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Adherence to non-pharmacological preventive measures among healthcare workers in a middle-income country during the first year of the COVID-19 pandemic: Hospital and community setting

Published:December 24, 2021DOI:https://doi.org/10.1016/j.ajic.2021.12.004

      Highlights

      • This study assessed the adherence to PPE (mask, gowns, and gloves) at the workplace, as well as to non-pharmacological preventive measures (NPPM) outside of the workplace among healthcare workers.
      • NPPM was defined as physical distance as hardly ever and/or never approaches other people within 1.5 meters, social isolation as leaving home less than once a week; hand hygiene as performing hand hygiene ≥ 6 times per period; and adherence to the use of a mask outside of the workplace was defined as on all outings and hardly ever/never removes the mask.
      • High adherence to PPE was independently associated with younger age, professional category, work in an area of direct patient assistance; use of public transportation, or adherence to NPPM outside of the workplace.
      This study assessed, using a self-reported questionnaire, the adherence to PPE (mask, gowns, and gloves) at the workplace, as well as to non-pharmacological preventive measures (NPPM) (physical distance defined as hardly ever and/or never approaches other people within 1.5 meters, social isolation as leaving home less than once a week, hand hygiene was defined as performing hand hygiene ≥ 6 times per period, and adherence to the use of a mask outside of the workplace was defined as on all outings and hardly ever and/or never removes the mask) outside of the workplace among 1,296 health care workers (HCWs), including if NPPM adherence was associated with COVID-19 in HCWs. High adherence to PPE was independently associated with younger age, professional category, work in an area of direct patient assistance; use of public transportation, or adherence to NPPM outside of the workplace.

      Keywords

      Non-pharmacological preventive measures (NPPMs) (eg, avoiding travel, limiting physical contact with people outside of one's household, and maintaining a 1-2 meter distance between oneself and others when in public) are the primary strategies used to prevent transmission of SARS-CoV-2 recommended by the World Health Organization (WHO). Healthcare workers (HCWs) are the first line of care for COVID-19 patients.
      • Chou R
      • Dana T
      • Buckley DI
      • et al.
      Epidemiology of and risk factors for coronavirus infection in health care workers.
      ,
      • Costa SF
      • Giavina-Bianchi P
      • Buss L
      • et al.
      Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) seroprevalence and risk factors among oligo/asymptomatic healthcare workers: estimating the impact of community transmission.
      Although work in the healthcare system may be considered a risk factor, HCWs can acquire COVID-19 in the community, especially categories such as housekeeping and security.
      • Chou R
      • Dana T
      • Buckley DI
      • et al.
      Epidemiology of and risk factors for coronavirus infection in health care workers.
      ,
      • Costa SF
      • Giavina-Bianchi P
      • Buss L
      • et al.
      Severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) seroprevalence and risk factors among oligo/asymptomatic healthcare workers: estimating the impact of community transmission.
      However, data regarding the compliance to NPPM, such as physical distance, social distance, hand hygiene, and adherence to the use of a mask outside of the workplace among HCWs is scarce.
      The goals of this study were to evaluate the adherence to NPPM by HCWs to prevent COVID-19, as well as to investigate whether adherence to these measures was associated with having had an infection by SARS-CoV-2.

