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Effects of Hemodynamic Factors and Oxygenation on the Incidence of Pressure Ulcers in the ICU

Soodmand, Mostafa MSc; Moghadamnia, Mohammad Taghi PhD; Aghaei, Iraj PhD; Ghasemzadeh, Golshan BSN; Kazemnejad Lili, Ehsan PhD; Homaie Rad, Enayatollah PhD

doi: 10.1097/01.ASW.0000553599.20444.f4

OBJECTIVE To investigate the roles of hemodynamic factors and oxygenation on the incidence of pressure ulcers in patients in the ICU on mechanical ventilation.

METHODS This prospective analytical cross-sectional study was performed in several ICUs for a period of 8 months in Iran. Researchers checked patients for pressure ulcers on a daily basis. They collected demographic, hemodynamic, and oxygenation data until a pressure ulcer occurred, the patient’s artificial airway was removed, the patient died, or the patient was discharged.

RESULTS From August 2017 to February 2018, a total of 2,581 patients were admitted to the study ICUs; of these, 133 patients were eligible for the study. The results indicated that 41.4% (n = 55) of the patients ended up with pressure ulcers. Investigation of the variables using a Cox regression model showed that, among other variables considered in this study, age, mean arterial pressure, and positive end-expiratory pressure in the mechanical ventilator can contribute to the risk of pressure ulcers.

CONCLUSIONS Providers should pay attention to changes in hemodynamic parameters, especially mean arterial pressure; carefully determine the most appropriate positive end-expiratory pressure for patients connected to mechanical ventilation; and take special care of susceptible groups such as older adults and hospitalized patients to decrease the incidence of pressure ulcers.

At the Guilan University of Medical Sciences, in Rasht, Iran, Mostafa Soodmand, MSc, is a medical-surgical nursing student, School of Nursing and Midwifery; Mohammad Taghi Moghadamnia, PhD, is Assistant Professor of Health in Disasters and Emergencies, Department of Medical-Surgical Nursing, School of Nursing and Midwifery; Iraj Aghaei, PhD, is Assistant Professor of Neurosciences, Social Determinants of Health Research Center; Golshan Ghasemzadeh, BSN, is a researcher, Healthy Heart Research Center, Heshmat Hospital; Ehsan Kazemnejad Lili, PhD, is Associate Professor of Biostatistics, School of Nursing and Midwifery; and Enayatollah Homaie Rad, PhD, is Assistant Professor of Health Economics, Social Determinants of Health Research Center.

Acknowledgments: The authors thank the participants of the study. This research project was financially supported by the Deputy of Research and Technology at the Guilan University of Medical Sciences.

Submitted June 23, 2018; accepted in revised form August 3, 2018; published ahead of print April 2, 2019

Online date: April 4, 2019

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One of the most common types of complex wound, a pressure ulcer is localized tissue damage that occurs because of pressure, friction, incision, or a combination of these and other factors, usually on bony prominences. Pressure ulcers often occur in hospitalized patients, especially those in the ICU. Pressure ulcers increase mortality and morbidity, nurse workload, and length of hospital stay while negatively affecting the patient’s quality of life.1–6

Patients in the ICU exhibit high rates of pressure ulcers. Further, because of hemodynamic failure, inefficient blood circulation, defective oxygenation, anemia, and edema, these patients are always susceptible to hemodynamic disorders and reduced arterial oxygen supply.3 One of the most important aspects of nursing care is the preservation of skin integrity. The prevention and treatment of pressure ulcers have been a concern and significant duty for nurses for years, and identification of the individuals exposed to such risk is a fundamental step toward preventing pressure ulcers.7 This study was designed to investigate the roles of hemodynamic factors and oxygenation on the incidence of pressure ulcers in patients who require mechanical ventilation. The findings of this research can be used to improve planning and interventions that decrease costs associated with pressure ulcers.

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This prospective analytical cross-sectional study was performed in the ICUs of medical centers supervised by the Guilan University of Medical Sciences from August 2017 to February 2018. Samples were taken from four ICUs, including the neurological, general, and trauma ICUs at Poorsina Hospital and the general ICU at Razi Hospital in Rasht (Guilan Province, Iran). In total, the ICUs comprised 37 beds (8, 11, and 10 beds in neurological, general, and trauma ICUs at Poorsina Hospital, respectively, and 8 beds in general ICU at Razi Hospital).

