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Infections With Oseltamivir-Resistant Influenza A(H1N1) Virus in the United States

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The map illustrates the number of oseltamivir-resistant influenza A H1N1 viruses that were identified as of September 5, An interactive eFigure is available here. Scatterplot of proportion of total filled anti-infective prescriptions that were prescriptions for oseltamivir during by state prevalence of oseltamivir-resistant influenza A H1N1 and the line of best fit determined using least squares regression. Total anti-infective prescriptions include antibiotics, antifungals, antiparasitic, and antiviral medications except for antiretroviral drugs. Context During the influenza season, oseltamivir resistance among influenza A H1N1 viruses increased significantly for the first time worldwide. Early surveillance data suggest that the prevalence of oseltamivir resistance among A H1N1 viruses will most likely be higher during the season. Objectives To describe patients infected with oseltamivir-resistant influenza A H1N1 virus and to determine whether there were any differences between these patients and patients infected with oseltamivir-susceptible A H1N1 virus in demographic or epidemiological characteristics, clinical symptoms, severity of illness, or clinical outcomes. Design, Setting, and Patients Influenza A H1N1 viruses that were identified and submitted to the Centers for Disease Control and Prevention by US public health laboratories between September 30, , and May 17, , and between September 28, , and February 19, , were tested as part of ongoing surveillance. Oseltamivir resistance was determined by neuraminidase inhibition assay and pyrosequencing analysis. Information was collected using a standardized case form from patients with oseltamivir-resistant A H1N1 infections and a comparison group of patients with oseltamivir-susceptible A H1N1 infections during Main Outcome Measures Demographic and epidemiological information as well as clinical information, including symptoms, severity of illness, and clinical outcomes. Among influenza A H1N1 viruses tested from 45 states, Data were available for 99 oseltamivir-resistant cases and oseltamivir-susceptible cases from this period. None reported oseltamivir exposure before influenza diagnostic sample collection. No significant differences were found between cases of oseltamivir-resistant and oseltamivir-susceptible influenza in demographic characteristics, underlying medical illness, or clinical symptoms. Preliminary data from the influenza season identified resistance to oseltamivir among of influenza A H1N1 viruses Conclusions Oseltamivir-resistant A H1N1 viruses circulated widely in the United States during the influenza season, appeared to be unrelated to oseltamivir use, and appeared to cause illness similar to oseltamivir-susceptible A H1N1 viruses. Circulation of oseltamivir-resistant A H1N1 viruses will continue, with a higher prevalence of resistance, during the season. However, during the influenza season, increased levels of resistance to oseltamivir, 1 of the 2 licensed NAIs, were detected for the first time in the United States and worldwide. In this study, we described patients infected with oseltamivir-resistant influenza A H1N1 identified from influenza surveillance in the United States during the influenza season and described risk factors for infection with oseltamivir-resistant viruses. In addition, we compared characteristics of patients with oseltamivir-resistant and oseltamivir-susceptible influenza A H1N1 infection to determine whether there were any differences in demographic or epidemiological characteristics, clinical symptoms, severity of illness, or clinical outcomes. Each year, US public health laboratories submit a sample of influenza isolates to the CDC for virus stain and antiviral resistance surveillance. During the influenza season September 30, May 17, , the US public health laboratories were asked to submit all A H1N1 virus isolates, clinical specimens, or both, in addition to a sample of other virus types and subtypes. Early during the season September 28, February 19, , the number of isolates sent to the CDC was standardized, the first 10 or 20 depending on state population isolates were sent to the CDC. After the early season aliquot was sent, each laboratory was asked to send a random sample of isolates selected each week the number selected depended on state population. Testing for NAI resistance was performed by the neuraminidase inhibition assay with chemiluminescent substrate as previously described. The presence of the oseltamivir-resistance conferring mutation HY in the neuraminidase of virus isolates with elevated IC 50 values was determined by sequencing, pyrosequencing, or both, as previously described. Because a majority of A H1N1 viruses but only a sample of reported A H3N2 and B viruses were submitted to the CDC for antiviral resistance testing during the