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The daily direct costs of isolating patients identified with highly resistant micro-organisms in a non-outbreak setting

Open AccessPublished:December 24, 2020DOI:https://doi.org/10.1016/j.jhin.2020.12.013

      Summary

      Background

      Isolation precautions are recommended when caring for patients identified with highly resistant micro-organisms (HRMOs). However, the direct costs of patients in isolation are largely unknown.

      Aim

      To obtain detailed information on the daily direct costs associated with isolating patients identified with HRMOs.

      Methods

      This study was performed from November until December 2017 on a 12-bed surgical ward. This ward contained solely isolation rooms with anterooms. The daily direct costs of isolation were based on three cost items: (1) additional personal protective equipment (PPE), measured by counting the consumption of empty packaging materials; (2) cleaning and disinfection of the isolation room, based on the costs of an outsourced cleaning company; and (3) additional workload for healthcare workers, based on literature and multiplied by the average gross hourly salary of nurses. A distinction was made between the costs for strict isolation, contact-plus isolation, and contact isolation.

      Findings

      During the study period, 26 patients were nursed in isolation because of HRMO carriage. Time for donning and doffing of PPE was 31 min per day. The average daily direct costs of isolation were the least expensive for contact isolation (gown, gloves), €28/$31, and the most expensive for strict isolation (surgical mask, gloves, gown, cap), €41/$47.

      Conclusion

      Using a novel, easy method to estimate consumption of PPE, we conclude that the daily direct costs of isolating a patient differ per type of isolation. Insight into the direct costs of isolation is of utmost importance when developing or updating infection prevention policies.

      Keywords

      Introduction

      Patients admitted to a hospital can be placed in protective or source isolation during their admission. Protective isolation is used to protect immunocompromised (e.g., prolonged neutropenia) patients from getting a fungal or viral infection which is transmitted by air [
      • Siegel J.D.
      • Rhinehart E.
      • Jackson M.
      • Chiarello L.
      the Healthcare Infection Control Practices Advisory Committee. Guideline for isolation precautions: preventing transmission of infectious agents in health care settings.
      ]. In this study, we focus on source isolation, which is used to prevent transmission of highly resistant micro-organisms (HRMOs) from carriers to other patients [
      • Siegel J.D.
      • Rhinehart E.
      • Jackson M.
      • Chiarello L.
      the Healthcare Infection Control Practices Advisory Committee. Guideline for isolation precautions: preventing transmission of infectious agents in health care settings.
      ,
      • Tacconelli E.
      • Cataldo M.A.
      • Dancer S.J.
      • De Angelis G.
      • Falcone M.
      • Frank U.
      • et al.
      ESCMID guidelines for the management of the infection control measures to reduce transmission of multidrug-resistant Gram-negative bacteria in hospitalized patients.
      ]. The HRMO involved determines the type of source isolation, including the recommended additional infection prevention and control (IPC) precautions (e.g., personal protective equipment (PPE)) [
      • Gysin D.V.
      • Cookson B.
      • Saenz H.
      • Dettenkofer M.
      • Widmer A.F.
      ESCMID Study Group for Nosocomial Infections (ESGNI). Variability in contact precautions to control the nosocomial spread of multi-drug resistant organisms in the endemic setting: a multinational cross-sectional survey.
      ,
      • Roth J.A.
      • Hornung-Winter C.
      • Radicke I.
      • Hug B.L.
      • Biedert M.
      • Abshagen C.
      • et al.
      Direct Costs of a Contact Isolation Day: A Prospective Cost Analysis at a Swiss University Hospital.
      ,
      European Centre for Disease Prevention and Control
      Annual epidemiological report on communicable diseases in Europe.
      ]. In general, a distinction is made between universal IPC precautions that need to be applied to all patients, regardless of the presence or absence of HRMOs, and transmission-based precautions (IPC precautions on top of universal precautions), which differ per HRMO and thus per type of source isolation.
      The World Health Organization (WHO) and Centres for Disease Control and prevention (CDC) formulated guidelines with recommendations on transmission-based precautions, including the selection and use of PPE in healthcare settings [
      • Siegel J.D.
      • Rhinehart E.
      • Jackson M.
      • Chiarello L.
      the Healthcare Infection Control Practices Advisory Committee. Guideline for isolation precautions: preventing transmission of infectious agents in health care settings.
      ,
      • Ducel G.
      • Fabry J.
      • Nicolle L.
      Prevention of hospital-acquired infections: a practical guide.
      ]. Local guidelines are usually derived from these international guidelines, but are often adapted to the local situations (e.g., design of the hospital, availability and costs), and based on findings in literature or on expert opinion [

      Working party on Infection Prevention (WIP). Ziekenhuizen - Bijzonder Resistente Micro-Organismen (BRMO). 2017.

