Facial pressure ulcers in inpatients undergoing non-invasive ventilation in intermediate care units

Background: Facial pressure ulcers are one of the most common complications associated with non-invasive ventilation (NIV ). Objectives: To determine the frequency of facial pressure ulcers in patients admitted to an intermediate care unit (ICU) and submitted to NIV, as well as to identify the associated factors. Methodology: A prospective study was conducted between September and December 2015. Inclusion criteria: age ≥ 18 years, admitted to ICU, submitted to NIV and without facial ulcers at time of admission. A sample of 30 participants was obtained. Data were collected through a questionnaire, the Braden Scale and the Glasgow Scale. Results: The frequency of facial pressure ulcers was 26.7%, 16.7% of stage II and with a mean onset of 3.3 days. Most participants were male (70.0%), and the mean age was 74.2 years. Patients undergoing more hours of VNI per day, more days of NIV and more days of hospitalization had a higher frequency of facial pressure ulcers. Conclusion: Given that the number of hours of NIV increased the frequency of Facial pressure ulcers, we suggest periods of interruption of NIV use.


Introduction
Non-invasive ventilation (NIV ) is a ventilation modality using a mask as patient-ventilator interface without the need for an artificial airway and sedation, thus improving patient comfort and reducing hospital length of stay (Cruz & Zamora, 2013).NIV has proven to be effective in the treatment of respiratory failure (RF) of various causes.The use of NIV in the treatment of patients with acute or chronic RF has certainly been one of the greatest advances in mechanical ventilation in recent decades (Silva et al., 2013).For 20 years now, its application in clinical practice has increased, as well as the availability of technological resources for its implementation, being currently considered the first-line treatment of acute RF (Cruz & Zamora, 2013).Although NIV is a safe and effective ventilation modality which is more comfortable for the patient than invasive mechanical ventilation (IMV ), evidence shows that its implementation can lead to the development of facial pressure ulcers and ulceration of the nasal dorsum (Maruccia, Ruggieri, & Onesti, 2015;Silva et al., 2013).Pressure ulcers (PUs) are localized areas of the body surface exposed to prolonged high pressure, friction or shearing, so as to prevent local circulation, with consequent tissue destruction and/ or necrosis (Ministério da Saúde, Direcção-Geral da Saúde, Rede Nacional de Cuidados Continuados Integrados, 2007).Maruccia et al. (2015) argue that facial skin breakdown is very often, and can range from 2.0 to 70.0%.In Portugal, studies on the frequency and incidence of facial pressure ulcers in patients with NIV are rare.Thus, this study aims to determine the frequency of facial pressure ulcers in patients admitted to an intermediate care unit (ICU) and submitted to NIV, as well as to identify associated factors.

