Pressure ulcers (PrUs) are a common complication in intensive care unit (ICU) patients who are sedated, ventilated, and/or bedridden for long periods. Clough1 compared ICU patients in a prospective study and reported 63% mortality in patients with PrUs and 15% mortality in patients without PrUs. Although previous studies have shown that the development of a PrU has no direct effect on mortality in patients hospitalized in an ICU, hospital-acquired PrUs (HAPUs) may indirectly contribute to mortality in certain patients.2,3 Patients who develop HAPUs experience added morbidity, pain, and psychosocial distress, which are associated with a loss of independence and social isolation.
The incidence of HAPUs is a quality-of-care indicator in an institution, and failure to provide appropriate preventive care may increase the risk of litigation. In addition, HAPUs contribute to increased healthcare costs.4 Previous reports on the rate of PrUs in ICU patients have ranged from less than 1% to greater than 50%.1,5–15
Standard nursing practices to prevent PrUs, timely evaluation of an ICU patient’s risk of PrUs, and assessment within 12 hours after admission have been recommended for critically ill patients.16
Multiple studies of the risk factors for PrUs in ICU patients have been performed.17–20 The relationships between PrU development and skin barrier factors, however, have not been fully characterized. Skin contributes to the maintenance of homeostasis by acting as a barrier against infection and water loss and protects against noxious physical and chemical stimuli in the environment. The epidermis, especially the stratum corneum, is primarily responsible for the protective properties of the skin. The complex laminate layers of lipid-enveloped dead cells in the stratum corneum form a keratinized cuticle at the surface of the skin, the physical properties of which mediate skin barrier function. Factors affecting skin barrier function include the moisture and sebum content of the stratum corneum and the pH of the skin surface. The moisture in the stratum corneum affects the shape, smoothness, and elasticity of skin. As the stratum corneum matures, the membranes of dying epithelial cells are replaced by ceramides, and a network of keratin fibers forms. This fibrous hydrophobic layer protects the underlying soft tissue and prevents water loss by evaporation (Figure 1). Moisture normally comprises 30% to 50% of the mass of the stratum corneum.
Sebaceous glands secrete sebum on the surface of the stratum corneum. Sebum consists of a variety of lipids, including triglycerides, diglycerides, free fatty acids, waxy esters, and squalene, which moisturize the stratum corneum, inhibit the growth of bacteria, and transport fat-soluble substances throughout the epidermis. The pH of the skin surface is the result of the combined effects of water-soluble substances in the stratum corneum, the secretion of sweat and sebum at the skin surface, the lipid content of the stratum corneum, and the effusion of carbon dioxide. The pH of the skin surface influences the maturation of the stratum corneum and inhibits microbial growth. The skin surface pH normally ranges from 4 to 6. Elevated pH can contribute to increased microbial growth on the skin surface and diminish skin barrier function.21,22
The relatively high incidence of PrUs in ICU patients, despite the implementation of preventive nursing practices and various methods of PrU risk assessment, warrants further investigation of the underlying causes of PrUs. Although certain aspects of skin physiology are related to the healing of PrUs,21 possible risk factors related to skin physiology for the development PrUs in immobile ICU patients have not been thoroughly investigated. In addition, data regarding risk factors for PrUs in Asian patients are scant. The aim of the authors’ descriptive study was to determine whether certain skin barrier factors correlated with the incidence of PrUs in immobile ICU patients in China. The authors focused their investigation on the contribution of skin-associated factors to the moisture and sebum content of the stratum corneum and the pH of the skin surface at anatomical sites where PrUs commonly develop.23
PATIENTS AND METHODS
This multiphase project was performed from November 2012 to September 2013 in a 1200-bed university hospital in China that provides care to both urban residents of Hangzhou City and rural residents from the surrounding areas of the Zhejiang Province. The authors enrolled patients who were admitted to the surgical ICU at the People’s Liberation Army Hospital No. 117, Hangzhou, China, for a minimum of 7 days. Patients with PrUs on admission to the ICU and patients with any dermatologic condition that might have affected the evaluation of skin barrier factors were excluded from the study. None of the patients were malnourished on admission to the ICU.
The authors’ study was performed in accordance with good clinical practice guidelines and the Declaration of Helsinki with regard to ethical principles for research involving human subjects. The authors’ study was approved by the ethics committee of their institution. Written, informed consent was obtained from all of the patients or their guardians/family caregivers before enrollment.
Age, sex, diagnosis, and the score for the Acute Physiology and Chronic Health Evaluation (APACHE) IV24 were recorded on admission to the ICU. Measurements of skin barrier factors and the Braden Scale for Predicting Pressure Sore Risk25 were performed once daily from ICU admission to discharge or to the development of a PrU. The length of stay (LOS) was recorded for each patient and was defined as the time from ICU admission to discharge.
