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Estimating incidence of infection from diverse data sources: Zika virus in Puerto Rico, 2016 (preprint)
Quandelacy TM , Healy JM , Greening B , Rodriguez DM , Chung KW , Kuehnert MJ , Biggerstaff BJ , Dirlikov E , Mier YTeran-Romero L , Sharp TM , Waterman S , Johansson MA . medRxiv 2020 2020.10.14.20212134 Emerging epidemics are challenging to track. Only a subset of cases is recognized and reported, as seen with the Zika virus (ZIKV) epidemic where large proportions of infection were asymptomatic. However, multiple imperfect indicators of infection provide an opportunity to estimate the underlying incidence of infection. We developed a modeling approach that integrates a generic Time-series Susceptible-Infected-Recovered epidemic model with assumptions about reporting biases in a Bayesian framework and applied it to the 2016 Zika epidemic in Puerto Rico using three indicators: suspected arboviral cases, suspected Zika-associated Guillain-Barré Syndrome cases, and blood bank data. Using this combination of surveillance data, we estimated the peak of the epidemic occurred during the week of August 15, 2016 (the 33rd week of year), and 120 to 140 (50% credible interval [CrI], 95% CrI: 97 to 170) weekly infections per 10,000 population occurred at the peak. By the end of 2016, we estimated that approximately 890,000 (95% CrI: 660,000 to 1,100,000) individuals were infected in 2016 (26%, 95% CrI: 19% to 33%, of the population infected). Utilizing multiple indicators offers the opportunity for real-time and retrospective situational awareness to support epidemic preparedness and response.Competing Interest StatementThe authors have declared no competing interest.Funding StatementThe author(s) received no specific funding for this work.Author DeclarationsI confirm all relevant ethical guidelines have been followed, and any necessary IRB and/or ethics committee approvals have been obtained.YesThe details of the IRB/oversight body that provided approval or exemption for the research described are given below:Exemption was obtained from the CDC Human Subjects Research Office as the data were collected as part of regular surveillance activities.All necessary patient/participant consent has been obtained and the appropriate institutional forms have been archived.YesI understand that all clinical trials and any other prospective interventional studies must be registered with an ICMJE-approved registry, such as ClinicalTrials.gov. I confirm that any such study reported in the manuscript has been registered and the trial registration ID is provided (note: if posting a prospective study registered retrospectively, please provide a statement in the trial ID field explaining why the study was not registered in advance).YesI have followed all appropriate research reporting guidelines and uploaded the relevant EQUATOR Network research reporting checklist(s) and other pertinent material as supplementary files, if applicable.YesAll relevant data are within the manuscript and its Supporting Information files. |
Identification of risk factors and mosquito vectors associated with dengue virus infection in American Samoa, 2017
Sharp TM , Tufa AJ , Cotter CJ , Lozier MJ , Santiago GA , Johnson SS , Mataia'a M , Waterman SH , Muñoz-Jordán JL , Paz-Bailey G , Hemme RR , Schmaedick MA , Anesi S . PLOS Glob Public Health 2023 3 (7) e0001604 INTRODUCTION: The first outbreak of dengue in American Samoa was reported in 1911. Sporadic outbreaks have been reported since, as were outbreaks of other pathogens transmitted by Aedes species mosquitoes including Ross River, chikungunya, and Zika viruses. During an outbreak of dengue virus-type 2 (DENV-2) in 2016-2018, we conducted household-based cluster investigations to identify population-specific risk factors associated with infection and performed entomologic surveillance to determine the relative abundance of Ae. aegypti and Ae. polynesiensis. METHODS AND FINDINGS: We contacted dengue patients who had tested positive for DENV infection and offered them as well as their household members participation in household-based cluster investigations. For those that accepted participation, we also offered participation to residents of households within a 50-meter radius of each case-patient's home. Questionnaires were administered and serum specimens collected for testing by RT-PCR and anti-DENV IgM ELISA. Adult female mosquitoes were aspirated from inside and outside participating households and tested by RT-PCR. We analyzed characteristics associated with DENV infection in bivariate analyses. A total of 226 participants was enrolled from 91 households in 20 clusters. Median age of participants was 34 years (range: <1-94), and 56.2% were female. In total, 7 (3.2%) participants had evidence of DENV infection by IgM ELISA (n = 5) or RT-PCR (n = 2). Factors significantly associated with DENV infection were reporting a febrile illness in the past three months (prevalence ratio: 7.5 [95% confidence interval: 1.9-29.8]) and having a household septic tank (Fisher's Exact Test, p = 0.004). Of 93 Ae. aegypti and 90 Ae. polynesiensis females collected, 90% of Ae. aegypti were collected inside homes whereas 83% of Ae. polynesiensis were collected outside homes. DENV nucleic acid was not detected in any mosquito pools. Sequencing of the DENV-2 from patient specimens identified the Cosmopolitan genotype of DENV-2 and was most closely related to virus detected in the Solomon Islands during 2016. CONCLUSIONS: This investigation demonstrated that dengue is a continuing risk in American Samoa. Increased frequency of infection among residents with a septic tank suggests a need to investigate whether septic tanks serve as larval habitats for mosquito vectors of DENV in American Samoa. Future efforts should also evaluate the role of Ae. polynesiensis in DENV transmission in the wild. |
Persistence of Zika Virus in Body Fluids - Final Report