      METHODS

      Setting

      The Hospital das Clínicas da Faculdade de Medicina da Universidade de São Paulo (HC-FMUSP) is a public teaching hospital with 2,200-beds spread across seven buildings. The Central Institute was the designated location for receiving COVID-19 cases and comprised an emergency department, 300 ICUs, 300 ward beds, with 6,000 HCWs.
      Serology chemiluminescence test for IgG (DiaSorin, Italy)
      • Oliveira BLCA
      • Campos MAG
      • Queiroz RCS
      • et al.
      Prevalence and factors associated with covid-19 vaccine hesitancy in Maranhão.
      was offered to all HCWs, including contractors in cleaning and security. These HCWs were requested to answer an online questionnaire using the SurveyMonkey platform. The questionnaire included questions on the use of PPE (mask, gowns, and gloves) at work and NPPM (physical distance, social isolation, hand hygiene, and adherence to the use of a mask) outside of the workplace and were based on a questionnaire used in another study in Brazil
      • Lisboa Bastos M
      • Tavaziva G
      • Abidi SK
      • et al.
      Diagnostic accuracy of serological tests for covid-19: systematic review and meta-analysis.
      which was validated as a pilot study and has been applied several times during the pandemic.
      A HCW was considered to have had oligo/asymptomatic COVID-19 if they presented positive serology
      • Corman VM
      • Landt O
      • Kaiser M
      • et al.
      Detection of 2019 novel coronavirus (2019- nCoV) by real-time RT-PCR.
      without previously having been tested with RT-PCR.
      • Corman VM
      • Landt O
      • Kaiser M
      • et al.
      Detection of 2019 novel coronavirus (2019- nCoV) by real-time RT-PCR.
      PPE were made available to all HCWs. HCWs providing direct patient care wore N95 masks and scrubs during their entire shifts. When examining or touching patients they added disposable gloves and a gown.

      Data analysis

      Two analyses were performed. HCWs who had had a documented infection by SARS-CoV-2 (positive serology or positive RT-PCR) were compared with those who had not; and HCWs who reported high adherence to PPE within the hospital were compared with those who did not. Some variables were evaluated as follows:
      • 1.
        Adherence to PPE use within the hospital. One point was attributed to each PPE item used by the HCW during work: mask, gloves, face-shield, goggles, gown, and cap. The scores were then categorized as follows: (1) Low adherence to PPE: 0-2 points; (2) moderate adherence: 3-4 points; and (3) high adherence: 5-6 points.
      • 2.
        Intensity of previous symptoms. One point was considered for each symptom: fever, nasal discharge, sore throat, cough, wheezing, chest pain, anosmia, ageusia, and diarrhea. The scores were then categorized as follows: (1) Asymptomatic: 0 points; (2) Mild symptoms: 1-3 points; (3) Moderate and/or intense symptoms: >3 points.
      • 3.
        Professional category. HCWs considered to provide direct patient assistance were: Physicians and/or Residents and/or Medical students, nurses, nursing technicians, physiotherapists. The following categories were considered to not have direct physical contact with patients: pharmacists, nutritionists, psychologists, Laboratory and/or Radiology and/or Pathology technicians, administrative workers, and others.
      • 4.
        Hospital workplace was divided into 2 categories: direct patient assistance areas (ICU, Emergency room, and medical and/or surgical units); and areas without direct assistance.
      • 5.
        NPPM. Questionnaire included categorical multi-choice answers, but they were grouped for bi- and multivariate analyses such as dichotomy variables. Physical distance was defined as hardly ever/never approaches other people within 1.5 meters; social isolation as leaving home less than once a week; hand hygiene was defined as performing hand hygiene ≥ 6 times per period; and adherence to the use of a mask outside of the workplace was defined as on all outings and hardly ever and/or never removes the mask.
        • Lisboa Bastos M
        • Tavaziva G
        • Abidi SK
        • et al.
        Diagnostic accuracy of serological tests for covid-19: systematic review and meta-analysis.
      Multivariate logistic regression was performed including the variables with P-value ≤ .2 in the bivariate analysis using the software SPSS version 22.00 (SPSS v22, IBM, USA). The inclusion of age and sex was decided a priori. Significance was set at ∂ = 5%.