      ]. In the Netherlands, the Inspectorate of the Ministry of Health, Welfare and Sport (VWS) audits the implementation of the guidelines from the Working Party on Infection Prevention (WIP) in hospitals [

      Working party on Infection Prevention (WIP). Ziekenhuizen - Bijzonder Resistente Micro-Organismen (BRMO). 2017.

      ].
      Isolation costs are an addition to the basic cost of care, and would not have been made if the patient was not cared for in isolation. The direct costs of isolation can roughly be divided into the following three items: (1) the costs of using additional PPE; (2) the costs of cleaning and disinfection of an isolation room, during admission and after discharge, and (3) additional personnel costs, because healthcare workers (HCWs) need time for donning and doffing of PPE [
      • Roth J.A.
      • Hornung-Winter C.
      • Radicke I.
      • Hug B.L.
      • Biedert M.
      • Abshagen C.
      • et al.
      Direct Costs of a Contact Isolation Day: A Prospective Cost Analysis at a Swiss University Hospital.
      ,
      • Verlee K.
      • Berriel-Cass D.
      • Buck K.
      • Nguyen C.
      Cost of isolation: daily cost of isolation determined and cost avoidance demonstrated from the overuse of personal protective equipment in an acute care facility.
      ]. In this study, indirect costs, which are often costs due to loss of productivity of the hospital, such as a stop on new admissions on a room or ward, or using a multiple-occupancy room for isolation of only one patient, are not included [
      • Ducel G.
      • Fabry J.
      • Nicolle L.
      Prevention of hospital-acquired infections: a practical guide.
      ,
      • Birgand G.
      • Moore L.S.
      • Bourigault C.
      • Vella V.
      • Lepelletier D.
      • Holmes A.H.
      • et al.
      Measures to eradicate multidrug-resistant organism outbreaks: how much do they cost?.
      ,
      • Otter J.A.
      • Burgess P.
      • Davies F.
      • Mookerjee S.
      • Singleton J.
      • Gilchrist M.
      • et al.
      Counting the cost of an outbreak of carbapenemase-producing Enterobacteriaceae: an economic evaluation from a hospital perspective.
      ].
      The aim of this study was to obtain detailed information on the daily direct costs generated by isolating patients with HRMOs for different types of isolation. Furthermore, to facilitate extrapolation of our results to local situations and policies, we also provide an overview of recommended use of PPE per type of isolation as described by the most common international guidelines.

      Methods

      Study design and setting

      This observational study was performed during a non-outbreak period from November until December 2017, and conducted at a 12-bed surgical ward at the Erasmus MC University Medical Centre (Erasmus MC), Rotterdam, the Netherlands. This ward contained solely isolation rooms with anterooms. All patients received an isolation label in their electronic patient record, stating the required type of isolation and the isolation indication.

      Types of isolation

      Patients could be placed into contact isolation (when identifying Enterobacterales, Stenotrophomonas maltophilia, Pseudomonas aeruginosa, Streptococcus pneumoniae, or Enterococcus faecium, with specific resistance profiles), contact-plus isolation (when identifying carbapenemase-producing Enterobacterales) or strict isolation (when identifying meticillin-resistant Staphylococcus aureus (MRSA) or resistant Acinetobacter spp.). The indications for the different types of isolation were according to the Dutch WIP guideline for HRMOs [

      Working party on Infection Prevention (WIP). Ziekenhuizen - Bijzonder Resistente Micro-Organismen (BRMO). 2017.

      ]. Contact-plus isolation was initiated and implemented by the Erasmus MC for patients identified with carbapenemase-producing HRMOs and is now being used by more Dutch hospitals. We compared the Erasmus MC policy with common IPC guidelines.

      Data collection

      In all 12 anterooms, we placed a waste bin for the disposal of PPE packaging materials. We informed all HCWs on the ward in multiple ways about the study. Additionally, on the lid of the waste bin we attached an instruction paper with pictures of the packaging materials that had to be thrown in (Supplementary material). We collected the following packaging materials: (1) empty glove boxes, (2) empty packages of disposable gowns, (3) empty packages of surgical masks, (4) empty packages of FFP2-masks, and (5) empty packages of disposable hair caps. Furthermore, at the start of the study, all open packages in the anterooms were replaced by new boxes.
      During the study period every workday at around 15.00 h the contents of all 12 waste bins were collected, the amount of packaging materials was counted, and the type of isolation per patient was noted.

      Data analyses

      We calculated the number of isolation days per patient, using admission and discharge dates of patients admitted to the isolation rooms. Patients without isolation, with protected isolation, or with non-HRMO indication (e.g., viral infections or other contagious diseases) were excluded from the analyses.
      The numbers of used packaging material were multiplied by the number of PPE per unit of packaging material (Figure 1, step one). For glove boxes it was multiplied by 100, for disposable gowns by 10, for surgical masks by 50 and for disposable hair caps by 150. The consumption of PPE per type of isolation, and the number of isolation days per type of isolation, were counted (Figure 1, steps two and three). The total consumption of PPE per type of isolation was divided by the total number of isolation days for the same type of isolation (Figure 1, step four), resulting in the average use of PPE per type of isolation per day (Figure 1, step five).
      Figure 1
      Figure 1Flowchart of the average use of personal protective equipment (PPE) per type of isolation per day.