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Based on the results of Wilczweski et al8 and considering a confidence interval of 95% and an absolute tolerance of 5% according to Cochran’s sampling formula, the required sample size for determining the incidence of pressure ulcers in ICU patients was calculated to be 133 individuals. Inclusion criteria included patients who were 18 years or older, a minimum of 24 hours of ventilator use, absence of pressure ulcer or any damage to skin integrity at the beginning of the study,9,10 normal body temperature, absence of paraplegia or quadriplegia before admission to the ICU, continuous feeding via nasogastric tube, normal levels of albumin and total protein, no sedative or vasoactive medicine, sampling of arterial blood via radial artery, and availability of the required nursing equipment. Patients must also have received the necessary measures for preventing pressure ulcers at the beginning of each working shift (including medical air mattresses, change of position every 2 hours, daily bedding change, change of patient’s bedding for any reason, and preventing placement of monitoring equipment under the patient).

A total of 96 nurses served patients in the study ICUs (19, 30, and 25 nurses in neurological, general, and trauma ICUs at Poorsina Hospital, respectively, and 22 nurses at Razi Hospital). Each nurse served two or three patients. During the data collection period, a total of 2,851 patients were hospitalized in the ICUs; 133 of these patients qualified for the study based on the inclusion criteria.

Researchers provided patients with a detailed description of the study, and written informed consent was obtained from conscious patients or the guardians of unconscious patients.

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The research instrument was a 6-part checklist: (1) demographic information and disease-related factors including age, gender, body mass index (BMI), smoking and tobacco consumption, hospitalization date, date of admission to the ICU, type of ICU, and diagnosis at admission; (2) respiration indices including positive end-expiratory pressure (PEEP), fractional concentration of inspired oxygen, tidal volume, mode of respiration, duration of connection to mechanical ventilator, partial arterial oxygen pressure, partial arterial carbon dioxide pressure (PaCO2), oxygen saturation, and power of hydrogen (PH); (3) hemodynamic indices including heart rate (HR), systolic blood pressure (SBP), diastolic blood pressure (DBP), mean arterial pressure (MAP), hemoglobin level, and urinary output; (4) the Charlson comorbidity index (CCI); (5) the Glasgow Coma Scale (GCS); and (6) the Braden risk assessment scale.

In order to check for the presence of associated illnesses, the CCI was used. Designed by Charlson in 1987, the index is based on the International Classification of Diseases, Ninth Revision, under 19 sets of disease conditions. Accordingly, the diseases registered on the patient’s file or those under treatment, as per the patient’s or his/her companion’s declaration, were considered associated illnesses.11

In order to collect the required data, upon approval from the Committee of Ethics at Guilan University of Medical Sciences (IR.GUMS.REC.1396.111) and following the required coordination with hospital officials, two members of the research team visited each patient’s bedside on a daily basis to record demographic information. Then, information related to hemodynamics and oxygenation during the last working shift (the last 24 hours) was recorded on a related checklist using the vital signs registration flowchart and hospital information system.

In each ICU, oxygenation-related data including PEEP, fractional concentration of inspired oxygen, tidal volume, mode of respiration, duration of respiration via artificial airway, partial arterial oxygen pressure, PaCO2, oxygen saturation, and PH were recorded on a daily basis; hemodynamic information including HR, SBP, DBP, and MAP was recorded once every 2 hours; hemoglobin level was measured once a day; and total urinary output was recorded over 24 hours. Data collection was continued until either a pressure ulcer appeared, the patient’s tracheostomy tube was removed, the patient was discharged, or the patient died.

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Statistical Analysis

In order to verify simultaneous reliability between any two individuals in determining the incidence or absence of pressure ulcer, the κ consistency coefficient was used, which was 0.79 (P = .001) for 20 patients.

The data were analyzed using SPSS version 20 (IBM, Armonk, New York) and survival analysis tests (Tarone-Ware and Cox regression tests).

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In this study, the incidence of pressure ulcers among patients in the ICU was 41.4% (n = 55). Results showed that 68.4% (n = 91) of the patients were male, and 31.6% (n = 42) were female. In addition, 45.1% (n = 60) of the patients were admitted to the ICUs because of trauma. As for smoking or tobacco or drug consumption, 87.2% (n = 116) of the sampled patients had no history. See Table 1 for a comparison of some demographic and clinical factors in patients with and without pressure ulcer. Tables 2 and 3 show details on the hemodynamic and oxygenation indices of the patients.

Table 1

Table 1

Table 2

Table 2

Table 3

Table 3

Results of the Tarone-Ware test showed that duration of hospitalization, duration of stay in the ICU, duration of connection to mechanical ventilator, mean hemoglobin, mean urinary output, mean blood PH, and mean PEEP were significantly related to the incidence of pressure ulcers (Table 4).