Paz-Bailey G , Rosenberg ES , Sharp TM . N Engl J Med 2019 380 (2) 198-199 In reply to Sánchez-Montalvá and colleagues: in contrast to dengue, which has a well-defined spectrum of severe disease, most cases of noncongenital ZIKV disease are mild, except for rare complications such as Guillain–Barré syndrome.1 In the participants in our study, the signs and symptoms were consistent with uncomplicated ZIKV disease. Furthermore, with respect to the duration of detectable ZIKV RNA, we saw no difference between the 35% of participants who were enrolled at outpatient clinics and those who were enrolled at emergency departments (P = 0.22). We agree that it is not known whether humans can be reinfected with ZIKV; however, studies in mice have shown protection from reinfection, including an absence of detectable viremia.2 In vitro evidence of antibody-dependent enhancement can occur in flaviviruses in the absence of in vivo evidence.3 A study from Colombia showed no evidence of in vivo enhancement of ZIKV in patients with previous dengue virus infection.4 Moreover, findings in men from the continental United States, where dengue virus rarely circulates, were similar to those of our study.5 Finally, sexual transmission contributes to a small percentage of ZIKV infections and would not affect our findings. |
Predominance of severe plasma leakage in pediatric patients with severe dengue in Puerto Rico
Paz-Bailey G , Sánchez-González L , Torres-Velasquez B , Jones E , Perez-Padilla J , Sharp TM , Lorenzi O , Delorey M , Munoz-Jordan J , Tomashek KM , Waterman SH , Alvarado LI , Rivera-Amil V . J Infect Dis 2022 226 (11) 1949-1958 BACKGROUND: We evaluated clinical and laboratory findings among patients with non-severe or severe dengue in Puerto Rico to examine whether clinical manifestations vary by age. METHODS: During 2012-2014, we enrolled patients who arrived at the emergency department with fever or history of fever within 7 days of presentation. Serum samples were tested for dengue virus (DENV) by RT-PCR and IgM ELISA. Severe dengue was defined as severe plasma leakage or shock, severe bleeding, or organ involvement at presentation, during hospitalization, or follow-up. RESULTS: Of 1089 dengue patients identified, 281 (26%) were severe. Compared to those with non-severe dengue, patients with severe dengue were more often aged 10-19 years (55% vs. 40%, p < 0.001) and hospitalized (87% vs. 30%, p < 0.001). Severe plasma leakage or shock was more common among children aged 0-9 (59%) or 10-19 years (86%) than adults (49%) (p < 0.01). Severe bleeding was less common among 10-19 year-olds (24%) compared to 0-9 year-olds (45%) and adults (52%; p < 0.01). CONCLUSIONS: Severe plasma leakage was the most common presentation among children, highlighting important differences with adults. Vaccination against dengue could help prevent severe dengue among children in Puerto Rico. |
Novel Assay to Measure Seroprevalence of Zika Virus in the Philippines
Medina FA , Sharp TM , Munoz-Jordan JL . Emerg Infect Dis 2021 27 (12) 3073-3081 Zika virus (ZIKV) is a member of the Flaviviridae family, which includes other clinically notable viruses such as the 4 dengue virus serotypes (DENV-1-4). Distinguishing DENVs from ZIKV using the established serologic assays widely used for monitoring DENV transmission is difficult because of antibody cross-reactivity between these closely related flaviviruses. We describe a modified and improved recombinant envelope domain III-based serologic assay for detecting ZIKV type-specific antibodies in regions with endemic DENV transmission. When the assay was used to measure ZIKV seroprevalence in 2017 among children 9-14 years of age living in a region of the Philippines with endemic DENV transmission, we observed a ZIKV seroprevalence of 18%. Investigators should consider using the ZIKV envelope domain III-based assay, which is simple and readily adaptable for use in standard clinical and public health laboratories, to assess ZIKV seroprevalence in areas with endemic DENV transmission. |
Tracing the Origin, Spread, and Molecular Evolution of Zika Virus in Puerto Rico, 2016-2017.
Santiago GA , Kalinich CC , Cruz-López F , González GL , Flores B , Hentoff A , Charriez KN , Fauver JR , Adams LE , Sharp TM , Black A , Bedford T , Ellis E , Ellis B , Waterman SH , Paz-Bailey G , Grubaugh ND , Muñoz-Jordán JL . Emerg Infect Dis 2021 27 (11) 2971-2973 We reconstructed the 2016-2017 Zika virus epidemic in Puerto Rico by using complete genomes to uncover the epidemic's origin, spread, and evolutionary dynamics. Our study revealed that the epidemic was propelled by multiple introductions that spread across the island, intricate evolutionary patterns, and ≈10 months of cryptic transmission. |
Knowledge gaps in the epidemiology of severe dengue impede vaccine evaluation
Sharp TM , Anderson KB , Katzelnick LC , Clapham H , Johansson MA , Morrison AC , Harris E , Paz-Bailey G , Waterman SH . Lancet Infect Dis 2021 22 (2) e42-e51 The most severe consequences of dengue virus infection include shock, haemorrhage, and major organ failure; however, the frequency of these manifestations varies, and the relative contribution of pre-existing anti-dengue virus antibodies, virus characteristics, and host factors (including age and comorbidities) are not well understood. Reliable characterisation of the epidemiology of severe dengue first depends on the use of consistent definitions of disease severity. As vaccine trials have shown, severe dengue is a crucial interventional endpoint, yet the infrequency of its occurrence necessitates the inclusion of thousands of study participants to appropriately compare its frequency among participants who have and have not been vaccinated. Hospital admission is frequently used as a proxy for severe dengue; however, lack of specificity and variability in clinical practices limit the reliability of this approach. Although previous infection with a dengue virus is the best characterised risk factor for developing severe dengue, the influence of the timing between dengue virus infections and the sequence of dengue virus infections on disease severity is only beginning to be elucidated. To improve our understanding of the diverse factors that shape the clinical spectrum of disease resulting from dengue virus infection, prospective, community-based and clinic-based immunological, virological, genetic, and clinical studies across a range of ages and geographical regions are needed. |
Fatal Dengue Acquired in Florida
Sharp TM , Morris S , Morrison A , de Lima Corvino D , Santiago GA , Shieh WJ , Rico E , Kopp E , Muñoz-Jordán JL , Marttos A , Paz-Bailey G , Abbo LM , Stanek D . N Engl J Med 2021 384 (23) 2257-2259 The global burden of dengue, a mosquito-borne viral acute febrile illness common throughout the tropics, is worsening.1,2 Approximately 5% of patients have progression to severe dengue, including plasma leakage, shock, and hemorrhage, but they may also present with acute cholecystitis.1,3 | | In 2019, a total of 413 dengue cases were probably imported to Florida, including 14 cases of severe dengue (3.4%), resulting in 18 locally acquired cases, predominantly in the Miami area (Figs. S1 and S2 in the Supplementary Appendix, available with the full text of this letter at NEJM.org). Most persons with travel-associated cases reported recent travel to Cuba and were infected with dengue virus (DENV) serotype 2 (DENV-2). |
