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Received: 20 July 2022 Revised: 23 December 2022 Accepted: 11 January 2023
DOI: 10.1111/nicc.12888

SERVICE EVALUATION

Determinants of increased nursing workload in the COVID-era:

A retrospective analysis of prospectively collected data

Alberto Lucchini RN, Head Nurse 1 | Marta Villa RN, CCN, Staff Nurse 1 |
Arianna Del Sorbo RN, CCN, Critical care nursing master degree student 2 |
Irene Pigato RN, CCN, Critical care nursing master degree student 2 |
Luca D'Andrea RN, CCN, Critical care nursing master degree student 2 |
Matteo Greco RN, CCN, Critical care nursing master degree student 2 |
Colombo Chiara RN, CCN, Staff Nurse 1 |
Matteo Cesana RN, MSc, Emergency Department Nurse Manager 1 |
1
Roberto Rona MD, ICU Medical Director |
Marco Giani MD, Head of Local ECMO Program 1

1
General Intensive Care Unit, Emergency
Department – ASST Monza, San Gerardo Abstract
Hospital, University of Milano-Bicocca,
Background: COVID-19 is associated with increased nursing workload, therefore a
Monza, Italy
2
School of Medicine and Surgery, University of high nurse-to-patient ratio would be required.
Milano-Bicocca, Monza, Italy Aim: To analyse difference in nursing workload, as expressed with the Nursing Activities

Correspondence
Score (NAS), between COVID-19 patients versus control patients without COVID-19
Alberto Lucchini, General Intensive Care Unit, disease (NCOVID-19 group) in an Italian Extracorporeal Membrane Oxygenation
Fondazione IRCCS San Gerardo dei Tintori -
Monza, University of Milano-Bicocca, Via
(ECMO) centre.
Pergolesi 33, Monza (MB), Italy. Study Design: Retrospective analysis of prospectively collected data, enrolling con-
Email: alberto.lucchini@unimib.it, a.lucchini@
asst-monza.it
secutive patients admitted to a general Intensive Care Unit, between 1st May 2019
and 28th February 2021. A multivariate analysis was then performed to assess if
COVID-19 disease was an independent predictor of higher NAS and to assess which
other factors and procedures are independently associated with increased workload.
Results: We enrolled 574 patients, of which 135 (24%) were in the COVID-19 group
and 439 (76%) in the NCOVID-19 group. The average NAS was higher in the
COVID-19 group (79 ± 11 vs. 65 ± 15, T = 10.026; p < 0.001). Prone positioning,
continuous renal replacement therapy (CRRT) and ECMO were used more frequently
in the COVID-19 group. A higher fraction of patients in the COVID group showed
colonization from multidrug resistant bacteria. COVID-19 group had a higher dura-
tion of mechanical ventilation and longer ICU stay. The COVID-19 diagnosis was
independently associated with a higher NAS. Other independent predictors of higher
NAS were the use of prone positioning and continuous renal replacement therapy

The present study was performed at the General Intensive Care Unit, Emergency Department and Intensive Care, San Gerardo Hospital – ASST Monza, Milan-Bicocca University, Via Pergolesi
33, Monza (MB), Italy.

Nurs Crit Care. 2023;1–12. wileyonlinelibrary.com/journal/nicc © 2023 British Association of Critical Care Nurses. 1
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2 LUCCHINI ET AL.

(CRRT). Colonization from multidrug resistant bacteria and ECMO support were not
independently associated with higher NAS.
Conclusions: The higher nursing workload in COVID-19 patients is mainly due to
specific procedures required to treat the most hypoxemic patients, such as prone
positioning. Colonization with multidrug resistant bacteria and ECMO support were
not independently associated with a higher NAS.
Relevance to Clinical Practice: Higher workload in COVID-19 patients was due to
specific interventions, such as prone positioning and CRRT, with the related nursing
activities, as continuous presence at patient's bed, mobilization, positioning and com-
plex hygienic procedures.