Background
NIV is a ventilation support method applied to the patient's airway through masks (facial/nasal) or respirators, instead of endotracheal tubes, and operate as patient/ventilator interface (Marcelino, 2009).This ventilation modality is used in several situations, such as deterioration of gas exchange, hypercapnic respiratory failure and respiratory acidosis, dyspnea with use of accessory muscles and/ or paradoxical breathing, tachypnea, exacerbation of chronic obstructive pulmonary disease (COPD), asthma, facilitation of extubation, cardiogenic pulmonary edema, pneumonia, acute respiratory distress syndrome, immunosuppressed patients, postoperative period, extubation failure, end--of-life stage, pre-intubation oxygenation, and facilitation of bronchoscopy (Cruz & Zamora, 2013).However, despite the broad spectrum of indications, contraindications should be taken into account, namely cardiac arrests and/or respiratory disorders, severe encephalopathy with Glasgow Coma Scale (GCS) <10 with risk of aspiration, severe upper gastrointestinal bleeding, hemodynamic or electrocardiographic instability, facial deformity or trauma, upper airway obstruction, inability to protect the airways, inability to remove secretions, severe hypoxemia, untreated pneumothorax, need for sedation, increased risk of aspiration, multiple organ failure, and acute myocardial infarction (Marcelino, 2009;Cruz & Zamora, 2013).The primary benefit of using such a ventilation method is the prevention of complications from invasive ventilation, such as the aspiration of gastric contents, oropharynx trauma, ventilator-associated pneumonia, tracheal stenosis, and pneumothorax (Passarini, Zambon, Morcillo, Kosour, & Saad, 2012).NIV also maintains the ability to speak and cough, reduces the need for sedation, the risk of hemodynamic instability, and delirium, preserves the activity of respiratory muscles, and leads to less time on mechanical ventilation, ICU stay, and increased survival (Marcelino, 2009;Cruz & Zamora, 2013).However, it has been shown that one of the most common complications during this ventilation method is the ulceration of the nasal dorsum (Maruccia et al., 2015;Silva et al., 2013).The National Pressure Ulcer Advisory Panel (NPUAP) defines pressure ulcer as a localized injury to the skin and/or underlying tissue usually over a bony prominence, as a result of pressure, or pressure in combination with shear, associated with a number of factors yet to be elucidated (National Pressure Ulcer Advisory Panel [NPUAP], 2015).PUs are divided into four stages: I, II, III and IV, which correspond to non-blanchable erythema, partial thickness skin loss, full thickness skin loss, and full thickness skin loss, respectively (Direção Geral de Saúde [DGS], 2011;NPUAP, 2015).Some researchers in this area argue that there are a number of risk factors for the development of PUs, such as advanced age, moisture, malnutrition, loss of lean body mass, length of hospital stay, reduced mobility, mechanical forces and shearing, level of consciousness, sensory perception, and skin characteristics (Rogensk & Santos, 2005;Campos, Chagas, Costa, França, & Jansen, 2010;Furman et al., 2010).They also believe that some comorbidities and associated disorders play a key role in the development of PUs, such as diabetes mellitus, hypertension, anemia, infection, cardiovascular diseases (CVD), and neurological, respiratory or terminal diseases (Rogenski & Santos, 2005;Campos et al., 2010;Furman et al., 2010).The DGS (2011) estimates that approximately 95.0% of PUs are avoidable through early identification of the risk level.The knowledge of the etiology and risk factors associated with the development of PUs are key to the success of prevention strategies (DGS, 2011).Thus, the risk of developing PUs should be assessed in all care settings within the first 6 hours after patient admission (DGS, 2011).According to Fernandes and Torres (2008), in a study on the incidence and risk factors of PUs in ICU patients, the most common PU sites are the sacrum (40.0%), the calcaneus (36.0%), the ears (8.0%), and the nose (4.0%).Schallom et al. (2015) conducted a study on the use of full-face or oronasal masks in patients undergoing NIV, concluding that the development of PUs differed significantly (p < 0.001) between both masks: 20.0% of patients with oronasal masks developed PUs on the nose or the face area under the mask, 16 patients developed stage I PUs, and four patients developed stage II PUs.The identification of PUs during the use of oronasal mask occurred during the data collection period with the identification of three to six ulcers per month (Schallom et al., 2015).In 2014, in a study conducted by Yamaguti et al. involving 375 participants undergoing NIV, 54 (14.4%) of them developed PUs: 49 (13.1%)developed stage I PUs, and 5 (1.3%) developed stage II PUs (Yamaguti et al., 2014).No differences were found between the groups, with and without PUs, according to age, gender, body mass and primary medical diagnosis (half of the sample presented lung disease as the primary medical diagnosis).Fifty of the 54 patients who developed PUs used an oronasal mask (42.0%) and the remaining 4 patients (1.6%) used a full-face mask (Yamaguti et al., 2014).
Based on the records of the ICU where this study was conducted, 634 patients were admitted in 2013, 386 (61.0%) of whom underwent NIV.

Research questions
What is the frequency of facial pressure ulcers in ICU patients undergoing NIV? Which factors are associated with the development of facial pressure ulcers in ICU patients undergoing NIV?