      Calculation of cost items

      To calculate the average daily direct costs of isolating a patient per type of isolation, we included the following costs items: (1) additional PPE, (2) cleaning and disinfection of the isolation room, and (3) additional workload for HCWs. Throughout the manuscript, we used the exchange rate of €1 = $1.1387 (as at 16th August 2018). All mentioned prices are without 21% VAT. Costs of additional PPE were calculated by multiplying the average use per day of PPE, per type of isolation, by the manufacturers’ catalogue prices.
      To calculate the costs of cleaning and disinfection we used the amounts the Erasmus MC pays to an outsourced cleaning company. We took the average cleaning costs of 35 weekdays and 12 weekend days, where we made a distinction between types of isolation but also between daily cleaning and cleanings after discharge of the patient.
      Time of additional workload for HCWs was based on the study by Roth et al. [
      • Roth J.A.
      • Hornung-Winter C.
      • Radicke I.
      • Hug B.L.
      • Biedert M.
      • Abshagen C.
      • et al.
      Direct Costs of a Contact Isolation Day: A Prospective Cost Analysis at a Swiss University Hospital.
      ]. They calculated that the extra time a nurse needs for donning and doffing of PPE, for a patient in contact isolation while using gowns, gloves and when applicable surgical masks, was approximately 31 min per day. The average gross monthly salary of a nurse, according to the collective agreement of the University Medical Centres 2015–2017 in the Netherlands, is €2632/$2997, resulting in an average gross hourly wage of €17/$19 [
      Netherlands Federation of University Medical Centres (NFU)
      CAO University Medical Centres 2015–2017.
      ]. This means €9/$10 per day of additional personnel costs for nurses who are caring for patients in isolation. We used the average ‘extra workload’ of certified nurses, nursing assistants and trainee nurses combined.

      Ethics

      The Medical Ethics Committee of the Erasmus MC agreed to the ethical requirements of this study, and decided that the study did not require approval according to the Dutch law on Medical Research in Humans (MEC-2015-306).

      Results

      Guidelines

      The recommendations, of the European Society of Clinical Microbiology and Infectious Diseases (ESCMID), WHO and CDC, on the use of PPE for contact isolation are almost the same (Table I). Only the ESCMID guideline does not recommend wearing a gown in contact isolation. The guidelines differ in their recommendations on using surgical masks and hair caps in strict isolation. The ESCMID guidelines do not provide clear recommendations on the use of PPE in strict isolation.
      Table IOverview of national and international guidelines regarding infection prevention and control (IPC) measures
      Table thumbnail fx1
      CDC-HICPAC, Centres for Disease Control and prevention – Healthcare Infection Control Practices Advisory Committee [
      • Nulens E.
      Chapter 7: Isolation of Communicable Diseases.
      ]; Erasmus MC, Erasmus MC University Medical Centre Rotterdam; ESCMID, European Society of Clinical Microbiology and Infectious Diseases [
      • Tacconelli E.
      • Cataldo M.A.
      • Dancer S.J.
      • De Angelis G.
      • Falcone M.
      • Frank U.
      • et al.
      ESCMID guidelines for the management of the infection control measures to reduce transmission of multidrug-resistant Gram-negative bacteria in hospitalized patients.
      ]; HCW, healthcare worker; HCWs/visitors, IPC measures apply to both HCWs and visitors; IPC, infection prevention and control; N.A, not applicable; N.D. no data; WHO, World Health Organization [
      World Health Organization
      Practical guidelines for infection control in health care facilities.
      ,
      World Health Organization
      Guidelines on prevention and control of hospital associated infections.
      ]; WIP, Working Party on Infection Prevention [
      Working party on Infection Prevention (WIP)
      Ziekenhuizen – Contactisolatie.
      ,
      Working party on Infection Prevention (WIP)
      Ziekenhuizen – Strikte isolatie.
      ,
      Working party on Infection Prevention (WIP)
      Ziekenhuizen – Reiniging en desinfectie van ruimte, meubilair en voorwerpen.
      ].
      +/green = recommended in guideline; -/red = not recommended in guideline.
      ∗Type IIR or FFP1 surgical mask.