Dengue Virus Infections among Peace Corps Volunteers in Timor-Leste, 2018-2019
Sánchez-González L , Venuto M , Poe S , Major CG , Baskara L , Abdiyeva S , Murphy D , Munoz-Jordan JL , Medina FA , Paz-Bailey G , Petersen K , Becker K , Sharp TM . Am J Trop Med Hyg 2021 104 (6) 2202-2209 Dengue is an ongoing health risk for Peace Corps Volunteers (PCVs) working in the tropics. On May 2019, the Peace Corps Office of Health Services notified the Centers for Disease Control and Prevention (CDC) of a dengue outbreak among PCVs in Timor-Leste. The purpose of this investigation was to identify the clinical, demographic, and epidemiological characteristics of PCVs with dengue and recommend dengue preventive measures. To identify PCVs with dengue and describe disease severity, the medical records of PCVs reporting fever during September 2018-June 2019 were reviewed. To identify factors associated with dengue virus (DENV) infection, we administered a questionnaire on demographics, travel history, and mosquito avoidance behaviors and collected blood specimens to detect the anti-DENV IgM antibody to diagnose recent infection. Of 35 PCVs in-country, 11 (31%) tested positive for dengue (NS1, IgM, PCR), eight requiring hospitalization and medical evacuation. Among 27 (77%) PCVs who participated in the investigation, all reported having been recently bitten by mosquitoes and 56% reported being bitten most often at home; only 16 (59%) reported having screens on bedroom windows. Nearly all (93%) PCVs reported using a bed net every night; fewer (70%) reported using mosquito repellent at least once a day. No behaviors were significantly associated with DENV infection. Raising awareness of dengue risk among PCVs and continuing to encourage mosquito avoidance behavior to prevent dengue is critical. Access to and use of measures to avoid mosquito bites should be improved or implemented. Peace Corps medical officers should continue to receive an annual refresher training on dengue clinical management. |
Estimating incidence of infection from diverse data sources: Zika virus in Puerto Rico, 2016
Quandelacy TM , Healy JM , Greening B , Rodriguez DM , Chung KW , Kuehnert MJ , Biggerstaff BJ , Dirlikov E , Mier YTeran-Romero L , Sharp TM , Waterman S , Johansson MA . PLoS Comput Biol 2021 17 (3) e1008812 Emerging epidemics are challenging to track. Only a subset of cases is recognized and reported, as seen with the Zika virus (ZIKV) epidemic where large proportions of infection were asymptomatic. However, multiple imperfect indicators of infection provide an opportunity to estimate the underlying incidence of infection. We developed a modeling approach that integrates a generic Time-series Susceptible-Infected-Recovered epidemic model with assumptions about reporting biases in a Bayesian framework and applied it to the 2016 Zika epidemic in Puerto Rico using three indicators: suspected arboviral cases, suspected Zika-associated Guillain-Barré Syndrome cases, and blood bank data. Using this combination of surveillance data, we estimated the peak of the epidemic occurred during the week of August 15, 2016 (the 33rd week of year), and 120 to 140 (50% credible interval [CrI], 95% CrI: 97 to 170) weekly infections per 10,000 population occurred at the peak. By the end of 2016, we estimated that approximately 890,000 (95% CrI: 660,000 to 1,100,000) individuals were infected in 2016 (26%, 95% CrI: 19% to 33%, of the population infected). Utilizing multiple indicators offers the opportunity for real-time and retrospective situational awareness to support epidemic preparedness and response. |
Notes from the field: Interpretation of rapid diagnostic tests for leptospirosis during a dengue outbreak - Yap State, Federated States of Micronesia, 2019
Dawson P , Marfel M , Galloway R , Tareg A , Paz-Bailey G , Muñoz-Jordán JL , Sharp TM , Adams LE , Bower WA . MMWR Morb Mortal Wkly Rep 2020 69 (48) 1832-1833 On August 30, 2019, Yap State declared a public health crisis caused by concurrent outbreaks of dengue and leptospirosis, two clinically similar illnesses, resulting in 545 suspected dengue cases and 515 suspected leptospirosis cases during January–August 2019. Dengue virus type 3 (DENV-3) was identified by reverse transcription–polymerase chain reaction (RT-PCR) for 38 patients. Leptospirosis is endemic in Yap State (pop. approximately 11,500) with an anecdotal baseline of 0–2 cases/month.* Dengue is a potentially fatal mosquitoborne acute febrile viral illness (1). Leptospirosis is caused by infection with Leptospira bacteria and commonly acquired from contact with water or soil contaminated with infected animal urine (2). Approximately 90% of patients with leptospirosis experience self-limiting acute febrile illness, and 10% develop severe, potentially life-threatening illness (3). Early antibiotic treatment is generally associated with less severe and shorter illness (4). A team of outbreak investigators from Yap State and CDC identified suspected dengue and leptospirosis cases among patients with dengue-like illness (DLI),† which is clinically compatible with both illnesses. The majority of patients with DLI were reported and tested as having suspected cases of both dengue and leptospirosis during the outbreak. |
Laboratory-acquired dengue virus infection, United States, 2018
Sharp TM , Fisher TG , Long K , Coulson G , Medina FA , Herzig C , Koza MB , Muñoz-Jordán J , Paz-Bailey G , Moore Z , Williams C . Emerg Infect Dis 2020 26 (7) 1534-1537 Investigation of a dengue case in a laboratory worker in North Carolina, USA, revealed that the case-patient prepared high-titer dengue virus stocks soon before illness onset. Improper doffing of gloves with an open finger wound likely resulted in cutaneous exposure. This case reinforces recommendations for enhanced precautions when working with high-titer dengue virus. |
Epidemiologic and spatiotemporal trends of Zika Virus disease during the 2016 epidemic in Puerto Rico
