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      Chikungunya outbreak (2015) in the Colombian Caribbean: Latent classes and gender differences in virus infection

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          Abstract

          Chikungunya virus (CHIKV), a mosquito-borne alphavirus of the Togaviridae family, is part of a group of emergent diseases, including arbovirus, constituting an increasing public health problem in tropical areas worldwide. CHIKV causes a severe and debilitating disease with high morbidity. The first Colombian autochthonous case was reported in the Colombian Caribbean region in September 2014. Within the next two to three months, the CHIKV outbreak reached its peak. Although the CHIKV pattern of clinical symptomatology has been documented in different epidemiological studies, understanding of the relationship between clinical symptomatology and variation in phenotypic response to CHIKV infection in humans remains limited. We performed a cross sectional study following 1160 individuals clinically diagnosed with CHIKV at the peak of the Chikungunya outbreak in the Colombian Caribbean region. We examined the relationship between symptomatology and diverse phenotypic responses. Latent Class Cluster Analysis (LCCA) models were used to characterize patients’ symptomatology and further identify subgroups of individuals with differential phenotypic response. We found that most individuals presented fever (94.4%), headache (73.28%) and general discomfort (59.4%), which are distinct clinical symptoms of a viral infection. Furthermore, 11/26 (43.2%) of the categorized symptoms were more frequent in women than in men. LCCA disclosed seven distinctive phenotypic response profiles in this population of CHIKV infected individuals. Interestingly, 282 (24.3%) individuals exhibited a lower symptomatic “extreme” phenotype and 74 (6.4%) patients were within the severe complex “extreme” phenotype. Although clinical symptomatology may be diverse, there are distinct symptoms or group of symptoms that can be correlated with differential phenotypic response and perhaps susceptibility to CHIKV infection, especially in the female population. This suggests that, comparatively to men, women are a CHIKV at-risk population. Further study is needed to validate these results and determine whether the distinct LCCA profiles are a result of the immune response or a mixture of genetic, lifestyle and environmental factors. Our findings could contribute to the development of machine learning approaches to characterizing CHIKV infection in other populations. Preliminary results have shown prediction models achieving up to 92% accuracy overall, with substantial sensitivity, specificity and accuracy values per LCCA-derived cluster.

          Author summary

          The Chikungunya virus (CHIKV) infection is a mosquito-borne virus of the Togaviridae family, part of the arbovirus group of mosquito-transmitted pathogens. CHIKV causes a severe and debilitating disease with high morbidity. In this study, we comprehensively analysed clinical data from 1160 individuals from the Colombian Caribbean, who were diagnosed with CHIKV infection during the 2014 epidemic peak and before the Zika epidemic (registered back in 2015). Further, the presence of latent classes and predictors of CHIKV susceptibility and severity of the CHIKV infection were analysed. Although it is well known that people respond differently to infection, our results showed that these differences are not arbitrary and may come from the specific orchestration of our immune response and specific genetic makeup. For example, we identified that females infected with CHIKV exhibited significant and heterogeneous phenotypic response patterns compared to men. Overall, these results inform about potential predictors and outlining strategies to study the natural history of CHIKV infection. Future studies assessing the contribution of demographic, immunological and genetic factors to symptom co-occurrence could shed some light on the severity of the clinical symptomatology and, ultimately, lead to more accurate, more efficient and differential diagnosis. These results could contribute to the development of machine learning approaches to characterizing CHIKV infection in other populations and provide more accurate and differential diagnosis.

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          Most cited references31

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          Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing

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            Outbreak of chikungunya on Reunion Island: early clinical and laboratory features in 157 adult patients.

            Chikungunya is a reemerging disease. In 2005-2006, a severe outbreak occurred on Reunion Island in the southwestern part of the Indian Ocean. Other islands in this area were affected during the same period. Adult patients with acute chikungunya (defined as onset of fever and/or polyarthralgia in the 5 days preceding consultation) and laboratory-confirmed chikungunya who were referred to Groupe Hospitalier Sud Reunion during the period from March 2005 through April 2006 were included in this retrospective study. Their clinical and laboratory features are reported. Laboratory-confirmed acute chikungunya was documented in 157 patients. The mean age of patients was 57.9 years, and the ratio of male to female patients was 1.24 : 1. Sixty percent of patients had at least 1 comorbidity. Ninety-seven patients (61.8%) were hospitalized, and 60 (38.2%) were treated as outpatients. Five fatalities were reported. One hundred fifty-one patients (96.1%) experienced polyarthralgia, and 129 (89%) experienced fever. Gastrointestinal symptoms were reported by 74 patients (47.1%), and skin rash was reported by 63 (40.1%). Hemorrhagic signs were rare. Lymphopenia and hypocalcemia were the prominent laboratory findings. Severe thrombocytopenia was rarely observed. Chikungunya virus can be responsible for explosive outbreaks of disease. Polyarthralgia and fever are the 2 main clinical features. In this era of travel and globalization, chikungunya should be considered in the differential diagnosis of febrile polyarthralgia with an abrupt onset.
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              Replication cycle of chikungunya: a re-emerging arbovirus.

