This article is made available for unrestricted research re-use and secondary analysis in any form or by any means with acknowledgement of the original source. These permissions are granted for the duration of the World Health Organization (WHO) declaration of COVID-19 as a global pandemic.Ho and colleagues recently drew attention to the consequences of co-infection with Influenza and HIV.1 We present four cases of combined infection with influenza and Middle East Respiratory Syndrome Coronavirus (MERS-CoV) infection. Nasopharyngeal swabs or tracheal aspirates were tested for MERS-CoV using real-time reverse-transcription polymerase chain reaction (RT-PCR).2,  3 Samples were tested for Influenza A, B and H1N1 by rapid molecular test (GenEXper for detection of flu A, B and 2009 H1N1, Cepheid)

Al-Tawfiq, Jaffar A.

Alfaraj, Sarah H.

Altwaijri, Talal A.

Alzahrani, Nojoom A.

Memish, Ziad A.

English

IUPUIScholarWorks

Fabrizio BruschiDepartment of Translational Research on New Technologiesin Medicine and Surgery, University of Pisa, ItalyValentina GiuffraDivision of Paleopathology, Department of TranslationalResearch on New Technologies in Medicine and Surgery,University of Pisa, Italy*Corresponding author. Department of TranslationalResearch on New Technologies in Medicine and Surgery, ViaRoma 57, 56126 Pisa, Italy. Fax: þ39 050 992706.E-mail address: gaeta-raffaele@libero.it (R. Gaeta)Accepted 2 February 2017http://dx.doi.org/10.1016/j.jinf.2017.02.002ª 2017 The British Infection Association. Published by Elsevier Ltd.All rights reserved.The impact of co-infection of influenza Avirus on the severity of Middle EastRespiratory Syndrome CoronavirusKEYWORDSMiddle East RespiratorySyndrome Coronavirus;MERS-CoV;Influenza;Co-infectionHo and colleagues recently drew attention to the conse-quences of co-infection with Influenza and HIV.1 We presentfour cases of combined infection with influenza and MiddleEast Respiratory Syndrome Coronavirus (MERS-CoV) infec-tion. Nasopharyngeal swabs or tracheal aspirates weretested for MERS-CoV using real-time reverse-transcriptionpolymerase chain reaction (RT-PCR).2,3 Samples were testedfor Influenza A, B and H1N1 by rapid molecular test (Gen-EXper for detection of flu A, B and 2009 H1N1, Cepheid).Case 1In the first case, a 39 year-old male, health care worker, anengineer who became ill seven days before admission. He hadfever >38 C, cough and sore throat. He had no nausea,vomiting, diarrhoea or shortness of breath (SOB). He deniedhistory of travel or contact with positive case or camels. Hewas febrile with a temperature of 39.5 C. Chest X-rayshowed non-homogenous opacity at the lower right lungzone. A nasopharyngeal swab was positive for MERS-CoV withCt value upE gene 34, and ORF1A 34 (Table 1). The test wasnegative for influenza but a repeat swab after 48 h was nega-tive for MERS-CoV and positive for H1N1. The patientTable1Asummaryofthefourcasesofco-infectionofMERS-CoVandinfluenza.#AgeGenderSymptomsComorbiditySampletypeViralloadCTvalue(upEgene)Co-infectionCXRIntensivecareOutcomeDaysillbeforehospitalisationOxygenrequirement139MaleFever,cough,sorethroatNoneNPS34H1N1Non-homogenousopacityinlowerrightlungzone.NoDischargedhome7Nil261FemaleProductivecough,SOBDM,hypothyroidismNPS35H1N1PatchyopacitiesinvolvingmiddleandlowerzonesofbothlungfieldsYesDischargedhome3Ventilatorfor13days329FemaleFever,coughNoneNPS32H1N1NormalNoDischargedhome2Nil473FemaleSOB,productivecoughCHF,hypothyroidismNPS36InfluenzaABilateraldiffuseinfiltrateNoDischargedhome4NasalcannulaNPSZnasopharyngealswab;DMZdiabetesmellitus;SOBZshortnessofbreath;CHFZcongestiveheartfailure.Letters to the Editor 521received azithromycin, ceftriaxone and oseltamivir. The pa-tient was discharged home after two negative swabs ofMERS-CoV and being asymptomatic for 48 h.Case 2In the second case, a 61 year-old female with diabetesmellitus and dyslipidemia was admitted with a three-dayhistory of shortness of breath and productive cough. Shehad no nausea, vomiting, or diarrhoea. She denied historyof travel or contact with positive case or camels. She wasafebrile with a temperature of 37 C. Chest X-ray showedpatchy opacities involving middle and lower zones of bothlung fields.A nasopharyngeal swab was positive for MERS-CoVwith Ct value upE gene 34, ORF1A 35 and negative for influ-enza. A repeat swab after 48 h was negative for MERS-CoVbut positive for H1N1. She required BIPAP and she was sub-sequently intubated and was started on mechanical ventila-tion. She was extubated after 13 days. The patient receivedpiperacillinetazobactam, and erythromycin. The patientwas discharged home after she had 2 negative swabs ofMERS-CoV and being asymptomatic for 48 h.Case 3In the third case, a 29 year-old housekeeper female wasadmitted with two days history of fever and cough. She