Sharp TM , Quandelacy TM , Adams LE , Aponte JT , Lozier MJ , Ryff K , Flores M , Rivera A , Santiago GA , Muñoz-Jordán JL , Alvarado LI , Rivera-Amill V , Garcia-Negrón M , Waterman SH , Paz-Bailey G , Johansson MA , Rivera-Garcia B . PLoS Negl Trop Dis 2020 14 (9) e0008532 BACKGROUND: After Zika virus (ZIKV) emerged in the Americas, laboratory-based surveillance for arboviral diseases in Puerto Rico was adapted to include ZIKV disease. METHODS AND FINDINGS: Suspected cases of arboviral disease reported to Puerto Rico Department of Health were tested for evidence of infection with Zika, dengue, and chikungunya viruses by RT-PCR and IgM ELISA. To describe spatiotemporal trends among confirmed ZIKV disease cases, we analyzed the relationship between municipality-level socio-demographic, climatic, and spatial factors, and both time to detection of the first ZIKV disease case and the midpoint of the outbreak. During November 2015-December 2016, a total of 71,618 suspected arboviral disease cases were reported, of which 39,717 (55.5%; 1.1 cases per 100 residents) tested positive for ZIKV infection. The epidemic peaked in August 2016, when 71.5% of arboviral disease cases reported weekly tested positive for ZIKV infection. Incidence of ZIKV disease was highest among 20-29-year-olds (1.6 cases per 100 residents), and most (62.3%) cases were female. The most frequently reported symptoms were rash (83.0%), headache (64.6%), and myalgia (63.3%). Few patients were hospitalized (1.2%), and 13 (<0.1%) died. Early detection of ZIKV disease cases was associated with increased population size (log hazard ratio [HR]: -0.22 [95% confidence interval -0.29, -0.14]), eastern longitude (log HR: -1.04 [-1.17, -0.91]), and proximity to a city (spline estimated degrees of freedom [edf] = 2.0). Earlier midpoints of the outbreak were associated with northern latitude (log HR: -0.30 [-0.32, -0.29]), eastern longitude (spline edf = 6.5), and higher mean monthly temperature (log HR: -0.04 [-0.05, -0.03]). Higher incidence of ZIKV disease was associated with lower mean precipitation, but not socioeconomic factors. CONCLUSIONS: During the ZIKV epidemic in Puerto Rico, 1% of residents were reported to public health authorities and had laboratory evidence of ZIKV disease. Transmission was first detected in urban areas of eastern Puerto Rico, where transmission also peaked earlier. These trends suggest that ZIKV was first introduced to Puerto Rico in the east before disseminating throughout the island. |
Clinical characteristics, histopathology, and tissue immunolocalization of chikungunya virus antigen in fatal cases
Sharp TM , Keating MK , Shieh WJ , Bhatnagar J , Bollweg BC , Levine R , Blau DM , Torres JV , Rivera A , Perez-Padilla J , Munoz-Jordan J , Sanabria D , Fischer M , Garcia BR , Tomashek KM , Zaki SR . Clin Infect Dis 2020 73 (2) e345-e354 BACKGROUND: Death in patients with chikungunya is rare, and has been associated with encephalitis, hemorrhage, and septic shock. We describe clinical, histologic and immunohistochemical findings in individuals who died following chikungunya virus (CHIKV) infection. METHODS: We identified individuals who died in Puerto Rico during 2014 following an acute illness, and had CHIKV RNA detected by RT-PCR in a pre- or post-mortem blood or tissue specimen. We performed histopathology and immunohistochemistry (IHC) for CHIKV antigen on tissue specimens and collected medical data via record review and family interviews. RESULTS: Thirty CHIKV-infected fatal cases were identified (0.8 per 100,000 population). Median age was 61 years (range: 6 days-86 years), and 19 (63%) were male. Death occurred a median of four days (range: 1-29) after illness onset. Nearly all (93%) had at least one co-morbidity, most frequently hypertension, diabetes, or obesity. Nine had severe co-morbidities (e.g., chronic heart or kidney disease, sickle cell anemia) or co-infection (e.g., leptospirosis). Among 24 fatal cases with tissue specimens, 11 (46%) were positive by IHC. CHIKV antigen was most frequently detected in mesenchymal tissues and mononuclear cells including tissue macrophages, blood mononuclear cells, splenic follicular dendritic cells, and Kupffer cells. Common histopathologic findings were intra-alveolar hemorrhage and edema in the lung, chronic or acute tenosynovitis, and increased immunoblasts in the spleen. CHIKV infection likely caused fatal septic shock in two patients. CONCLUSIONS: Evaluation of tissue specimens provided insights into the pathogenesis of CHIKV, which may rarely result in septic shock and other severe manifestations. |
Travel-associated and locally acquired dengue cases - United States, 2010-2017
Rivera A , Adams LE , Sharp TM , Lehman JA , Waterman SH , Paz-Bailey G . MMWR Morb Mortal Wkly Rep 2020 69 (6) 149-154 Dengue is a potentially fatal acute febrile illness caused by any of four mosquito-transmitted dengue viruses (DENV-1 to DENV-4) belonging to the family Flaviviridae and endemic throughout the tropics. Competent mosquito vectors of DENV are present in approximately one half of all U.S. counties. To describe epidemiologic trends in travel-associated and locally acquired dengue cases in the United States, CDC analyzed cases reported from the 50 states and District of Columbia to the national arboviral surveillance system (ArboNET). Cases are confirmed by detection of 1) virus RNA by reverse transcription-polymerase chain reaction (RT-PCR) in any body fluid or tissue, 2) DENV antigen in tissue by a validated assay, 3) DENV nonstructural protein 1 (NS1) antigen, or 4) immunoglobulin M (IgM) anti-DENV antibody if the patient did not report travel to an area with other circulating flaviviruses. When travel to an area with other flaviviruses was reported, IgM-positive cases were defined as probable. During 2010-2017, totals of 5,009 (93%) travel-associated and 378 (7%) locally acquired confirmed or probable dengue cases were reported to ArboNET. Cases were equally distributed between males and females, and median age was 41 years. Eighteen (three per 1,000) fatal cases were reported, all among travelers. Travelers should review country-specific recommendations (https://wwwnc.cdc.gov/travel/notices/watch/dengue-asia) for reducing their risk for DENV infection, including using insect repellent and staying in residences with air conditioning or screens on windows and doors. |
Reverse Transcription-Polymerase Chain Reaction Testing on Filter Paper-Dried Serum for Laboratory-Based Dengue Surveillance-American Samoa, 2018.
