Major ArticleInfection control influence of Middle East respiratory syndromecoronavirus: A hospital-based analysisD1XXJaffar A. Al-Tawfiq MD, FACP, FRCPE, FRCPLD2XXa,b,c,*, D3XXRana Abdrabalnabi RN, MPHD4XXd, D5XXAlla Taher RND6XXd,D7XXShantymole Mathew RND8XXd, D9XXKamal Abdul Rahman RND10XXdaSpecialty Internal Medicine, Johns Hopkins Aramco Healthcare, Dhahran, Saudi ArabiabIndiana University School of Medicine, Indianapolis, IN, USAcJohns Hopkins University School of Medicine, Baltimore, MD, USAdInfection Control Unit, Johns Hopkins Aramco Healthcare, Dhahran, Saudi ArabiaBackground: Middle East respiratory syndrome coronavirus (MERS-CoV) caused multiple outbreaks. Suchoutbreaks increase economic and infection control burdens. We studied the infection control influence ofMERS-CoV using a hospital-based analysis.Methods: Our hospital had 17 positive and 82 negative cases of MERS-CoV between April 1, 2013, and June 3,2013. The study evaluated the impact of these cases on the use of gloves, surgical masks, N95 respirators,alcohol-based hand sanitizer, and soap, as well as hand hygiene compliance rates.Results: During the study, the use of personal protective equipment during MERS-CoV compared withthe period before MERS-CoV increased dramatically from 2,947.4 to 10,283.9 per 1,000 patient-days(P .0000001) for surgical masks and from 22 to 232 per 1,000 patient-days (P .0000001) for N95 masks.The use of alcohol-based hand sanitizer and soap showed a significant increase in utilized amount(P .0000001). Hand hygiene compliance rates increased from 73% just before the occurrence of the firstMERS case to 88% during MERS cases (P =.0001). The monthly added cost was $16,400 for included infectioncontrol items.Conclusions: There was a significant increase in the utilization of surgical masks, respirators, soap and alco-hol-based hand sanitizers. Such an increase is a challenge and adds cost to the health care system. 2018 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. Allrights reserved.Key Words:MERSPersonal Protective EquipmentCostEconomic impactHealthcareMiddle East respiratory syndrome coronavirus (MERS-CoV) emergedin June 2012 in the Kingdom of Saudi Arabia (KSA),1and the first healthcareassociatedMERSinfectionwas describedinmultiplefacilitiesinAl-Hasa, KSA.2Since then, a total of 2,229 cases have been reported to theWorldHealthOrganizationfrom27countries,withanoverallcasefatalityrateof35.6%.3MostcasesofMERS-CoVhavebeenreportedintheArabianPeninsula,withKSAhavingthemajorityofreportedcases.4MERS-CoV causes multiple outbreaks within and outside SaudiArabia.4Such outbreaks may cause economic and infection con-trol burdens on affected health care facilities. During the severeacute respiratory syndrome (SARS) outbreak, the disease had agreat impact on infection control measures.5In a simulationinvolving outbreaks of SARS, 2009 pandemic H1N1, and 1918Spanish influenza, these situations resulted in additional costs of$25,000-$99,000whennoalertwaspresenttoashighas$1,537,000 for SARS during an orange alert level.6During the ini-tial years of MERS-CoV outbreaks, the exact infection controlrequirements were not known,7although there was a knownneed to increase infection control capacity in health care set-tings.8Although a few articles have addressed the preparednessof hospitals to face MERS, there are no data on the impact ofMERS-CoV on infection control resources within hospitals.9,10Here, we study the infection control influence of MERS-CoV byanalyzing data on specific infection control parameters using ahospital-based analysis.METHODSOur hospital was the first outside the United States to beaccredited by the Joint Commission and to subsequently main-tain accreditation by the Joint Commission International. The* Address correspondence to Jaffar A. Al-Tawfiq, MD, Specialty Internal Medicine,Johns Hopkins Aramco Healthcare, PO Box 11705, Dhahran 31311, Saudi Arabia.E-mail address: jaltawfiyahoo.com (J.A. Al-Tawfiq).Conflicts of interest: None to report.https:/doi.org/10.1016/j.ajic.2018.09.0150196-6553/ 2018 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.ARTICLE IN PRESSAmerican Journal of Infection Control 000 (2018) 14Contents lists available at ScienceDirectAmerican Journal of Infection Controljournal homepage: www.ajicjournal.orgorganization has state-of-the-art infection control practices andprocedures. The hospital was one of the first in the world todeal with MERS-CoV cases, when 99 patients who met the casedefinitionofsuspectedMERS-CoVwereadmitted.Ofthosecases, 17 tested positive and 82 tested negative for MERS-CoVbetween April 1, 2013, and June 3, 2013.11-13Of the positivecases, as described previously, 30% had health careassociatedinfections, because the hospital received patients in transferfrom other facilities.2In this study, we aimed to re-evaluate theimpact of these cases on infection control practices, includingthe use of gloves, surgical masks, N95 respirators, alcohol-basedhand sanitizer, and soap, expressed as mL per 1,000 patient-days. Data on the monthly use of gloves (pairs), surgical masks,and N95 respirators were obtained from the central supply ser-vice, assessed based on retrospective analysis of overall supplyordering by the hospital, and expressed per 1,000 patient-days.We also evaluated any change in monthly hand hygiene compli-ance rates. The data span from May 2012 to July 2013 andinclude the pre-MERS period (May 2012 to March 2013), theMERS period (April to May 2013), and the post-MERS period(June to July 2013). Data were