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Medical device-related pressure injuries: An exploratory descriptive study in an acute tertiary hospital in Australia
Journal of Tissue Viability xxx (2017) 1e8
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Medical device-related pressure injuries: An exploratory descriptive study in an acute tertiary hospital in Australia Michelle Barakat-Johnson a, *, Catherine Barnett b, Timothy Wand c, Kathryn White d a Sydney Nursing School, The University of Sydney and Sydney Local Health District, Patient Safety and Quality, Level 7, KGV, Royal Prince Alfred Hospital, Missenden Road, Camperdown, Australia b Sydney Nursing School, The University of Sydney and Sydney Local Health District, The Cancer Nursing Research Unit, Lifehouse, Missenden Road, Camperdown, Australia c Sydney Nursing School, The University of Sydney and Sydney Local Health District, Emergency Department, Royal Prince Alfred Hospital, Missenden Road, Camperdown, Australia d Sydney Nursing School, The University of Sydney and Sydney Local Health District, The Cancer Nursing Research Unit, Lifehouse, Missenden Road, Camperdown, Australia
a r t i c l e i n f o
a b s t r a c t
Article history: Received 30 November 2016 Received in revised form 22 September 2017 Accepted 29 September 2017
Aim: To examine and explore medical device-related pressure injuries in an 800-bed tertiary hospital. Materials and methods: An exploratory descriptive study design was employed. A prospective review of all data on reported hospital-acquired pressure injuries was conducted on a weekly basis from July 2015 to August 2016. This included a patient assessment and medical record review as well as brief semistructured interviews with nurses. Results: The overall incidence of medical device-related pressure injuries was 27.9% (50/179) with the majority (68%, 34/50) occurring in intensive care. The most common cause of a medical device-related pressure injury was oxygen tubing behind ears (n ¼ 21) and endotracheal tubes (n ¼ 13). Nurses were unaware of the implications of medical devices in contact with the skin and patient medical records did not present a valuable source of information in relation to pressure injury prevention. Conclusion: Medical device-related pressure injuries were represented in 27.9% of our entire patient cohort; primarily occurring on the ear from oxygen tubing and on the mouth from endotracheal tubes in patients in intensive care. Additional support, education and monitoring for nurses at a local level on the prevention of medical device-related pressure injuries is necessary to prevent their occurrence. Furthermore, consensus on the classification and reporting of medical device-related pressure injuries is still in development, making reporting and monitoring challenging. Medical device-related pressure injuries are a continuing clinical issue that require further exploration. © 2017 Published by Elsevier Ltd on behalf of Tissue Viability Society.
Keywords: Medical device Device-related Pressure ulcer Pressure injury Hospital-acquired Exploratory descriptive study
What is already known Hospital-acquired pressure injuries are adverse events that are largely preventable. Medical device-related pressure injuries are a significant clinical problem. Patients who have a medical device are at high risk of developing pressure injuries.
* Corresponding author. E-mail addresses: [email protected] (M. BarakatJohnson), [email protected] (C. Barnett), [email protected] (T. Wand), [email protected] (K. White).
What this manuscript contributes This manuscript contributes to the international literature by identifying issues on the prevention, causes, and reporting of medical device-related pressure injuries. This study provides quantitative and qualitative data which demonstrates that medical device-related pressure injuries remain a significant clinical issue requiring further investigation. Collecting and analysing data on medical device-related pressure injuries will assist in devising strategies and interventions to prevent their occurrence.
https://doi.org/10.1016/j.jtv.2017.09.008 0965-206X/© 2017 Published by Elsevier Ltd on behalf of Tissue Viability Society.
Please cite this article in press as: Barakat-Johnson M, et al., Medical device-related pressure injuries: An exploratory descriptive study in an acute tertiary hospital in Australia, Journal of Tissue Viability (2017), https://doi.org/10.1016/j.jtv.2017.09.008
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M. Barakat-Johnson et al. / Journal of Tissue Viability xxx (2017) 1e8
1. Introduction Hospital-Acquired Pressure Injury (HAPI) is a serious health care complication, with significant implications for the patient and their family [1e3], the clinical setting and organisational funding [4,5]. HAPI contributes to hospital morbidity and mortality [6], yet many are largely preventable with research evidence emphasising preventative strategies [7]. A Pressure injury (PI) is defined as a ‘localised injury to the skin or underlying tissue, usually over a bony prominence or a medical device, resulting from sustained pressure [8].’ They commonly occur on the sacrum, coccyx and heels and are staged according to the National and European Pressure Ulcer Advisory Panel (NPUAP & EPUAP) classification system. Most recently, the NPUAP and EPUAP updated the classification system to include the additional wording “and related to a medical or other device” [8]. Medical Device-Related Pressure Injury (MDRPI) differ from most PIs as they (i) are caused by a device (ii) usually mimic the shape of the device [9] and (iii) can occur in mucosal membranes [8]. MDRPIs are caused by prolonged unrelieved pressure from a medical device and/or the way in which it is secured [10,11]. Additional contributing factors include failure to check under the device [12] and a lack of staff awareness of the risk of PIs. The occlusion of the device on the skin may cause excessive moisture [13] and increase temperature, which impairs microclimate and causes friction. The combination of pressure, friction and impaired microclimate predisposes tissue damage [14]. Failure to check under the device prevents the identification of early warning signs, such as blanchable erythema, which may lead to the development of a stage 1 PI [8,15]. When classifying mucosal PIs, staging may be difficult because of the anatomical location, such as the mucosa, and therefore should only be classified and reported as a mucosal PI [8]. MDRPIs can develop at any anatomical location and at insertion sites for devices. The most common locations reported are the head, face, neck and extremities [9,12]. MDRPIs tend to progress rapidly as they typically occur over areas lacking adipose tissue, where the pressure is constant and microclimate becomes impaired [11]. Importantly, any patient who has a medical device in contact with their skin or mucosa has the potential to develop a PI associated with the device [16]. Preventing MDRPIs can be challenging when the device itself is an essential part of the patient's treatment. Patients who are dependent on medical devices, such as those who are critically ill, have a higher chance of developing a MDRPI due to severity of their condition, duration of the use of the medical device and/or sedation [20]. Patients who are sedated or confused are at higher risk because they are unable to report discomfort or pain associated with the device. The types of medical devices associated with PIs are wideranging and presented in Box 1. Orthopaedic braces and cervical collars [21], catheters, drains and compression stockings have also been shown to cause MDRPIs [13]. Adhesive tapes and cannulas are also associated with MDRPIs, although the rate is higher in neonates due to their fragile skin, environment and inability to move [22e24]. MDRPIs have been reported for many years, however the literature is limited despite the high prevalence and incidence. Prevalence and incidence for MDRPI rates range from 1.7% [9] in adults in medical and surgical units through to 86% in intensive care services (ICS) [25]. MDRPIs are a frequently cited risk in the and neonate population. Incidence rates are as high as 50%, with the most common attributable devices being Continuous Positive Airway Pressure (CPAP), Bilevel Positive Airway Pressure (BI-PAP) and pulse oximeter [26]. Almost one-third of serious PIs are device-
related and are usually not identified until they are at stage 3 or 4, or unable to be staged [12]. This current study is part of a larger study examining reported HAPIs in the Incident Information Management System© (IIMS) (Box 2). Of the 179 confirmed HAPIs, 50 were related to medical devices. It was identified that MDRPI required further exploration. Therefore, the aim of this study was to conduct an examination of MDRPIs in relation to medical device management and PI prevention in order to inform preventative strategies. This included repositioning, off-loading, correct sizing and cleaning under the device. 2. Methods 2.1. Study design Between July 2015 and August 2016 an exploratory descriptive study was conducted on all confirmed MDRPIs. Various steps were then undertaken: (i) a prospective clinical review and patient assessment involving a head-to-toe skin inspection, (ii) a prospective medical record review of PI prevention and treatment strategies, and (iii) brief semi-structured interviews with nurses. Informed verbal consent was obtained from all patients prior to the review. Ethical approval to conduct the study was granted by the local district research ethics review committee (ref: HREC/15/ RPAH/482). 2.2. Setting and sample This study was conducted in an 800-bed urban tertiary referral hospital in Australia comprising of acute and sub-acute care inpatient units and Intensive Care Services (ICS). All hospitalised patients who had a MDRPI over a 13-month period were reviewed (N ¼ 50). Patients were reviewed in different units across the hospital including neurology, cardiothoracic, aged care, paediatric, maternity, as well as ICS which comprises of 48 beds across four units. 2.3. Study procedures 2.3.1. Clinical patient review A prospective patient assessment was conducted on a weekly basis following the collation of all HAPIs reported in IIMS, which was obtained via a computer-generated report. The audit team consisted of two senior wound nurse consultants, a quality patient safety manager and an incident information manager (Box 2). Nurses were consulted prior to patient assessment to understand any relevant medical conditions. Once the patient's verbal consent Box 1 Common Causes of Medical Device-Related Pressure Injury
Oxygen tubing [17] Endotracheal tube (ETT) Nasal prongs Respiratory masks Anti-embolism stockings Saturation probe [9] Continuous Positive Airway Pressure (CPAP) [18] Nasogastric tube (NGT) [19] Ankle band Epistaxis balloon
Please cite this article in press as: Barakat-Johnson M, et al., Medical device-related pressure injuries: An exploratory descriptive study in an acute tertiary hospital in Australia, Journal of Tissue Viability (2017), https://doi.org/10.1016/j.jtv.2017.09.008
M. Barakat-Johnson et al. / Journal of Tissue Viability xxx (2017) 1e8
Box 2 Information on Incident Information Management System and Incident Information Manager
3
preventative strategies for medical devices in contact with the skin were also recorded. In some situations, patients' written consent was obtained to take an image of the skin injury. This was on a separate consent form and recorded in the patient's medical record.