All of the PrUs that developed were evaluated according to the 2007 recommendations of the National Pressure Ulcer Advisory Panel (NPUAP 2007).26 (Note: The NPUAP has recently changed the terminology of PrU to pressure injury and made updates to its stages of pressure injury. The authors of this study used the 2007 recommendations at the time of their study.) The patients’ room temperatures were maintained at 18° C to 22° C and 40% to 60% relative humidity. The rooms received natural light, but patients were not exposed to direct sunlight at any time. The following standard nursing interventions were used to prevent the development of PrUs27:
- Patients were turned in bed every 2 hours.
- A pressure-relieving foam or air mattress was used.
- The patient was protected from friction and moisture by straightening or changing the bed linens.
- Patients received daily sponge baths.
The APACHE IV was used to evaluate the severity of disease,24,28,29 quantify 12 physiological variables during the first 24 hours after ICU admission, and classify patients by mortality risk based on severity of disease.24 The APACHE IV model has been validated for the evaluation of patients in an ICU.29,30 The maximum score for the APACHE IV is 71, with higher scores indicating more severe disease and a greater risk of mortality.
The risk of a PrU was assessed using the Braden Scale,5 which has been validated for evaluating the risk of PrUs in ICU patients.31,32 The Braden Scale consists of the following 6 subscales: mobility, activity, sensory perception, skin moisture, friction and shear, and nutrition.31 Possible subscale scores range from 1 to 3 or 1 to 4, yielding a total Braden score ranging from 6 to 23, with a lower score indicating a higher risk of PrU.33 Based on the total score, the risk of PrU is categorized as follows: highest risk (<9), high risk (10–12), moderate risk (13–14), low risk (15–18), and minimal risk (19–23). The authors used a cutoff score of <12 to identify patients at significant risk of PrU development.
The skin barrier factors included the moisture and sebum content of the stratum corneum and the pH of the skin surface. The authors confirmed that the patients used no skin care products within 4 hours before the skin barrier factors were measured. The testing sites were cleaned with 75% alcohol using a cotton ball and allowed to dry for 10 to 20 minutes before the skin barrier measurements were recorded. The skin barrier factors were measured at the scapula, lower sacrum, hip, and heel, and each measurement was recorded 3 times. The moisture and sebum content were measured separately using a CM825 Corneometer and a SM815 Sebumeter (Courage & Khazaka Electronics, Cologne, Germany), respectively. Higher values for the moisture and sebum measurements indicate a higher water and lipid content, respectively. The skin surface pH was measured using a PH900 Skin-PH-Meter (Courage & Khazaka Electronics).
Assessment of Pressure Ulcer Severity
All of the PrUs that developed were evaluated according to the NPUAP 2007, as previously described.26 The PrU staging was assessed independently by 3 nurses trained in PrU care, including 2 unit nurses and the head nurse. Inconsistencies between the assessments of the unit nurses were resolved based on the assessment of the head nurse.
Data analysis was performed using the Statistical Package for Social Sciences, version 17.0, computer software (IBM, Armonk, New York). The continuous data are expressed as the mean and SD. Descriptive statistics were used to examine the distributions of the demographic, clinical, and hospitalization data. Intergroup differences in age, moisture content, sebum content, skin surface pH, APACHE IV score, and Braden score were evaluated using Student t tests and a χ2 analysis. Correlations between study variables were evaluated using bivariate logistic regression. The level of statistical significance was set at P < .05.
The demographic, clinical, and hospitalization data are shown in Table 1. The authors’ study sample included 102 patients, 54 (52.9%) men and 48 (47.1%) women. The patients ranged in age from 23 to 88 years, with a mean age of 55.7 (SD, 19.1) years. Initial diagnoses were femoral neck fracture (56 cases), femoral intertrochanteric fracture (26 cases), femoral shaft fracture (10 cases), and craniocerebral trauma (10 cases). The diagnoses for ICU admission included postoperative complications (38.2%), respiratory failure (30.4%), trauma (16.7%), and organ failure (12.7%). The mean LOS in the ICU was 15.8 (SD, 10.9) days. The incidence of PrU in the authors’ study sample was 31.4%. Among the patients with PrUs, 56% of them developed a PrU within 7 days following admission to the ICU.