KEYWORDS
COVID-19, ECMO, NAS, nursing workload, prone position

1 | I N T RO DU CT I O N
What is known about the topic
The Sars-Cov-2 pandemics has fundamentally changed the global • COVID-19 is associated with increased nursing workload;
healthcare systems. Intensive Care Units (ICUs) were forced to quickly therefore a high nurse-to-patient ratio would be required.
increase capacity in order to admit many critically ill patients.1 Italy • The high number of urgent ICU admissions due to the
was the first western country facing a COVID-19 outbreak.1 At the COVID-pandemic caused an extreme pressure on the
beginning of the first COVID-19 wave in Lombardy (north of Italy), nursing staff and therefore on the ICU bed capacity
many patients required ICU admission in a short time.2 The ICU • Previous research showed that the nursing workload,
capacity had to be rapidly increased in many hospitals. The experience assessed by the Nursing Activities Score (NAS), suggests
in the treatment of patients with acute respiratory failure, the nurse- an ideal nurse-to-patient ratio of about 0.6 for a generic
to-patient ratio and physician-to-patient ratio and varied among the patient admitted to a general Intensive Care Unit.
centres.3 The high number of urgent ICU admissions due to the
COVID-pandemic caused an extreme pressure on the nursing staff
What this paper adds
and therefore on the ICU bed capacity, in the context of a pre-existing
shortage of intensive care nurses.4 Before the COVID-era the median • The higher NAS of COVID-19 patients is mainly due to
nurse-to-patient ratio in Italy was generally 0.5.4 Previous research specific procedures required to treat the most hypoxemic
showed that the nursing workload, assessed by the Nursing Activities patients, such as prone positioning
Score (NAS), suggests an ideal nurse-to-patient ratio of about 0.6 for • Colonization with multidrug resistant bacteria and ECMO
a generic patient admitted to a general Intensive Care Unit.5 This support were not independently associated with a
workload need might be increased in specific patient populations higher NAS
requiring a high level of assistance, such as patients suffering from • In the context of an experienced ECMO centre, the
severe acute respiratory distress syndrome (ARDS) who require prone ECMO support did not result as an independent determi-
positioning or Extracorporeal Membrane Oxygenation (ECMO). In this nant of increased workload. Similarly, MDR colonization
context, a higher ideal nurse-to-patient ratio (0.75–1) can be was not independently associated with higher NAS.
hypothesized.5–7 Lower nurse-to-patient ratio may be associated with
an increase in incidents, adverse events8 and nosocomial infec-
tions.9,10 When high levels of assistance are required (i.e., high NAS), a
low nurse-to-patient ratio is associated with higher in-hospital mortal- positioning and ECMO14–16 which are often required to treat the
ity.11 These findings suggest that it is more important to focus on the severe respiratory failure due to COVID-19. Therefore, the usual high
nursing workload rather than on the number of patients the nurse standard care must be delivered with the additional difficulty caused
must take care of in the ICU. by wearing personal protective equipment (PPE) for prolonged time
Recent research showed that a nurse-to-patient ratio of 0.75–1 periods.17,18 Moreover, higher rates of hospital-acquired infections
might be required to care for COVID-19 patients,12 with a suggested (HAIs) from multidrug-resistant (MDR) organisms, particularly
nurse-to patient-ratio ranging from 0.75 and 1, as the NAS of these ventilator-associated pneumonia and bloodstream infections, are
patient is higher if we compare with other ICU patients.13 This might reported in COVID-19 patients.19 The procedures to prevent or con-
be partly explained by the advanced treatments, such as prone tain the spread of MDR bacteria may further increase the workload
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LUCCHINI ET AL. 3

for the working staff. Last, the nursing workload may further increase cases. All other patients without COVID-19 diagnosis (patients
in COVID-19 patients due to the absence of family,20 as external visi- admitted from 1st May 2019 to 19th February 2020 and from 16th
tors are usually not allowed to enter COVID-19 ICUs. June 2020 to 30th September 2020) were used as controls and
were included in the NCOVID-19 group. During the study period,
the ICU nursing staff was composed of 30 nurses (among which
2 | AIMS 12 were university certified critical care nurses), five nurses' assis-
tants, and a perfusionist on call. The daily shifts were made up of
The primary aim of this study was to analyse the difference in nursing seven nurses in the morning, six nurses in the afternoon and five
workload, as assessed by the Nursing Activities Score, between during the night shift. The scheduled nurse-to-patient ratio during
COVID-19 and NCOVID-19 patients. The secondary aim was to iden- the study period was 0.6. A nurse assistant was guaranteed on the
tify the determinants of increased nursing workload. 24 h. In the first wave, the ICU had no isolated beds. Thus, from
20th February 2020 to 15th June 2020, during the first COVID-19
wave, the entire clinical ICU area (bed unit, nurses' station, meeting
3 | D E S I G N A N D M E T H O DS area, etc.) was considered a “contaminated area”. Two separate areas
were created for donning (putting on) and doffing (taking off) heath
3.1 | Study design and population care workers' personal protective equipment (PPE). As the use of
protective devices was tolerable only for a few hours, we re-
A retrospective analysis of prospectively collected data was per- organized shifts to allow resting for one nurse at a time outside the
formed. We enrolled all consecutive patients admitted to a referral “contaminated area”, in order to guarantee a rotation every 2–3 h
ICU/ECMO centre of a tertiary University Hospital in the north of for operators dedicated to isolated patients.
Italy from 1st May 2019 until 28st February 2021. On February The original 10 ICU beds were increased up to 50 during the
20th 2020, our mobile ECMO service retrieved a 66-year-old male surge, due to the growing demand for COVID-19 ICU beds in north of
with severe acute respiratory distress syndrome (ARDS) from a hos- Italy region. The original ICU staff were divided between the new and
pital in northern Italy.21 The other ICU patients were tested for the old ICU beds. Nurses from the operating theatre were made avail-
SARS-CoV-2 and were found negative. They were then transferred able by closing elective surgical admissions and were recruited as new
to an alternative “clean” ICU, whereas our 10-bed Intensive Care ICU staff. More complex procedures, as intubation, haemofiltration
Unit (ICU) was transformed in a COVID unit. Before 20th February and ECMO were managed only by a team of Critical Care Nurses,
2020, the ICU was a ten-bed unit (5 rooms with two beds). After while the nurses from the operating theatre managed stable patients
20Th February 2020 the ICU was converted in COVID-ICU and with lower nursing complexity. In order to guarantee a safe prone
admitted patients from the first (till 15th June 2020) and second position procedure, at least three experienced operators (critical care
COVID-wave (from 1st October 2020 to 28th February 2021). The nurses and/or Intensivist physicians) were present during each prone
COVID-19 group include all laboratory-confirmed SARS-CoV-2 position manoeuvre.

FIGURE 1 Flow chart of the study population.

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4 LUCCHINI ET AL.

TABLE 1 Patients' characteristics and NAS description.