Incident Information Management System© The Incident Information Management System (IIMS) is a statewide initiative from the New South Wales Department of Health that records incidents in public health facilities including pressure injuries for monitoring. All nurses are required to report a pressure injury in IIMS if observed on daily skin inspection. Specific information reported includes the location of the pressure injury, stage, whether it was hospital-acquired and management. All HAPIs are documented in this system are then collated on a monthly basis by the IIMS manager and reported to the clinical units and regulatory bodies as a measure of patient safety. Other examples of similar systems include, Patient Safety Network, Pennsylvania Safety Reporting System [27], Clinical Risk Management [28], National Reporting Learning System [29]. Incident information manager The incident information manager is the custodian of incident data and has associated activities with interpretation, management, operation and support of data. Incident information managers provide support to clinicians with data across the district, organisation and at ward level. Any change in data trends is reported by the incidence information manager to the senior nurse responsible for further investigation. For example, incidents relating to pressure injuries are flagged by the incident manager with the wound care consultant or Patient Safety Manager both at a district level and at the organisational level.
was obtained, the senior wound nurse consultants conducted a patient assessment. The results of the patient assessment were documented. 2.3.2. Review of medical records Medical records were reviewed for documentation of PI prevention and management strategies, particularly relating to the medical device. This included application, rotation and removal of the device, as well as skin assessment. Results were tabled and grouped. 2.3.3. Brief semi-structured interviews with nurses Brief semi-structured interviews with nurses were conducted to explore current practice for patients with medical devices. Participation was voluntary. Nurses were approached and asked about their practice and knowledge on MDRPIs (Box 3). Comments were tabled and content analysis was conducted. In addition, education on MDRPI prevention and management was provided to nurses caring for the patient at the time of assessment. 2.4. Data collection An audit tool was developed by the authors and reviewed for face validity by senior wound nurses. The data elements of the audit tool included the ward, demographic data, such as age and sex, clinical data such as diagnosis and comorbidities, as well as incident data such as the review date, stage and location of PI, and medical device used. Wound assessment, risk assessment and PI
2.5. Data analysis 2.5.1. Prospective patient review and medical records All data on patients identified as having a MDRPI were collated, de-identified and were assigned a study number. All data were imported into Statistical Packages for Social Sciences (SPSS) (Version 22) and grouped for analysis. Data were then crosschecked for accuracy. Simple descriptive statistics was used to analyse and summarise data. In line with the NPUAP/EPUAP classification [8], the dataset was updated to reflect the introduction of the mucosal category in accordance with Australian practice [16]. Traditional categories of stage 1, 2 and 3 were all updated where appropriate to ‘mucosal’.’ 2.5.2. Brief semi structured nurse interviews Content analysis of nurses' responses was conducted to examine and interpret the collected data. Initial descriptive codes were applied to nurses' responses [30]. The first author analysed the data and the co-authors reviewed it. Codes were grouped into three key categories presented in this paper. Data were also entered into SPSS and quantified (Table 4). 3. Results 3.1. MDRPI sample demographics and incidence Almost two-thirds of the sample (n ¼ 38) examined were over 51 years of age. The mean age was 59.1 (SD ¼ 22.0). The median age was 63.0 (IQR: 50e75). Patients were predominantly from ICS. More males developed MDRPIs than females. The proportion of male to female during data collection was considerably higher (37/ 50, 74%) than the admission rate to adult ICS which was 60% male and 40% female. Table 1 provides an overview of the sample demographic characteristics, sex and specialty/unit. The overall incidence of MDRPI was 27.9% (50/179). The majority of MDRPI occurred in patients who were in ICS (68%, 34/50) (Table 3). All oxygen tubing MDRPI occurred in males (Table 2). MDRPIs, as a result of endotracheal tubes (ETT), CPAP and nasal prongs, were higher in males compared to females (Table 2). In the age groupings, the three neonates developed a MDRPI from an ETT, CPAP and ankle band respectively (Table 3). Oxygen tubing (n ¼ 17), followed by ETT (n ¼ 11) were the most common types of medical devices that caused PIs. Other medical devices that increased the risk of PIs included anti-embolism stockings (n ¼ 7), nasogastric tubes (NGT) (n ¼ 4), saturation probes (n ¼ 3), an epistaxis balloon (n ¼ 1) and an ankle band (n ¼ 1) were also reported. Box 3 Questions for nurses caring for the patient with a medical devicerelated pressure injury at time of patient review
1. How do you think this injury was caused? 2. Tell me about the care of the device. Prompt nurses, for example, how often would you off-load or reposition the _____ (state device) 3. What preventative measures are in place?
Please cite this article in press as: Barakat-Johnson M, et al., Medical device-related pressure injuries: An exploratory descriptive study in an acute tertiary hospital in Australia, Journal of Tissue Viability (2017), https://doi.org/10.1016/j.jtv.2017.09.008
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M. Barakat-Johnson et al. / Journal of Tissue Viability xxx (2017) 1e8
“When patients are too ill.......... lifesaving priorities come into play; sometimes repositioning gets overlooked” (P 8,15,16).
3.2. Stage and location of MDRPI There were 20 patients with a mucosal PI (Table 3), making it the most common PI stage associated with a medical device. Most of these patients were reported as stage 2 (n ¼ 17) which was the second most common stage, followed by stage 1 (n ¼ 12). ETTs were the most common cause of mucosal PIs (n ¼ 11, 55%), occurring on the mouth/lip and tongue, followed by NGT (n ¼ 4, 20%), and oxygen tubing (n ¼ 3, 15%) causing nose/nare PIs (Table 3). The most common location for MDRPIs to develop was the ear (n ¼ 16), followed by the nose (n ¼ 12). Thirteen (65%) males and 7 (35%) females had a mucosal PI. 3.3. Interviews with nurses Twenty-one (out of fifty) brief semi-structured face-to-face interviews were conducted with nurses caring for the patient who had a medical device (Appendices 1, 2 and 3). The remaining nurses were either unavailable at time of patient review or the nurse had already been interviewed. In ICS, the nurse-to-patient ratio was 1:1; on the ward, it was 1:4 at the time of the study. Through content analysis, nurses' views relating to three areas emerged: (i) skin assessment under the device, (ii) repositioning of the device, and (iii) device fitting and securing. 3.3.1. Skin assessment under the device Over half of the participants spoke about assessing the skin under the device, including lack of assessment (Table 4). Participants stated that even though skin assessment is maintained for patients at high risk of developing a PI, assessing the skin under a device was not something they would do on a daily basis. This is especially the case with anti-embolism stockings, under oxygen tubing around the ear, NGT and saturation probes. 3.3.2. Repositioning of the device Several (5, 23.8%) participants spoke about the repositioning of the device, or lack of repositioning. Nurses who knew that devices in contact with the skin needed to be rotated or offloaded stated they often forgot to do this, especially in ICS where lifesaving matters were prioritised. One key statement mentioned by several interviewees in the intensive care setting supports this: Table 1 Sample demographics (N ¼ 50).
Sex Male Female Age group Neonate < 21 21-30 31-40 41-50 51-60 61-70 71-80 81-90 > 90 Specialty/Unit Adult and neonate intensive care services Cardiovascular Cardiology Ante/Post-natal Orthopaedics Coronary Care Unit Upper GIT Neurology n: population; %: percentage.