      Patient characteristics

      During the 47 days of observation, a total of 44 unique patients were hospitalized on the observed ward. Of these 44 patients, 26 (59.1%) were placed in isolation because they were identified with, or suspected of carrying an HRMO. The 26 patients were admitted for a total of 304 isolation days, with a median stay of seven isolation days (range 1–44) (Table II). The most frequently identified HRMOs were MRSA (N = 5, 19.2%) and carbapenem-resistant P. aeruginosa (N = 4, 15.4%) (Table III).
      Table IICharacteristics of the study population
      CharacteristicsIsolation type
      Contact isolationContact-plus isolationStrict isolation
      No. of patients13211
      Total no. of isolation days16028116
      Average no. of isolation days (median; IQR)12 (4; 20)14 (14; 3)11 (6; 8)
      Minimum no. of isolation days1111
      Maximum no. of isolation days441744
      HCW, healthcare worker; IQR, interquartile range.
      Table IIIIdentified highly resistant micro-organisms (HRMOs) per type of isolation
      Identified HRMOs
      Identification is according to the Dutch WIP guideline for HRMOs [7].
      Isolation type
      Contact isolationContact-plus isolationStrict isolation
      Acinetobacter spp.1
      Carbapenemase-producing Klebsiella aerogenes1
      Carbapenem-resistant Pseudomonas aeruginosa4
      ESBL-producing Enterobacter spp.1
      ESBL-producing Escherichia coli3
      ESBL-producing Klebsiella pneumoniae2
      Escherichia coli1
      Klebsiella pneumoniae1
      MRSA5
      Stenotrophomonas maltophilia1
      Suspected MRSA5
      Vancomycin-resistant Enterococcus faecium1
      ESBL, extended-spectrum beta lactamase; HRMO, highly resistant micro-organism; MRSA, meticillin-resistant Staphylococcus aureus; WIP,Working Party on Infection Prevention.
      Identification is according to the Dutch WIP guideline for HRMOs [

      Working party on Infection Prevention (WIP). Ziekenhuizen - Bijzonder Resistente Micro-Organismen (BRMO). 2017.

      ].

      Additional PPE

      Table IV gives an overview of the average daily consumption and costs of additional PPE. The mean (median; interquartile range) consumption of PPE for gloves was 33 (34; 34), gowns 8 (8; 5), surgical masks 6 (0; 14), and hair caps 3 (0; 0). The consumption of PPE for strict isolation per day was the most expensive (€17/$20) while the consumption of PPE for contact isolation was the least expensive (€9/$10).
      Table IVAverage daily consumption and costs of additional personal protective equipment (PPE)
      Isolation type
      Contact isolationContact-plus isolationStrict isolation
      Average (median; IQR)Average (median; IQR)Average (median; IQR)
      Non-sterile gloves
      Consumption32 (33; 34)36 (35; 30)31 (33; 31)
      Costs€4/$5€5/$6€4/$5
      Gowns
      Consumption7 (6; 5)13 (11; 2)10 (9; 5)
      Costs€4/$5€8/$9€6/$7
      Surgical masks
      Consumption0 (0)5 (7; 13)17 (15; 20)
      Costs€-/$-€2/$2€5/$6
      Hair caps
      Consumption0 (0)0 (0)14 (0; 13)
      Costs€-/$-€-/$-€2/$2
      Total
      Costs€9/$10€15/$17€17/$20
      Average use of PPE per type of isolation, according to the guideline of the Erasmus MC University Medical Centre (accessed 6th June 2018). If a package was not completely used, the minimum number was set to 0. In this case PPE was used, but not enough to empty the package and be counted with that patient. Exchange rate on 16th August 2019: € 1 = $ 1.1387. IQR, interquartile range.

      Cleaning and disinfection of the isolation room

      Cleaning and disinfection of the isolation room included daily cleaning while the patient was present, and cleaning and disinfection after discharge. The average costs of daily cleaning were €13/$14, ranging from €10/$11 for contact isolation to €15/$17 for strict isolation. The costs of room disinfection after discharge were €18/$20 for contact isolation, €20/$23 for contact-plus, and €25/$29 for strict isolation. The costs per type of isolation were based on the costs of cleaning products and on personnel costs, which equate to €26/$29 per hour.

      Costs of isolation per patient

      The average daily direct cost per patient were for contact isolation €28/$31, for contact-plus isolation €36/$41 and for strict isolation €41/$47 (Table V).
      Table VAverage daily direct costs of isolation, per isolation day and type of isolation
      Contact isolationContact-plus isolationStrict isolation
      $$$
      Cost item 1: additional PPE91015171720
      Cost item 2: cleaning and disinfection
      Final cleaning/disinfection of the isolation room after discharge of the patient is not included. The average cleaning costs are based on 35 weekdays and 12 weekend days.
      101113141517
      Cost item 3: additional workload for HCWs
      We used 31 min for donning and doffing, based on the study by Roth et al. [4].
      910910910
      Total costs (95% CI)28 (27.7–28.3)31 (30.7–31.3)36 (35.0–37.0)41 (40.0–42.0)41 (39.6–42.4)47 (45.5–48.5)
      Average use of PPE per type of isolation, according to the guideline of the Erasmus MC University Medical Centre (accessed at 6th June 2018). Exchange rate on 16th August 2019: € 1 = $ 1.1387. CI, confidence interval; HCW, healthcare worker; PPE, personal protective equipment.
      a Final cleaning/disinfection of the isolation room after discharge of the patient is not included. The average cleaning costs are based on 35 weekdays and 12 weekend days.
      b We used 31 min for donning and doffing, based on the study by Roth et al. [
      • Roth J.A.
      • Hornung-Winter C.
      • Radicke I.
      • Hug B.L.
      • Biedert M.
      • Abshagen C.
      • et al.
      Direct Costs of a Contact Isolation Day: A Prospective Cost Analysis at a Swiss University Hospital.
      ].
      The additional direct costs per patient, for the entire isolation period, were for contact isolation €111/$126 (median of four isolation days), contact-plus isolation €504/$573 (median of 14 isolation days) and strict isolation €248/$283 (median of six isolation days).