COVID-19 NCOVID-19
n = 135 (24%) n = 439 (76%) p value
Age, years 59 ± 12 60 ± 20 T-test T = 0.18 0.855
Females 24 (24%) 176 (40%) Chi-square test X2 = 12.00 <0.001
BMI, kg/m2 30 ± 7 27 ± 10 T-test T = 3.39 <0.001
Length of ICU stay, days 13 ± 14 4±8 T-test T = 10.17 0.019
Use of mechanical ventilation 131 (97%) 299 (68%) Chi-square test X = 45.97
2
<0.001
Duration of mechanical ventilation, days 15.33 (14.58) 4.46 (9.49) T-test T = 8.24 <0.001
SAPS 2 34 ± 10 30 ± 15 T-test T = 1.48 0.139
Use of prone positioning 89 (65%) 26 (6%) Chi-square test X2 = 232.03 <0.001
CRRT 18 (13%) 34 (8%) Chi-square test X2 = 3.91 0.048
Veno-venous ECMO 15 (11%) 13 (3%) Chi-square test X2 = 14.77 <0.001
Vasoactive drugs 106 (78%) 162 (37%) Chi-square test X2 = 71.49 <0.001
Rate of ICU readmission 2 (2%) 28 (6%) Chi-square test X2 = 4.99 0.025
Survival at ICU discharge 111 (82%) 388 (88%) Chi-square test X = 3.45
2
0.454
Colonization with multidrug resistant bacteria 39 (29%) 12 (3%) Chi-square test X2 = 60.84 0.001
Acinetobacter baumannii 22 (16%) 3 (0.7%) Chi-square test X = 60.41
2
<0.001
Klebsiella pneumoniae 8 (6%) 8 (2%) Chi-square test X2 = 6.41 0.011
Vancomycin-resistant enterococcus 9 (7%) 1 (0.2%) Chi-square test X = 25.00
2
<0.001
ICU admission from
Emergency department 28 (21%) 126 (29%) Chi-square test p < 0.001
Medical wards 58 (43%) 64 (15%) X2 = 146.74

Other ICU 44 (33%) 34 (8%)

Elective surgery 1 (0.7%) 152 (35%)
Urgent surgery 3 (2.3%) 63 (13%)
Diagnosis at ICU admission
ARDS 134 (98%) 63 (14%) Chi-square test X2 = 388.00 p < 0.001
Cardiogenic shock --- 5 (1%)
Trauma --- 47 (11%)
COPD exacerbation --- 5 (1%)
Cardiac arrest --- 5 (1%)
Post-operative monitoring 1 (0.7%) 160 (37%)
Emergency surgery 2 (1.3%) 55 (13%)
Intoxication --- 5 (1%)
Other --- 92 (21%)
Daily NAS 79 ± 11 66 ± 15 T-test T = 10.02 <0.001
NAS at the ICU admission 87 ± 20 71 ± 46 T-test T = 9.129 <0.001
NAS at the ICU discharge 73 ± 16 65 ± 8 T-test T = 4.70 <0.001
NAS – ECMO patients 90 ± 9 82 ± 11 T-test T = 2.07 <0.001
NAS – patients who underwent prone positioning 82 ± 11 81 ± 11 T-test T = 0.47 0.684

Note: Data are presented as mean (± standard deviation) or as absolute (relative) frequency.
Abbreviations: ARDS, acute respiratory distress syndrome; BMI, body mass index; COPD, chronic obstructive pulmonary disease; CRRT, continuous renal
replacement therapy; ECMO, extracorporeal membrane oxygenation; ICU, Intensive Care Unit; NAS, nursing activities score; SAPS 2, simplified acute
physiology score.

At the end of the first COVID-19 wave (June 2020), the Intensive only the patients' room was considered “contaminated area”, while
Care Unit was renovated, and the 5 rooms were transformed into iso- the others part of ICU (nurses' station, meeting area, etc.) were con-
lated rooms with an inlet/outlet filter area. During the second wave sidered a “cleaned area”. Therefore, healthcare workers wore full PPE
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LUCCHINI ET AL. 5

TABLE 2 Comparing NAS-interventions in enrolled patients and difference between groups.

Nursing activities score (NAS) – items COVID-19 (2475 days) NCOVID-19 (1750 days) p value
1. Monitoring and titration
1a. Hourly vital signs (4.5) 684 (28%) 342 (20%) X2 = 100.53 p ≤ 0.001
1b. Present at bedside and continuous observation 1335 (54%) 865 (50%)
or active for 2 h or more in any shift (12.1)
1c. Present at bedside and active for 4 h or more 456 (18%) 543 (30%)
(19.6)
2. Laboratory: Biochemical and microbiological 2475 (100%) 1750 (100%) p = 1.000
investigations (4.3)
3. Medication: Vasoactive drugs excluded (5.6) 2475 (100%) 1750 (100%) p = 1.000
4. Hygiene procedures
4a. Performing hygiene procedures (4.1) 1034 (44%) 433 (27%) X2 = 140.67 p < 0.001
4b. The performance of hygiene procedures took 1201 (52%) 1066 (66%)
more than 2 h in any shift. (16.5)
4c. The performance of hygiene procedures took 96 (4%) 127 (8%)
more than 4 h in any shift (20.0)
5. Care of drains: All (except gastric tube) (1.8) 1557 (62%) 158 (10%) X2 = 60.59 p < 0.001
6. Mobilization and positioning
6a. Performing procedure(s) up to 3 times per 24 h 1018 (44%) 450 (26%) X2 = 207.84 p < 0.001
(5.5)
6b. Performing procedures(s) more frequently than 943 (40%) 700 (41%)
3 times per 24 h. or with 2 nurses. any
frequency (12.4)
6c. Performing procedure with three or more 371 (16%) 574 (33%)
nurses – any frequency. 817.0)
7. Support and care of relatives and patient
7a. Support and care of either relatives or patient 2161 (96%) 1374 (97%) X2 = 1.01 p = 0.119
(4.0)
7b. Support and care – full dedication for 3 h or 87 (4%) 24 (3%)
more (32.0)
8. Administrative and managerial tasks
8a. Performing routine tasks 4.2 2065 (88%) 1325 (82%) X2 = 33.33 p < 0.001
8b. Performing administrative and managerial 266 (11%) 272 (17%)
tasks requiring full dedication for about 2 h
(23.2)
8c. Performing administrative and managerial tasks 7 (1%) 3 (1%)
4 h or more (30.0)
Ventilatory support
9. Respiratory support: Endotracheal tube 1891 (76%) 1555 (89%) X2 = 5.10 p = 0.04
supplementary oxygen by any method. (1.4)
10. Care of artificial airways (1.8) 1651 (67%) 1440 (82%) X2 = 5.92 p = 0.001
11. Treatment for improving lung function (4.4) 1897 (77%) 1537 (88%) X2 = 3.54 p = 0.014
Cardiovascular support
12. Vasoactive medication: Disregard type or dose. 784 (32%) 809 (46%) X2 = 3.03 p < 0.001
(1.2)
13. Intravenous replacement of large fluid losses 90 (4%) 38 (2%) X2 = 0.41 p = 0.003
(2.5)
14. Left atrium monitoring: Pulmonary artery 188 (8%) 203 (12%) X2 = 0.89 p < 0.001
catheter with or without cardiac output
measurement.
15. Cardiopulmonary resuscitation after arrest (7.1) 11 (0.5) 6 (0.1%) X2 = 0.34 p = 0.845

