Missed Nursing Care in Intensive Care Patients Subjected to Interhospital Capacity Transfers: A Retrospective Matched Case–Control Chart Review

Background The number of patients undergoing an interhospital intensive care unit-to-unit capacity transfer has dramatically increased. These transfers are complex, pose a risk for the patients and have been linked to increased intensive care unit length of stay and mortality, but the reasons for this are not known. We hypothesised that there was a difference in the incidence of missed nursing care among patients subjected to capacity transfer compared with patients not subjected to any transfer during their intensive care stay. A retrospective case–control chart review was conducted on adult patients who between January 1, 2009, and January 31, 2020, underwent an interhospital intensive care unit-to-unit capacity transfer. We applied a matched control group by 1:2 matching. Missed nursing care was based on four variables: mobilisation, tooth brushing, oral care and nutrition. Data were retrieved from the local database and the patient’s medical charts at two general level 3 ICUs. consider missed nursing care when the causes of increased intensive care unit length of stay and mortality are to be investigated.


Background
Over the past decade in Sweden, the number of patients undergoing interhospital intensive care unit-to-unit transfers because of a lack of intensive care resources (capacity transfers), such as beds or health personnel, has increased more than threefold (1), and a similar trend has also been seen internationally (2,3). In situations with a lack of intensive care unit (ICU) capacity, a selection process is carried out with the aim of selecting the patient who is the most stable and suitable for a transfer and who is not expected to be adversely affected by a transfer and care at another ICU. Previous research (4,5) has shown the tendency for interhospital intensive care unit-to-unit capacity transfers may be associated with an increased length of intensive care and hospital stay. In general, interhospital intensive care unit-to-unit transfers are also associated with adverse events that may affect patient safety (6)(7)(8)(9). Regarding mortality, the state of knowledge is more unclear, without a clear consensus (4,5,10,11). Transfers are complex and require clinical skill and efficiency, as well as well-functioning interprofessional collaboration and communication (2,6,12). However, when a decision to transfer a patient is made, there is a risk that the essential nursing activities important for critically ill patients are being missed while focusing solely on the transfer. Proper communication and teamwork have previously been considered important factors in reducing the incidence of missed nursing care (MNC) (13)(14)(15)(16). MNC is known to adversely affect patients' clinical outcomes, such as causing adverse events, 30-day hospital readmission and mortality (16)(17)(18)(19). Research focusing on MNC within an intensive care context-especially in relation to intensive care unit-to-unit transfers-is sparsely illuminated (16,19,20). Therefore, in the current study, we adopted the hypothesis that there was a difference in the incidence of MNC among patients who underwent an interhospital intensive care unit-to-unit capacity transfer compared with patients who did not undergo any interhospital intensive care unit-to-unit transfer during their intensive care stay.

Study design
The current study was based on a retrospective case-control chart review of patients subjected to an interhospital intensive care unit-to-unit capacity transfer. The manuscript was conducted in accordance with the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) statement: Guidelines for Reporting Observational Studies (21).

Setting
The study was conducted in two general level 3 (22,23) ICUs (primary and secondary ICU) in Sweden that were located within the same region and that contained six and seven beds, respectively. The hospitals served a population of almost 325,000 people. Depending on the burden of care in the ICUs, the critical care registered nurse (CCRN) was generally assisted by one or two assistant nurses. Transfers were carried out according to existing guidelines and recommendations, but no dedicated transfer teams existed (24). The ambulances allowed for the necessary equipment for ongoing full intensive care. A CCRN or certified registered nurse anaesthetist (CRNA) was responsible for the patient's care, and in special circumstances, an ICU physician accompanied the nurse.

Definition and characteristics of the cases and controls
We used the hospital's local ICU register to identify the cases and controls and extract validated data that were sent to the Swedish Intensive Care Registry (SIR). Inclusion criteria were adult patients admitted to the primary ICU between January 1, 2009, and January 31, 2020, who, because of lack of ICU resources, underwent a capacity transfer to the secondary ICU. The exclusion criteria were being transferred to another ICU than the secondary ICU; an arrival route to the primary ICU by interhospital transfer from an ICU or a ward at another hospital; having an ICU stay at the primary or secondary ICU for less than 15 hours; and missing or incomplete medical records preventing chart review. The time period was defined by the introduction of 'transfer to another ICU due to lack of resource' as a SIR national quality indicator in the ICUs. The inclusion and exclusion criteria used to determine the case group are shown in Fig. 1. Second, the patients in the control group were selected based on patients at the primary ICU who did not undergo any form of interhospital intensive care unit-to-unit transfer during their intensive care stay. Here, we applied a matched control group by matching two controls to each patient in the case group (1:2 matching). We initiated the matching by selecting patients who had an ICU stay within the same year as the case patient. Then, matching was based on a Fulfilling the inclusion criteria; adult patients admitted to the primary ICU between January 1, 2009, and January 31, 2020, who because of lack of ICU resources, underwent a capacity transfer to the secondary ICU (n=106).
Exclusion: Transferred to another ICU than the secondary ICU (n=17).
Exclusion: Arrival route to the primary ICU by interhospital transfer from an ICU or a ward at another hospital (n=17).