Curren EJ , Tufa AJ , Hancock WT , Biggerstaff BJ , Vaifanua-Leo JS , Montalbo CA , Sharp TM , Fischer M , Hills SL , Gould CV . Am J Trop Med Hyg 2020 102 (3) 622-624 Laboratory-based surveillance for arboviral diseases is challenging in resource-limited settings. We evaluated the use of filter paper-dried sera for detection of dengue virus (DENV) RNA during an outbreak in American Samoa. Matched liquid and filter paper-dried sera were collected from patients with suspected dengue and shipped to a reference laboratory for diagnostic testing. RNA was extracted from each sample and tested for DENV RNA by real-time reverse transcription-polymerase chain reaction (RT-PCR). Of 18 RT-PCR-positive liquid specimens, 14 matched filter paper-dried specimens were positive for a sensitivity of 78% (95% CI, 55-91%). Of 82 RT-PCR-negative liquid specimens, all filter paper-dried specimens were negative for a specificity of 100% (95% CI, 96-100%). Shipping of filter paper-dried specimens was similarly timely but less expensive than shipping liquid sera. Using filter paper-dried serum or blood can be a cost-effective and sustainable approach to surveillance of dengue and other arboviral diseases in resource-limited settings. |
Persistent Zika virus infection associated with early fetal demise: A case report
Perez-Padilla J , Paz-Bailey G , Meaney-Delman D , Doyle K , Gary J , Rodriguez DM , Bhatnagar J , Perez-Rodriguez NM , Montalvo S , Alvarado L , Sharp TM . Open J Obstet Gynecol 2019 9 (5) 698-706 Background: Infection with Zika virus (ZIKV) during pregnancy is known to cause birth defects and could also be linked to pregnancy loss. Case: A pregnant woman in Puerto Rico contracted ZIKV at 16 weeks gestation. ZIKV RNA persisted in serum from her initial test at 16 weeks through 24 weeks gestation, when fetal demise occurred, and was detected in placental tissue. Conclusion: Prolonged detection of ZIKV RNA in maternal serum was associated with ZIKV RNA detection in the placenta of a patient who experienced fetal demise. While detection of placenta ZIKV RNA does not establish that ZIKV conclusively caused the demise, these findings support emerging evidence that the placenta may serve as a reservoir for ZIKV, which may be associated with prolonged detection of ZIKV RNA in serum. |
Prevalence and incidence of Zika virus infection among household contacts of patients with Zika virus disease, Puerto Rico, 2016-2017
Rosenberg ES , Doyle K , Munoz-Jordan JL , Klein L , Adams L , Lozier M , Weiss K , Sharp TM , Paz-Bailey G . J Infect Dis 2019 220 (6) 932-939 BACKGROUND: Little is known about the prevalence or incidence of Zika virus (ZIKV) infection in settings affected by the 2015-2016 Zika pandemic and associated risk factors. We assessed these factors among household contacts of patients with ZIKV disease enrolled in a cohort study in Puerto Rico during 2016-2017. METHODS: Household contacts of index case patients completed a questionnaire and gave specimens for real-time polymerase chain reaction (RT-PCR) and immunoglobulin M enzyme-linked immunosorbent assay testing to detect ZIKV infection. We measured the prevalence of ZIKV infection among contacts and associated individual and household factors, examined sexual transmission using a sexual-networks approach, and assessed incident infection among initially uninfected household contacts 2-4 months later. RESULTS: Of 366 contacts, 34.4% had evidence of ZIKV infection at enrollment, including 11.2% by RT-PCR. Having open doors and windows that were either screened (prevalence ratio [PR], 2.1 [95% confidence interval {CI}, 1.2-3.6]) or unscreened (PR, 2.5 [95% CI, 1.5-4.1]) was associated with increased prevalence. Sexual partners were more likely to both be RT-PCR positive relative to other relationships (odds ratio, 2.2 [95% CI, 1.1-4.5]). At follow-up, 6.1% of contacts had evidence of incident infection. CONCLUSIONS: This study identified sexual contact as a risk factor for ZIKV infection. Persons living with ZIKV-infected individuals should be a focus of public health efforts. |
Epidemiology of dengue, chikungunya, and Zika virus disease in the U.S. states and territories, 2017
Adams LE , Martin SW , Lindsey NP , Lehman JA , Rivera A , Kolsin J , Landry K , Staples JE , Sharp TM , Paz-Bailey G , Fischer M . Am J Trop Med Hyg 2019 101 (4) 884-890 Dengue, chikungunya, and Zika viruses, primarily transmitted by Aedes species mosquitoes, have caused large outbreaks in the Americas, leading to travel-associated cases and local mosquito-borne transmission in the United States. We describe the epidemiology of dengue, chikungunya, and noncongenital Zika virus disease cases reported from U.S. states and territories in 2017, including 971 dengue cases, 195 chikungunya cases, and 1,118 Zika virus disease cases. Cases of all three diseases reported from the territories were reported as resulting from local mosquito-borne transmission. Cases reported from the states were primarily among travelers, with only seven locally acquired mosquito-transmitted Zika virus disease cases reported from Texas (n = 5) and Florida (n = 2). In the territories, most dengue cases (n = 508, 98%) were reported from American Samoa, whereas the majority of chikungunya (n = 39, 100%) and Zika virus disease (n = 620, 93%) cases were reported from Puerto Rico. Temporally, the highest number of Zika virus disease cases occurred at the beginning of the year, followed by a sharp decline, mirroring decreasing case numbers across the Americas following large outbreaks in 2015 and 2016. Dengue and chikungunya cases followed a more seasonal pattern, with higher case numbers from July through September. Travelers to the United States and residents of areas with active virus transmission should be informed of both the ongoing risk from dengue, chikungunya, and Zika virus disease and personal protective measures to lower their risk of mosquito bites and to help prevent the spread of these diseases. |
Prior dengue virus infection is associated with increased viral load in patients infected with dengue but not Zika virus
Santiago GA , Sharp TM , Rosenberg E , Sosa Cardona II , Alvarado L , Paz-Bailey G , Munoz-Jordan JL . Open Forum Infect Dis 2019 6 (7) To evaluate potential enhancement of Zika virus (ZIKV) infection among patients with prior dengue virus (DENV) infection, we compared loads of viral RNA among patients infected with ZIKV (n = 1070), DENV-2 (n = 312), or DENV-3 (n = 260). Compared to patients without prior DENV infection, patients with prior DENV infection had significantly higher mean loads of viral RNA if infected with DENV-2 (10.6 vs 11.6 log10 GCE/mL, respectively; t test, P < .0001) or DENV-3 (10.3 vs 10.9 log10 GCE/mL; P < .0001), but not ZIKV (4.7 vs 4.7 log10 GCE/mL; P = .959). These findings provide evidence against in vivo enhancement of ZIKV by anti-DENV antibodies. |