      Discussion

      In this observational study on a surgical ward, with solely isolation rooms with anterooms, in a tertiary-care centre, we have shown that strict isolation is the most expensive (€41/$47 per patient/day), while contact isolation is the least expensive (€28/$31 per patient/day). This difference in costs can mainly be explained by the difference in consumption of PPE and only partly by the differences in cleaning. The overview with the most common IPC guidelines shows that guidelines sometimes lack recommendations or recommendations differ per guideline, which has an impact on the costs of isolation. In this study, the costs were calculated in detail for the Erasmus MC, which enables other healthcare organizations to alter the data and calculate costs for their own organization.
      The method we used to estimate the consumption of PPE, was novel and less complex and labour-intensive than already published methods [
      • Roth J.A.
      • Hornung-Winter C.
      • Radicke I.
      • Hug B.L.
      • Biedert M.
      • Abshagen C.
      • et al.
      Direct Costs of a Contact Isolation Day: A Prospective Cost Analysis at a Swiss University Hospital.
      ,
      • Verlee K.
      • Berriel-Cass D.
      • Buck K.
      • Nguyen C.
      Cost of isolation: daily cost of isolation determined and cost avoidance demonstrated from the overuse of personal protective equipment in an acute care facility.
      ,
      • Spence M.R.
      • Dammel T.
      • Courser S.
      Contact precautions for methicillin-resistant Staphylococcus aureus colonization: costly and unnecessary?.
      ]. When comparing the costs of PPE for patients identified with MRSA, the costs of PPE in our study (€17/$20) were slightly higher than the costs mentioned by Spence et al.($14) [
      • Spence M.R.
      • Dammel T.
      • Courser S.
      Contact precautions for methicillin-resistant Staphylococcus aureus colonization: costly and unnecessary?.
      ]. In the Netherlands, patients identified with MRSA are nursed in strict isolation, while in the study of Spence et al., these patients were placed in contact isolation. Using surgical masks and hair caps in strict isolation, besides using gloves and gowns, partly explains the difference in cost. However, the different methods of measuring PPE consumption could have played a role as well. Souverein et al. showed costs (e.g., €18) and consumption (e.g., 35 masks/gloves and 15 gowns per day) of PPE for strict isolation, which are more in line with our study [
      • Souverein D.
      • Houtman P.
      • Euser S.M.
      • Herpers B.L.
      • Kluytmans J.
      • Den Boer J.W.
      Costs and benefits associated with the MRSA search and destroy policy in a hospital in the region Kennemerland, The Netherlands.
      ]. In the study of Verlee et al. the daily costs of contact isolation ($35) are higher than in our study (€28/$31) [
      • Verlee K.
      • Berriel-Cass D.
      • Buck K.
      • Nguyen C.
      Cost of isolation: daily cost of isolation determined and cost avoidance demonstrated from the overuse of personal protective equipment in an acute care facility.
      ]. Verlee et al. did not include the costs of cleaning and disinfection of the isolation room, but they did report 43 min of daily excess staff time, which might explain the difference in costs of contact isolation. These studies emphasize that it is of utmost importance that authors clearly state which PPE are used per type of isolation and which cost items are included, because this has a great influence on the costs of isolation.