influenza season, we estimated an adjusted overall proportion of influenza viruses resistant to oseltamivir in the United States. We assumed that the proportion of A H1N1 and A H3N2 viruses among subtyped influenza A viruses was equal to the proportion among those influenza A viruses that were not subtyped. As infections with oseltamivir-resistant A H1N1 viruses were identified during the season, each case-patient was contacted by telephone and information on demographic characteristics, medical history, whether the patient received the influenza vaccine, influenza illness, and illness in household members was collected by using a standardized questionnaire. Race and ethnicity were collected for demographic characterization and were determined by the patients from options read to them by the interviewer. In addition, the health care professional for each patient was contacted by telephone and information was obtained regarding medications prescribed to the patient, temperature documented at the visit, and whether the patient had received the influenza vaccine. Data on vaccination status were obtained from the patient interview. Data on prescribed antiviral medications and length of illness before seeking care were obtained from the patient's health care clinician interview when available. In states in which oseltamivir-resistant A H1N1 cases had been identified, the state health department identified a comparison group of persons who had oseltamivir-susceptible A H1N1 infections by randomly selecting from the list of oseltamivir-susceptible A H1N1 viruses from each state's laboratory log. There were no matching criteria. Each state chose 1 to 4 comparison cases for each person infected with an oseltamivir-resistant A H1N1 virus depending on the number of identified A H1N1 viruses isolated within the state and state resources. The patients with oseltamivir-susceptible A H1N1 infections were called and interviewed using the same standardized questionnaire as patients with oseltamivir-resistant A H1N1 infections. Health care clinicians of patients with oseltamivir-susceptible A H1N1 infections were not contacted. Because univariate analysis did not identify variables that significantly differed between the 2 groups, multivariable analysis was not performed. However, we did control for age and state. Underlying illness and symptoms vary between age groups and state surveillance and laboratory practices vary. In the comparison of age groups, we only controlled for state. Statistical analysis was conducted by using SAS version 9. We excluded 7 oseltamivir-resistant A H1N1 cases from 1 state that was unable to interview a comparison group of oseltamivir-susceptible A H1N1 cases. We compared the proportion of A H1N1 viruses tested for antiviral resistance that were resistant to oseltamivir during the season and the proportion of total filled anti-infective prescriptions including antibiotics, antifungals, antiparasitic, and antiviral drugs except for antiretroviral medications that were prescriptions for oseltamivir during The annual number of total filled anti-infective prescriptions and filled oseltamivir prescriptions from was supplied by BioSense. A correlation coefficient between the proportion of state A H1N1 viruses from the influenza season resistant to oseltamivir and the proportion of filled total anti-infective prescriptions that were for oseltamivir was calculated by using SAS version 9. The investigation of oseltamivir-resistant influenza A H1N1 cases during the influenza season was deemed public health practice surveillance, not human subjects research and therefore did not require institutional review board review. Before we asked any state to contact A H1N1 cases identified through routine surveillance, we submitted a summary of the current situation, reasons additional information needed to be collected, and the data forms and telephone scripts for determination of applicability of human subjects regulations. After the final determination that this was public health practice surveillance , we asked the state influenza coordinators to collect additional information from the surveillance A H1N1 cases by telephone interview. All A H1N1 cases were contacted by telephone and gave oral consent before answering questions. The proportion of influenza A H1N1 among all influenza viruses identified in the United States, including type A and B, was greatest early in the season, between September 30, , and February 2, Preliminary data from the early influenza season demonstrate that oseltamivir resistance among A H1N1 viruses continues to be detected. As of February 19, , resistance to oseltamivir had been identified among of US influenza A H1N1 viruses None of the oseltamivir-resistant A H1N1 cases reported taking oseltamivir before testing for influenza, and none of the cases had household contacts that took oseltamivir before the case's onset of illness. Of the 11 cases who reported travel in the 5 days before their onset of illness, 3 reported