      RESULTS

      A total of 1,296 HCWs participated in the study. HCWs who had had a documented infection by SARS-CoV-2 (159; 12.2%) were compared with the group that did not. The bivariate analysis of factors associated with having had an infection by SARS-CoV-2 can be seen in Table 1-suplementary material. The multivariate analysis revealed 2 factors associated with infection by SARS-CoV-2: reporting moderate/intense symptoms; and working in an area with direct patient assistance (Table 2-suplementary material).
      Table 1Characteristics of 1,296 healthcare workers evaluated as to previous infection by SARS-CoV-2, and their self-reported adherence to non-pharmacologic measures to prevent COVID-19 (Hospital das Clínicas, University of Sao Paulo, Brazil)
      VariablesTotal N (%)Previous infection by SARS-CoV-2 N (%)OR (95% CI)P-value
      Yes (N = 159)No (N = 1,137)
      Age≥60 years123 (107 (4)116 (10)0.02
      <60 years1173 (90)152 (96)1021 (90)2.46 (1.12 - 5.39)
      SexFemale983 (76)115 (72)868 (76)0.26
      Male313 (24)44 (28)269 (24)1.23 (0.85 – 1.79)
      Professional categoryAdministrative (does not carry out direct patient assistance)144 (11)15 (9)129 (11)0.01
      Pharmacist/Nutritionist/Psychologist83 (6)3 (2)80 (7)
      Housekeeping/Security4 (<1)1 (1)3 (<1)
      Laboratory/Radiology/Pathology technician69 (5)5 (3)64 (6)
      Others professions (no patient assistance)184 (14)17 (11)167 (15)
      Physicians/Residents/Medical students426 (33)56 (35)370 (33)1.84 (1.27 – 2.68)
      Nurse155 (12)21 (13)134 (12)
      Nursing technician154 (12)31 (20)123 (11)
      Physiotherapist73 (6)10 (6)63 (5)
      Data not available4 (<1)-
      Workplace at the hospitalAdministrative office

      (areas in which there is no direct patient assistance)
      130 (10)12 (8)118 (10)<0.01
      Laboratory184 (14)12 (8)172 (15)
      Other local (no medical care)395 (31)36 (23)359 (32)
      Intensive care unit186 (14)32 (20)154 (13)2.19 (1.56 – 3.09)
      Medical and surgical units279 (22)51 (32)228 (20)
      Emergency room115 (9)15 (10)100 (9)
      Data not available7 (<1)-
      Unit dedicated to COVID-19No721 (56)90 (57)631 (56)
      Yes575 44)69 (43)506 (44)0.95 (0.68 – 1.33)0.79
      Adherence to PPE at workLow635 (49)64 (40)571 (50)<0.01
      Moderate357 (28)43 (27)314 (28)
      High304 (24)52 (33)252 (22)1.70 (1.19 – 2.44)
      Intensity of previous symptomsAsymptomatic723 (56)85 (54)638 (56)Reference
      Mild480 (37)51 (32)429 (38)0.89 (0.61 – 1.28)0.54
      Moderate/intense81 (6)22 (14)66 (6)2.50 (1.46 – 4.26)0.01
      Data not available5 (<1)-
      Use of public transportationDoes not use307 (24)30 (19)277 (25)0.30
      Almost never uses (less than once a week)276 (21)36 (23)240 (21)
      1-3 times per week137 (11)20 (13)117 (10)1.19 (0.85 – 1.67)
      4-5 times per week341 (26)43 (27)298 (26)
      ≥ 6 times per week211 (16)28 (18)183 (16)
      Don't know / Did not want to answer14 (1)2 (1)12 (1)--
      Data not available10 (<1)-
      Adherence to use of mask outside of the hospital workplaceDoes not use7 (<1)1 (1)6 (<1)0.01
      Uses on all outings and frequently removes from face52 (4)7 (4)45 (4)
      Uses on all outings and removes mask now and again287 (22)48 (30)239 (21)
      Uses on all outings and hardly ever/never removes the mask943 (73)102 (65)841 (74)0.62 (0.44 – 0.89)
      Data not available7 (<1)-
      Adherence to hand hygiene (HH) when away from home and from workOccasionally or never when away from home15 (1)2 (1)13 (1)0.04
      HH 1-2 times per period (eg, morning, afternoon)86 (7)15 (10)71 (6)
      HH 3-5 times per period390 (30)54 (34)336 (30)
      HH ≥6 times per period792 (61)84 (54)708 (63)0.70 (0.50 – 0.98)
      Not applicable (never leaves home)3 (<1)2 (1)1 (<1)--
      Data not available10 (<1)-
      Adherence to physical distancingFrequently approaches other people within 1.5 meters106 (8)14 (9)92 (8)0.94
      Sometimes approaches other people within 1.5 meters404 (31)61 (39)343 (30)
      Rarely approaches other people within 1.5 meters530 (41)53 (34)477 (42)
      Hardly ever/never approaches other people within 1.5 meters247 (19)30 (19)217 (19)0.98 (0.64 – 1.50)
      Data not available9 (<1)-
      Adherence to social isolation