      Strengths and limitations

      A major strength of this study is that we used an easy to apply, quick method to estimate consumption of PPE by counting empty packaging material. This is in contrast to, for example, the method used by Roth et al. where they observed 10 patients for 24 consecutive hours [
      • Roth J.A.
      • Hornung-Winter C.
      • Radicke I.
      • Hug B.L.
      • Biedert M.
      • Abshagen C.
      • et al.
      Direct Costs of a Contact Isolation Day: A Prospective Cost Analysis at a Swiss University Hospital.
      ]. We believe that counting the used empty packaging material of PPE per room, instead of extracting this from hospital accounting systems or estimating it by IPC staff, as done by Murthy et al. and Spence et al., gives valuable and more detailed information [
      • Spence M.R.
      • Dammel T.
      • Courser S.
      Contact precautions for methicillin-resistant Staphylococcus aureus colonization: costly and unnecessary?.
      ,
      • Murthy A.
      • De Angelis G.
      • Pittet D.
      • Schrenzel J.
      • Uckay I.
      • Harbarth S.
      Cost-effectiveness of universal MRSA screening on admission to surgery.
      ]. Another strength of this study is that daily direct costs were analysed per type of isolation. This provides insights that can be used for IPC policy decision making. A third strength of this study is that the costs per type of isolation were calculated in detail and step by step. This will facilitate translation of our findings to other settings, even though the data were based on Dutch IPC guidelines and on a limited number of patients and isolation days. Unlike our study, most studies focus solely on the costs of contact isolation or on the total costs of an outbreak, instead of defining the costs for all types of isolation [
      • Birgand G.
      • Moore L.S.
      • Bourigault C.
      • Vella V.
      • Lepelletier D.
      • Holmes A.H.
      • et al.
      Measures to eradicate multidrug-resistant organism outbreaks: how much do they cost?.
      ,
      • Otter J.A.
      • Burgess P.
      • Davies F.
      • Mookerjee S.
      • Singleton J.
      • Gilchrist M.
      • et al.
      Counting the cost of an outbreak of carbapenemase-producing Enterobacteriaceae: an economic evaluation from a hospital perspective.
      ,
      • Spence M.R.
      • Dammel T.
      • Courser S.
      Contact precautions for methicillin-resistant Staphylococcus aureus colonization: costly and unnecessary?.
      ,
      • Escaut L.
      • Bouam S.
      • Frank-Soltysiak M.
      • Rudant E.
      • Saliba F.
      • Kassis N.
      • et al.
      Eradication of an outbreak of vancomycin-resistant Enterococcus (VRE): the cost of a failure in the systematic screening.
      ].
      A limitation of this study is that empty packaging material was counted instead of actual used PPE. If a package was not completely used during a patient admission period, the minimum number of used PPE was 0. Even though PPE had been used during this patient period, the empty package was counted with the next patient. However, as we report on group level (i.e. type of isolation), underestimation of actual used PPE is probably small. A second limitation is that we did not measure the time for donning and doffing ourselves. Instead we used the average time for donning and doffing reported by Roth et al. [
      • Roth J.A.
      • Hornung-Winter C.
      • Radicke I.
      • Hug B.L.
      • Biedert M.
      • Abshagen C.
      • et al.
      Direct Costs of a Contact Isolation Day: A Prospective Cost Analysis at a Swiss University Hospital.
      ]. Moreover, when calculating the additional time for donning and doffing, we did not take into account the different types of isolation nor the different HCWs (e.g., physicians, residents, nurses) or visitors that enter the room daily. Verlee et al. also calculated the time for donning and doffing, for contact isolation using gloves and gown, of healthcare personnel [
      • Verlee K.
      • Berriel-Cass D.
      • Buck K.
      • Nguyen C.
      Cost of isolation: daily cost of isolation determined and cost avoidance demonstrated from the overuse of personal protective equipment in an acute care facility.
      ]. They reported 43 min of daily excess time when entering an isolation room in comparison to the 31 min used by Roth et al. [
      • Roth J.A.
      • Hornung-Winter C.
      • Radicke I.
      • Hug B.L.
      • Biedert M.
      • Abshagen C.
      • et al.
      Direct Costs of a Contact Isolation Day: A Prospective Cost Analysis at a Swiss University Hospital.
      ]. A third limitation of our study is that we did not include the indirect costs of isolation. Birgand et al., Montecalvo et al. and Otter et al. did include indirect costs caused by ward or bed closure, decolonization of patients, increased length of stay and admission stop on a ward [
      • Birgand G.
      • Moore L.S.
      • Bourigault C.
      • Vella V.
      • Lepelletier D.
      • Holmes A.H.
      • et al.
      Measures to eradicate multidrug-resistant organism outbreaks: how much do they cost?.
      ,
      • Otter J.A.
      • Burgess P.
      • Davies F.
      • Mookerjee S.
      • Singleton J.
      • Gilchrist M.
      • et al.
      Counting the cost of an outbreak of carbapenemase-producing Enterobacteriaceae: an economic evaluation from a hospital perspective.
      ,
      • Montecalvo M.A.
      • Jarvis W.R.
      • Uman J.
      • Shay D.K.
      • Petrullo C.
      • Horowitz H.W.
      • et al.
      Costs and savings associated with infection control measures that reduced transmission of vancomycin-resistant Enterococci in an endemic setting.
      ]. Birgand et al. found that 69% of the overall mean cost, during an HRMO outbreak, was related to loss of hospital income due to a decrease in hospital activity [
      • Birgand G.
      • Moore L.S.
      • Bourigault C.
      • Vella V.
      • Lepelletier D.
      • Holmes A.H.
      • et al.
      Measures to eradicate multidrug-resistant organism outbreaks: how much do they cost?.
      ]. Moreover, Otter et al. reported €822,000 of ‘opportunity costs’ (i.e. staff time, bed closure and elective surgical missed revenue) in comparison with €312,000 of ‘actual expenditure’ (i.e. anti-infective costs, enhanced screening, contact precautions, temporary ward-based monitors of hand and environmental practice, and environmental decontamination) [
      • Otter J.A.
      • Burgess P.
      • Davies F.
      • Mookerjee S.
      • Singleton J.
      • Gilchrist M.
      • et al.
      Counting the cost of an outbreak of carbapenemase-producing Enterobacteriaceae: an economic evaluation from a hospital perspective.
      ]. These studies show that early detection and isolation of HRMO-positive patients is cost-effective, even though long-term isolation and preventive screening are also costly. The fourth limitation is that we did not collect any information on which we can estimate the care burden of the patient. The care a patient needs has a direct effect on the consumption of PPE. Our data were not corrected for this, which could have led to an under- or overestimation of the calculated consumption of PPE per type of isolation. Evans et al. showed that patients in isolation often have a higher severity of illness than non-isolated patients [
      • Evans H.L.
      • Shaffer M.M.
      • Hughes M.G.
      • Smith R.L.
      • Chong T.W.
      • Raymond D.P.
      • et al.
      Contact isolation in surgical patients: a barrier to care?.
      ]. However, other papers, including the study of Evans et al., also show that patients in isolation tend to get less and shorter attention of HCWs when compared with non-isolated patients [
      • Evans H.L.
      • Shaffer M.M.
      • Hughes M.G.
      • Smith R.L.
      • Chong T.W.
      • Raymond D.P.
      • et al.
      Contact isolation in surgical patients: a barrier to care?.
      ,
      • Morgan D.J.
      • Pineles L.
      • Shardell M.
      • Graham M.M.
      • Mohammadi S.
      • Forrest G.N.
      • et al.
      The effect of contact precautions on healthcare worker activity in acute care hospitals.
      ,
      • Saint S.
      • Higgins L.A.
      • Nallamothu B.K.
      • Chenoweth C.
      Do physicians examine patients in contact isolation less frequently? A brief report.
      ,
      • Vinski J.
      • Bertin M.
      • Sun Z.
      • Gordon S.M.
      • Bokar D.
      • Merlino J.
      • et al.
      Impact of isolation on hospital consumer assessment of healthcare providers and systems scores: is isolation isolating?.
      ]. To be able to calculate the costs of isolation even more accurately in the future, it is important to also take into account the care burden of the patient.
      In conclusion, the direct costs of isolating a patient for one day differs per type of isolation, with strict isolation (i.e. isolation in single-patient room and using surgical mask, gloves, gown and cap) being the most expensive. Furthermore, in our study, the costs of PPE contributed the most to the differences in costs of isolation. Insight into the direct costs of isolation is of utmost importance when developing or updating IPC policies and to be able to perform cost-effectiveness analyses where costs and effects of IPC measures are studied.