The APACHE IV scores ranged from 2 to 51, with a mean score of 19.6 (SD, 7.43), and the Braden scores ranged from 6 to 20, with a mean score of 11.2 (SD, 1.60) (Table 2). According to the Braden Scale assessments, 43.5% of the patients were at high risk for PrUs (score 10–12). Patients at the highest risk for PrUs (score <9) comprised 19.8% of the sample. Of the 32 patients who developed PrUs, 4 of them (12.5%) had more than 1 PrU. Eighteen of the patients (56.2%) had suspected deep tissue injuries. Eleven of the patients (34.4%) had Stage I PrUs. Three of the patients (9.4%) had Stage II PrUs. None of the patients developed a Stage III, Stage IV, or unstageable PrU. The incidence of PrUs was significantly higher in men (33.3%) than in women (29.2%, P = .031; Table 3).
The results of comparisons of the study variables between the patients who developed PrUs and those who did not are shown in Table 3. No significant difference in mean age (P = .059) or the scapular (P = .053, P = .061, P = .058) or heel (P = .057, P = .072, P = .062) skin barrier factors was observed between the patients who developed PrUs and those who did not. The LOS in the ICU (P < .001), the moisture content and skin surface pH of the lower sacrum and hip (P < .001 for all), the APACHE IV score (P < .001), and the Braden score (P < .001) differed significantly between the patients who developed PrUs and those who did not.
The results of the bivariate correlational analysis are shown in Table 4. Weak positive correlations were observed between the Braden score and moisture content (r = 0.31, P < .01), the APACHE IV score and age (0.36, P = .01), and the APACHE IV score and moisture content (0.24, P < .01). Moderate positive correlations were observed between the Braden and APACHE IV scores (r = 0.46, P < .01) and between moisture content and skin surface pH (r = 0.54, P < .01). Strong positive correlations were observed between the LOS and moisture content (r = 0.61, P < .01) and between the LOS and skin surface pH (r = 0.72, P = .03). A weak negative correlation was observed between moisture content and sebum content (r = -0.33, P < .01). No significant correlation was observed between sebum content and skin surface pH (P = .74).
Despite the implementation of preventive nursing strategies, PrUs remain a common complication in ICUs. Previous reports of the incidence of PrUs in ICU patients have varied widely, with occurrences of more than 50% reported in some studies. The role of skin barrier factors in the development of PrUs has not been fully characterized, and studies of the risk of PrUs in Asian patients are lacking. The authors investigated the incidence of PrUs in a cohort of Chinese ICU patients. They included skin surface pH and the moisture and sebum content of the stratum corneum in their analysis of risk factors for PrUs.
Patient prognosis for PrUs may be less favorable in a surgical ICU, compared with other types of ICUs, such as long-term-care or rehabilitation ICUs. This might explain why the PrU incidence in the authors’ study (31.4%) was higher than that of studies that included patients from other ICU settings.32 The PrU rate in the authors’ study was lower than that of a previous hospital-wide study of the risk of PrUs in acute care institutions in Mainland China.15 In contrast, Kwong et al14 reported a substantially lower rate of PrUs at 2 acute care hospitals in Mainland China. However, they reported the incidence of Stage I and Stage II PrUs only in patients from various acute care wards, whose mean LOS (11 days) was substantially shorter than that of the authors’ ICU patients (18 days).
The inclusion criteria for this study required an ICU stay of more than 7 days to help ensure the full range of PrUs was included in the authors’ analysis of skin barrier–related risk factors. This criterion likely contributed to a longer LOS (18 days) than that reported in a previous study of ICU patients in Mainland China (5 days).34 The definition of ICU does not differ considerably between the United States and China. Studies of PrU rates in Chinese ICUs, however, are scant; thus, direct comparisons of covariates, such as LOS, between Chinese studies and American or European studies are not straightforward because ICU conditions vary across Mainland China.35,36 The average LOS in Chinese hospitals is 10.9 days, which is considerably longer, compared with 5.6 days in the United States.15 Therefore, it is likely that the LOS in Chinese ICUs also reflects this trend.
The authors found that the incidence of PrUs in men was significantly higher than that in women, despite some conflicting reports in the literature. Previous studies have also reported a higher incidence of PrUs in men,37,38 but multiple other studies have reported a higher incidence of PrUs in women.39–41 Therefore, the role of sex as a risk factor for PrUs requires further investigation. The average age of the authors’ ICU patients (55.7 years) was similar to that reported by a previous study of ICUs in Mainland China (58.5 years).34 In the authors’ study, the men were older than the women, but without statistical significance. It is possible that age may have influenced the role of sex in the development of PrUs, but other factors such as body weight differences may have been the reason.