(Continues)
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6 LUCCHINI ET AL.

TABLE 2 (Continued)

Nursing activities score (NAS) – items COVID-19 (2475 days) NCOVID-19 (1750 days) p value
Renal support
16. Hemofiltration techniques/dialysis 402 (16%) 311 (18%) X2 = 0.45 p = 0.876
techniques (7.7)
17. Quantitative urine output measurement (7.0) 2229 (90%) 1571 (90%) X2 = 0.05 p = 0.754
Neurological support
18. Measurement of intracranial pressure (1.6) 2 (0.05%) 0 (0%) X2 = 2.20 p = 0.956
Metabolic support
19. Treatment of complicated metabolic acidosis/ 226 (9%) 216 (12%) X2 = 0.48 p = 0.09
alkalosis (1.3)
20. Intravenous hyperalimentation. (2.8) 308 (12%) 42 (2%) X2 = 7.68 p = 0.006
21. Enteral feeding (1.3) 1396 (56%) 1478 (84%) X2 = 18.67 p < 0.001
Specific interventions
22. Specific intervention(s) in the ICU (2.8) 605 (24%) 607 (35%) X2 = 2.91 p < 0.001
23. Specific interventions outside ICU (1.9) 155 (6%) 26 (1%) X2 = 3.70 p < 0.051

Note: p-value was obtained with Chi-square test.

Abbreviation: ICU, Intensive Care Unit.

only inside the patient's room (see Figures S1–S5). This strategy 3.4 | Statistical analysis
reduced the time operators wore PPE, and consequently resulted in
an increase of number of donning and doffing procedures All data were analysed using the Statistical Social Sciences software,
(i.e., increase of PPE consumption). During the second wave, unlike version 22.0, for Windows (SPSS Inc., Chicago, IL, USA). We used
February 2020, the elective surgical intervention program was not mean and standard deviation (SD) to describe continuous variables.
interrupted. This made it impossible to recruit previously trained oper- Categorical variables were described by numbers and percentages.
ative room nurses to increase the number of intensive beds. To over- The Shapiro–Wilk test was used to confirm that the data were nor-
come the shortage of staff with intensive care nursing competencies, mally distribute and Student's T test and Chi-square test were used
managers enrolled just graduated nurses. for comparisons. To assess the independent association of COVID-19
diagnosis with higher NAS, we performed a multivariate linear regres-
sion analysis including other factors and treatments which are not
3.2 | Nursing Activities Score included in the NAS score (use of prone positioning, CRRT, ECMO,
colonization with MDR bacteria). Estimates with 95% confidence
NAS score is made up of 13 main areas, split into 23 items, describing intervals (CI) and p-values were then reported. A p value <0.05 was
patient-related and non-patient-related works, administrative tasks, considered statistically significant.
and level of patient's dependency as well.22 The resulting score,
expressed out by percentage, represents the total amount of time
required to deliver nursing care. A NAS score of 100% corresponds to 3.5 | Ethical considerations
one nurse dedicated to a single patient over 24 h (nurse-to-patient
ratio 1:1 equal to 1440 min of nursing care/day). The nurse workload Data were collected as part of the “STORM” study (Spallanzani Insti-
was assessed through an Italian version of NAS.6 Nurses have tute approval number 84/2020) for COVID-19 patients and as a part
received special training to use NAS, since their initial period of work- of “NASINICU” study for NCOVID-19 patients (May 15, 2018 –
ing in ICU. The NAS filling criteria were the same to those published approval number: 877). Due to the observational nature of the study,
by Padilha et al.23 patient consent was not required from the local ethics committee.

3.3 | Data collection 4 | RE SU LT S

At our institution, NAS is prospectively recorded every day at 6 a.m., Five hundred and seventy-four patients were included, 135 (24%) in
reporting the previous 24 h. All the other parameters were recorded the COVID-19 group and 439 (76%) in the NCOVID-19 group.
from electronic medical record (Innovian SUITE® patient management Figure 1 shows the flow chart of the study population. The character-
system, Drager Medical GmbH, Lubeck, Germany). istics of the study population are shown in Table 1. The average NAS
 TABLE 3 Characteristics and NAS of enrolled patients stratified according to the ICU renovation and epidemic wave.