      (except for work)
      Leaves home ≥6 times per week112 (9)17 (11)95 (8)0.53
      Leaves home 4-5 times per week365 (28)51 (33)314 (28)
      Leaves home 1-3 times per week613 (47)68 (43)545 (48)
      Leaves homes less than once a week193 (15)21 (13)172 (15)0.85 (0.52 – 1.39)
      Data not available13 (1)-
      OR, odds ratio; CI, confidence interval.
      Table 2Multivariate analysis of the factors associated with having had a previous infection by SARS-CoV-2 among healthcare workers (Hospital das Clínicas, University of Sao Paulo, Brazil)
      VariableIndicatoradjusted OR (95% CI)
      Age<60 years1.87 (0.83 – 4.17)
      SexMale1.18 (0.79 – 1.76)
      Professional categoryInvolved in direct patient assistance1.29 (0.83 – 2.02)
      Hospital workspaceArea with direct patient assistance1.65 (1.10 – 2.47)
      Adherence to PPE at workModerate (3-4 points)1.00 (0.64 – 1.54)
      High (5-6 points)1.41 (0.91 – 2.19)
      Intensity of symptomsMild (1-3 points)0.92 (0.63 – 1.35)
      Moderate/Intense symptoms (>3 points)2.15 (1.21 – 3.81)
      Adherence to the use of a mask outside of the workplaceOn all outings and hardly ever/never removes the mask0.71 (0.48 – 1.07)
      Adherence to hand hygiene (HH) when away from home and from workHH ≥6 times per period0.83 (0.57 – 1.22)
      OR, odds ratio; CI, confidence interval.
      HCWs reported using a mask on all occasions when outside the home and never and/or hardly ever removing it (841; 74%), and adherence to hand washing ≥ 6 times and/or period (eg, morning, afternoon) when outside the workplace (708; 63%). Table 3 shows the bivariate analysis of factors associated with high adherence to PPE at the workplace. The multivariate analysis showed that high adherence to PPE at the workplace was independently associated with a younger age; professional category that performed direct patient assistance; working in an area of direct patient assistance; use of public transportation at least once a week; and adherence to NPPM outside of the workplace (physical distancing and social isolation) (Table 4).
      Table 3Bivariate analysis of potential factors associated with healthcare workers reporting high adherence to PPE against COVID-19 at the workplace (Hospital das Clínicas, University of Sao Paulo, Brazil)
      VariablesAdherence to the use of PPE at the workplaceOR (95% CI)P-value
      High (N = 304)Low/Moderate (N = 992)
      Age≥60 years12 (4)111 (11)Reference<0.01
      <60 years292 (96)881 (89)3.06 (1.66 – 5.64)
      SexFemale238 (25)745 (75)Reference0.25
      Male66 (21)247 (78)0.83 (0.61 – 1.13)
      Professional categoryAdministrative1 (<1)143 (15)Reference