Table 4

Table 4

Demographic data, Braden scale, GCS, CCI, and hemodynamic and respiration indices of the patients with pressure ulcer were investigated using the Tarone-Ware test. Variables with significance levels below 0.25 (age, duration of hospitalization, duration of stay in the ICU, type of ICU, mean time of connection to mechanical ventilator, mean urinary output, mean hemoglobin, mean MAP, mean SBP, mean PH, mean PEEP, CCI, and GCS) were entered into Cox regression model and modeled in 10 steps via likelihood ratio method. Eventually, only the variables listed on Table 5 (age, mean MAP, mean PEEP) were retained as factors influencing the incidence of pressure ulcer, and other variables were omitted. These results imply that in patients with ages and MAPs higher than the mean values the risk of pressure ulcer increases, 2.5 and 1.9 times, respectively. Further, in patients with a PEEP lower than the mean value, the risk of pressure ulcer increases 1.5 times. The cumulative effect of the significant variables on pressure ulcer risk follows a trend that increases significantly after the ninth day (Figure).

Table 5

Table 5



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These results indicated that 41.4% of the patients developed a pressure ulcer. This finding is higher than the results of similar studies, for example, the values in two studies performed in Turkey in 2009 (16.7%)12 and 2016 (15.5%).3 However, consistent with this study, other studies in Iran in 2012,13 2013,7 and 20162 showed the rate of pressure ulcers were 21.3%, 35.3%, and 45.7%, respectively. In a similar study conducted in the US in 2016,14 pressure ulcer incidence was reported to be 31%. A systematic review and meta-analysis performed in Iran showed that the rate of grade 1 pressure ulcers in Iran is 19% (95% confidence interval, 13%–25%).15 However, considering the results of other studies in ICUs, the rate varies from 21.3% to 45.7%.2,7,13 The differences observed among studies might stem from the preventive approaches followed by nurses, pressure relief equipment or measures, or the type of ICU where the patient populations were hospitalized.

Manzano et al16 reported that the risk of pressure ulcer increased by 4.2% for each day the patient used a ventilator. This study showed a similar correlation between duration of connection to mechanical ventilation and pressure ulcer occurrence.

Based on univariate analysis, none of the demographic variables including age, gender, BMI, or smoking and consumption of tobacco products were significantly related to pressure ulcer incidence. However, multivariate analysis showed the risk of pressure ulcer increased 2.5 times with age. Mohammadi et al7 showed that the average age of the patients with pressure ulcer was significantly higher.7 Moreover, results reported by Karayurt et al3 and Shahin et al17 demonstrated that a high BMI can add to the pressure applied to bony prominences, thereby increasing the risk of pressure ulcers. However, a study performed by Terekeci et al18 indicated that BMI has no significant impact on the incidence of pressure ulcers, similar to the present study.

The duration of hospitalization and duration of stay in the ICU are significantly related to the incidence of pressure ulcers; patients who experienced pressure ulcers were more likely stay in the hospital and ICU for longer periods. This result is in agreement with Bly et al.14 In addition, in the study conducted by Manzano et al,19 a significant relationship was found between length of hospital stay and pressure ulcer incidence, although no such relationship was observed between length of stay in the ICU and pressure ulcer incidence.19

These results showed that low hemoglobin level was significantly related to pressure ulcer incidence. Reports released by Bly et al14 and Tokgöz and Demir20 further confirm the significant relationship between hemoglobin level and pressure ulcer incidence: pressure ulcers occur more frequently among the patients with lower levels of hemoglobin. In other studies,3,7,21 hemoglobin level was not significantly related to pressure ulcer incidence. Researchers believe that low hemoglobin level can disturb blood delivery to tissues, thereby increasing the risk of tissue necrosis that may lead to pressure ulcers.

Consistent with Karayurt et al,3 the results of the present study showed that urinary output was significantly higher in the patients who developed a pressure ulcer. It is possible that dehydration from increased urine output may reduce tissue perfusion, accompanied by an increased risk of pressure ulcer.3

Although other studied hemodynamic variables were found to have no significant relationships to pressure ulcers, Cox regression modeling revealed that MAP is a predictor of pressure ulcers. A patient’s MAP is an important hemodynamic factor that is related to cardiac output and vascular resistance; changes in MAP may have significant consequences. Low MAP can result in the disruption of blood supply to organs, syncope, and shock. On the other hand, its increase can result in vascular injury, end organ damage, and stroke.22

Although there may be a direct relationship between MAP and a higher risk of pressure ulcer because of vessel fragility during the acute inflammatory phase,23 MAP is not an independent factor. Moreover, in older adults, because of arthrosclerosis, reduced elasticity of vascular wall fibers, and simultaneous collagen increase, vascular resistance increases, which is a precursor for increased MAP and its complications such as vascular damage. Finally, vascular alterations as patients age, in addition to increasing MAP, could predispose vessels to more damage and lead to pressure ulcers.22,24–27

Other studies, however, show different results. In Bly et al,14 low SBP, DBP, and MAP were more common in patients with pressure ulcers. In Senturan et al,12 low SBP was correlated with pressure ulcer incidence. Further, the results of Cox28 showed that lower values of SBP, DBP, and MAP were significantly related to pressure ulcer incidence.

