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Nosocomial Outbreak of the Pandemic Influenza a (H1N1)

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Nosocomial Outbreak of the Pandemic Influenza a (H1N1) Pollara et al. BMC Infectious Diseases 2013, 13:127 http://www.biomedcentral.com/1471-2334/13/127 RESEARCH ARTICLE Open Access Nosocomial outbreak of the pandemic Influenza A (H1N1) 2009 in critical hematologic patients during seasonal influenza 2010-2011: detection of oseltamivir resistant variant viruses Caterina P Pollara1,3*, Giorgio Piccinelli1, Giuseppe Rossi2, Chiara Cattaneo2, Francesca Perandin1, Silvia Corbellini1, Dolores De Tomasi1 and Carlo Bonfanti1 Abstract Background: The pandemic influenza A (H1N1) 2009 (H1N1pdm09) virus infection caused illness and death among people worldwide, particularly in hematologic/oncologic patients because influenza infected individuals can shed virus for prolonged periods, thus increasing the chances for the development of drug-resistant strains such as oseltamivir-resistant (OST-r) variant. Methods: The aim of our study was to retrospectively evaluate the clinical importance of OST-r variant in circulating strains of the pandemic H1N1pdm09 virus. By means of RT-PCR and Sanger sequencing we analysed the presence of OST-r variant in 76 H1N1pdm09 laboratory-confirmed cases, hospitalized at the hematologic/oncologic ward at Spedali Civili of Brescia –Italy. Results: Out of 76 hospitalized hematologic/oncologic patients, 23 patients (30.2%) were infected by H1N1pdm09 virus. Further investigation revealed that 3 patients were positive for the OST-r variant carrying the H275Y mutation. All the 23 infected patients were immuno-compromised, and were under treatment or had been treated previously with oseltamivir. Three patients died (13%) after admission to intensive care unit and only one of them developed H275Y mutation. Conclusions: Our retrospective observational study shows that pandemic influenza A (H1N1) 2009 virus can cause significant morbidity and even mortality in hematologic/oncologic patients and confirms the high rate of nosocomial transmission of pandemic H1N1pdm09 virus in these critical subjects. Indeed, the reduction in host defences in these hospitalized patients favoured the prolonged use of antiviral therapy and permitted the development of OST-r strain. Strategies as diagnostic vigilance, early isolation of patients and seasonal influenza A (H1N1) vaccination may prevent transmission of influenza in high risk individuals. Keywords: Pandemic, H1N1, Oseltamivir, Resistance * Correspondence: [email protected] 1Laboratory of Microbiology and Virology, A. O. Spedali Civili, Brescia, University of Brescia, Brescia, Italy 3Institute of Microbiology, A. O. Spedali Civili, Brescia, University of Brescia, P. le Spedali Civili, 1 25123 Brescia, Italy Full list of author information is available at the end of the article © 2013 Pollara et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Pollara et al. BMC Infectious Diseases 2013, 13:127 Page 2 of 7 http://www.biomedcentral.com/1471-2334/13/127 Background cases and reviewed the medical records. All patients The pandemic influenza A (H1N1) 2009 virus (H1N1- submitted to RT-PCR test for H1N1pdm09 presented pdm09) broke out in Mexico and USA during the late influenza-like illness (ILI) symptoms, and the positive cases spring and early summer of 2009. Due to its rapid wide- were administered oseltamivir therapy: 75 mg twice/ day, spread transmission, H1N1pdm09 virus was declared as for five days. novel influenza pandemic virus in June 2009 by the Clinical samples (nasopharyngeal swabs, bronchoalve- World Health Organization (WHO) [1-6]. Indeed the olar washings or respiratory secretions) were collected genomic analysis of this new 2009 influenza virus indi- from all patients using a pernasal flocked swab and cated a genetic viral reassortment and it contained genes stored in a UTM-RT tube (Kit Cat. No. 360c, Copan of influenza A virus strains that are endemic in swine, Italia, Brescia, Italy). Each sample was immediatly tested avian and human species [7,8]. by real-time PCR in order to identify A and B influenza The 2009 pandemic virus was found susceptible to viruses as previously described. Diagnosis of influenza neuraminidase inhibitors (NAI) antiviral drugs such as was invariably provided within 8–24 hours after the re- oseltamivir (Tamiflu TM) and zanamivir (Relenza TM) ceipt of the sample. that have been used extensively for chemoprophylaxis and treatment in 2009 pandemic virus. The emergence Ethical considerations of oseltamivir-resistant (OST-r) pandemic H1N1pdm09 The investigation of this outbreak did not involve any variant, characterized by the single amino acid change planned activity that could