to have abnormal findings in every organ system except the systemic and urorenal organ systems. Similar results were found in symptom survey data (Table 2). Interestingly, among physical exam variables, significant differences were only noted among inner and middle ear, gastrointestinal, and ophthalmologic exams (Table 2).
Symptom survey and physical exam organ system findings. Graph displays data gathered through symptom surveys and physical exams. Individual survey questions and physical exam maneuvers were aggregated according to the respective organ system affected
Logistic regression results of sensorineural and mixed hearing loss among EVD survivors. The organ systems listed on the Y axis of regression model were found to significantly affect the odds of developing the most common type of hearing loss associated with EVD. Each point represents the odds of having hearing loss if complaints or abnormal findings were noted affecting each respective organ systems. 95% confidence intervals represented by solid lines
Decision tree model predicting sensorineural or mixed hearing loss among EVD cohort. Decision tree modelling produced the following algorithm to detect the most common form of hearing loss noted among EVD survivors and contacts. Prevalence of hearing loss at each node displayed in parentheses. Model characteristics presented in table underneath model
Several viral diseases have been noted to cause hearing loss in the convalescent period. The more common viral etiologies include CMV, rubella, mumps, and tropical pathogens such as chikungunya, Zika, and Lassa fever viruses [16, 33, 42,43,44,45,46,47,48,49]. Although previous studies have suggested that direct viral damage to structures of the inner ear such as the stria vascularis, cochlea, and neuronal damage may be responsible in mumps and rubella, a host immune response to viral antigens in CMV, or the development of a vasculitis or autoimmune disease as in Lassa fever have been hypothesized [16, 45]. However, definitive evidence of any mechanism of pathogenesis is limited. Similarly, the mechanism through which Post-Ebola Syndrome hearing loss develops is still unknown. Previous studies have provided evidence of viral persistence in immune privileged sites such as the aqueous humor, semen, vaginal secretions, and the cerebrospinal fluid, as well as an association between this viral persistence and the development of convalescent symptoms [31, 50,51,52,53,54]. An additional study demonstrated that higher levels of viremia have been associated with the development of Post-Ebola Syndrome [55]. Collectively, these data indicate that a greater level of viremia may be required in order to penetrate immune privileged sites where delayed viral clearance and active replication may lead to greater amounts of direct viral damage to these protected structures. This hypothesis is in agreement with the results of the logistic regression modelling performed by this study which found that individuals who developed symptoms affecting the immune privileged sites of the eye or nervous system had 2.32 and 2.04 times the odds, respectively, of developing hearing loss. In contrast to the direct viral cytopathic effect, persistent immune activation has also been proposed as a possible mechanism partially responsible for the symptoms prevalent in Post-Ebola syndrome [56]. These two independent and competing processes of direct cytopathic effect and persistent immune activation may help to explain why the logistic regression model in this study found that individuals who developed pulmonary symptoms had significantly lower odds of developing an additional hearing impairment, as previous evidence has indicated that viral infections causing persistent immune activation can drive the development of a chronic lung disease [57].
To our knowledge, this is the largest systematic study of hearing loss among EVD survivors. The results of this study are unique in that they are the first to provide both air and bone conduction results in a cohort of EVD survivors and household contacts. These measurements found that 23% of EVD survivors had some form of hearing loss, which is significantly greater than their household contacts (9%). The most common type of hearing loss found among this survivor cohort was bilateral of either a mixed or sensorineural etiology. The majority of individuals with hearing loss were found to have mild hearing loss. Several previous studies have indicated that hearing loss is associated with an impaired ability to complete activities of daily living, increased rates of isolation, increased risk of depression, early cognitive decline in the elderly; increased risk of under- or unemployment, and lower socioeconomic status in adults; and increased risk of non-completion of secondary education, lower scores on IQ and verbal intelligence tests, and impaired language development in children [1, 58,59,60,61,62,63,64]. 152ee80cbc