Based on this research, among the oxygenation-related indices, the mean value of PH was significantly related to the incidence of pressure ulcers; that is, the value of PH was higher for the patients with pressure ulcers. These results are in agreement with those of Karayurt et al3 and Senturan et al.12 In this study, the value of PaCO2 was lower in the patients with higher PH values. Therefore, considering the vascular contraction attributable to alkalosis that can decrease tissue perfusion, this factor may also provide a basis for pressure ulcers.

Further, PEEP value was significantly related to pressure ulcer occurrence. However, in studies published by Mohammadi et al,7 Senturan et al,12 and Pender and Frazier,29 no such significant relationship was reported. Cox regression tests showed increases in mean PEEP cause decreases in pressure ulcer incidence. The optimal PEEP for prevention of small airways collapse is 5 cm H2O. Using PEEP in patients requiring mechanical ventilation will result in an increase in oxygen and carbon dioxide exchange via extending exhalation duration.30 In this study, 41.8% of patients with a pressure ulcer had a PEEP lower than 5 cm H2O, whereas 84.6% of patients without pressure ulcer had a PEEP higher than 5 cm H2O. It is likely that exact regulation of PEEP can help improve arterial blood oxygenation and consequently improve tissue oxygenation and potentially prevent pressure ulcers.

Braden scale scores were not significantly related to the incidence of pressure ulcers, which is in line with at least one other study.3 However, in the studies by Mohammadi et al,7 Cox and Roche,21 and Tayyib et al,31 Braden scale scores were significantly related to pressure ulcer incidence. Based on observed GCS scores, no significant relationship was identified between the level of consciousness and pressure ulcer incidence either. However, Mohammadi et al7 concluded that low consciousness level plays a major part in the incidence of pressure ulcer. Even though a low consciousness level can reduce patient mobility, consistent nursing care (eg, frequent position changes) can neutralize the impact of reduced mobility on pressure ulcer occurrence. Finally, no significant relationship was found between CCI values and the incidence of pressure ulcers. However, Bly et al14 noted a significant relationship between a history of respiratory disease and pressure ulcers.

Investigating the variables using a Cox regression model, it was found that among the studied variables, age, MAP, and PEEP were good predictors of pressure ulcer occurrence. In Mohammadi et al,7 the results obtained from logistic regression showed that age, duration of mechanical ventilation, and level of consciousness are the most important contributing factors. As a person ages, skin resistance decreases. A thinner dermis results in a decrease in the sense of touch, subcutaneous fat, and vascular fragility.7 Moreover, aging results in vascular system alterations, such as arthrosclerosis and higher peripheral vessel resistance (especially in persons aged 50-55 years). Based on Poiseuille’s law, by doubling the diameter of a vessel, blood flow increases 16 times; however, a decrease in vessel diameter as seen with aging will have a reverse effect.22,24–26 Researchers recommend that MAP should be measured regularly and precisely, and in older adults and those with higher- or lower-than-normal MAP, pressure point assessment should be performed more frequently.

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Implications for Future Research

The authors recommend that future research examine the relationship of ankle-brachial indices and blood viscosity to pressure ulcer. Moreover, in this study, patients were hospitalized in the ICU for a variety of reasons, such as trauma and surgery. Each circumstance may have different effects on pressure ulcer rates, so more studies on the effects of each precipitating disease on pressure ulcers individually are recommended, as well as studies with different time frames and those that focus on staging.

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Although the researchers tried to use rigorous inclusion criteria, this study like any other study has some limitations. Because nearly 50% of studied participants were trauma patients for whom no data on peripheral vascular diseases were provided, these results might not be easily generalized to other patient populations.

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Results showed that older age, abnormal MAP, and lower PEEP were significantly associated with pressure ulcers. Researchers recommend providers pay more attention to hemodynamic parameters (especially MAP) and determine the most appropriate PEEP; these should be emphasized in standard nursing education. Older adults should be regularly and carefully assessed for pressure ulcer risk. It is recommended that MAP monitoring be better incorporated into pressure ulcer prediction tools for patients using a mechanical ventilator.

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critical care; hemodynamics; ICU; nursing; oxygenation; pressure ulcer

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