NCOVID-19 COVID-19
LUCCHINI ET AL.

ICU renovation p value

Before After Before After NCOVID-19 COVID-19

n = 364 (63%) n = 75 (13%) n = 46 (8%) n = 89 (16%) All groups before/after before/after
Age. years 61 ± 20 55 ± 19 61 ± 10 59 ± 13 ANOVA 0.105 (F = 1.48) T-test 0.030 (T = 1.85) 0.571 (T = 0.95)
Females. – n (%) 145 (40%) 30 (40%) 9 (21%) 21 (23%) Chi-square test 0.004 (X2 = 12.15) Chi-square test 0.924 (X2 = 0.76) 0.683 (X2 = 0.08)
2
BMI. kg/m 26.7 ± 9.9 26.2 ± 7.9 29.4 ± 5.1 30 ± 7.8 ANOVA 0.009 (F = 4.03) T-test 0.705 (T = 0.35) 0.853 (T = 0.88)
Length of ICU stay. days 5.6 ± 7.9 6.6 ± 6.2 19.7 ± 20.2 16.1 ± 14.4 ANOVA <0.0001 (F = 35.43) T-test 0.322 (T = 0.77) 0.480 (T = 0.99)
Use of mechanical 245 (67%) 52 (70%) 42 (97%) 87 (98%) Chi-square test <0.0001 (X2 = 46.13) Chi-square test 0.641 (X2 = 0.07) 0.465 (X2 = 0.51)
ventilation – n (%)
Duration of mechanical 4.1 ± 7.5 5.3 ± 4.5 14.4 ± 17.9 14.2 ± 12.5 ANOVA <0.0001 (F = 39.54) T-test 0.692 (T = 0.77) 0.372 (T = 0.99)
ventilation. days
SAPS 2 30 ± 16 31 ± 14 34 ± 15 30 ± 8 ANOVA 0.558 (F = 0.75) T-test 0.889 (T = 0.19) 0.317 (T = 0.22)
2 2
CRRT 28 (8%) 5 (7%) 3 (7%) 15 (17%) Chi-square test <0.0001 (X = 2.34) Chi-square test 0.776 (X = 0.50) 0.07 (X2 = 1.66)
2 2
Veno-venous ECMO 12 (3%) 0 (0.0%) 9 (20%) 6 (7%) Chi-square test <0.0001 (X = 27.90) Chi-square test 0.113 (X = 2.63) 0.019 (X2 = 5.40)
Use of prone positioning 21 (6%) 4 (5%) 29 (65%) 59 (66%) Chi-square test <0.0001 (X2 = 232.29) Chi-square test 0.898 (X2 = 0.47) 0.965 (X2 = 0.06)
2 2
Vasoactive drugs 125 (34%) 36 (49%) 36 (82%) 69 (77%) Chi-square test <0.0001 (X = 78.73) Chi-square test 0.022 (X = 7.66) 0.568 (X2 = 0.08)
Rate of ICU readmission 27 (7%) 1 (1%) 2 (5%) 0 (0%) Chi-square test 0.013 (X2 = 10.55) Chi-square test 0.051 (X2 = 3.59) 0.043 (X2 = 4.06)
2 2
ICU survival 322 (89%) 65 (88%) 35 (80%) 75 (84%) Chi-square test 0.179 (X = 4.68) Chi-square test 0.831 (X = 0.06) 0.498 (X2 = 0.91)
Colonization with 16 (4.4%) 6 (8.1%) 1 (2%) 38 (42%) Chi-square test <0.001 (X2 = 67.88) Chi-square test 0.185 (X2 = 1.36) <0.001 (X2 = 3.00)
multidrug resistant
bacteria
Acinetobacter 2 (0.6%) 0 (0.0%) 0 (0%) 22 (25%) Chi-square test <0.001 (X2 = 103.55) Chi-square test 0.552 (X2 = 0.63) <0.001 (X2 = 13.14)
Baumanii
Klebsiella Pneumoniae 14 (3.84) 5 (6.66) 1 (2%) 7 (8%) Chi-square test 0.018 (X2 = 10.12) Chi-square test 0.539 (X2 = 0.43) 0.202 (X2 = 1.661)
2 2
Vancomycin-resistant 0 (0.0%) 1 (1.4%) 0 (0%) 9 (10%) Chi-square test <0.001 (X = 43.21) Chi-square test 0.027 (X = 5.10) 0.029 (X2 = 0.02)
enterococcus
Mean daily NAS 65 ± 14 69 ± 16 82 ± 10 78 ± 11 ANOVA <0.001 (F = 30.83) T-test 0.010 (T = 2.54) 0.498 (T = 0.70)
NAS at the ICU 70 ± 49 76 ± 22 88 ± 19 87 ± 20 ANOVA 0.001 (F = 7.45) T-test 0.331 (T = 2.83) 0.667 (T = 0.48)
admission
NAS at the ICU 65 ± 16 64 ± 16 74 ± 15 71 ± 10 ANOVA <0.001 (F = 20.88) T-test 0.573 (T = 0.01) 0.641 (T = 0.73)
discharge

Note: Data are presented as mean (±standard deviation) or as absolute (relative) frequency.
Abbreviations: BMI, body mass index; CRRT, continuous renal replacement therapy; ECMO, extracorporeal membrane oxygenation; ICU, Intensive Care Unit; NAS, Nursing Activities Score; SAPS 2, simplified
acute physiology score.
7

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8 LUCCHINI ET AL.