n
%
37 13
74.0 26.0
3 1 2 3 3 8 10 13 6 1
6.0 2.0 4.0 6.0 6.0 16.0 20.0 26.0 12.0 2.0
34 6 4 2 1 1 1 1
68.0 12.0 8.0 4.0 2.0 2.0 2.0 2.0
3.3.3. Device fitting and securing Just under half of the participants spoke either about the tight fitting of medical devices, or use of incorrect sized devices, or the incorrect securing of medical devices. Nurses in this study believed that MDRPIs sustained from a NGT were related to the way in which the securing tape was placed and that MDPRIs related to ETT were caused by ties being secured too tightly. In the case of anti-embolism stockings, when a particular size was unavailable, nurses stated they would choose the next available size (mostly small) for “more compression”. Nurses in this study stated they were unaware that incorrect anti-embolism stocking size could result in a MDRPI. 3.4. Medical record review For all patients who were confirmed as having a MDRPI, documentation in the medical records was inadequate as evidenced by the absence of preventative strategies and monitoring of skin under the device. Skin assessment did not include assessing under a device until a PI had developed. Once a PI developed, nurses documented the PI and treatment required. In addition, nurses only documented that skin was either intact or not. This suggested to the authors that medical records were not a reliable source of information. Interestingly, documentation of treatment was more consistent when compared with documentation on prevention. 4. Discussion Over one quarter of patients who were reviewed for a reported HAPI in this study were confirmed as having developed a MDRPI. The majority of MDRPIs occurred in critically ill patients, primarily men. The most common location was the head, predominantly due to oxygen tubing behind the ears and ETT on the mouth, which were largely mucosal PIs. Additionally, the study highlighted a number of issues around development, processes in clinical practice and prevention of MDRPIs. The majority of MDRPIs occurred in ICS where medical devices are used frequently on patients. Most critically ill patients are at high risk of developing PIs due to compromised skin or tissue perfusion, and lack of movement from either sedation or inability to reposition themselves [31]. These factors, coupled with a device, further increase the risk of developing a MDRPI. Even though skin assessment is performed for patients at risk of developing a PI, most nurses indicated that assessing the skin under a device was not routine practice especially in the case of oxygen tubing and anti-embolism stockings. A high number of the patients (n ¼ 17) in this study developed PIs from oxygen tubing; nurses stated that the tubing behind the ear was not an area they would routinely inspect. The number of PIs caused by anti-embolism stockings in this study was higher than previously reported [11,16]. This is noteworthy given anti-embolism stockings are used regularly on patients who are confined to the bed rendering them at high risk of developing a PI. Anti-embolism stockings are perceived as safe to use; however, care and attention is required for appropriate size selection. Changes in a patient's condition, such as oedema, may alter the fit and produce a tourniquet effect which can lead to a PI. However, this can be prevented if patients are measured and fitted correctly [32]. Regular skin assessment under anti-embolism stockings is key to detecting any skin complications and preventing development of a PI. In this study, it was identified that the documentation related to PI preventative strategies in individual patient medical records was insufficient. On the occasions when skin integrity was mentioned it
Please cite this article in press as: Barakat-Johnson M, et al., Medical device-related pressure injuries: An exploratory descriptive study in an acute tertiary hospital in Australia, Journal of Tissue Viability (2017), https://doi.org/10.1016/j.jtv.2017.09.008
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Table 2 Type of medical device, location, mean age by sex. O2 tubing (location, mean age)
ET tube
Anti-embolism stocking
CPAP
Nasogastric tube
Saturation probe
Nasal prong
Ankle band
Epistaxis balloon
3 (3 nose, M ¼ 36.0)a 1 (1 nose, M ¼ 77.0) 4
2 (2 nose, M ¼ 72.5) 2 (2 nose, M ¼ 45.5) 4
2 (2 forehead, M ¼ 57.0) 1 (1 forehead, M ¼ 76.0) 3
0
17
4 (4 lower leg, M ¼ 67.0) 3 (3 lower leg, M ¼ 38.0) 7
2 (2 ear, M ¼ 72.0) 0
Total
7 (6 mouth/lip, 1 tongue, M ¼ 65.7) 4 (4 mouth/lip, M ¼ 45.5)a 11
0
Female (n ¼ 13)
17 (14 ear, 3 nose, M ¼ 66.7) 0
1 (1 lower leg, M ¼ 0.01)a 1
1 (1 nose, M ¼ 44.0) 1
Male (n ¼ 37)
a
2
There was one neonate patient.
Table 3 Medical device-related pressure injury (MDRPI), stage, and anatomical location (N ¼ 50).
Medical device-related PI Oxygen tubing (tubing, nasal prongs and mask) ETT Anti-embolism stocking NGT CPAP Saturation probe Nasal prong Ankle band Epistaxis balloon Reported stage Mucosal 1 2 3
Frequency (%)
ICS (N ¼ 34)
Non-ICS (N ¼ 16)
Location Ear (N ¼ 16)
Nose/Nare (N ¼ 12)
Mouth/Lip (N ¼ 10)
Lower leg (N ¼ 8)
Forehead (N ¼ 3)
Tongue (N ¼ 1)
17 (34.0)
9 (26.5)
8 (50.0)
14 (87.5)
3 (25.0)
0
0
0
0
11 (22.0) 7 (14.0) 4 (8.0) 4 (8.0) 3 (6.0) 2 (4.0) 1 (2.0) 1 (2.0)
10 (29.4) 4 (11.8) 3 (8.8) 3 (8.8) 2 (5.9) 2 (5.9) 0 1 (2.9)
1 3 1 1 1 0 1 0
(6.2) (18.8) (6.2) (6.2) (6.2)
0 0 0 0 0 2 (12.5) 0 0
0 0 4 (33.3) 4 (33.3) 0 0 0 1 (8.3)
10 (100.0) 0 0 0 0 0 0 0
0 7 (87.5) 0 0 0 0 1 (12.5) 0
0 0 0 0 3 (100.0) 0 0 0
1 (100.0) 0 0 0 0 0 0 0
20 (40.0) 12 (24.0) 17 (34.0) 1 (2.0)
17 (50.0) 7 (20.6) 10 (29.4) 0
3 5 7 1
(18.7) (31.3) (43.8) (6.2)
0 5 (31.2) 10 (62.5) 1 (6.2)
9 (75.0) 2 (16.7) 1 (8.3) 0
10 (100.0) 0 0 0
0 3 (37.5) 5 (62.5) 0
0 2 (66.7) 1 (33.3) 0
1 (100.0) 0 0 0
(6.2)
was only documented as intact or not, with little or no mention of assessment under the device. Current international guidelines recommend that a thorough assessment of the skin under a medical device be performed regularly and documented in the patient's medical record [7]. This includes rotating the device to offload pressure from one single point. In addition, oedema increases the potential for skin breakdown, and frequent skin assessment is required to identify pressure caused from a medical device. Given ICS was the specialty with greatest occurrence of MDRPI, ICS patients are most vulnerable for disruptions in skin integrity. Even though nurses in this study were unaware of the greater implications of not examining the skin under the device or repositioning it, several nurses did state that the way in which a device is secured or fitted such as the tape for NGT or the ties for ETT may cause injury to the skin. In addition to strategies mentioned above to reduce the development of MDRPI, the technique of applying and securing a device should also be considered in any education plan to reduce MDRPI. The high number of MDPRIs in the present study is comparable with other studies. Black and colleagues [9] reported a 34.5% prevalence of MDRPI occurring mainly in ICS. Apold and Rydrych [12] found that nearly a third (29%) of reported PIs in their study were caused by medical devices. In this study, MDRPI most frequently occurred on the ears, similar to Black et al. [9] and Van Gilder et al. [33], mainly due to respiratory equipment as well as on the mouth. This is also comparable to the study by Hanonu and Karadag [34] where 45% of MDRPIs occurred in patients with an
Table 4 Nurse responses regarding devices (N ¼ 21). Frequency (%) Expressed that sizing or fitting was a problem Spoke about repositioning of the device (including lack of) Spoke about skin assessments (including lack of)
10 (47.6) 5 (23.8) 11 (52.4)
ETT. Nurses in this study reported that the way ETTs or tracheostomy tubes were secured determined whether or not a patient developed a PI, especially if they were tied too tightly. We found that the majority that the majority of mucosal PIs occurred in patients in the ICS. The high number of mucosal PIs is in line with Coyer et al.’s findings [16] where half of the MDRPIs were mucosal PIs in ICS patients with ETTs or NGTs. Although mucosal classification is still emergent [8] and under discussion in Australia [35], this data indicates that increased clinician awareness on the classification, prevention and management of mucosal PIs is necessary. Inclusion of assessment of the mucosa should be incorporated in the minimal standard care and operating procedures for patients who have an ETT or NGT. The rate of MDRPIs in the neonatal population in our study was low (3/50 and 0.0000378. per occupied bed days) compared with previous studies [24,25]. This finding is encouraging given studies [24,25,36] have found neonatal patients are at high risk of developing MDRPI. Prior to the commencement of this study, staff in the neonatal ICS in this study have had an active focus on the prevention of PIs, such as purchasing appropriate equipment and championing efforts to prevent MDRPIs. Recent consensus in the NPAUP consensus statement highlight the updated reporting and classification of MDRPIs [8]. International guidelines suggest that MDRPIs occurring on the skin should be staged as a PI. If the MDRPI is found on the mucous membranes, these injuries cannot be staged using the current PI [7] staging system and should be reported as a mucosal PI. Classifying and reporting at facility, local or statewide level of MDRPI is still emerging. The IIMS currently records incidents in the state-wide database using the previous NPUAP/EPUAP classification system [7]. Therefore, correctly recording and reporting of MDRPI poses a challenge especially for monitoring, quality improvement and benchmarking activities. Given the results of this study, it is suggested that further efforts be made at a statewide level to develop
Please cite this article in press as: Barakat-Johnson M, et al., Medical device-related pressure injuries: An exploratory descriptive study in an acute tertiary hospital in Australia, Journal of Tissue Viability (2017), https://doi.org/10.1016/j.jtv.2017.09.008
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M. Barakat-Johnson et al. / Journal of Tissue Viability xxx (2017) 1e8
consensus on reporting practices in line with the updated NPUAP [8] classification system. Medical devices have been recognised for many years as causing PIs, with a handful of studies highlighting it as a pertinent clinical issue; nevertheless, the emphasis has continued to remain on PIs that develop from immobility. This study site has concentrated largely on preventative interventions and monitoring of high-risk patients prone to PIs due to immobility in areas of bony prominences. PIs that develop under a device may be easily missed. It is only within the past 5e10 years, internationally, that there has been an emphasis on preventing their occurrence [9e11,37]. Our study has fundamentally raised awareness of MDRPI development at a local level. The importance of implementing preventative strategies targeted specifically at medical devices has been highlighted. Several interventions at the study site commenced after the study results were disseminated. Interventions include identifying devices that can cause pressure injuries, the use of prophylactic dressings under devices, adjusting the way in which a device is secured, frequent repositioning of the device and skin assessment. However, there is still significant work to be carried out to facilitate the prevention of pressure injuries related to medical devices.