Lessons learned from dengue surveillance and research, Puerto Rico, 1899-2013
Sharp TM , Ryff KR , Santiago GA , Margolis HS , Waterman SH . Emerg Infect Dis 2019 25 (8) 1522-1530 Dengue was first reported in Puerto Rico in 1899 and sporadically thereafter. Following outbreaks in 1963 and 1969, the Centers for Disease Control and Prevention has worked closely with the Puerto Rico Department of Health to monitor and reduce the public health burden of dengue. During that time, evolving epidemiologic scenarios have provided opportunities to establish, improve, and expand disease surveillance and interventional research projects. These initiatives have enriched the tools available to the global public health community to understand and combat dengue, including diagnostic tests, methods for disease and vector surveillance, and vector control techniques. Our review serves as a guide to organizations seeking to establish dengue surveillance and research programs by highlighting accomplishments, challenges, and lessons learned during more than a century of dengue surveillance and research conducted in Puerto Rico. |
Distinguishing patients with laboratory-confirmed chikungunya from dengue and other acute febrile illnesses, Puerto Rico, 2012-2015
Alvarado LI , Lorenzi OD , Torres-Velasquez BC , Sharp TM , Vargas L , Munoz-Jordan JL , Hunsperger EA , Perez-Padilla J , Rivera A , Gonzalez-Zeno GE , Galloway RL , Glass Elrod M , Mathis DL , Oberste MS , Nix WA , Henderson E , McQuiston J , Singleton J , Kato C , Garcia-Gubern C , Santiago-Rivera W , Muns-Sosa R , Ortiz-Rivera JD , Jimenez G , Rivera-Amill V , Andujar-Perez DA , Horiuchi K , Tomashek KM . PLoS Negl Trop Dis 2019 13 (7) e0007562 Chikungunya, a mosquito-borne viral, acute febrile illness (AFI) is associated with polyarthralgia and polyarthritis. Differentiation from other AFI is difficult due to the non-specific presentation and limited availability of diagnostics. This 3-year study identified independent clinical predictors by day post-illness onset (DPO) at presentation and age-group that distinguish chikungunya cases from two groups: other AFI and dengue. Specimens collected from participants with fever </=7 days were tested for chikungunya, dengue viruses 1-4, and 20 other pathogens. Of 8,996 participants, 18.2% had chikungunya, and 10.8% had dengue. Chikungunya cases were more likely than other groups to be older, report a chronic condition, and present <3 DPO. Regardless of timing of presentation, significant positive predictors for chikungunya versus other AFI were: joint pain, muscle, bone or back pain, skin rash, and red conjunctiva; with dengue as the comparator, red swollen joints (arthritis), joint pain, skin rash, any bleeding, and irritability were predictors. Chikungunya cases were less likely than AFI and dengue to present with thrombocytopenia, signs of poor circulation, diarrhea, headache, and cough. Among participants presenting <3 DPO, predictors for chikungunya versus other AFI included: joint pain, skin rash, and muscle, bone or back pain, and absence of thrombocytopenia, poor circulation and respiratory or gastrointestinal symptoms; when the comparator was dengue, joint pain and arthritis, and absence of thrombocytopenia, leukopenia, and nausea were early predictors. Among all groups presenting 3-5 DPO, pruritic skin became a predictor for chikungunya, joint, muscle, bone or back pain were no longer predictive, while arthritis became predictive in all age-groups. Absence of thrombocytopenia was a significant predictor regardless of DPO or comparison group. This study identified robust clinical indicators such as joint pain, skin rash and absence of thrombocytopenia that can allow early identification of and accurate differentiation between patients with chikungunya and other common causes of AFI. |
Seroprevalence, risk factors, and rodent reservoirs of leptospirosis in an urban community of Puerto Rico, 2015
Briskin EA , Casanovas-Massana A , Ryff KR , Morales-Estrada S , Hamond C , Perez-Rodriguez NM , Benavidez KM , Weinberger DM , Castro-Arellano I , Wunder EA , Sharp TM , Rivera-Garcia B , Ko AI . J Infect Dis 2019 220 (9) 1489-1497 BACKGROUND: The burden of leptospirosis in Puerto Rico remains unclear due to underreporting. METHODS: A cross-sectional survey and rodent trapping was performed in a community within San Juan, Puerto Rico to determine the seroprevalence and risk factors for Leptospira infection. The microscopic agglutination test was used to detect anti-Leptospira antibodies as a marker of previous infection. We evaluated Leptospira carriage by qPCR among rodents trapped at the community site. RESULTS: Of 202 study participants, 55 (27.2%) had Leptospira agglutinating antibodies. Among the 55 seropositive individuals, antibodies were directed most frequently against serogroups Icterohaemorrhagiae (22.0%) and Autumnalis (10.6%). Of 18 captured rodents, 11 (61.1%) carried pathogenic Leptospira (L. borgpetersenii, 7 and L. interrogans, 2). Four participants showed their highest titer against an isolate obtained from a rodent (serogroup Ballum). Increasing household distance to the canal that runs through the community was associated with decreased risk of infection (OR = 0.934 per 10m increase, 95% CI: 0.952-0.992). CONCLUSION: There are high levels of Leptospira exposure in an urban setting in Puerto Rico, for which rodents may be an important reservoir for transmission. Our findings indicate that prevention should focus on mitigating risk posed by infrastructure deficiencies such as the canal. |
Autocidal gravid ovitraps protect humans from chikungunya virus infection by reducing Aedes aegypti mosquito populations
Sharp TM , Lorenzi O , Torres-Velasquez B , Acevedo V , Perez-Padilla J , Rivera A , Munoz-Jordan J , Margolis HS , Waterman SH , Biggerstaff BJ , Paz-Bailey G , Barrera R . PLoS Negl Trop Dis 2019 13 (7) e0007538 BACKGROUND: Public health responses to outbreaks of dengue, chikungunya, and Zika virus have been stymied by the inability to control the primary vector, Aedes aegypti mosquitos. Consequently, the need for novel approaches to Aedes vector control is urgent. Placement of three autocidal gravid ovitraps (AGO traps) in ~85% of homes in a community was previously shown to sustainably reduce the density of female Ae. aegypti by >80%. Following the introduction of chikungunya virus (CHIKV) to Puerto Rico, we conducted a seroprevalence survey to estimate the prevalence of CHIKV infection in communities with and without AGO traps and evaluate their effect on reducing CHIKV transmission. METHODS AND FINDINGS: Multivariate models that calculated adjusted prevalence ratios (aPR) showed that among 175 and 152 residents of communities with and without AGO traps, respectively, an estimated 26.1% and 43.8% had been infected with CHIKV (aPR = 0.50, 95% CI: 0.37-0.91). After stratification by time spent in their community, protection from CHIKV infection was strongest among residents who reported spending many or all weekly daytime hours in their community:10.3% seropositive in communities with AGO traps vs. 48.7% in communities without (PR = 0.21, 95% CI: 0.11-0.41). The age-adjusted rate of fever with arthralgia attributable to CHIKV infection was 58% (95% CI: 46-66%). The monthly number of CHIKV-infected mosquitos and symptomatic residents were diminished in communities with AGO traps compared to those without. CONCLUSIONS: These findings indicate that AGO traps are an effective tool that protects humans from infection with a virus transmitted by Ae. aegypti mosquitos. Future studies should evaluate their protective effectiveness in large, urban communities. |