T A B L E 4 Multivariate analysis of factors associated with mean continuous renal replacement therapy. Conversely, ECMO and MDR col-
Nursing Activities Score. onization were not independently associated with higher NAS.
Estimate (95% C.I.) p. value
COVID-19 3.5 (1.8–5.2) <0.001
Use of prone positioning 4.7 (2.8–6.5) <0.001
5 | DI SCU SSION
CRRT 4.2 (1.5–6.9) 0.0278
This study aimed to assess the difference in nursing workload between
ECMO 1.2 ( 2.5–4.9) 0.534
NCOVID-19 and COVID-19 patients, and the factors associated with
MDR colonization 1.1 ( 0.8–3) 0.265
its increase. The mean NAS in COVID-19 patients (79 ± 11%) in this
Abbreviations: CRRT, continuous renal replacement therapy; ECMO, study was similar compared with other recently published studies.12
extracorporeal membrane oxygenation; MDR, multi drug resistant
Some preliminary monocentric reports identified that nursing workload
bacteria.
was dramatically higher in first COVID-19 patients managed in the Ital-
ian (mean NAS: 84 ± 10) and Belgian (82 ± 9) ICUs24,25 compared with
was higher for COVID-19 patients (79 ± 11 vs. 65 ± 15, T = 10.026; patients without COVID-19 diagnosis. More recently, Bruyneel and col-
p < 0.0001). NAS in the COVID-19 group was higher both at ICU leagues12 with a large sample size, from Belgium ICUs network, showed
admission (87 ± 20 vs. 71 ± 46, T = 9.129; p < 0.001) and on the how the average NAS, in COVID-19 versus NCOVID-19 patients,
day before discharge from the ICU (73 ± 12 vs. 65 ± 8, T = 4.701; increased significantly by 20% (92 ± 16 vs. 72 ± 18). Hoogendoorn and
p < 0.001). Mechanical ventilation (MV) was more common in the colleagues26 reported a significantly higher NAS (76 vs. 50, p < 0.001)
COVID-19 group, duration of MV and the length of ICU stay were in the COVID-19 time compared with the NCOVID time, in
higher than in controls. Vasoactive drugs, prone positioning and Netherlands ICUs and they recorded a greater NAS score on first ICU
ECMO were used more frequently in COVID-19 patients as showed day and the day before ICU discharge (in COVID-19 patients, respect
in Table 1. Patients who underwent prone positioning had a higher to NCOVID-19). The average NAS for NCOVID-19 group in this study,
NAS compared with controls (82 ± 11 vs. 65 ± 14, T = 9.118; was equal to 65 ± 15, which was similar to the value recorded in other
p < 0.001), with no difference between COVID-19 group and NCOVID- studies. Several countries have estimated the nursing workload,
19 group. ECMO patients in the COVID-19 group had a higher NAS through the NAS, in general ICUs, before the COVID-era in Belgium:
compared with ECMO patients in the NCOVID-19 group (90 ± 8 vs. 83 mean NAS 69,27 Brasil: 74 ± 9,28 Italy: median 68 (IQR: 58–77),5 and
± 10, T = 2.070; p < 0.0001). 62% of ECMO COVID-19 patients Spain: 67 (55–77).29
underwent prone positioning, compared with 28% of ECMO NCOVID- The coordination centre of the Intensive Care Units of Lombardy
19 patients (X2 = 0.123; p = 0.13). 20 (71%) patients treated with defined the following criteria for ICU admission for COVD-19 patients:
ECMO were discharged alive from ICU. Survival at ICU discharge of (a) failure of noninvasive respiratory support, defined as persistent hyp-
ECMO patients did not differ significantly between COVID-19 and oxemia, tachypnea and respiratory distress or development of hypercap-
NCOVID-19 (80% vs. 62%, respectively, X2 = 0.153; p = 0.281). Patients nia despite the application of CPAP/NIV; (b) expected imminent need for
with COVID-19 need higher time for monitoring/time spent at patient's invasive mechanical ventilation; (c) absence of a do-not-intubate order,
bed, mobilization, hygiene care and isolation procedures, managing of eventually defined by the intensivist together with the ward staff physi-
mechanical ventilation and cardiovascular support (Table 2). cians caring for the patient.3,30 All COVID-19 patients included in the
In the study period we identified four groups of patients: NCOVID- study underwent evaluation by a senior intensivist, who decided accord-
19 (n = 364 [63%]) and COVID-19 (n = 46 [8%]) patients admitted ing to her/his clinical judgement and to local protocols whether to treat
before ICU renovation, and NCOVID-19 (n = 75 [13%]) and COVID-19 the patient in a ward under supervision of the ICU team or to admit the
(n = 89 [16%]) patients admitted in the renovated ICU (Table 3). patient to the ICU. Conversely, many patients were managed with nonin-
In the COVID-19 group, we observed an increase in incidence of vasive support29 in the hospital general wards. This might explain the
patients colonized with Multi Drug resistant (MDR) bacteria (Acineto- higher duration of mechanical ventilation and a longer ICU stay recorded
bacter baumannii, Klebsiella pneumonia and Vancomycin-resistant in our COVID-19 cohort, when compared with a NCOVID-19 popula-
Enterococci -VRE) during the second wave (42% vs. 2% during the first tion, as only the most severe patients were managed invasively. The situ-
wave, X2 = 3.002; p < 0.0001) and a reduction of patients treated ation of the health system in northern Italy, in the two COVID-19 waves,
with veno-venous ECMO (20% first wave vs. 7% second wave; required an “emergency” management due to the high number of
X2 = 0.019; p = 0.019). Despite these two findings, the average NAS patients to be treated. Limiting the ICU admission to patients who
was similar during before and after ICU renovation (82 ± 10 vs.78 required immediate endotracheal intubation could have increased the
± 11, T = 0.703; p = 0.498) for COVID-19 group. Conversely, we nursing workload. Bruyneel and colleagues12 report an average NAS of
observed an increase in mean daily NAS, in NCOVID group after ICU 92.0 ± 16.1in COVID patients, but with only 65% of patients being
renovation (65 ± 14 vs. 69 ± 16, T = 2.540; p = 0.010). mechanical ventilated patients, while Hoogendoorn and colleagues26
After adjusting for confounders, the diagnosis of COVID-19 was reported a median NAS of 55 (45–65) with 83% of patients requiring
independently associated with higher NAS (see Table 4). Other indepen- mechanical ventilation. In our hospitals, we have been using helmet
dent predictors of higher NAS were the use of prone positioning and CPAP for several years to deliver PEEP outside the ICU.31,32 In 2020,
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LUCCHINI ET AL. 9