implications when devices are incorrectly fitted. The findings from this study add to the literature and confirm previous studies suggesting that MDRPIs are a continuing clinical issue. Preventative PI care of patients with medical devices needs to be included in hospital education campaigns. Research into areas of prevention, primarily intervention strategies, will further inform and assist in the development of programs aimed at reducing MDRPIs. Conflicts of interest Nil to declare. Author contributions Study design MBJ, TW and KW. MBJ and CB undertook primary data collection. All authors were involved in data analysis and interpretation of findings. MBJ prepared the original draft and revised it critically based on comments from co-authors. CB, TW and KW all reviewed the manuscript for final approval to be submitted. The authors report no competing interests. Funding
5. Limitations This present study has important limitations. Patient-related factors which may influence the development of MDRPIs were not investigated. There were also limitations in the availability of certain clinical variables in the dataset, including information on patient comorbidities and diagnosis, as well as patients unavailable for review. Another limitation was the time between the date the incident was reported and the date it was assessed by the audit team. Since the audit team assessed all incidents on the same day of each week, occasionally, there was a three to five-day gap after the incident had been reported. This could have led to inaccurate assessment. 6. Conclusion Findings from this study of MDRPIs were similar to previous studies with the highest incidence occurring in ICS, primarily on the ear from oxygen tubing and on the mouth from ETTs. Antiembolism stockings were of concern, contributing to a higher number of PIs than reported in the literature. Nurses were not aware of preventative strategies for MDRPIs or the significant
The lead author is the recipient of a Clinical Researcher Scholarship by Sydney Research, which in part, supported this study and the preparation of this article. Acknowledgements We are most grateful to the patients and nurses who participated in this study. We thank the District Director of Nursing of the Sydney Local Health District, as well as the Executive of Royal Prince Alfred Hospital for their support of this study. In particular, we wish to thank Thomas Leong, Deborah Wolak and Cassandra Chan who contributed to data collection. Finally, we would like to thank Michelle Lai for her tremendous assistance with statistical analysis and review of this article. Appendix 1. Responses of nurses caring for the patient at time of review on what they thought the injury was caused by (N ¼ 21)
Question
Participant
Role
Response
How do you think this injury was caused?
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21
RN RN RN RN CNS RN RN RN CNS RN RN RN RN RN RN RN CNS RN RN RN RN
From the tightness of the NGT and ETT Pressure and not looking under Pressure The pressure and friction Pressure TEDS [compression stockings] Pressure and heat The tube The ETT sometimes is secured too tightly that’s what causes the pressure It’s the compression around the legs especially if they [compression stockings] roll down Pressure, friction Because they are very unwell, checking under the device is not a priority… and it’s the tape as well and how it is secured It’s the tape sometimes that can be an irritant and also cause pressure It’s the [ETT] ties that cause the pressure Pressure and fiction The tube and pressure The [ETT] ties might be too tight I think sometimes people tie ETT too tightly Pressure and friction The tubing that could cause the pressure Nasogastric tubes are hard because the damage could be done just by the insertion
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M. Barakat-Johnson et al. / Journal of Tissue Viability xxx (2017) 1e8
7
Appendix 2. Responses of nurses caring for the patient at time of review on the care of the device (N ¼ 17)
Question
Participant Role Response
Tell me about the 1 care of the device. 2
RN RN
3
RN
4 5
RN CNS
6
RN
7 8
RN RN
9 10 11
RN RN RN
13 15
RN RN
16
RN
17
CNS
19 20
RN RN
We don’t really check under the device unless we think it is too tight When the ETT ties are changed that’s when we look under it. Should be fitted correctly…usually pressure from the device causes it We usually just grab a size on the shelf, didn’t realize how important the sizing is and if it’s too tight it will cause this pressure behind the leg It’s not the sizing so much but it’s checking…checking behind the ears is not something we would do They should check under patient’s skin regularly and under device daily but with ETT it’s hard because you don’t want to shift them Check should be daily, after shower but not sure how vigilant this is…I didn’t realize that the TEDS could be so damaging, we opt for a smaller size if the other size is unavailable for more compression We try and shift the saturation probe but not everyone does, definitely pressure from the saturation probe causes the injury Check under nasogastric tube? Definitely not…when patients are too ill, lifesaving priorities come into play sometimes repositioning gets overlooked We check under it when the ties are changed If we don’t have the [compression stocking] size we usually either go up or down a size We try and rotate the device when we go to reposition, sometimes it doesn’t happen because there are other things going on but I also think it’s sizing. If it’s not fitted correctly it’s a problem The way it is secured and with saturation probes they are just stuck on Repositioning is not often as we need to, it’s hard because these patients are very sick and we have other lifesaving priorities… Definitely it would heal if we could put a dressing under the tube to prevent the pressure and friction Check under nasogastric tube…we don’t think about that. Repositioning of device gets overlooked because all the other lifesaving priorities going on...It’s hard when they are on inotropes and you can’t move them, there are lifesaving priorities… you don’t think of the device really We always try to assess underneath and rotate the ETT, we are usually vigilant with skin assessment but I am not sure everyone does Sometimes we rotate them and look at the skin when we change the tapes No, we don’t check often around the ear
Appendix 3. Responses of nurses caring for the patient at time of review on what preventative measures were in place (N ¼ 11)
Question
Participant
Role
Response
What preventative measures are in place?
1 4 5
RN RN CNS
6
RN
8 10 13 15 16 17 18
RN RN RN RN RN CNS RN
Skin assessment daily, we try and rotate it at least once a shift We try and use those comfy ears but even that slips off We are trialing the new silicone gel pads under devices but they don’t tend to stay in place as well as we would have liked them to Some nurses keep them [compression stockings] on and wrap plastic bag around to shower… we will have to include that in our education It’s the pressure from the tube…they are looking at a new way to secure the tube We should check more often but we don’t We have been educating the nurses on rotating the area at least daily or each shift We are trying the silicone pads but they don’t really stay in place Skin assessment every chance we get, they are looking at a new way to secure the [nasogastric] tube, this might help We have been educating the nurses this week, it’s been a problem, we are looking into dressings like the silicone pads We are looking at other ways to prevent the ETT pressure injury
References [1] Essex HN, Clark M, Sims J, Warriner A, Cullum N. Health-related quality of life in hospital inpatients with pressure ulceration: assessment using generic health-related quality of life measures. Wound Repair Regen Off Publ Wound Heal Soc Eur Tissue Repair Soc 2009;17(6):797. [2] Gorecki C, et al. Impact of pressure ulcers on quality of life in older patients: a systematic review: clinical investigations. J Am Geriatrics Soc 2009;57(7): 1175e83. [3] Spilsbury K, Nelson A, Cullum N, Iglesias C, Nixon J, Mason S. Pressure ulcers and their treatment and effects on quality of life: hospital inpatient perspectives. J Adv Nurs 2007;57(5):494e504. [4] Dealey C, Posnett J, Walker A. The cost of pressure ulcers in the United Kingdom. J Wound Care 2012;21(6):261e2. 264, 266. [5] Nguyen KH, Chaboyer W, Whitty JA. Pressure injury in Australian public hospitals: a cost-of-illness study. Aust Health Rev 2015;39(3):329e36. [6] Manzano F, et al. Hospital-acquired pressure ulcers and risk of hospital mortality in intensive care patients on mechanical ventilation. J Eval Clin Pract
2014;20(4):362e8. [7] National Pressure Ulcer Advisory Panel European Pressure Ulcer Advisory Panel and Pan Pacific Pressure Injury Alliance. Prevention and treatment of pressure ulcers: clinical practice guideline. second ed. Cambridge Media on behalf of National Pressure Ulcer Advisory Panel, European Pressure Ulcer Advisory Panel and Pan Pacific Pressure Injury Alliance; 2014. [8] The National Pressure Ulcer Advisory Panel. National Pressure Ulcer Advisory Panel (NPUAP) announces a change in terminology from pressure ulcer to pressure injury and updates the stages of pressure injury. 2016 [press release]. [9] Black JM, Cuddigan JE, Walko MA, Didier LA, Lander MJ, Kelpe MR. Medical device related pressure ulcers in hospitalized patients. Int Wound J 2010;7(5): 358e65. [10] Ambutas S, Staffileno BA, Fogg L. Reducing nasal pressure ulcers with an alternative taping device. Medsurg Nurs: Off J Acad Med Surg Nurses 2014;23(2):96. [11] Black J, et al. Use of wound dressings to enhance prevention of pressure ulcers caused by medical devices: MDR ulcers. Int Wound J 2015;12(3):322e7. [12] Apold J, Rydrych D. Preventing device-related pressure ulcers: using data to guide statewide change. J Nurs Care Qual 2012;27(1):28e34.