Methodology
A prospective study was conducted in an ICU of a hospital in the northern area of Portugal, between 30 September and 21 December 2015.The following inclusion criteria were applied to obtain the sample: patients aged 18 years or more, admitted to ICU, undergoing NIV and without facial PUs at admission.The study included all participants admitted to the ICU during the study who fulfilled the above-mentioned criteria.A convenience sample of 30 participants was obtained.We designed a questionnaire for data collection on the sociodemographic and clinical characteristics of patients: age, gender, date of admission, diagnosis at admission, medical history, ulcers at admission, weight, height, body mass index (BMI), sensitivity changes, characteristics of NIV during hospital stay, such as mask status, facial skin characteristics, length of NIV in hours/day and days, number of days for facial pressure ulcer development, and length of hospital stay.BMI was assessed in accordance with the DGS guidelines, which relates weight with height and ranges from a minimum value < 18.5 Kg/m 2 to a maximum value ≥ 30.0 Kg/m 2 .Within these values, participants were classified as being low weight with BMI < 18.5 Kg/m 2 , normal weight with BMI between 18.5 kg/m 2 and 24.9 Kg/m 2 , pre-obese with BMI between 25.0 kg/m 2 and 29.9 Kg/m 2 , and obese with BMI = 30.0kg/m 2 .Patient sensitivity was assessed by one of the researchers by touching the patients' extremities, hands and feet with the tip of the finger.Patients were unable to see this intervention.Patients were considered to have sensitivity changes if they showed no verbal reaction or otherwise to the stimulus.The Braden Scale was used to assess the risk of PU.This scale was validated for the Portuguese population and is recommended by the DGS (2011).It consists of six subscales: sensory perception, moisture, activity, mobility, nutrition, and friction/ shear.The first five subscales are scored from 1 to 4, where 1 represents the less favorable score and 4 the most favorable score.The sixth subscale is scored from 1 to 3. The score obtained in the Braden scale ranges from a minimum of six to a maximum of 23.Scores ≤16 indicate high risk of PU and ≥ 17 low risk of PU (DGS, 2011).The GCS was used to assess the participants' level of consciousness.It consists of the observation of three parameters: eye, motor and verbal responses.It implies the application of standardized stimuli to achieve a homogenous and independent assessment.Eye response ranges from a minimum score of 1 to a maximum of 4, in which 1 corresponds to no eye opening and 4 to spontaneous eye opening.Motor response ranges from a minimum of 1 to a maximum of 6, in which 1 corresponds to no response to pain and 6 to obeying command.Verbal response ranges from a minimum of 1 to a maximum of 5, in which 1 corresponds to no verbal response and 5 to oriented.The maximum score is 15, which corresponds to a fully awake and aware person, and the minimum score is 3, which corresponds to deep coma.The researchers or the nurse responsible for the patient performed the direct observation of skin characteristics on a daily basis, during facial hygiene care, which allowed identifying the onset of the facial pressure ulcer.All data collection tools were applied to each participant at admission.PU development was recorded when identified.The NIV in hours and days and the length of hospital stay were collected at discharge.During the study, the researchers collected the data at patient admission or, when absent, in the following shift based on the existing records and with the collaboration of the nurse who had admitted the patient to the unit.Permission for data collection was previously requested to the Chairman of the Board of Directors, who, after consulting with the Ethics Committee, ruled in favor on 19 January 2016.Data were coded and entered into a database in the Social Package Statistical Science ® software, version 23, with a code number, thus ensuring the participants' confidentiality and anonymity.Data were analyzed using descriptive statistics with estimation of absolute and relative frequencies for ordinal variables, and means and standard deviations for continuous variables.Using the Kolmogorov-Smirnov test, we checked for the distribution of variables.Since the variables were not normally distributed, we used non-parametric tests.Spearman's correlation was used to analyze the association between the facial PU development and the other variables.The level of significance was set at 0.05%.

Results
Of the 30 participants, 8 (26.7%) developed PUs.The mean age was 74.2±10.3years, ranging from 57 to 92 years.Patients who developed PUs had a mean age higher than Ẋ = 76.5 years.Twenty-one were male (70.0%), 7 (23.3%) of whom developed PUs.The mean weight was 76.43 Kg, the mean height was 1.64 meters and the mean BMI was 28.4 kg/m 2 , ranging from 20.9 to 58.5 Kg/m 2 (Table 1).We found that 18 (60.0%) of the participants had a high risk of developing PUs according to the Braden Scale, 6 (20.0%) of whom developed PUs.Eleven patients (36.7%) had sensitivity changes in the extremities, 5 (16.7%) of whom developed PUs.Respiratory failure, alone or in association with other diseases, was the most common disease in the patients' medical history.A higher frequency of PU development was found in participants with intact and dry skin 5 (16.7%).RF was the most common diagnosis at admission leading to NIV, with 6 (20.0%) of these patients developing PUs (Table 2).Twenty-seven (90.0%) patients used a reused mask, 8 of whom developed PUs (26.7%).Among these participants, 5 (16.6%) developed stage II PU, 2 (6.7%) developed stage III PU and 1 (3.3%) developed stage I PU.In case of NIV exceeding 18 hours, 8 patients (26.7%) developed facial PUs; in case of NIV between 4 -7 days and for more than 8 days, 6 patients developed facial PUs, 3 (10.0%) in each case; and in case of length of hospital stay between 5 and 10 days, 4 patients (13.3%) developed facial PUs.In case of GCS scores between 11 and 15, 7 patients (23.3%) developed facial PUs.The mean pressure applied in case of inspiratory positive airway pressure (IPAP) was 18.73 cmH 2 O, ranging from 10 cmH 2 O to 26 cmH 2 O, whereas the mean pressure in case of expiratory positive airway pressure (EPAP) was 6.57 cmH 2 O, ranging from 2 cmH 2 O to 10cmH 2 O (Table 3).