international travel 2 to Europe and 1 to the Bahamas and Central America. Five cases were hospitalized; 3 of these recovered and 2 died. Four patients with oseltamivir-resistant influenza A H1N1 infection died. Two patients died on the way to the hospital or in the emergency department, 1 patient was 4 years old and previously healthy, and 1 patient was 4 years old with neurological problems. Both were thought to die from complications of their influenza infection. Two deaths were among hospitalized patients, 1 patient was a 1-year-old with multiple medical problems admitted in respiratory failure and subsequently was deemed do not resuscitate and 1 patient, hospitalized for a stem cell transplant, was 22 years old and diagnosed with influenza infection on the fifth day of hospitalization. Influenza vaccination status was available for 2 of the patients, both with underlying medical conditions; 1 had been vaccinated and 1 had not. In our comparison of patients with oseltamivir-resistant and oseltamivir-susceptible influenza A H1N1 infections, we excluded 7 cases from 1 state. As a result, we compared 92 cases of oseltamivir-resistant A H1N1 infection with cases of oseltamivir-susceptible A H1N1 infection Table 1. Also, there were no differences in whether cases received the influenza vaccine, whether they had traveled in the 5 days before they sought care for their influenza illness, or whether they presented first for care to an emergency department or hospital vs a clinic. We found no significant difference in our comparison of the clinical symptoms and outcomes of untreated patients with oseltamivir-resistant and oseltamivir-susceptible influenza A H1N1 infections, excluding patients who were treated with antiviral agents Table 2. Patients with oseltamivir-susceptible A H1N1 infections were statistically more likely to report myalgias or arthralgias and to be hospitalized. However, 1 of the untreated patients with oseltamivir-resistant influenza A H1N1 infection died on the way to the hospital and a second patient died in the emergency department before admission. If these 2 cases had been included as hospital admissions in the analysis, the difference would be no longer significant. We report the first, to our knowledge, detailed description of persons infected with oseltamivir-resistant influenza A H1N1 viruses identified during the influenza season in the United States. We did not find an association between use of oseltamivir and cases of illness due to infection with oseltamivir-resistant A H1N1 viruses in the United States. Similar findings were reported to the WHO and by investigators in Norway. The prevalence of underlying medical conditions, the age distribution, and the clinical symptoms of patients with oseltamivir-resistant and oseltamivir-susceptible A H1N1 infections were similar. Although oseltamivir-resistant cases reported fewer hospitalizations compared with oseltamivir-susceptible cases, 2 oseltamivir-resistant cases died on the way to the hospital and were not included as hospital admissions. Thus, it is likely that there were no significant clinical differences between patients with oseltamivir-resistant and oseltamivir-susceptible A H1N1 infections. A study 28 from in Norway found similar results. We identified 4 deaths among cases with oseltamivir-resistant influenza A H1N1 infections. Three of these deaths were among patients with severe underlying medical conditions that put them at high risk for complications associated with influenza virus infection, similar conditions as the 1 previously reported death in a patient with oseltamivir-resistant A H1N1 infection. Mutations that confer resistance to NAI occur in or nearby the active site of the neuraminidase, an enzyme that plays an important role in the ability of the virus to infect host cells, and it was expected previously that NAI-resistant viruses would be less viable than sensitive ones. Further studies are needed to better understand the mechanisms of emergence of NAI-resistant mutants in influenza viruses. Our study had the following limitations. The number of A H1N1 cases identified from surveillance was small and the confidence intervals in our comparison analysis were large. Viral strain surveillance was passive; states received varying numbers of influenza specimens and submitted varying proportions of influenza viruses for oseltamivir-resistance testing at the CDC. Therefore, these results may not be representative of all A H1N1 infections during the season in the United States. The emergence of oseltamivir resistance has highlighted the need for the development of new antiviral drugs and rapid diagnostic tests that determine viral subtype or resistance, as well as improved representativeness and timeliness of national influenza surveillance for antiviral resistance. Timely monitoring and weekly reporting of resistance during the influenza season will be conducted to help inform policy for antiviral use in the United States and inform clinical antiviral