extracted from the infection con-trol database, and monthly patient days were obtained from thehealth information unit. This study was approved by the institu-tional review board of the Johns Hopkins Aramco Healthcare.RESULTSDuring the observation period, the utilization of personal protec-tive equipment (PPE) with cases of MERS-CoV compared with theperiod before MERS-CoV cases increased dramatically from 2,947.4 to10,283.9 per 1,000 patient-days (P .0000001) for surgical masksand from 22 to 232 per 1,000 patient days (P .0000001) for N95masks (Fig 1). It is interesting to note that the increase in utilizationof N95 masks preceded the increase in surgical mask utilization byabout 1 month.The utilization of alcohol-based hand sanitizer and soap is shownin Figure 2; there was a significant increase in the used amount(P .0000001). Hand hygiene compliance rates are shown in Figure 2.The hand hygiene compliance rate increased from 73% just before theoccurrence of the first MERS case to 88% during MERS cases(P=.0001) (Fig 3). The monthly added cost was $16,400 for theincluded infection control items, such as hand sanitizers, soap, surgi-cal masks, and N95 respirators.DISCUSSIONIn the most recent updates by the World Health Organization,a total of 2,040 (31%) cases were health care facilityassociatedinfections.14In addition, initial MERS-CoV symptoms tend to benonspecific and might not be noticed. Thus, adherence to stan-dard precautions is a critical factor in the prevention of MERS-CoV transmission.14This adherence, as well as the initial uncer-tainty about transmission routes early in the course of the dis-ease, had resulted in widespread fear of MERS-CoV. It is knownthat application of standard infection control results in the termi-nation of MERS-CoV outbreaks.2,4,15,16Here, we showed a signifi-cantincreaseintheuseofPPE(mainlysurgicalmasks,respirators, alcohol-based hand sanitizer, and soap). There was asignificant increase in the utilization of surgical masks and respi-rators during the study period. There are mixed recommendationsfor the care of patients with MERS-CoV with regard to placingpatients in airborne isolation and thus the use of N95 respirators,droplet precautions, and surgical masks.7,15,17,18The use of surgi-cal masks was noted to increase significantly during the 2009H1N1 influenza pandemic, with a reported 52% increase in use.19This increase in the use of PPE is paralleled by an increase incost. It is recommended that hospitals maintain an adequate sup-ply of PPE for use during infectious disease outbreaks. In 1 study,it was calculated that 4 sets of PPE (N95 respirators, doublegloves, gowns, and goggles) per day are needed for each healthcare worker in the high-risk group, and 2 sets of PPE are requiredfor medium- and low-risk groups.20Another implication for theincreased use of PPE is the generation of medical waste, whichwe did not address in this study. In 1 simulation exercise, anadditional 570 L of waste was generated per day.21We were not able to show a significant increase in handhygiene practices despite the significant increase in utilizationofalcohol-basedhandsanitizers.Thisobservationmayberelated to the fact that baseline hand hygiene was about 88% inthe preceding months. However, the hand hygiene complianceFig 1. A run chart showing the utilization of surgical masks (solid line) and respirators (dashed line) in the period before Middle East respiratory syndrome cases (May 2012 toMarch 2013) and during Middle East respiratory syndrome cases (April to July 2013).ARTICLE IN PRESS2J.A. Al-Tawfiq et al. / American Journal of Infection Control 00 (2018) 14rate dropped to 73% just before the occurrence of the first MERScase and then picked up to 88% (P = .0001). It has been shownthat both observation and a multifaceted approach increasehand hygiene compliance,22,23and that utilization of secretshoppers may give a false sense of the actual rates of handhygiene compliance.24Another possible explanation is that theutilized soap and hand sanitizer may have been used by patientsand visitors.Although the data are from 2013, which may be considered alimitation, they are still valid because this is the only study docu-menting the burden of this new virus on health infrastructureeven though 5 years have elapsed since its emergence. Otherlimitations of the study include the fact that the presented dataare small and represent only one nonMinistry of Health hospital,and it was not possible to use the data to draw conclusionsregarding a national estimate of disease burden. There are multi-ple hospitals supervised by the Ministry of Health, in addition toother hospitals supervised by various institutions and the privatesector.CONCLUSIONSThere was a significant increase in the utilization of surgicalmasks, respirators, soap, and alcohol-based hand sanitizers duringFig 2. A run chart showing the utilization of alcohol-based hand sanitizers (solid line) and soap (dashed line) in the period before Middle East respiratory syndrome cases (May 2012to March 2013) and during Middle East respiratory syndrome cases (April to July 2013).Fig 3. A run chart showing hand hygiene compliance rates in the period before Middle East respiratory syndrome cases (May 2012 to March 2013) and during Middle East respira-tory syndrome cases (April to July 2013). UCL, Upper Control Limits; LCL, lower control limits.ARTICLE IN PRESSJ.A. Al-Tawfiq et al. / American Journal of Infection Control 00 (2018) 143the study period. 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