Discussion
In this study, the frequency of cases of facial PU development in patients undergoing NIV in the ICU was 26.7%.These data are in line with those found in another study which reported that face skin breakdown in patients with NIV can vary between 2.0 and 70.0% according to age, mask status, and treatment duration (Maruccia et al., 2015).In our study, we observed that most participants were older than 65 years (70.0%), with a mean age of 74.2 years, and that the mean age was higher among participants who developed facial ulcers (76.5 years).These data are corroborated by a Brazilian study, conducted in 2005, on the incidence of facial PUs that found a statistically significant difference (p=.003) between the groups' mean age, with it being higher in patients with facial PUs (Rogenski & Santos, 2005).Skin loses elasticity, thickness and resistance with age, making it more vulnerable when submitted to pressure or aggression, thus increasing the risk of ulceration, as shown by Maruccia et al. (2015) in a study on facial skin breakdown in patients with NIV treatment and prevention.This predisposition to develop facial PUs, mainly in areas with little subcutaneous tissue such as the nasal dorsum, can be associated with skin changes caused by aging (Maruccia et al., 2015).Moreover, another study conducted in Brazil, in 2014, on the frequency of PUs, risk factors and lesions in adult inpatients concluded that the frequency of PUs increases with age, with it being higher above 70 years of age (Silva, Oliveira, Diniz, & Fernandes, 2014).The changes resulting from the effects of senescence affect the organic systems, including the integumentary system, exposing the older person to the development of skin lesions (Silva et al., 2014).The gradual impairment of cellular activity in old age, especially of fibroblasts, directly affects the production of local collagen, which is the main protein responsible for the formation of the integumentary tensile structure and strength.Age brings about reduced elasticity, texture, decreasing frequency of cell replacement and increased length of the healing process, which can contribute to a greater risk of skin and tissue lesion (Furman et al., 2010).
In our sample, we found a predominance of male patients (70.0%), which can result from the fact that the study was conducted in a geographic region with a high rate of employment in mines, quarries, and wood (p=.035).Hypertensive patients show an increase of vascular resistance, along with a hypertrophy of the muscle layer, which worsen with other disorders, such as diabetes mellitus, and obesity.This clinical status promotes ischemia and cellular hypoxia, facilitating the development of PUs (Furman et al., 2010).The diagnosis at admission which led to a greater use of NIV was RF (60.0 %) and 6 of the participants with this pathology developed facial PUs (20.0%).
In addition, in the study of Silva et al. (2013) on the adaptation to different NIV interfaces in critically ill patients, 71.3% of the patients who needed NIV had RF, since acute RF leads to a severe deterioration of gas exchange (Silva et al., 2013).As mentioned above, ICU inpatients usually have a high risk of developing PUs.These patients often have sensitivity changes (36.7%), which make them less reactive to excessive pressure and more prone to lesions, which is in line with the results obtained by Rogenski & Santos (2005), Campos et al. ( 2010), Furman et al. (2010), and Albuquerque et al. (2014).This change may be associated with decreased sensory perception caused by sedatives, analgesics and muscle relaxants, which are commonly used in these units (Silva et al., 2011).Some studies report that moisture is a risk factor for the development of PU (Rogenski & Santos, 2005;Furman et al., 2010).In our study, we found a higher frequency of facial PU development in participants with intact and dry skin (16.7%).This fact can be associated with dehydration in critically ill patients, as shown by Campos et al. (2010).Furman et al. (2010) also found dry skin in 73.1% of patients, which is described as a possible sign of dehydration that is characterized by a lower amount of water and total electrolytes in the body, making the skin dry and susceptible to breakdown due to decreased elasticity.Tolerance to friction is also lower.One aspect which was not assessed in the questionnaire, although it raised the researchers' attention throughout the study, was the fact that most participants who developed PU had pale and cold skin in the extremities.According to Furman et al. (2010), this aspect may influence tissue perfusion and nutrition, which makes the individual more vulnerable to tissue damage.We believe that further studies should include this variable.With regard to mask status, 90% of the masks were reused, with 26.7% of the patients developing facial PUs.Although the literature states that several and furniture factories.According to the latest census, in this area, 9,430 of the 29,991 employed inhabitants develop their professional activity in one of the areas of Group 7 (workers, craftsmen and similar), which are mostly performed by men (Instituto Nacional de Estatística, 2012).Therefore, these workers are more exposed to the risk of developing respiratory diseases and, consequently, needing treatment with NIV.We found a higher frequency of facial PU development in male participants (23.3%), as did Silva et al. (2014), with a rate of 54.3% in men.