      (no direct patient assistance)
      <0.01
      Pharmacist/Nutritionist/Psychologist5 (2)78 (8)
      Cleaning/Security0 (0)4 (<1)
      Laboratory/Radiology/Pathology technician6 (2)63 (6)
      Others professions (no patient assistance)20 (7)164 (17)
      Physicians/Residents/Medical students82 (27)344 (35)7.16 (4.86 – 10.55)
      Nurse64 (21)91 (9)
      Nursing technician85 (28)69 (7)
      Physiotherapist41 (14)32 (3)
      Hospital WorkplaceAdministrative office1 (<1)129 (13)Reference

      (areas without direct patients assistance)
      <0.01
      Laboratory13 (4)171 (17)
      Other86 (28)309 (31)
      Intensive care unit108 (36)78 (8)3.30 (2.51 – 4.33)
      Medical and surgical units66 (22)213 (22)
      Emergency department30 (10)85 (9)
      covid-19 edicated unitNo177 (58)544 (55)Reference0.29
      Yes127 (42)448 (45)0.87 (0.67 – 1.13)
      Intensity of previous symptomsAsymptomatic (0 points)173 (57)550 (56)Reference
      Mild (1-3 points)106 (35)374 (38)0.90 (0.68 – 1.18)0.45
      Moderate/intense(>3 points)24 (8)64 (6)1.19 (0.72 – 1.96)0.49
      Use of public transportationDoes not use66 (21)241 (25)Reference

      0.07
      Rarely (less than once a week)57 (19)219 (22)
      1-3 times per week35 (12)102 (10)1.27 (0.97 – 1.65)
      4-5 times per week92 (31)249 (25)
      ≥ 6 times per week48 (16)163 (17)
      Adherence to the use of a mask outside of the workplaceDoes not use mask1 (<1)6 (1)Reference0.01
      Uses on all outings and frequently removes it4 (1)48 (5)
      Uses on all outings and removes mask now and again59 (20)228 (23)
      Uses on all outings and hardly ever/never removes the mask239 (79)704 (71)1.49 (1.09 – 2.03)
      Adherence to hand hygiene (HH) when away from home and from workOccasionally or never when away from home3 (1)12 (1)Reference0.02
      HH 1-2 times per period (eg, morning, afternoon)9 (3)77 (8)
      HH 3-5 times per period87 (29)303 (31)
      HH ≥6 times per period202 (67)590 (60)1.35 (1.03 – 1.78)
      Adherence to physical distancingFrequently approaches other people within 1.5 meters17 (6)89 (9)Reference<0.01
      Sometimes approaches other people within 1.5 meters85 (28)319 (32)
      Rarely approaches other people within 1.5 meters119 (40)411 (42)
      Hardly ever/never approaches other people within 1.5 meters80 (27)167 (17)1.77 (1.30 – 2.40)
      Adherence to social isolation (except for work)Leaves home ≥6 times per week16 (5)96 (10)Reference<0.01
      Leaves home 4-5 times per week77 (26)288 (29)
      Leaves home 1-3 times per week141 (47)472 (48)
      Leaves homes less than once a week65 (22)128 (13)1.85 (1.33 – 2.58)
      OR, odds ratio; CI, confidence interval.
      Table 4Multivariate analysis of factors associated with healthcare workers reporting high adherence to personal protective equipment (PPE) against COVID-19 at the workplace (Hospital das Clínicas, University of Sao Paulo, Brazil)
      VariablesIndicatoradjusted OR (95%CI)
      Age<60 years-old2.87 (1.46 – 5.63)
      SexMale0.83 (0.59 – 1.17)
      Professional categoryInvolved in direct patient assistance6.66 (4.32 – 10.27)
      Hospital workplaceArea with direct patient assistance1.80 (1.31 – 2.47)
      Use of public transportationAt least once a week1.80 (1.34 – 2.43)
      Adherence to the use of a mask outside of the workplaceOn all outings and hardly ever/never removes the mask1.39 (0.96 – 2.01)
      Adherence to hand hygiene (HH) when away from home and from workHH ≥6 times per period1.07 (0.77 – 1.49)
      Adherence to physical distancingHardly ever/never approaches other people within 1.5 meters1.70 (1.16 – 2.47)
      Adherence to social isolation (except for work)Leaves homes less than once a week1.71 (1.15 – 2.54)
      OR, odds ratio; CI, confidence interval.