Dengue and Zika virus diagnostic testing for patients with a clinically compatible illness and risk for infection with both viruses
Sharp TM , Fischer M , Munoz-Jordan JL , Paz-Bailey G , Staples JE , Gregory CJ , Waterman SH . MMWR Recomm Rep 2019 68 (1) 1-10 Dengue and Zika viruses are closely related mosquitoborne flaviviruses with similar transmission cycles, distribution throughout the tropics and subtropics, and disease manifestations including fever, rash, myalgia, and arthralgia. For patients with suspected dengue or Zika virus disease, nucleic acid amplification tests (NAATs) are the preferred method of diagnosis. Immunoglobulin M (IgM) antibody testing can identify additional infections and remains an important tool for the diagnosis of these diseases, but interpreting the results is complicated by cross-reactivity, and determining the specific timing of infection can be difficult. These limitations are a particular challenge for pregnant women in determining whether Zika virus infection occurred during or before the pregnancy.This report summarizes existing and new guidance on dengue and Zika virus diagnostic testing for patients with a clinically compatible illness who live in or recently traveled to an area where there is risk for infection with both viruses. CDC recommendations for screening of asymptomatic pregnant women with possible Zika virus exposure are unchanged. For symptomatic nonpregnant persons, dengue and Zika virus NAATs should be performed on serum collected </=7 days after symptom onset. Dengue and Zika virus IgM antibody testing should be performed on NAAT-negative serum specimens or serum collected >7 days after onset of symptoms. For symptomatic pregnant women, serum and urine specimens should be collected as soon as possible within 12 weeks of symptom onset for concurrent dengue and Zika virus NAATs and IgM antibody testing. Positive IgM antibody test results with negative NAAT results should be confirmed by neutralizing antibody tests when clinically or epidemiologically indicated, including for all pregnant women. Data on the epidemiology of viruses known to be circulating at the location of exposure and clinical findings should be considered when deciding which tests to perform and for interpreting results.Patients with clinically suspected dengue should receive appropriate management to monitor and treat shock and hemorrhage. Women with laboratory evidence of possible Zika virus infection during pregnancy and their infants should be evaluated and managed for possible adverse outcomes. Dengue and Zika virus disease are nationally notifiable conditions, and cases should be reported to public health authorities. |
Risk factors for hospitalization of patients with chikungunya virus infection at sentinel hospitals in Puerto Rico
Hsu CH , Cruz-Lopez F , Vargas Torres D , Perez-Padilla J , Lorenzi OD , Rivera A , Staples JE , Lugo E , Munoz-Jordan J , Fischer M , Garcia Gubern C , Rivera Garcia B , Alvarado L , Sharp TM . PLoS Negl Trop Dis 2019 13 (1) e0007084 BACKGROUND: Hospitalization of patients during outbreaks of chikungunya virus has been reported to be uncommon (0.5-8.7%), but more frequent among infants and the elderly. CHIKV was first detected in Puerto Rico in May 2014. We enrolled patients with acute febrile illness (AFI) presenting to two hospital emergency departments in Puerto Rico and tested them for CHIKV infection to describe the frequency of detection of CHIKV-infected patients, identify risk factors for hospitalization, and describe patients with severe manifestations. METHODOLOGY/PRINCIPAL FINDINGS: Serum specimens were collected from patients with AFI and tested by rRT-PCR. During May-December 2014, a total of 3,035 patients were enrolled, and 1,469 (48.4%) had CHIKV infection. A total of 157 (10.7%) CHIKV-infected patients were hospitalized, six (0.4%) were admitted to the intensive care unit, and two died (0.1%). Common symptoms among all CHIKV-infected patients were arthralgia (82.6%), lethargy (80.6%), and myalgia (80.5%). Compared to patients aged 1-69 years (7.3%), infant (67.2%) and elderly (17.3%) patients were nine and two times more likely to be hospitalized, respectively (relative risk [RR] and 95% confidence interval [CI] = 9.16 [7.05-11.90] and 2.36 [1.54-3.62]). Multiple symptoms of AFI were associated with decreased risk of hospitalization, including arthralgia (RR = 0.31 [0.23-0.41]) and myalgia (RR = 0.29 [0.22-0.39]). Respiratory symptoms were associated with increased risk of hospitalization, including rhinorrhea (RR = 1.68 [1.24-2.27) and cough (RR = 1.77 [1.31-2.39]). Manifestations present among <5% of patients but associated with patient hospitalization included cyanosis (RR = 2.20 [1.17-4.12) and seizures (RR = 3.23 [1.80-5.81). DISCUSSION: Among this cohort of CHIKV-infected patients, hospitalization was uncommon, admission to the ICU was infrequent, and death was rare. Risk of hospitalization was higher in patients with symptoms of respiratory illness and other manifestations that may not have been the result of CHIKV infection. |
Incidence and outcome of severe and nonsevere thrombocytopenia associated with Zika virus infection - Puerto Rico, 2016