Facial PU development was higher in the group of participants with a pre-obese BMI (13.3%).Further studies pointed in the opposite direction, associating low weight with malnutrition and decreased percentage of body mass as a predisposing factor for developing PUs (Rogenski & Santos, 2005;Campos et al., 2010;Furman et al., 2010) As mentioned by Passarini et al. (2012), in most situations, the choice of equipment depends on its availability at the time of patient admission and the severity of the patient's condition, , which does not always allow using the most adequate mask.Mask use, and cleaning and sterilization procedures cause its clear deterioration.This will increase air leaks and, consequently, the need for greater pressure to adjust the mask and avoid these leaks.To prevent the occurrence of ulceration of the nasal dorsum, the authors suggest the use of special masks and that the mask contact surface should be inflated using water instead of air (Passarini et al., 2012).
In our study, we found that 60.0% of the participants had undergone NIV for 18 hours, being that 26.7% of these patients had developed facial PUs.NIV routine usually depends on its objective, based on medical indication and the patient's clinical status.In this study, as in the study by Silva et al. (2013), we found that participants sometimes had a very reserved prognosis, which made it impossible to remove NIV for facial rest, namely for feeding, oral hygiene, expectoration, and secretion aspiration.In relation to the time of NIV in days, we observed an increase of facial PUs after the fourth day.The mean time of facial PU development was 3.3 days, which leads us to infer that patients have a higher risk of developing facial PUs after three days of NIV.We found a higher frequency of facial PUs with a hospital stay of 5 to 10 days, which can be explained by the fact that participants are more debilitated as they get older, and have a more severe clinical diagnosis, thus requiring a longer period of treatment.On the other hand, PU development can extend the length of hospital stay due to the specificities of their treatment (Primo et al., 2014;Rogenski & Santos, 2005).
Stage II facial PUs (16.7%) were the most frequent PU developed among the participants, which is similar to the results found by Sousa et al. (2013).We believe that nursing care, such as the daily inspection of facial skin, the use of a nasal protection, comfort massages and continuous monitoring, can minimize the development and worsening of lesions, since these lesions can be detected at an earlier stage.
This study had a few limitations, such as the short period of time for data collection and, consequently, the small sample, which did not allow us to establish associations or draw conclusions from the results.The reduced period was due to the fact that the researchers were only present at the unit during the development of the study.Therefore, we recommend the development of longitudinal studies with larger samples so as to identify the factors associated with facial PU development in patients undergoing NIV.

Conclusion
The frequency of facial PUs was higher in patients who underwent more than 18 hours of NIV per day.We recommend interruption of NIV, whenever possible, and the implementation of preventive actions, such as continuous nursing care, adequacy of equipment, and ongoing in-service training.We suggest the development of longitudinal studies with representative samples so as to assess the cause-effect relationship, taking into account the duration of NIV.

Table 1
Absolute and relative distributions of the participants according to the presence of pressure ulcer, age, gender and BMI

Table 2
Absolute and relative distributions of the participants according to the presence of pressure ulcer, Braden Scale, sensitivity changes, medical history, skin characteristics and diagnosis at admission

Table 3
Distribution of participants according to the presence of pressure ulcer, mask status, length of NIV in hours/ day and GCS score Ẋ IPAP = 18.73,Ẋ EPAP = 6.57,Ẋ Days of NIV = 4.33.Ẋ Days of hospital stay = 6.33 NIV -Non-invasive ventilation