treatment decision making. These guidelines provide options, including preferential use of zanamivir or a combination of oseltamivir and rimantadine, which might be more appropriate in treating patients who might have influenza caused by an oseltamivir-resistant virus. Additional options for the treatment and prophylaxis of influenza virus infection are critically needed. Corresponding Author: Nila J. Published Online: March 2, doi Author Contributions: Dr Dharan had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. George, Epperson, Fry. Analysis and interpretation of data : Dharan, Gubareva, St. George, Epperson, Brammer, Klimov, Fry. George, Epperson, Bresee. Role of the Sponsor: Members of the Epidemiology and Prevention Branch of the Influenza Division of the Centers for Disease Control and Prevention are responsible for the design and conduct of the study, for the collection, management, analysis, and interpretation of the data, and for the preparation, review, and approval of the manuscript. Sheu, Teresa R. Shult, PhD, Tam T. The members of the Oseltamivir-Resistance Working Group helped with the acquisition of data but did not receive any extra compensation for their contribution. Disclaimer: The findings and conclusions in this article are those of the authors and do not necessarily represent the views of the Centers for Disease Control and Prevention. Additional Information: Online eFigure is available here. Figure 1. View Large Download. Figure 2. Table 1. Table 2. High levels of adamantane resistance among influenza A H3N2 viruses and interim guidelines for use of antiviral agents—United States, influenza season. Adamantane resistance among influenza A viruses isolated early during the influenza season in the United States. Detection of influenza viruses resistant to neuraminidase inhibitors in global surveillance during the first 3 years of their use. Antimicrob Agents Chemother. Surveillance for neuraminidase inhibitor resistance among human influenza A and B viruses circulating worldwide from to Surveillance of influenza isolates for susceptibility to neuraminidase inhibitors during the influenza seasons. Virus Res. World Health Organization. Influenza A H1N1 virus resistance to oseltamivir; last quarter to first quarter Accessed January 2, Influenza activity—United States and worldwide, season. Update: influenza activity—United States, September November 29, Oseltamivir Tamiflu and its potential for use in the event of an influenza pandemic. J Antimicrob Chemother. Prolonged shedding of multidrug-resistant influenza A virus in an immunocompromised patient. N Engl J Med. Selection of influenza virus mutants in experimentally infected volunteers treated with oseltamivir. J Infect Dis. Oral oseltamivir treatment of influenza in children. Pediatr Infect Dis J. Resistant influenza A viruses in children treated with oseltamivir: descriptive study. Moscona A. Neuraminidase inhibitors for influenza. Influenza virus susceptibility and resistance to oseltamivir. Antivir Ther. Antiviral Res. Roberts NA. Treatment of influenza with neuraminidase inhibitors: virological implications. Influenza viruses resistant to the antiviral drug oseltamivir: transmission studies in ferrets. Pyrosequencing as a tool to detect molecular markers of resistance to neuraminidase inhibitors in seasonal influenza A viruses. Incidence of adamantane resistance among influenza A H3N2 viruses isolated worldwide from to a cause for concern. Surveillance of antiviral resistant influenza from by a network of U. Loonsk JW. BioSense: a national initiative for early detection and quantification of public health emergencies. Update: influenza activity—United States, September December 1, Update: influenza activity—United States, September 30, February 9, A weekly influenza surveillance report prepared by the Influenza Division. Accessed February 3, Centers for Disease Control and Prevention. Oseltamivir-resistant influenza viruses A H1N1 , Norway, Emerg Infect Dis. Influenza A H1N1 virus resistance to oseltamivir; 14 October Influenza A H1N1 virus resistance to oseltamivir; 20 August, The potential impact of neuraminidase inhibitor resistant influenza. Curr Opin Infect Dis. Fatal oseltamivir-resistant influenza virus infection. Kroes, MD, PhD. Save Preferences. Privacy Policy Terms of Use. This Issue. Citations View Metrics. X Facebook More LinkedIn. Original Contribution. Nila J. Dharan, MD ; Larisa V. Gubareva, PhD ; John J. Marshall, MS ; Kirsten St. Klimov, PhD ; Joseph S. Bresee, MD ; Alicia M. Brief Report. Back to top Article Information. Financial Disclosures: None reported. Access your subscriptions. Access through your institution. Add or change institution. Free access to newly published articles. Purchase access. Rent article Rent this article from DeepDyve. Sign in to access free PDF. Save your search. Customize your interests. Create a personal account or sign in to:. Privacy Policy. Make a comment.

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