              Arboviruses (or arthropod-borne viruses), represent a threat for the new century. The 2005-2006 year unprecedented epidemics of chikungunya virus (CHIKV) in the French Reunion Island in the Indian Ocean, followed by several outbreaks in other parts of the world such as India, have attracted the attention of clinicians, scientists, and state authorities about the risks linked to this re-emerging mosquito-borne virus. CHIKV, which belongs to the Alphaviruses genus, was not previously regarded as a highly pathogenic arbovirus. However, this opinion was challenged by the death of several CHIKV-infected persons in Reunion Island. The epidemic episode began in December 2005 and four months later the seroprevalence survey report indicated that 236,000 persons, more than 30% of Reunion Island population, had been infected with CHIKV, among which 0.4-0.5% of cases were fatal. Since the epidemic peak, the infection case number has continued to increase to almost 40% of the population, with a total of more than 250 fatalities. Although information available on CHIKV is growing quite rapidly, we are still far from understanding the strategies required for the ecologic success of this virus, virus replication, its interactions with its vertebrate hosts and arthropod vectors, and its genetic evolution. In this paper, we summarize the current knowledge of CHIKV genomic organization, cell tropism, and the virus replication cycle, and evaluate the possibility to predict its future evolution. Such understanding may be applied in order to anticipate future epidemics and reduce the incidence by development and application of, for example, vaccination and antiviral therapy.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: InvestigationRole: ResourcesRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: InvestigationRole: Writing – review & editing
                Role: InvestigationRole: ResourcesRole: SupervisionRole: ValidationRole: Writing – review & editing
                Role: InvestigationRole: Supervision
                Role: InvestigationRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Formal analysisRole: MethodologyRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: InvestigationRole: MethodologyRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS Negl Trop Dis
                PLoS Negl Trop Dis
                plos
                plosntds
                PLoS Neglected Tropical Diseases
                Public Library of Science (San Francisco, CA USA )
                1935-2727
                1935-2735
                3 June 2020
                June 2020
                : 14
                : 6
                : e0008281
                Affiliations
                [1 ] Universidad del Norte, Barranquilla, Colombia
                [2 ] Epidemiological Surveillance Team, Health Secretary Program, Barranquilla, Colombia
                [3 ] Grupo de Investigación en Psiquiatría (GIPSI), Departamento de Psiquiatría, Instituto de Investigaciones Médicas, Facultad de Medicina, Universidad de Antioquia, Medellín, Colombia
                Mahidol University, THAILAND
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0003-4303-3243
                http://orcid.org/0000-0001-8657-7916
                http://orcid.org/0000-0002-3146-7899
                Article
                PNTD-D-19-01462
                10.1371/journal.pntd.0008281
                7304630
                32492017
                887d2e0a-b0d1-4a36-83c3-f88d08063d85
                © 2020 Vidal et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 30 September 2019
                : 8 April 2020
                Page count
                Figures: 4, Tables: 3, Pages: 18
                Funding
                The author(s) received no specific funding for this work.
                Categories
                Research Article
                Medicine and Health Sciences
                Tropical Diseases
                Neglected Tropical Diseases
                Chikungunya Infection
                Medicine and Health Sciences
                Infectious Diseases
                Viral Diseases
                Chikungunya Infection
                Biology and life sciences
                Organisms
                Viruses
                RNA viruses
                Togaviruses
                Alphaviruses
                Chikungunya Virus
                Biology and Life Sciences
                Microbiology
                Medical Microbiology
                Microbial Pathogens
                Viral Pathogens
                Togaviruses
                Alphaviruses
                Chikungunya Virus
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Microbial Pathogens
                Viral Pathogens
                Togaviruses
                Alphaviruses
                Chikungunya Virus
                Biology and Life Sciences
                Organisms
                Viruses
                Viral Pathogens
                Togaviruses
                Alphaviruses
                Chikungunya Virus
                Medicine and Health Sciences
                Epidemiology
                Medicine and Health Sciences
                Diagnostic Medicine
                Signs and Symptoms
                Fevers
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Signs and Symptoms
                Fevers
                Medicine and Health Sciences
                Diagnostic Medicine
                Signs and Symptoms
                Headaches
                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Signs and Symptoms
                Headaches
                Biology and Life Sciences
                Physiology
                Sensory Physiology
                Somatosensory System
                Pain Sensation
                Medicine and Health Sciences
                Physiology
                Sensory Physiology
                Somatosensory System
                Pain Sensation
                Biology and Life Sciences
                Neuroscience
                Sensory Systems
                Somatosensory System
                Pain Sensation
                People and places
                Geographical locations
                North America
                Caribbean
                Biology and Life Sciences
                Immunology
                Immune Response
                Medicine and Health Sciences
                Immunology
                Immune Response
                Custom metadata
                vor-update-to-uncorrected-proof
                2020-06-19
                The data underlying the results presented in the study are available from https://doi.org/10.6084/m9.figshare.12478004.

                Infectious disease & Microbiology
                Infectious disease & Microbiology

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