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[13] Holden-Mount SS,M. Medical device- related pressure ulcers: pediatrics & adults. 2013. National Pressure Ulcer Advisory Panel. [14] Bhattacharya S, Mishra RK. Pressure ulcers: current understanding and newer modalities of treatment. Indian J plastic Surg Off Publ Assoc Plastic Surg India 2015;48(1):4e16. [15] Coleman S, et al. Patient risk factors for pressure ulcer development: systematic review. Int J Nurs Stud 2013;50(7):974e1003. [16] Coyer FM, Stotts NA, Blackman VS. A prospective window into medical devicerelated pressure ulcers in intensive care. Int Wound J 2014;11(6):656e64. [17] Turjanica MA, Clark L, Martini C, Miller P, Turner BL, Jones S. Incidence, correlates, and interventions used for pressure ulcers of the ear. Medsurg Nurs Off J Acad Medical-Surgical Nurses 2011;20(5):241. [18] Rathore FA, Ahmad F, Zahoor MUU. Case report of a pressure ulcer occurring over the nasal bridge due to a non-invasive ventilation facial mask. Cureus 2016;8(10):1e4. [19] Seyedhejazi M, Hamidi M, Sheikhzadeh D, Aliakbari Sharabiani B. Nasogastric tube placement errors and complications in pediatric intensive care unit: a case report. J Cardiovasc Thorac Res 2011;3(4):133e4. [20] Makic MBF. Medical device-related pressure ulcers and intensive care patients. J Perianesthesia Nurs Off J Am Soc PeriAnesthesia Nurses/Am Soc PeriAnesthesia Nurses 2015;30(4):336e7. [21] Powers J, Daniels D, McGuire C, Hilbish C. The incidence of skin breakdown associated with use of cervical collars. J Trauma Nurs Off J Soc Trauma Nurses 2006;13(4):198. [22] Black JM, et al. Pressure ulcers: avoidable or unavoidable? Results of the national pressure ulcer advisory Panel consensus conference. Ostomy Wound Manage 2011;57(2):24e37. [23] Scheans P. Neonatal pressure ulcer prevention. Neonatal Netw 2015;34(2): 126. [24] Visscher M, Taylor T. Pressure ulcers in the hospitalized neonate: rates and risk factors. Sci Rep 2014;4:7429. [25] Fujii K, Sugama J, Okuwa M, Sanada H, Mizokami Y. Incidence and risk factors of pressure ulcers in seven neonatal intensive care units in Japan: a multisite
prospective cohort study. Int Wound J 2010;7(5):323e8. [26] Curley MAQ, Quigley SM, Lin M. Pressure ulcers in pediatric intensive care: incidence and associated factors. Pediatr Crit Care Med 2003;4(3):284e90. [27] Pham JC, Girard T, Pronovost PJ. What to do with healthcare incident reporting systems. J Public Health Res 2013;2(3). 27-e27. [28] Victoria Health. Victorian health incident management system. In: V. Health, editor. Rural and regional health and aged care service division. Melbourne, Victoria, Australia: Victorian Government Department of Human Services; 2017. [29] NHS Improvement. The national reporting and learning system. 2016. [30] Hsieh H-F, Shannon SE. Three approaches to qualitative content analysis. Qual Health Res 2005;15(9):1277e88. [31] Alderden J, Rondinelli J, Pepper G, Cummins M, Whitney J. Risk factors for pressure injuries among critical care patients: a systematic review. Int J Nurs Stud 2017;71:97e114. [32] Lim CS, Davies AH. Graduated compression stockings. Can Med Assoc J 2014;186(10):391e8. [33] VanGilder C, Amlung S, Harrison P, Meyer S. Results of the 2008-2009 international pressure ulcer prevalence survey and a 3-year, acute care, unitspecific analysis. Ostomy Wound Manag 2009;55(11):39e45. [34] Hanonu S, Karadag A. A prospective, descriptive study to determine the rate and characteristics of and risk factors for the development of medical devicerelated pressure ulcers in intensive care units. Ostomy Wound Manag 2016;62(2):12e22. [35] Wounds Australia, NPUAP revised pressure injury definitions released on 14 May 2016. [36] Schluer AB, Halfens RJ, Schols JM. Pediatric pressure ulcer prevalence: a multicenter, cross-sectional, point prevalence study in Switzerland. Ostomy Wound Manag 2012;58(7):18e31. [37] Tayyib N, Coyer F, Lewis PA. A two-arm cluster randomized control trial to determine the effectiveness of a pressure ulcer prevention bundle for critically ill patients. J Nurs Scholarsh 2015;47(3):237e47.
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Contents lists available at ScienceDirect
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Medical device-related pressure injuries: An exploratory descriptive study in an acute tertiary hospital in Australia Michelle Barakat-Johnson a, *, Catherine Barnett b, Timothy Wand c, Kathryn White d a Sydney Nursing School, The University of Sydney and Sydney Local Health District, Patient Safety and Quality, Level 7, KGV, Royal Prince Alfred Hospital, Missenden Road, Camperdown, Australia b Sydney Nursing School, The University of Sydney and Sydney Local Health District, The Cancer Nursing Research Unit, Lifehouse, Missenden Road, Camperdown, Australia c Sydney Nursing School, The University of Sydney and Sydney Local Health District, Emergency Department, Royal Prince Alfred Hospital, Missenden Road, Camperdown, Australia d Sydney Nursing School, The University of Sydney and Sydney Local Health District, The Cancer Nursing Research Unit, Lifehouse, Missenden Road, Camperdown, Australia
a r t i c l e i n f o
a b s t r a c t
Article history: Received 30 November 2016 Received in revised form 22 September 2017 Accepted 29 September 2017
Aim: To examine and explore medical device-related pressure injuries in an 800-bed tertiary hospital. Materials and methods: An exploratory descriptive study design was employed. A prospective review of all data on reported hospital-acquired pressure injuries was conducted on a weekly basis from July 2015 to August 2016. This included a patient assessment and medical record review as well as brief semistructured interviews with nurses. Results: The overall incidence of medical device-related pressure injuries was 27.9% (50/179) with the majority (68%, 34/50) occurring in intensive care. The most common cause of a medical device-related pressure injury was oxygen tubing behind ears (n ¼ 21) and endotracheal tubes (n ¼ 13). Nurses were unaware of the implications of medical devices in contact with the skin and patient medical records did not present a valuable source of information in relation to pressure injury prevention. Conclusion: Medical device-related pressure injuries were represented in 27.9% of our entire patient cohort; primarily occurring on the ear from oxygen tubing and on the mouth from endotracheal tubes in patients in intensive care. Additional support, education and monitoring for nurses at a local level on the prevention of medical device-related pressure injuries is necessary to prevent their occurrence. Furthermore, consensus on the classification and reporting of medical device-related pressure injuries is still in development, making reporting and monitoring challenging. Medical device-related pressure injuries are a continuing clinical issue that require further exploration. © 2017 Published by Elsevier Ltd on behalf of Tissue Viability Society.
Keywords: Medical device Device-related Pressure ulcer Pressure injury Hospital-acquired Exploratory descriptive study
What is already known Hospital-acquired pressure injuries are adverse events that are largely preventable. Medical device-related pressure injuries are a significant clinical problem. Patients who have a medical device are at high risk of developing pressure injuries.
* Corresponding author. E-mail addresses: [email protected] (M. BarakatJohnson), [email protected] (C. Barnett), [email protected] (T. Wand), [email protected] (K. White).
What this manuscript contributes This manuscript contributes to the international literature by identifying issues on the prevention, causes, and reporting of medical device-related pressure injuries. This study provides quantitative and qualitative data which demonstrates that medical device-related pressure injuries remain a significant clinical issue requiring further investigation. Collecting and analysing data on medical device-related pressure injuries will assist in devising strategies and interventions to prevent their occurrence.
https://doi.org/10.1016/j.jtv.2017.09.008 0965-206X/© 2017 Published by Elsevier Ltd on behalf of Tissue Viability Society.