      Acknowledgements

      We extend our appreciation to the unit infection prevention and the manager (L.F. Abel) and personnel of the participating ward of the Erasmus MC University Medical Centre Rotterdam, The Netherlands.

      Conflict of interest statement

      The authors state no conflicts of interest.

      Funding sources

      This study was funded by a grant provided by the Erasmus MC University Medical Centre Rotterdam, The Netherlands (grant no. 2015-15209 ).

      Appendix A. Supplementary data

      The following is the Supplementary data to this article:

      References

        • Siegel J.D.
        • Rhinehart E.
        • Jackson M.
        • Chiarello L.
        the Healthcare Infection Control Practices Advisory Committee. Guideline for isolation precautions: preventing transmission of infectious agents in health care settings.
        Am J Infect Control. 2007; 35: S65-S164
        • Tacconelli E.
        • Cataldo M.A.
        • Dancer S.J.
        • De Angelis G.
        • Falcone M.
        • Frank U.
        • et al.
        ESCMID guidelines for the management of the infection control measures to reduce transmission of multidrug-resistant Gram-negative bacteria in hospitalized patients.
        Clin Microbiol Infect. 2014; 20: 1-55
        • Gysin D.V.
        • Cookson B.
        • Saenz H.
        • Dettenkofer M.
        • Widmer A.F.
        ESCMID Study Group for Nosocomial Infections (ESGNI). Variability in contact precautions to control the nosocomial spread of multi-drug resistant organisms in the endemic setting: a multinational cross-sectional survey.
        Antimicrob Resist Infect Control. 2018; 7: 81
        • Roth J.A.
        • Hornung-Winter C.
        • Radicke I.
        • Hug B.L.
        • Biedert M.
        • Abshagen C.
        • et al.
        Direct Costs of a Contact Isolation Day: A Prospective Cost Analysis at a Swiss University Hospital.
        Infect Control Hosp Epidemiol. 2018; 39: 101-103
        • European Centre for Disease Prevention and Control
        Annual epidemiological report on communicable diseases in Europe.
        2008 (Stockholm)
        • Ducel G.
        • Fabry J.
        • Nicolle L.
        Prevention of hospital-acquired infections: a practical guide.
        World Health Organization, 2002
      1. Working party on Infection Prevention (WIP). Ziekenhuizen - Bijzonder Resistente Micro-Organismen (BRMO). 2017.