medical and surgical wards, in few days, were converted to COVID-19 workload in the two groups are also highlighted by the analysis of the
wards, capable of applying noninvasive Helmet-CPAP. The most severe single NAS score items. Nursing activities were significantly higher in
patients were referred to the medical emergency team (MET), composed the COVID-19 group in the following items: monitoring and titration,
by an intensivist, a critical care nurse and a resident. MET managed mobilization and positioning, and hygiene care. The first two items
patients underwent Helmet-CPAP on the hospital floor until intubation reflect the complexity of COVID-19 patients and are strongly linked
was required. ICU admissions in COVID-19 group were all unscheduled, to monitoring activity and prone position procedures. In addition,
but standardization of COVID-19 treatment (ICU admission, rapid intu- COVID-19 patients required a greater use of vasoactive drugs and
bation, prolonged prone position) helped to manage the nursing work- monitoring with a pulmonary artery catheter. According to Padilha
load compared with the first days of March 2020. and colleagues,23 “Hygienic care” item includes special procedures
Prone position was implemented in a large proportion of patients such as barrier nursing, cross-infection related. Additionally, critically
in COVID-19 group (65%). ECMO was used in 10% (n = 15) of ill patients with COVID-19 are at high risk for HAIs, particularly
COVID-19 patients, compared with 3% (n = 13) in the NCOVID group Ventilator-associated pneumonia and bloodstream infections, result-
(X2 = 14.77; p < 0.0001). The increase in the use of respiratory rescue ing from MDR organisms.19 The frequent need for invasive life sup-
therapies (PP and ECMO) is not an unexpected result.14,33 The man- port procedures, comorbidities, the immune suppression associated
agement of persistent severe hypoxemia under VV-ECMO requires a with COVID-19 infection and the use of steroids, increase the risk of
multi-step clinical approach including prone positioning during extra- HAIs.45 In our study, the incidence of patients with MDR infection
34,35
corporeal support, which improves oxygenation. The application was negligible in the first wave, but very frequent in the second one
of PP in mechanically ventilated patients requires efforts and time by (2% vs. 42%, respectively; X2 = 3.002; p < 0.0001), perhaps due to a
36,37
dedicated healthcare personnel, mainly during position changes. greater use of steroid therapy. Despite this increase, the NAS in the
The PP manoeuvre might become demanding and difficult to imple- two waves, in the COVID-19 group, remained essentially unchanged.
ment in an overwhelming condition of a pandemic, coupled with lim- A possible explanation could be found in the renovation of the Inten-
ited resources. Prone positioning of a sedated and mechanically sive Care Unit. Before February 2020, our ICU was an open ICU with
ventilated patient requires a minimum of five experienced people to 5 rooms, but without isolated beds. At the end of the first COVID-19
safely manage lines and airways while turning the patient.18,35,36 Dif- wave the ICU was renovated and during the second wave, COVID-19
ferently from what occurred during first COVID-19 wave, to over- patients were completely managed in 5 isolated rooms (two beds per
come the shortage of staff with intensive care nursing competencies room, see Figure S3). In addition to the normal ICU equipment, each
due to new ICU beds opened, managers enrolled just graduated room was equipped with an access filter, intercom for communica-
nurses. This solution lowered the staff skill mix below the required tions, blood gas analyser and tablet for patients (for video calls with
standards, with potential risks to patients' safety and quality of care. relatives). Every ICU room was equipped with special infrastructure
To guarantee safe PP procedures with at least three experienced for audio and visual communication devices. The new design also
operators (critical care nurses and/or intensivists), we implemented included a special control zone in the clean area (Figure S4 and S5)
the use of extended PP (>24 h) during the second pandemic with telemedicine devices to remotely supervise, communicate, and
wave.38,39 Prolonged prone position was feasible and helped to control the operations in the contaminated zone. The objective was
reduce nursing workload.39 to reduce infection exposure of the staff by having minimal staffing
ECMO implementation in pandemic conditions is possible when inside the contaminated zone, while recognizing the necessary bed-
adequate human and technological resources are available.40 In side care of physicians, nurses, and support personnel for critically ill
COVID-19 patients, ECMO is recommended in a specifical ICU patient patients. During the second wave, ICU staff wore PPE only when
population. Critical care nurses during ECMO are responsible for entering the isolated rooms. Differently from what happened during
patient monitoring, complex hygienic care procedures, mobilization and the first COVID-19 wave, the central area and others ICU zone
monitoring the ECMO device, responding to ECMO pitfalls, while fol- remained accessible without wearing PPE. Isolation procedures, PPE
lowing strict infection prevention and control procedures specific to adoption and PPE management could increase nursing workload.46
COVID-19.41–43 As reported in previous studies, ECMO is an interven- Patient isolation is recommended and used in healthcare institutions,
tion that require an appropriate nurse-to-patient ratio. The ultimate before COVID-19 era, to prevent transmission of MDR. However, its
nurse-to-patient ratio for ECMO patients, should be between 0.75 and risk–benefit ratio was debated. Recently, a metanalysis by Saliba and
1.5.7,44 ELSO suggested that, when centre capacity is lower due to the colleagues,47 showed that no adverse events were related to clinical
COVID-19 surge, there should be a transition to a nurse-to-patient care or patient's experience with patient isolation. In our sample,
ratio of 1:2, with the ECMO specialist overseeing more than one cir- MDR colonization were not independently associated with higher
cuit.14,40,45 This was achieved, during the study period in our ICU, NAS. As discussed in the introduction section, the workload for
cohorting ECMO patients, to optimize infection control and staffing. healthcare providers may further increase in COVID-19 ICU because
The use of prone positioning and continuous renal replacement of the prohibition for family members to enter COVID-19 ICUs.20
therapy, and the diagnosis of COVID-19 were independent predictors Jansen et al.48 suggested that restrictive visitation ICU policies in
of higher NAS. Conversely, ECMO and MDR colonization were not COVID-19 era may have increased psychological distress among
independently associated with higher NAS. Differences in nursing nurses.
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10 LUCCHINI ET AL.