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M. Barakat-Johnson et al. / Journal of Tissue Viability xxx (2017) 1e8
1. Introduction Hospital-Acquired Pressure Injury (HAPI) is a serious health care complication, with significant implications for the patient and their family [1e3], the clinical setting and organisational funding [4,5]. HAPI contributes to hospital morbidity and mortality [6], yet many are largely preventable with research evidence emphasising preventative strategies [7]. A Pressure injury (PI) is defined as a ‘localised injury to the skin or underlying tissue, usually over a bony prominence or a medical device, resulting from sustained pressure [8].’ They commonly occur on the sacrum, coccyx and heels and are staged according to the National and European Pressure Ulcer Advisory Panel (NPUAP & EPUAP) classification system. Most recently, the NPUAP and EPUAP updated the classification system to include the additional wording “and related to a medical or other device” [8]. Medical Device-Related Pressure Injury (MDRPI) differ from most PIs as they (i) are caused by a device (ii) usually mimic the shape of the device [9] and (iii) can occur in mucosal membranes [8]. MDRPIs are caused by prolonged unrelieved pressure from a medical device and/or the way in which it is secured [10,11]. Additional contributing factors include failure to check under the device [12] and a lack of staff awareness of the risk of PIs. The occlusion of the device on the skin may cause excessive moisture [13] and increase temperature, which impairs microclimate and causes friction. The combination of pressure, friction and impaired microclimate predisposes tissue damage [14]. Failure to check under the device prevents the identification of early warning signs, such as blanchable erythema, which may lead to the development of a stage 1 PI [8,15]. When classifying mucosal PIs, staging may be difficult because of the anatomical location, such as the mucosa, and therefore should only be classified and reported as a mucosal PI [8]. MDRPIs can develop at any anatomical location and at insertion sites for devices. The most common locations reported are the head, face, neck and extremities [9,12]. MDRPIs tend to progress rapidly as they typically occur over areas lacking adipose tissue, where the pressure is constant and microclimate becomes impaired [11]. Importantly, any patient who has a medical device in contact with their skin or mucosa has the potential to develop a PI associated with the device [16]. Preventing MDRPIs can be challenging when the device itself is an essential part of the patient's treatment. Patients who are dependent on medical devices, such as those who are critically ill, have a higher chance of developing a MDRPI due to severity of their condition, duration of the use of the medical device and/or sedation [20]. Patients who are sedated or confused are at higher risk because they are unable to report discomfort or pain associated with the device. The types of medical devices associated with PIs are wideranging and presented in Box 1. Orthopaedic braces and cervical collars [21], catheters, drains and compression stockings have also been shown to cause MDRPIs [13]. Adhesive tapes and cannulas are also associated with MDRPIs, although the rate is higher in neonates due to their fragile skin, environment and inability to move [22e24]. MDRPIs have been reported for many years, however the literature is limited despite the high prevalence and incidence. Prevalence and incidence for MDRPI rates range from 1.7% [9] in adults in medical and surgical units through to 86% in intensive care services (ICS) [25]. MDRPIs are a frequently cited risk in the and neonate population. Incidence rates are as high as 50%, with the most common attributable devices being Continuous Positive Airway Pressure (CPAP), Bilevel Positive Airway Pressure (BI-PAP) and pulse oximeter [26]. Almost one-third of serious PIs are device-
related and are usually not identified until they are at stage 3 or 4, or unable to be staged [12]. This current study is part of a larger study examining reported HAPIs in the Incident Information Management System© (IIMS) (Box 2). Of the 179 confirmed HAPIs, 50 were related to medical devices. It was identified that MDRPI required further exploration. Therefore, the aim of this study was to conduct an examination of MDRPIs in relation to medical device management and PI prevention in order to inform preventative strategies. This included repositioning, off-loading, correct sizing and cleaning under the device. 2. Methods 2.1. Study design Between July 2015 and August 2016 an exploratory descriptive study was conducted on all confirmed MDRPIs. Various steps were then undertaken: (i) a prospective clinical review and patient assessment involving a head-to-toe skin inspection, (ii) a prospective medical record review of PI prevention and treatment strategies, and (iii) brief semi-structured interviews with nurses. Informed verbal consent was obtained from all patients prior to the review. Ethical approval to conduct the study was granted by the local district research ethics review committee (ref: HREC/15/ RPAH/482). 2.2. Setting and sample This study was conducted in an 800-bed urban tertiary referral hospital in Australia comprising of acute and sub-acute care inpatient units and Intensive Care Services (ICS). All hospitalised patients who had a MDRPI over a 13-month period were reviewed (N ¼ 50). Patients were reviewed in different units across the hospital including neurology, cardiothoracic, aged care, paediatric, maternity, as well as ICS which comprises of 48 beds across four units. 2.3. Study procedures 2.3.1. Clinical patient review A prospective patient assessment was conducted on a weekly basis following the collation of all HAPIs reported in IIMS, which was obtained via a computer-generated report. The audit team consisted of two senior wound nurse consultants, a quality patient safety manager and an incident information manager (Box 2). Nurses were consulted prior to patient assessment to understand any relevant medical conditions. Once the patient's verbal consent Box 1 Common Causes of Medical Device-Related Pressure Injury
Oxygen tubing [17] Endotracheal tube (ETT) Nasal prongs Respiratory masks Anti-embolism stockings Saturation probe [9] Continuous Positive Airway Pressure (CPAP) [18] Nasogastric tube (NGT) [19] Ankle band Epistaxis balloon
Please cite this article in press as: Barakat-Johnson M, et al., Medical device-related pressure injuries: An exploratory descriptive study in an acute tertiary hospital in Australia, Journal of Tissue Viability (2017), https://doi.org/10.1016/j.jtv.2017.09.008
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Box 2 Information on Incident Information Management System and Incident Information Manager
3
preventative strategies for medical devices in contact with the skin were also recorded. In some situations, patients' written consent was obtained to take an image of the skin injury. This was on a separate consent form and recorded in the patient's medical record.
Incident Information Management System© The Incident Information Management System (IIMS) is a statewide initiative from the New South Wales Department of Health that records incidents in public health facilities including pressure injuries for monitoring. All nurses are required to report a pressure injury in IIMS if observed on daily skin inspection. Specific information reported includes the location of the pressure injury, stage, whether it was hospital-acquired and management. All HAPIs are documented in this system are then collated on a monthly basis by the IIMS manager and reported to the clinical units and regulatory bodies as a measure of patient safety. Other examples of similar systems include, Patient Safety Network, Pennsylvania Safety Reporting System [27], Clinical Risk Management [28], National Reporting Learning System [29]. Incident information manager The incident information manager is the custodian of incident data and has associated activities with interpretation, management, operation and support of data. Incident information managers provide support to clinicians with data across the district, organisation and at ward level. Any change in data trends is reported by the incidence information manager to the senior nurse responsible for further investigation. For example, incidents relating to pressure injuries are flagged by the incident manager with the wound care consultant or Patient Safety Manager both at a district level and at the organisational level.
was obtained, the senior wound nurse consultants conducted a patient assessment. The results of the patient assessment were documented. 2.3.2. Review of medical records Medical records were reviewed for documentation of PI prevention and management strategies, particularly relating to the medical device. This included application, rotation and removal of the device, as well as skin assessment. Results were tabled and grouped. 2.3.3. Brief semi-structured interviews with nurses Brief semi-structured interviews with nurses were conducted to explore current practice for patients with medical devices. Participation was voluntary. Nurses were approached and asked about their practice and knowledge on MDRPIs (Box 3). Comments were tabled and content analysis was conducted. In addition, education on MDRPI prevention and management was provided to nurses caring for the patient at the time of assessment. 2.4. Data collection An audit tool was developed by the authors and reviewed for face validity by senior wound nurses. The data elements of the audit tool included the ward, demographic data, such as age and sex, clinical data such as diagnosis and comorbidities, as well as incident data such as the review date, stage and location of PI, and medical device used. Wound assessment, risk assessment and PI
2.5. Data analysis 2.5.1. Prospective patient review and medical records All data on patients identified as having a MDRPI were collated, de-identified and were assigned a study number. All data were imported into Statistical Packages for Social Sciences (SPSS) (Version 22) and grouped for analysis. Data were then crosschecked for accuracy. Simple descriptive statistics was used to analyse and summarise data. In line with the NPUAP/EPUAP classification [8], the dataset was updated to reflect the introduction of the mucosal category in accordance with Australian practice [16]. Traditional categories of stage 1, 2 and 3 were all updated where appropriate to ‘mucosal’.’ 2.5.2. Brief semi structured nurse interviews Content analysis of nurses' responses was conducted to examine and interpret the collected data. Initial descriptive codes were applied to nurses' responses [30]. The first author analysed the data and the co-authors reviewed it. Codes were grouped into three key categories presented in this paper. Data were also entered into SPSS and quantified (Table 4). 3. Results 3.1. MDRPI sample demographics and incidence Almost two-thirds of the sample (n ¼ 38) examined were over 51 years of age. The mean age was 59.1 (SD ¼ 22.0). The median age was 63.0 (IQR: 50e75). Patients were predominantly from ICS. More males developed MDRPIs than females. The proportion of male to female during data collection was considerably higher (37/ 50, 74%) than the admission rate to adult ICS which was 60% male and 40% female. Table 1 provides an overview of the sample demographic characteristics, sex and specialty/unit. The overall incidence of MDRPI was 27.9% (50/179). The majority of MDRPI occurred in patients who were in ICS (68%, 34/50) (Table 3). All oxygen tubing MDRPI occurred in males (Table 2). MDRPIs, as a result of endotracheal tubes (ETT), CPAP and nasal prongs, were higher in males compared to females (Table 2). In the age groupings, the three neonates developed a MDRPI from an ETT, CPAP and ankle band respectively (Table 3). Oxygen tubing (n ¼ 17), followed by ETT (n ¼ 11) were the most common types of medical devices that caused PIs. Other medical devices that increased the risk of PIs included anti-embolism stockings (n ¼ 7), nasogastric tubes (NGT) (n ¼ 4), saturation probes (n ¼ 3), an epistaxis balloon (n ¼ 1) and an ankle band (n ¼ 1) were also reported. Box 3 Questions for nurses caring for the patient with a medical devicerelated pressure injury at time of patient review
1. How do you think this injury was caused? 2. Tell me about the care of the device. Prompt nurses, for example, how often would you off-load or reposition the _____ (state device) 3. What preventative measures are in place?
Please cite this article in press as: Barakat-Johnson M, et al., Medical device-related pressure injuries: An exploratory descriptive study in an acute tertiary hospital in Australia, Journal of Tissue Viability (2017), https://doi.org/10.1016/j.jtv.2017.09.008
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“When patients are too ill.......... lifesaving priorities come into play; sometimes repositioning gets overlooked” (P 8,15,16).
3.2. Stage and location of MDRPI There were 20 patients with a mucosal PI (Table 3), making it the most common PI stage associated with a medical device. Most of these patients were reported as stage 2 (n ¼ 17) which was the second most common stage, followed by stage 1 (n ¼ 12). ETTs were the most common cause of mucosal PIs (n ¼ 11, 55%), occurring on the mouth/lip and tongue, followed by NGT (n ¼ 4, 20%), and oxygen tubing (n ¼ 3, 15%) causing nose/nare PIs (Table 3). The most common location for MDRPIs to develop was the ear (n ¼ 16), followed by the nose (n ¼ 12). Thirteen (65%) males and 7 (35%) females had a mucosal PI. 3.3. Interviews with nurses Twenty-one (out of fifty) brief semi-structured face-to-face interviews were conducted with nurses caring for the patient who had a medical device (Appendices 1, 2 and 3). The remaining nurses were either unavailable at time of patient review or the nurse had already been interviewed. In ICS, the nurse-to-patient ratio was 1:1; on the ward, it was 1:4 at the time of the study. Through content analysis, nurses' views relating to three areas emerged: (i) skin assessment under the device, (ii) repositioning of the device, and (iii) device fitting and securing. 3.3.1. Skin assessment under the device Over half of the participants spoke about assessing the skin under the device, including lack of assessment (Table 4). Participants stated that even though skin assessment is maintained for patients at high risk of developing a PI, assessing the skin under a device was not something they would do on a daily basis. This is especially the case with anti-embolism stockings, under oxygen tubing around the ear, NGT and saturation probes. 3.3.2. Repositioning of the device Several (5, 23.8%) participants spoke about the repositioning of the device, or lack of repositioning. Nurses who knew that devices in contact with the skin needed to be rotated or offloaded stated they often forgot to do this, especially in ICS where lifesaving matters were prioritised. One key statement mentioned by several interviewees in the intensive care setting supports this: Table 1 Sample demographics (N ¼ 50).