hadno nausea, vomiting, diarrhoea nor shortness of breathing.She had a history of contactwithMERS-CoV positive case. Shewas afebrile with a temperature of 36.9 C. Chest X-ray wasnormal. A nasopharyngeal swab collected upon presentationwas positive for MERS-CoV with CT value upE gene 32 ORF1A32. The swabwas negative for influenza. A repeated swab af-ter 48 hwas positiveMERS-CoVand positive for H1N1. The pa-tient received oseltamivir, azithromycin and ceftriaxone.The patient was discharged home after she had 2 negativeswab of MERS-CoV and being asymptomatic for 48 h.Case 4In the fourth case, thepatientwas a 73 year-old femalewith ahistory of hypothyroidism, heart failure, lymphoma, and lungfibrosis. She has no history of travel or contact with positivecase or camels. Four days prior to her presentation, she hadproductive cough and shortness of breath. She had no fever,diarrhoea, vomiting or nausea. She was afebrile with atemperature of 36.7 C. Chest X-ray showed bilateral diffuseinfiltrate (Fig. 1). A nasopharyngeal swab was positive forMERS-CoV with Ct value upE gene 37; ORF1A 36 and negativefor Influenza. A repeat swab after 3 days was negative forMERS-CoV but positive for influenza A. The patient wastreatedwith piperacillinetazobactam for six days and oselta-mivir for 5 days. The patient was discharged home after twonegative MERS-CoV and being asymptomatic for 48 h.These patients highlight the co-infection with MERS-CoVand influenza. The exact reason to have a negative influenzatest at the time of positive MERS-CoV is not completelyunderstood. It is possible that the presence of MERS-CoVinhibits the PCR reaction for influenza virus. However, anearlier case of MERS-CoV tested initially positive for influenzaA(H1N1)pdm09.4 On the other hand, the positivity of nasalswabs for influenza is specimen type and technique depen-dent.5 Thus, initially negative influenza tests could be a falsetest result. Positive results for viral respiratory pathogensshould not preclude testing for MERS-CoV because co-infection can occur.6 Only a small number of MERS cases hadco-infection with influenza A, parainfluenza, herpes simplex,and Streptococcus pneumoniae.7 In one case, a co-infectionwith Herpes simplex virus type 1 DNA13 and rhinovirusRNA14 were detected by RT-PCR.8 The investigation of thefirst 47 cases showed no co-infection with MERS-CoV.2 Thereis a controversy regarding the risk of increased or decreasedseverity of co-infections. For example co-infections with Res-piratory Syncytial Virus (RSV) and human meta-pneumovirus(hMPV) causes more severe infection than either virus alonewith longer hospitalization and oxygen requirement.9 Otherstudies did not demonstrate these effects.10 The associationand the impact of co-infection with MERS-CoV and influenzaviruses deserve further evaluation and studies.Conflicts of interestAll authors have no conflict of interest to report.References1. Ho A, Aston SJ, Mitchell T, Alaerts M, Menyere M, Mallewa J,et al. The impact of HIV on the burden and severity of influenzaillness in Malawian adults: the bash-flu study. J Infect 2015;71:687e8. http://dx.doi.org/10.1016/j.jinf.2015.09.030.2. Assiri A, Al-Tawfiq JA, Al-Rabeeah AA, Al-Rabiah FA, Al-Hajjar S, Al-Barrak A, et al. Epidemiological, demographic,and clinical characteristics of 47 cases of Middle East respira-tory syndrome coronavirus disease from Saudi Arabia: adescriptive study. Lancet Infect Dis 2013;13:752e61. http://dx.doi.org/10.1016/S1473-3099(13)70204-4.Figure 1 A chest radiograph showing bilateral diffuseopacities.522 Letters to the Editor3. Corman VM, M€uller MA, Costabel U, Timm J, Binger T, Meyer B,et al. Assays for laboratory confirmation of novel human coro-navirus (hCoV-EMC) infections. Euro Surveill 2012;17:49.4. Health Protection Agency (HPA) UK Novel Coronavirus Investi-gation team. Evidence of person-to-person transmission withina family cluster of novel coronavirus infections, UnitedKingdom, February 2013. Euro Surveill 2013;18:20427.5. Cunha BA, Dumont M, Abruzzo E. An adult returned travelerfrom Dubai hospitalized with an influenza-like illness (ILI): Mid-dle East Respiratory Syndrome (MERS) or influenza? Infectioncontrol implications from a near MERS case. Infect ControlHosp Epidemiol 2015;36:858e60. http://dx.doi.org/10.1017/ice.2015.91.6. Saudi Ministry of Health. Case definition and surveillance guid-ance for MERS-CoV testing in Saudi. 2014. http://www.moh.gov.sa/en/Documents/MoHCaseDefinitionMERSCoVVersionMay132014.pdf [Accessed 17 January 2017].7. World Health Organization. WHO guidelines for investigationof cases of human infection with Middle East Respiratory Syn-drome Coronavirus (MERS-CoV). 