Missed nursing care-definition of measured variables
MNC was based on four variables: mobilisation, tooth brushing, oral care and nutrition, which were collected from the patient's medical chart. All variables were considered significant for the care of critically ill patients (29)(30)(31)(32). According to the ICUs' guidelines, all these variables must be routinely documented in the patient's medical chart. Mobilisation included all forms of documented activities in the form of changes in position, sitting on a bed or in an armchair, bed cycling, standing with walking aids and exercise with a physiotherapist. According to ICU guidelines, tooth brushing should be performed twice a day. Based on the time period for the chart review, we determined the maximum number of tooth brushings the patient could receive.
Oral care includes mouth moisturiser to lips and mucous membranes with a saliva substitute or moistening gel with or without oral chlorhexidine. The variable nutrition was examined based on the patient's prescribed number of kilocalories (kcal) for the day of transfer in relation to the documented number of kcal the patient actually received.

Data collection
First, with the aim of ensuring optimal data collection, we designed a data collection tool (

Statistical analysis
Descriptive data are presented as the mean (SD), median (IQR), ratio and number. Closeness of matching is also presented as percentage. Data were checked for normality, and equality of variances (homogeneity of variance) were verified with a parametric or nonparametric Levene's test (35)(36)(37). Based on either a normal or nonnormal distribution, closeness of matching across the case and control groups and variables for MNC were tested with Mann-Whitney U-tests,

Case and control group characteristics
The median ages of the case and control groups were 73 (65-80) and 72 (65-79), respectively, and within the total cohort, most patients were men. Most of the patients in both the groups had a medical affiliation, followed by surgical, orthopaedic and urological affiliations. Matching was successful in the form of an equal distribution across the case and control groups for age, sex, clinical affiliation, SAPS and EMR. For matching criterion concerning the burden of care, in the form of total burden of care per hour or day and NEMS per day during the ICU stay, no equal distribution across the case and control group was achieved. For all of these criteria, the case group showed a higher burden of care compared with the control group (Table 1).

Discussion
The main finding of the present study was that critically ill patients undergoing interhospital intensive care unit-to-unit capacity transfer between two level 3 ICUs were affected by MNC in the form of less mobilisation and less oral care compared with a matched control group that did not undergo any interhospital intensive care unit-to-unit transfer during their intensive care stay. Although there have been studies (4,5,10,11) focusing on the relationship between interhospital intensive care unit-to-unit transfers and mortality and ICU length of stay, to the best of our knowledge, this is the first study focusing on the possible relationships between transfers and MNC. MNC can adversely affect patient outcomes (16). With today's centralisation of specialised intensive care in combination with the fact that Sweden has among Europe's lowest number of available ICU beds (38,39), the effect of interhospital intensive care unit-to-unit capacity transfers on MNC is an important issue. Physiotherapy together with early active mobilisation have been some of the strategies to prevent the negative effects of critical illness, such as functional consequences, postintensive care syndrome and ICU-acquired weakness (40,41). Delayed mobilisation has previously been linked to longer ICU and hospital lengths of stay (42,43). Therefore, MNC in the form of less mobilisation that may occur during transfers could also be a contributing factor to longer ICU and hospital length of stay, as previously noted among transferred patients (4,5). At the same time, one must be humble to the fact that more research is needed to fully understand the effects of mobilisation on critically ill patients (40,44). One reason for the lack of significant differences for tooth brushing and oral care in the first analysis may be that there were significantly more patients in the control group, n = 7 for the case group and n = 46 for the control group, who were not treated with any form of positive pressure ventilation. We assume that there is more of a focus on tooth brushings and oral care when patients are treated with NIPPV or IPPV. Regardless, in a subanalysis, our study shows that patients who are transferred receive less oral care. Oral care reduces the incidence of developing ventilator-associated pneumonia (VAP) in critically ill patients, which is a potentially serious complication that can affect patients who have received mechanical ventilation (32). In addition, oral care is a basic hygiene requirement and essential component of the care for critically ill patients, which provides comfort and enhances their sense of wellbeing (45,46). Although documentation regarding nutrition was lacking, it is interesting that the amount of missing data was lower in the case group. The possible reasons for this may be that more ICU personnel are involved and actively take responsibility for the prescription of nutrition or that the primary ICU wants to submit documentation in optimal condition. As an incidental finding, this is important because a lack of documentation is associated with poorer quality of care (47). Although the differences were not significant, there were tendencies for patients who were transferred to receive less prescribed nutrition. It has previously been shown that it is difficult to achieve the nutritional goals of critically ill patients (48)(49)(50). We argue that achieving the goals may be further hampered in connection with transfers, so consideration should be given to compensating for this.

Strengths and limitations
Studying the incidence of MNC among patients undergoing an interhospital intensive care unitto-unit capacity transfer was complex and challenging. First, we argue that a retrospective matched case-control chart review was an appropriate method to answer the research question.
However, retrospective chart reviews have the potential for observer bias and systematic error, especially when there is no access to tested and validated instruments for data collection. To minimise this problem, a data collection tool was designed based on a logical flow for the data collection process. In addition, data collection was performed by only one of the authors.

Conclusion
The present study identified a significantly increased incidence of MNC in the form of missed

Declarations Ethics approval and consent to participate
This study was approved by the Regional Ethical Review Board in Sweden (Dnr 507-16).
Because this was a registry and medical record-based study of an observational nature, individual patient consent was waived by the ethical review board.

Consent for publication
Not applicable.

Availability of data and materials
The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Competing interests
The authors declare that they have no competing interests.

Funding
This research did not receive any specific grant from funding agencies in the public, commercial or not-for-profit sectors.

Authors' contributions
All the authors-JK, IF, KS and MH-have substantially and equally contributed to the manuscript, including the design, analysis, interpretation of data, drafting and editing of the final manuscript. All data collection was conducted by JK. All authors read, reviewed and approved the final manuscript.