Sex Male Female Age group Neonate < 21 21-30 31-40 41-50 51-60 61-70 71-80 81-90 > 90 Specialty/Unit Adult and neonate intensive care services Cardiovascular Cardiology Ante/Post-natal Orthopaedics Coronary Care Unit Upper GIT Neurology n: population; %: percentage.
n
%
37 13
74.0 26.0
3 1 2 3 3 8 10 13 6 1
6.0 2.0 4.0 6.0 6.0 16.0 20.0 26.0 12.0 2.0
34 6 4 2 1 1 1 1
68.0 12.0 8.0 4.0 2.0 2.0 2.0 2.0
3.3.3. Device fitting and securing Just under half of the participants spoke either about the tight fitting of medical devices, or use of incorrect sized devices, or the incorrect securing of medical devices. Nurses in this study believed that MDRPIs sustained from a NGT were related to the way in which the securing tape was placed and that MDPRIs related to ETT were caused by ties being secured too tightly. In the case of anti-embolism stockings, when a particular size was unavailable, nurses stated they would choose the next available size (mostly small) for “more compression”. Nurses in this study stated they were unaware that incorrect anti-embolism stocking size could result in a MDRPI. 3.4. Medical record review For all patients who were confirmed as having a MDRPI, documentation in the medical records was inadequate as evidenced by the absence of preventative strategies and monitoring of skin under the device. Skin assessment did not include assessing under a device until a PI had developed. Once a PI developed, nurses documented the PI and treatment required. In addition, nurses only documented that skin was either intact or not. This suggested to the authors that medical records were not a reliable source of information. Interestingly, documentation of treatment was more consistent when compared with documentation on prevention. 4. Discussion Over one quarter of patients who were reviewed for a reported HAPI in this study were confirmed as having developed a MDRPI. The majority of MDRPIs occurred in critically ill patients, primarily men. The most common location was the head, predominantly due to oxygen tubing behind the ears and ETT on the mouth, which were largely mucosal PIs. Additionally, the study highlighted a number of issues around development, processes in clinical practice and prevention of MDRPIs. The majority of MDRPIs occurred in ICS where medical devices are used frequently on patients. Most critically ill patients are at high risk of developing PIs due to compromised skin or tissue perfusion, and lack of movement from either sedation or inability to reposition themselves [31]. These factors, coupled with a device, further increase the risk of developing a MDRPI. Even though skin assessment is performed for patients at risk of developing a PI, most nurses indicated that assessing the skin under a device was not routine practice especially in the case of oxygen tubing and anti-embolism stockings. A high number of the patients (n ¼ 17) in this study developed PIs from oxygen tubing; nurses stated that the tubing behind the ear was not an area they would routinely inspect. The number of PIs caused by anti-embolism stockings in this study was higher than previously reported [11,16]. This is noteworthy given anti-embolism stockings are used regularly on patients who are confined to the bed rendering them at high risk of developing a PI. Anti-embolism stockings are perceived as safe to use; however, care and attention is required for appropriate size selection. Changes in a patient's condition, such as oedema, may alter the fit and produce a tourniquet effect which can lead to a PI. However, this can be prevented if patients are measured and fitted correctly [32]. Regular skin assessment under anti-embolism stockings is key to detecting any skin complications and preventing development of a PI. In this study, it was identified that the documentation related to PI preventative strategies in individual patient medical records was insufficient. On the occasions when skin integrity was mentioned it
Please cite this article in press as: Barakat-Johnson M, et al., Medical device-related pressure injuries: An exploratory descriptive study in an acute tertiary hospital in Australia, Journal of Tissue Viability (2017), https://doi.org/10.1016/j.jtv.2017.09.008
M. Barakat-Johnson et al. / Journal of Tissue Viability xxx (2017) 1e8
5
Table 2 Type of medical device, location, mean age by sex. O2 tubing (location, mean age)
ET tube
Anti-embolism stocking
CPAP
Nasogastric tube
Saturation probe
Nasal prong
Ankle band
Epistaxis balloon
3 (3 nose, M ¼ 36.0)a 1 (1 nose, M ¼ 77.0) 4
2 (2 nose, M ¼ 72.5) 2 (2 nose, M ¼ 45.5) 4
2 (2 forehead, M ¼ 57.0) 1 (1 forehead, M ¼ 76.0) 3
0
17
4 (4 lower leg, M ¼ 67.0) 3 (3 lower leg, M ¼ 38.0) 7
2 (2 ear, M ¼ 72.0) 0
Total
7 (6 mouth/lip, 1 tongue, M ¼ 65.7) 4 (4 mouth/lip, M ¼ 45.5)a 11
0
Female (n ¼ 13)
17 (14 ear, 3 nose, M ¼ 66.7) 0
1 (1 lower leg, M ¼ 0.01)a 1
1 (1 nose, M ¼ 44.0) 1
Male (n ¼ 37)
a
2
There was one neonate patient.
Table 3 Medical device-related pressure injury (MDRPI), stage, and anatomical location (N ¼ 50).
Medical device-related PI Oxygen tubing (tubing, nasal prongs and mask) ETT Anti-embolism stocking NGT CPAP Saturation probe Nasal prong Ankle band Epistaxis balloon Reported stage Mucosal 1 2 3
Frequency (%)
ICS (N ¼ 34)
Non-ICS (N ¼ 16)
Location Ear (N ¼ 16)
Nose/Nare (N ¼ 12)
Mouth/Lip (N ¼ 10)
Lower leg (N ¼ 8)
Forehead (N ¼ 3)
Tongue (N ¼ 1)
17 (34.0)
9 (26.5)
8 (50.0)
14 (87.5)
3 (25.0)
0
0
0
0
11 (22.0) 7 (14.0) 4 (8.0) 4 (8.0) 3 (6.0) 2 (4.0) 1 (2.0) 1 (2.0)
10 (29.4) 4 (11.8) 3 (8.8) 3 (8.8) 2 (5.9) 2 (5.9) 0 1 (2.9)
1 3 1 1 1 0 1 0
(6.2) (18.8) (6.2) (6.2) (6.2)
0 0 0 0 0 2 (12.5) 0 0
0 0 4 (33.3) 4 (33.3) 0 0 0 1 (8.3)
10 (100.0) 0 0 0 0 0 0 0
0 7 (87.5) 0 0 0 0 1 (12.5) 0
0 0 0 0 3 (100.0) 0 0 0
1 (100.0) 0 0 0 0 0 0 0
20 (40.0) 12 (24.0) 17 (34.0) 1 (2.0)
17 (50.0) 7 (20.6) 10 (29.4) 0
3 5 7 1
(18.7) (31.3) (43.8) (6.2)
0 5 (31.2) 10 (62.5) 1 (6.2)
9 (75.0) 2 (16.7) 1 (8.3) 0
10 (100.0) 0 0 0
0 3 (37.5) 5 (62.5) 0
0 2 (66.7) 1 (33.3) 0
1 (100.0) 0 0 0
(6.2)
was only documented as intact or not, with little or no mention of assessment under the device. Current international guidelines recommend that a thorough assessment of the skin under a medical device be performed regularly and documented in the patient's medical record [7]. This includes rotating the device to offload pressure from one single point. In addition, oedema increases the potential for skin breakdown, and frequent skin assessment is required to identify pressure caused from a medical device. Given ICS was the specialty with greatest occurrence of MDRPI, ICS patients are most vulnerable for disruptions in skin integrity. Even though nurses in this study were unaware of the greater implications of not examining the skin under the device or repositioning it, several nurses did state that the way in which a device is secured or fitted such as the tape for NGT or the ties for ETT may cause injury to the skin. In addition to strategies mentioned above to reduce the development of MDRPI, the technique of applying and securing a device should also be considered in any education plan to reduce MDRPI. The high number of MDPRIs in the present study is comparable with other studies. Black and colleagues [9] reported a 34.5% prevalence of MDRPI occurring mainly in ICS. Apold and Rydrych [12] found that nearly a third (29%) of reported PIs in their study were caused by medical devices. In this study, MDRPI most frequently occurred on the ears, similar to Black et al. [9] and Van Gilder et al. [33], mainly due to respiratory equipment as well as on the mouth. This is also comparable to the study by Hanonu and Karadag [34] where 45% of MDRPIs occurred in patients with an
Table 4 Nurse responses regarding devices (N ¼ 21). Frequency (%) Expressed that sizing or fitting was a problem Spoke about repositioning of the device (including lack of) Spoke about skin assessments (including lack of)
10 (47.6) 5 (23.8) 11 (52.4)
ETT. Nurses in this study reported that the way ETTs or tracheostomy tubes were secured determined whether or not a patient developed a PI, especially if they were tied too tightly. We found that the majority that the majority of mucosal PIs occurred in patients in the ICS. The high number of mucosal PIs is in line with Coyer et al.’s findings [16] where half of the MDRPIs were mucosal PIs in ICS patients with ETTs or NGTs. Although mucosal classification is still emergent [8] and under discussion in Australia [35], this data indicates that increased clinician awareness on the classification, prevention and management of mucosal PIs is necessary. Inclusion of assessment of the mucosa should be incorporated in the minimal standard care and operating procedures for patients who have an ETT or NGT. The rate of MDRPIs in the neonatal population in our study was low (3/50 and 0.0000378. per occupied bed days) compared with previous studies [24,25]. This finding is encouraging given studies [24,25,36] have found neonatal patients are at high risk of developing MDRPI. Prior to the commencement of this study, staff in the neonatal ICS in this study have had an active focus on the prevention of PIs, such as purchasing appropriate equipment and championing efforts to prevent MDRPIs. Recent consensus in the NPAUP consensus statement highlight the updated reporting and classification of MDRPIs [8]. International guidelines suggest that MDRPIs occurring on the skin should be staged as a PI. If the MDRPI is found on the mucous membranes, these injuries cannot be staged using the current PI [7] staging system and should be reported as a mucosal PI. Classifying and reporting at facility, local or statewide level of MDRPI is still emerging. The IIMS currently records incidents in the state-wide database using the previous NPUAP/EPUAP classification system [7]. Therefore, correctly recording and reporting of MDRPI poses a challenge especially for monitoring, quality improvement and benchmarking activities. Given the results of this study, it is suggested that further efforts be made at a statewide level to develop