2013. http://www.who.int/csr/disease/coronavirus_infections/MERS_CoV_investigation_guideline_Jul13.pdf [Accessed 17 January 2017].8. Drosten C, Seilmaier M, Corman VM, Hartmann W, Scheible G,Sack S, et al. Clinical features and virological analysis of a caseof Middle East respiratory syndrome coronavirus infection. Lan-cet Infect Dis 2013;13:745e51. http://dx.doi.org/10.1016/S1473-3099(13)70154-3.9. Konig B, Konig W, Arnold R, Werchau H, Ihorst G, Forster J. Pro-spective study of human metapneumovirus infection in childrenless than 3 years of age. J Clin Microbiol 2004;42:4632e5. http://dx.doi.org/10.1128/JCM.42.10.4632-4635.2004.10. Debiaggi M, Canducci F, Ceresola ER, Clementi M. The role ofinfections and coinfections with newly identified and emergingrespiratory viruses in children. Virol J 2012;9:247. http://dx.doi.org/10.1186/1743-422X-9-247.Sarah H. AlfarajCorona Center, Infectious Diseases Division, Department ofPediatric, Prince Mohamed Bin Abdulaziz Hospital, Ministryof Health, Riyadh, Saudi ArabiaJaffar A. Al-TawfiqJohns Hopkins Aramco Healthcare, Dhahran, Saudi ArabiaIndiana University School of Medicine, Indianapolis, IN, USANojoom A. AlzahraniCorona Center Department, Prince Mohamed Bin AbdulazizHospital, Ministry of Health, Riyadh, Saudi ArabiaTalal A. AltwaijriDepartment of Surgery, Prince Mohamed Bin AbdulazizHospital, Ministry of Health, Riyadh, Saudi ArabiaZiad A. Memish*School of Public Health, Emory University, Atlanta, GA,USAInfectious Diseases Division, Department of Medicine,Prince Mohamed Bin Abdulaziz Hospital, Ministry ofHealth, Riyadh, Saudi Arabia*Corresponding author.E-mail address: zmemish@yahoo.com (Z.A. Memish)Accepted 2 February 2017http://dx.doi.org/10.1016/j.jinf.2017.02.001ª 2017 The British Infection Association. Published by Elsevier Ltd.All rights reserved.Completeness of case ascertainment andavailability of environmental data inLegionnaires’ disease enhancedsurveillance in England, 2012e2014To the Editor,Bai et al.1 previously highlighted the importance ofeffective communicable disease surveillance in China forthe detection of outbreaks to inform infectious diseaseprevention and control. To achieve similar aims with rela-tion to the control of Legionnaires’ disease in England a na-tional enhanced surveillance scheme operates.Surveillance data must be both complete and as timely aspossible, as highlighted by Freeman et al. in this journal.2Thereforewesought toassess the completeness of caseascer-tainment in addition to the availability of environmental datareported to the national enhanced legionella surveillancescheme (NELSS) for residents in England. The valueof environ-mental data is particularly important for Legionnaires’ dis-ease in order to inform the attribution of potentialenvironmental sources of cases and clusters of this infection.In England, the National Legionella Surveillance Team(NLST) leads on surveillance and control of Legionnaires’disease, while Field Epidemiology Services (FES) teamscollect surveillance data and investigate sporadic cases,clusters and outbreaks in conjunction with local HealthProtection Teams (HPTs). The NLST worked with the FESteams in the North West (NW) and West Midlands (WMids)regions of England to audit the reporting of Legionella caseswith onset dates during each calendar year between 2012and 2014, inclusive. Eligible cases were those cases ofLegionella spp. infections resident in either of these re-gions in England, which were laboratory confirmed by uri-nary antigen testing, culture or serological testing. Thesecases were identified in the month of February followingeach calendar year by the NLST and were compared tothose known by the FES teams for NW and WMids regions.Completeness of case ascertainment was calculated asthe proportion of cases recorded by FES teams for caseswith onset of symptoms between 2012 and 2014 inclusivewhich were reported to the NLST. The availability ofenvironmental data reported to the national enhancedsurveillance scheme was calculated as the proportion ofcases during the same time period with any environmentalinvestigation data reported to the NLST.The results are summarised in Table 1; in the NW region, amean of 34 cases were reported per year between 2012 and2014. In the WMids region, the mean number of cases peryear was 46. Both regions reported 100% of cases to the NLST.Mean availability of environmental data reported was80.8% in the NW and 42.8% in WMids. However, there was aLetters to the Editor 523  Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website.  Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.  

The impact of co-infection of influenza A virus on the severity of Middle East Respiratory Syndrome Coronavirus

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The impact of co-infection of influenza A virus on the severity of Middle East Respiratory Syndrome Coronavirus

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