      DISCUSSION

      Among the hospital's HCWs, the only factors associated with having had a SARS-CoV-2 infection were working in an area with direct patient assistance and having reported symptoms. HCWs who adhered strongly to PPE at work also adhered more to NPPM outside of work. They were aged < 60 years and belonged to professional categories involved in direct patient assistance. The adherence to NPPM was significantly less frequent in the physicians and/or residents and/or students group when compared to other HCWs (P-value < .001).
      Although the WHO clearly recommended the use of cloth masks in the community, in Brazil, the federal government did not recommend the use of a mask nor NPPM in the first year of the pandemic. The amount of fake news on social media made the recommendations more confusing,
      • Aquino EML
      • Silveira IH
      • Pescarini JM
      • et al.
      Social distancing measures to control the COVID-19 pandemic: potential impacts and challenges in Brazil.
      ,
      • Galhardi CP
      • Freire NP
      • Minayo MCS
      • Fagundes MCM.
      Fact or fake? An analysis of disinformation regarding the Covid-19 pandemic in Brazil.
      with different recommendations at the state and municipal level. Data on population mobility based on mobile phones indicate that immobility in Brazil ranged from 30%-62.2%. This lack of clear recommendation might have had an impact on the adherence to NPPM among HCWs who participated in our study.
      Interestingly, we observed that high adherence to PPE at the workplace was independently associated with younger age, professional category that performed direct patient assistance, work in an area of direct patient assistance, use of public transportation at least once a week, and adherence to NPPM outside of the workplace. As we used a self-reported questionnaire, it is possible that this finding was related to a positive self-perception of the HCW in both the workplace and outside.
      Adherence to NPPM during the pandemic varies depending on behavioral and cultural conditions.
      • Coroiu A
      • Moran C
      • Campbell T
      • Geller AC.
      Barriers and facilitators of adherence to social distancing recommendations during COVID-19 among a large international sample of adults.
      A study that evaluated 2,013 adults in North America and Europe pointed out that the strongest barriers included having friends or family who needed help with running errands and socializing in order to avoid loneliness.
      • Coroiu A
      • Moran C
      • Campbell T
      • Geller AC.
      Barriers and facilitators of adherence to social distancing recommendations during COVID-19 among a large international sample of adults.
      A systematic review that included 16 studies
      • Brooks SK
      • Greenberg N
      • Wessely S
      • Rubin GJ.
      Factors affecting healthcare workers' compliance with social and behavioural infection control measures during emerging infectious disease outbreaks: rapid evidence review.
      on compliance with social and protective behaviors among HCWs during outbreaks observed that staff working in emergency or intensive care settings or in contact with confirmed cases appeared more likely to comply with recommendations as reported in our questionnaire. The review pointed out as well that anxiety and concern about the risk of infection were contributors to compliance, and that monitoring from superiors could improve compliance.
      • Brooks SK
      • Greenberg N
      • Wessely S
      • Rubin GJ.
      Factors affecting healthcare workers' compliance with social and behavioural infection control measures during emerging infectious disease outbreaks: rapid evidence review.
      Unfortunately, we did not evaluate anxiety neither monitoring from superiors in our study.
      Our study has limitations as the data were self-reported, single centered, and voluntary, and we did not evaluate anxiety on risk of infection nor monitoring from superiors.
      In summary, the factors associated with having had a SARS-CoV-2 infection among HCWs were working in an area with direct patient assistance and having reported symptoms. High adherence to PPE at the workplace was independently associated with a younger age; working in an area of direct patient assistance; use of public transportation at least once a week; and adherence to NPPM outside of the workplace that can be related to a positive self-perception of HCW.

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