Van Dyne EA , Neaterour P , Rivera A , Bello-Pagan M , Adams L , Munoz-Jordan J , Baez P , Garcia M , Waterman SH , Reyes N , Richardson LC , Rivera-Garcia B , Sharp TM . Open Forum Infect Dis 2019 6 (1) ofy325 Background: Zika virus (ZIKV) infection has been associated with severe thrombocytopenia. We describe the incidence, clinical manifestations, and outcomes of patients with ZIKV infection and thrombocytopenia. Methods: We reviewed medical records of patients with ZIKV infection and thrombocytopenia (platelet count <100 x10(9) cells/L) in Puerto Rico during 2016. Severe thrombocytopenia was defined by platelet count <20 x10(9)/L or a platelet count <50 x10(9)/L and treatment for immune thrombocytopenia (ITP). Results: Of 37 878 patients with ZIKV infection, 47 (0.1%) had thrombocytopenia in the absence of an alternative etiology (1.4 cases/100 000 population), including 12 with severe thrombocytopenia. Most patients with thrombocytopenia were adult (77%) and male (53%). Platelet nadir occurred a median (range) of 6 (1-16) and 5 (0-34) days after symptom onset for patients with severe and nonsevere thrombocytopenia, respectively. Among patients with severe thrombocytopenia, all had bleeding, 33% were admitted to the intensive care unit, and 8% died; 50% were treated for ITP. Among 5 patients with severe thrombocytopenia who received intravenous immunoglobulin, the median platelet count increase (range) was 112 (65-202) x10(9)/L. In contrast, among 4 patients who received platelet transfusion, the median increase in platelet count (range) was 8.5 (-6 to 52) x10(9)/L. Conclusions: Patients with severe thrombocytopenia and ZIKV infection experienced prominent acute morbidity. Consistent with recommended management, administration of ITP treatments to such patients may be more efficacious than platelet transfusion in resolving thrombocytopenia. Severe thrombocytopenia should be considered a rare outcome of ZIKV infection. |
Implementation and Evaluation of Guillain-Barre Syndrome Surveillance in Puerto Rico during the 2016 Zika Virus Epidemic
Major CG , Dirlikov E , Medina NA , Lugo-Robles R , Matos D , Munoz-Jordan J , Colon-Sanchez C , Garcia-Negron M , Olivero-Segarra M , Malave-Gonzalez G , Thomas DL , Luciano CA , Waterman SH , Sejvar J , Sharp TM , Rivera-Garcia B . P R Health Sci J 2018 37 S85-s92 OBJECTIVE: Guillain-Barre syndrome (GBS) is an uncommon autoimmune disorder that follows infection or vaccination, and increased incidence has been reported during Zika virus (ZIKV) transmission. During the 2016 ZIKV epidemic, the Puerto Rico Department of Health (PRDH) implemented the Enhanced GBS Surveillance System (EGBSSS). Here, we describe EGBSSS implementation and evaluate completeness, validity, and timeliness. METHODS: GBS cases were identified using passive surveillance and discharge diagnostic code for GBS. Completeness was evaluated by capture-recapture methods. Sensitivity and positive predictive value (PPV) for confirmed GBS cases were calculated for both case identification methods. Median time to completion of key time steps were compared by quarter (Q1-4) and hospital size. RESULTS: A total of 122 confirmed GBS cases with onset of neurologic illness in 2016 were identified. Capture-recapture methodology estimated that four confirmed GBS cases were missed by both identification methods. Identification of cases by diagnostic code had a higher sensitivity than passive surveillance (89% vs. 80%), but a lower PPV (60% vs. 72%). There was a significant decrease from Q1 to Q3 in median time from hospital admission to case reporting (11 days vs. 2 days, p = 0.032) and from Q2 to Q3 in median time from specimen receipt to arbovirus laboratory test reporting (35 days vs. 26 days, p = 0.004). CONCLUSION: EGBSSS provided complete, valid, and increasingly timely surveillance data, which guided public health action and supported healthcare providers during the ZIKV epidemic. This evaluation provides programmatic lessons for GBS surveillance and emergency response surveillance. |
Building laboratory-based arbovirus sentinel surveillance capacity during an ongoing dengue outbreak, Burkina Faso, 2017
Sanou AS , Dirlikov E , Sondo KA , Kagone TS , Yameogo I , Sow HE , Adjami AG , Traore SM , Dicko A , Tinto B , Diendere EA , Ouedraogo-Konate Smwk , Kiemtore T , Kangoye DT , Sangare L , Dama ETH , Fuller JA , Major CG , Tosado-Acevedo R , Sharp TM , Kone RG , Bicaba BW . Health Secur 2018 16 S103-s110 In West Africa, identification of nonmalarial acute febrile illness (AFI) etiologic pathogens is challenging, given limited epidemiologic surveillance and laboratory testing, including for AFI caused by arboviruses. Consequently, public health action to prevent, detect, and respond to outbreaks is constrained, as experienced during dengue outbreaks in several African countries. We describe the successful implementation of laboratory-based arbovirus sentinel surveillance during a dengue outbreak in Burkina Faso during fall 2017. We describe implementation, surveillance methods, and associated costs of enhanced surveillance during an outbreak response as an effort to build capacity to better understand the burden of disease caused by arboviruses in Burkina Faso. The system improved on existing routine surveillance through an improved case report form, systematic testing of specimens, and linking patient information with laboratory results through a data management system. Lessons learned will improve arbovirus surveillance in Burkina Faso and will contribute to enhancing global health security in the region. Elements critical to the success of this intervention include responding to a specific and urgent request by the government of Burkina Faso and building on existing systems and infrastructure already supported by CDC's global health security program. |
Outbreak of dengue virus type 2 - American Samoa, November 2016-October 2018
Cotter CJ , Tufa AJ , Johnson S , Matai'a M , Sciulli R , Ryff KR , Hancock WT , Whelen C , Sharp TM , Anesi MS . MMWR Morb Mortal Wkly Rep 2018 67 (47) 1319-1322 The U.S. territory of American Samoa has experienced recent outbreaks of illnesses caused by viruses transmitted by Aedes species mosquitoes, including dengue, chikungunya, and Zika virus. In November 2016, a traveler from the Solomon Islands tested positive for infection with dengue virus type 2 (DENV-2). Additional dengue cases were identified in the subsequent weeks through passive and active surveillance. Suspected dengue cases were tested locally with a dengue rapid diagnostic test (RDT) for DENV nonstructural protein 1 (NS1). Specimens from RDT-positive cases and patients meeting the dengue case definition were tested by real-time reverse transcription-polymerase chain reaction (real-time RT-PCR) at Hawaii State Laboratories. During November 2016-October 2018, a total of 3,240 patients were tested for evidence of DENV infection (118 by RDT-NS1 alone, 1,089 by real-time RT-PCR alone, and 2,033 by both methods), 1,081 (33.4%) of whom tested positive for dengue (19.5 per 1,000 population). All 941 real-time RT-PCR-positive specimens were positive for DENV-2. The monthly number of laboratory-confirmed cases peaked at 120 during December 2017. Among laboratory-confirmed dengue cases, 380 (35.2%) patients were hospitalized; one patient, who was transferred to American Samoa for care late in his illness, died. The public health response to this outbreak included disposal of solid waste to remove mosquito breeding sites, indoor residual spraying of pesticides in schools, reinforcement of dengue patient management education, and public education on mosquito avoidance and seeking medical care for symptoms of dengue. |
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