        • Verlee K.
        • Berriel-Cass D.
        • Buck K.
        • Nguyen C.
        Cost of isolation: daily cost of isolation determined and cost avoidance demonstrated from the overuse of personal protective equipment in an acute care facility.
        Am J Infect Control. 2014; 42: 448-449
        • Birgand G.
        • Moore L.S.
        • Bourigault C.
        • Vella V.
        • Lepelletier D.
        • Holmes A.H.
        • et al.
        Measures to eradicate multidrug-resistant organism outbreaks: how much do they cost?.
        Clin Microbiol Infect. 2016; 22: 162 e1-9
        • Otter J.A.
        • Burgess P.
        • Davies F.
        • Mookerjee S.
        • Singleton J.
        • Gilchrist M.
        • et al.
        Counting the cost of an outbreak of carbapenemase-producing Enterobacteriaceae: an economic evaluation from a hospital perspective.
        Clin Microbiol Infect. 2017; 23: 188-196
        • Netherlands Federation of University Medical Centres (NFU)
        CAO University Medical Centres 2015–2017.
        2017 (Houten)
        • Spence M.R.
        • Dammel T.
        • Courser S.
        Contact precautions for methicillin-resistant Staphylococcus aureus colonization: costly and unnecessary?.
        Am J Infect Control. 2012; 40: 535-538
        • Souverein D.
        • Houtman P.
        • Euser S.M.
        • Herpers B.L.
        • Kluytmans J.
        • Den Boer J.W.
        Costs and benefits associated with the MRSA search and destroy policy in a hospital in the region Kennemerland, The Netherlands.
        PLoS One. 2016; 11e0148175
        • Murthy A.
        • De Angelis G.
        • Pittet D.
        • Schrenzel J.
        • Uckay I.
        • Harbarth S.
        Cost-effectiveness of universal MRSA screening on admission to surgery.
        Clin Microbiol Infect. 2010; 16: 1747-1753
        • Escaut L.
        • Bouam S.
        • Frank-Soltysiak M.
        • Rudant E.
        • Saliba F.
        • Kassis N.
        • et al.
        Eradication of an outbreak of vancomycin-resistant Enterococcus (VRE): the cost of a failure in the systematic screening.
        Antimicrob Resist Infect Control. 2013; 2: 18
        • Montecalvo M.A.
        • Jarvis W.R.
        • Uman J.
        • Shay D.K.
        • Petrullo C.
        • Horowitz H.W.
        • et al.
        Costs and savings associated with infection control measures that reduced transmission of vancomycin-resistant Enterococci in an endemic setting.
        Infect Control Hosp Epidemiol. 2001; 22: 437-442
        • Evans H.L.
        • Shaffer M.M.
        • Hughes M.G.
        • Smith R.L.
        • Chong T.W.
        • Raymond D.P.
        • et al.
        Contact isolation in surgical patients: a barrier to care?.
        Surgery. 2003; 134: 180-188
        • Morgan D.J.
        • Pineles L.
        • Shardell M.
        • Graham M.M.
        • Mohammadi S.
        • Forrest G.N.
        • et al.
        The effect of contact precautions on healthcare worker activity in acute care hospitals.
        Infect Control Hosp Epidemiol. 2013; 34: 69-73
        • Saint S.
        • Higgins L.A.
        • Nallamothu B.K.
        • Chenoweth C.
        Do physicians examine patients in contact isolation less frequently? A brief report.
        Am J Infect Control. 2003; 31: 354-356
        • Vinski J.
        • Bertin M.
        • Sun Z.
        • Gordon S.M.
        • Bokar D.
        • Merlino J.
        • et al.
        Impact of isolation on hospital consumer assessment of healthcare providers and systems scores: is isolation isolating?.
        Infect Control Hosp Epidemiol. 2012; 33: 513-516
        • Working party on Infection Prevention (WIP)
        Ziekenhuizen – Contactisolatie.
        Leids Universitair Medisch Centrum, Leiden2011
        • Working party on Infection Prevention (WIP)
        Ziekenhuizen – Strikte isolatie.
        Leids Universitair Medisch Centrum, Leiden2011
        • Working party on Infection Prevention (WIP)
        Ziekenhuizen – Reiniging en desinfectie van ruimte, meubilair en voorwerpen.
        Leids Universitair Medisch Centrum, Leiden2007
        • World Health Organization
        Practical guidelines for infection control in health care facilities.
        World Health Organization, India2004
        • World Health Organization
        Guidelines on prevention and control of hospital associated infections.
        2002 (New Delhi)
        • Nulens E.
        Chapter 7: Isolation of Communicable Diseases.
        in: Bearman G. Guide to infection control in the hospital. International Society for Infectious Diseases, 2018