have been reviewed prospec- H275Y in the neuraminidase (NA) glycoprotein [9-13], tively by an institutional review board or ethics commit- was detected in many countries [14], especially in Italy tee. The Ethics commette was consulted retrospectively [15-18]. The OST-r variant has been detected in immuno- and agreed to the approach as described for reporting compromised patients that are at risk for serious com- clinical information obtained during the investigation. plications from seasonal influenza [2,19-22]. The nosoco- All patients received study information and signed in- mial transmission of H1N1pdm09 resistant variants may formed consent. cause an increase of morbility and mortality in this group of subjects. RNA extraction, real-time RT-PCR , multiplex and one step The aim of this study was to investigate nosocomial RT-PCR viral transmission of H1N1pdm09 in a cluster of critical DNA/RNA was extracted by an automatic nucleic acid hematologic patients and the clinical importance and platform (Nuclisens EasyMag - Biomerieux). Aliquots of impact of OST-r variant viruses. 400 μl of each respiratory sample were added to 1600 μl of lysis buffer and the mix was loaded in the instrument. Methods After a lysis step (10 minutes at room temperature), 65 μl Study population of magnetic silica, 10 μl of internal control (CPE, Nanogen In January 2011, an outbreak of H1N1pdm09 occurred in Advanced Diagnostics S.R.L), purified beta globin sequence a Hematology ward at Spedali Civili of Brescia (Italy). Re- and 55 μl of wash reagent were added to each specimen. spiratory specimens from symptomatic contact patients of Total nucleic acid was automatically extracted, eluted in the presumed index patient were analyzed by reverse 110 μl of specific buffer and immediately processed by real transcriptase-polymerase chain reaction (RT-PCR) for in- time PCR. Aliquots were stored at -80°C. fluenza A/B virus. Screening was performed on 134 speci- Extracted viral RNA was tested by Flu A/Flu B Q-PCR mens obtained from 76 hospitalized patients (age range: Alert Kit (Nanogen Advanced Diagnostics, Italy), using 23-76 years). H1N1pdm09 positive samples were further ABI Prism 7300 Fast Real Time PCR System (Applied tested for OST-r variant. Biosystems, Italy). This test is based on simultaneous In our laboratory, the current diagnostic algorithm for amplification of the matrix region of Influenza A and B testing of Influenza includes primary screening using a and of the internal control human beta globin gene. Beta multiplex commercial real-time RT-PCR assay (Flu A/ globin DNA was added to each sample to monitor the Flu B Q-PCR Alert Kit, Nanogen Advanced Diagnostics, efficiency of extraction and amplification procedures. Italy) targeting the matrix gene of all human influenza A Specific TaqMan probes labelled with different reporter and B viruses. Positive samples were subsequently tested molecules were used to detect amplification of the for H1N1pdm09 sub-type by a commercial assay (Fast targets. set H1N1v-Arrowdiagnostics, Italy). H1N1pdm09 posi- The positive samples for influenza A virus were tested tive samples were further tested for oseltamivir resis- for H1N1pdm09. Viral RNA was tested by Fast set tance using an in house RT-PCR [23,24] and the results H1N1v (Arrowdiagnostics, Italy) using ABI Prism 7300 confirmed using Sanger sequencing method. We retro- Fast Real Time PCR System (Applied Biosystems, Italy). spectively obtained the clinical data of the confirmed This test is constituted combining a two-step reverse Pollara et al. BMC Infectious Diseases 2013, 13:127 Page 3 of 7 http://www.biomedcentral.com/1471-2334/13/127 transcription-multiplex PCR with typing and sub-typing H1N1pdm09 infection and in the same period three pa- on the electronic microarray. This assay distinguishes in- tients who required transfer to the intensive care (ICU) fluenza virus types A and B, and identifies common in- because of their critical respiratory status died for fatal fluenza virus A subtypes H1N1 and H3N2, as well as the influenza virus pneumonia (13.1%, patients 3, 5 and 6). potentially pandemic avian influenza virus subtype The clinical characteristics and timeline of the out- H5N1. break of H1N1pdm09 in these patients are shown in The H1N1 positive samples were tested for OST-r var- Table 1 and Figure 1, respectively. The mean age of case iants by one step RT-PCR amplification using single nu- patients was 53 (range, 43-65 years) (Table 1). During cleotide polymorphism (SNP) and directly sequenced by the seasonal influenza peak all these patients were ad- cycle sequencing. This one step RT-PCR amplification mitted for reasons unrelated to influenza infection. All was made in house following
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