Please cite this article in press as: Barakat-Johnson M, et al., Medical device-related pressure injuries: An exploratory descriptive study in an acute tertiary hospital in Australia, Journal of Tissue Viability (2017), https://doi.org/10.1016/j.jtv.2017.09.008
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M. Barakat-Johnson et al. / Journal of Tissue Viability xxx (2017) 1e8
consensus on reporting practices in line with the updated NPUAP [8] classification system. Medical devices have been recognised for many years as causing PIs, with a handful of studies highlighting it as a pertinent clinical issue; nevertheless, the emphasis has continued to remain on PIs that develop from immobility. This study site has concentrated largely on preventative interventions and monitoring of high-risk patients prone to PIs due to immobility in areas of bony prominences. PIs that develop under a device may be easily missed. It is only within the past 5e10 years, internationally, that there has been an emphasis on preventing their occurrence [9e11,37]. Our study has fundamentally raised awareness of MDRPI development at a local level. The importance of implementing preventative strategies targeted specifically at medical devices has been highlighted. Several interventions at the study site commenced after the study results were disseminated. Interventions include identifying devices that can cause pressure injuries, the use of prophylactic dressings under devices, adjusting the way in which a device is secured, frequent repositioning of the device and skin assessment. However, there is still significant work to be carried out to facilitate the prevention of pressure injuries related to medical devices.
implications when devices are incorrectly fitted. The findings from this study add to the literature and confirm previous studies suggesting that MDRPIs are a continuing clinical issue. Preventative PI care of patients with medical devices needs to be included in hospital education campaigns. Research into areas of prevention, primarily intervention strategies, will further inform and assist in the development of programs aimed at reducing MDRPIs. Conflicts of interest Nil to declare. Author contributions Study design MBJ, TW and KW. MBJ and CB undertook primary data collection. All authors were involved in data analysis and interpretation of findings. MBJ prepared the original draft and revised it critically based on comments from co-authors. CB, TW and KW all reviewed the manuscript for final approval to be submitted. The authors report no competing interests. Funding
5. Limitations This present study has important limitations. Patient-related factors which may influence the development of MDRPIs were not investigated. There were also limitations in the availability of certain clinical variables in the dataset, including information on patient comorbidities and diagnosis, as well as patients unavailable for review. Another limitation was the time between the date the incident was reported and the date it was assessed by the audit team. Since the audit team assessed all incidents on the same day of each week, occasionally, there was a three to five-day gap after the incident had been reported. This could have led to inaccurate assessment. 6. Conclusion Findings from this study of MDRPIs were similar to previous studies with the highest incidence occurring in ICS, primarily on the ear from oxygen tubing and on the mouth from ETTs. Antiembolism stockings were of concern, contributing to a higher number of PIs than reported in the literature. Nurses were not aware of preventative strategies for MDRPIs or the significant
The lead author is the recipient of a Clinical Researcher Scholarship by Sydney Research, which in part, supported this study and the preparation of this article. Acknowledgements We are most grateful to the patients and nurses who participated in this study. We thank the District Director of Nursing of the Sydney Local Health District, as well as the Executive of Royal Prince Alfred Hospital for their support of this study. In particular, we wish to thank Thomas Leong, Deborah Wolak and Cassandra Chan who contributed to data collection. Finally, we would like to thank Michelle Lai for her tremendous assistance with statistical analysis and review of this article. Appendix 1. Responses of nurses caring for the patient at time of review on what they thought the injury was caused by (N ¼ 21)
Question
Participant
Role
Response
How do you think this injury was caused?
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21
RN RN RN RN CNS RN RN RN CNS RN RN RN RN RN RN RN CNS RN RN RN RN
From the tightness of the NGT and ETT Pressure and not looking under Pressure The pressure and friction Pressure TEDS [compression stockings] Pressure and heat The tube The ETT sometimes is secured too tightly that’s what causes the pressure It’s the compression around the legs especially if they [compression stockings] roll down Pressure, friction Because they are very unwell, checking under the device is not a priority… and it’s the tape as well and how it is secured It’s the tape sometimes that can be an irritant and also cause pressure It’s the [ETT] ties that cause the pressure Pressure and fiction The tube and pressure The [ETT] ties might be too tight I think sometimes people tie ETT too tightly Pressure and friction The tubing that could cause the pressure Nasogastric tubes are hard because the damage could be done just by the insertion
Please cite this article in press as: Barakat-Johnson M, et al., Medical device-related pressure injuries: An exploratory descriptive study in an acute tertiary hospital in Australia, Journal of Tissue Viability (2017), https://doi.org/10.1016/j.jtv.2017.09.008
M. Barakat-Johnson et al. / Journal of Tissue Viability xxx (2017) 1e8
7
Appendix 2. Responses of nurses caring for the patient at time of review on the care of the device (N ¼ 17)
Question
Participant Role Response
Tell me about the 1 care of the device. 2
RN RN
3
RN
4 5
RN CNS
6
RN
7 8
RN RN
9 10 11
RN RN RN
13 15
RN RN
16
RN
17
CNS
19 20
RN RN
We don’t really check under the device unless we think it is too tight When the ETT ties are changed that’s when we look under it. Should be fitted correctly…usually pressure from the device causes it We usually just grab a size on the shelf, didn’t realize how important the sizing is and if it’s too tight it will cause this pressure behind the leg It’s not the sizing so much but it’s checking…checking behind the ears is not something we would do They should check under patient’s skin regularly and under device daily but with ETT it’s hard because you don’t want to shift them Check should be daily, after shower but not sure how vigilant this is…I didn’t realize that the TEDS could be so damaging, we opt for a smaller size if the other size is unavailable for more compression We try and shift the saturation probe but not everyone does, definitely pressure from the saturation probe causes the injury Check under nasogastric tube? Definitely not…when patients are too ill, lifesaving priorities come into play sometimes repositioning gets overlooked We check under it when the ties are changed If we don’t have the [compression stocking] size we usually either go up or down a size We try and rotate the device when we go to reposition, sometimes it doesn’t happen because there are other things going on but I also think it’s sizing. If it’s not fitted correctly it’s a problem The way it is secured and with saturation probes they are just stuck on Repositioning is not often as we need to, it’s hard because these patients are very sick and we have other lifesaving priorities… Definitely it would heal if we could put a dressing under the tube to prevent the pressure and friction Check under nasogastric tube…we don’t think about that. Repositioning of device gets overlooked because all the other lifesaving priorities going on...It’s hard when they are on inotropes and you can’t move them, there are lifesaving priorities… you don’t think of the device really We always try to assess underneath and rotate the ETT, we are usually vigilant with skin assessment but I am not sure everyone does Sometimes we rotate them and look at the skin when we change the tapes No, we don’t check often around the ear
Appendix 3. Responses of nurses caring for the patient at time of review on what preventative measures were in place (N ¼ 11)
Question
Participant
Role
Response
What preventative measures are in place?
1 4 5
RN RN CNS
6
RN
8 10 13 15 16 17 18
RN RN RN RN RN CNS RN
Skin assessment daily, we try and rotate it at least once a shift We try and use those comfy ears but even that slips off We are trialing the new silicone gel pads under devices but they don’t tend to stay in place as well as we would have liked them to Some nurses keep them [compression stockings] on and wrap plastic bag around to shower… we will have to include that in our education It’s the pressure from the tube…they are looking at a new way to secure the tube We should check more often but we don’t We have been educating the nurses on rotating the area at least daily or each shift We are trying the silicone pads but they don’t really stay in place Skin assessment every chance we get, they are looking at a new way to secure the [nasogastric] tube, this might help We have been educating the nurses this week, it’s been a problem, we are looking into dressings like the silicone pads We are looking at other ways to prevent the ETT pressure injury
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Please cite this article in press as: Barakat-Johnson M, et al., Medical device-related pressure injuries: An exploratory descriptive study in an acute tertiary hospital in Australia, Journal of Tissue Viability (2017), https://doi.org/10.1016/j.jtv.2017.09.008