Finally, findings from this study are based on a tool, the Nursing 7 | CONC LU SIONS
Activites Score, that was developed in 2003 as an instrument to cate-
gorize the nursing activities in patient care and the average time con- Our study showed a higher nursing workload during the COVID-19
sumption of those activities.22,23 The NAS only explains 0.59–0.81 of period. This higher workload in COVID-19 patients was mainly due to
the actual nursing time.49 In recent decades, medical and nursing care specific interventions, such as prone positioning and CRRT, with the
has changed and focused mainly to the diagnosis and treatment of related nursing activities, as continuous presence at patient's bed,
acute illnesses. However, basic nursing care remains an essential and mobilization, positioning and complex hygienic procedures. Extended
underestimated factor for patient recovery if compared with intensive prone positioning could be considered in a scenario of a pandemic
care treatments. Furthermore, the weight of each included nursing outbreak to reduce nursing workload. In the context of an experi-
activity might not correspond to the current practice (e.g., decreasing enced ECMO centre, the ECMO support did not result as an indepen-
sedation, delirium monitoring, early mobilization and respiratory/ dent determinant of increased workload. Similarly, MDR colonization
cardiac extracorporeal support, open ICU policies/guidelines and the was not independently associated with higher NAS.
use of new communication technologies).50
Critical care nurses are experiencing a new challenging working AUTHOR CONTRIBU TIONS
17
scenario inside the COVID-19 ICUs. In these setting, they are called Alberto Lucchini: conception, design of the study, Original Draf
to provide the usual high standard care of patients with the additional Writing, Review & Editing, Formal analysis. Marta Villa: Original Draf
problems caused by the PPE, especially for long periods. Changes in Writing, Data Curation, Formal analysis. Arianna Del Sorbo: Original
how the ICU team communicates and the visual and acoustic hin- Draf Writing, Data Curation. Irene Pigato: Original Draf Writing, Data
drances caused by PPE should be monitored for potential increased Curation. Luca D'Andrea: Original Draf Writing, Data Curation. Matteo
risk for adverse events among patients and health care providers.51 Greco: Original Draf Writing, Data Curation. Colombo Chiara: concep-
Therefore, the time dedicated to communication with the patient tion, design of the study, Original Draf Writing, Data Curation. Matteo
increased.21,22 The various weights assigned to each nursing activity Cesana: conception, design of the study, Formal analysis. Roberto
need to be reconsidered and therefore the original NAS score needs Rona: conception, design of the study, Review & Editing. Marco Giani:
to be revise.50 Furthermore, the NAS does not consider the nurse skill conception, design of the study, Review & Editing, Formal analysis.
level, although the education level is an essential element for the qual-
ity of care.52 The set of interventions performed by a novice Regis- AC KNOW LEDG EME NT S
tered Nurse may be very different from those performed by an expert The authors thank Carlotta Spagnoli and Simone Buratto (Drager Medi-
or a certified Critical Care Nurse. Some of the interventions included cal) for their support in data extracting from the INNOVIAN warehouse.
in the NAS tool may be performed only by advanced or expert nurses
(e.g., nursing of ECMO patient) and this could influence the nursing DATA AVAILABILITY STAT EMEN T
time required by patients. Updating the NAS items may be worthy of The datasets generated during and analysed during the current study
attention, especially in light of recent reforms in the composition of are available from the corresponding author on reasonable request.
nursing staff and of technological support helping nurses to position
patients. Moreover, the size of the units (e.g., in terms of beds), their ET HICS S TAT E MENT
structural layout, as well as the visiting policies for relatives, play a sig- Data were collected as part of the “STORM” study (Spallanzani Insti-
nificant role in consuming nursing time. In addition, the NAS is suit- tute approval number 84/2020; NCT04424992) for COVID-19
able for estimating the cost of ICU nursing per stay, a factor that may patients and as a part of “NASINICU” study for NCOVID-19 patients
be of interest to hospital managers.51 (May 15, 2018 – approval number: 877). Due to the observational
nature of the study, the written consent of patients was waived.

6 | L I M I T A T I O NS RE FE RE NCE S
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doi:10.1001/jama.2020.4031
small and heterogenous sample is a significant limitation, especially
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LUCCHINI ET AL. 11

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