Most ICU patients have multiple risk factors for PrUs, and no consensus exists on how best to measure these factors. The authors’ study showed that patients who developed PrUs were hospitalized longer and had poorer skin barrier function, compared with those who did not develop PrUs. This indicates that the importance of skin barrier assessment may increase with a longer LOS in the ICU. The authors observed that the moisture content of the stratum corneum was significantly lower and the skin surface pH was significantly higher at the lower sacrum and hip of patients with PrUs compared with those without PrUs. Therefore, nursing strategies aimed at preventing the development of PrUs may benefit from increased attention on these regions.
It is important to consider the limitations of this study. The authors’ small sample size and the single-center study design may have influenced their results. In addition, the therapeutic modalities and individual patient characteristics, such as body mass index, were not considered in their analysis. Although the authors’ findings suggest that altering the skin surface pH and moisture content of the stratum corneum at the lower sacrum and hip might be beneficial in some cases, it remains unclear whether manipulating these variables can change the course of the underlying PrU pathology. Therefore, the interpretation of the authors’ results should be limited to the identification of risk factors for PrUs. Their findings warrant future studies of the contributions of skin surface pH and moisture content of the stratum corneum to PrU pathology and investigations of the effects of altering these variables on PrU progression at the lower sacrum and hip.
The incidence of PrUs among Chinese patients in a surgical ICU was 31.4%. The authors found that the skin surface pH and the moisture content of the stratum corneum at the lower sacrum and hip were independent risk factors for PrU development, whereas skin barrier factors at the scapula and heel were not. Skin barrier assessment might be useful for personalizing nursing care and skin care regimens as part of a comprehensive strategy for PrU prevention in ICU patients.
1. Clough N. The cost of pressure area management in an intensive care unit. J Wound Care 1994;3:33-5.
2. Thomas DR, Goode PS, Tarquine PH, Allman RM. Hospital-acquired pressure ulcers and risk of death. J Am Geriatr Soc 1996;44:1435-40.
3. Moore Z. US Medicare data show incidence of hospital-acquired pressure ulcers is 4.5%, and they are associated with longer hospital stay and higher risk of death. Evid Based Nurs 2013;16:118-9.
4. VanGilder C, Amlung S, Harrison P, Meyer S. Results of the 2008-2009 International Pressure Ulcer Prevalence Survey and a 3-year, acute care, unit-specific analysis. Ostomy Wound Manage 2009;55(11):39-45.
5. Bergstrom N, Demuth PJ, Braden BJ. A clinical trial of the Braden Scale for Predicting Pressure Sore Risk. Nurs Clin North Am 1987;22:417-28.
6. Weststrate JT, Bruining HA. Pressure sores in an intensive care unit and related variables: a descriptive study. Intensive Crit Care Nurs 1996;12:280-4.
7. Robnett MK. The incidence of skin breakdown in a surgical intensive care unit. J Nurs Qual Assur 1986;1:77-81.
8. Marchette L, Arnell I, Redick E. Skin ulcers of elderly surgical patients in critical care units. Dimens Crit Care Nurs 1991;10:321-9.
9. Jiricka MK, Ryan P, Carvalho MA, Bukvich J. Pressure ulcer risk factors in an ICU population. Am J Crit Care 1995;4:361-7.
10. Hunt J. Application of a pressure area risk calculator in an intensive care unit. Intensive Crit Care Nurs 1993;9:226-31.
11. Weststrate JT, Hop WC, Aalbers AG, Vreeling AW, Bruining HA. The clinical relevance of the Waterlow pressure sore risk scale in the ICU. Intensive Care Med 1998;24:815-20.
12. Lowery MT. A pressure sore risk calculator for intensive care patients: ‘the Sunderland experience’. Intensive Crit Care Nurs 1995;11:344-53.
13. Reddy M, Gill SS, Rochon PA. Preventing pressure ulcers: a systematic review. JAMA 2006;296:974-84.
14. Kwong E, Pang S, Wong T, Ho J, Shao-ling X, Li-jun T. Predicting pressure ulcer risk with the modified Braden, Braden, and Norton scales in acute care hospitals in Mainland China. Appl Nurs Research 2005;18:122-8.
15. Zhao G, Hiltabidel E, Liu Y, Chen L, Liao Y. A cross-sectional descriptive study of pressure ulcer prevalence in a teaching hospital in China. Ostomy Wound Manage 2010;56(2):38-42.
16. Carlson EV, Kemp MG, Shott S. Predicting the risk of pressure ulcers in critically ill patients. Am J Crit Care 1999;8:262-9.
17. Keller BP, Wille J, van Ramshorst B, van der Werken C. Pressure ulcers in intensive care patients: a review of risks and prevention. Intensive Care Med 2002;28:1379-88.
18. Frankel H, Sperry J, Kaplan L. Risk factors for pressure ulcer development in a best practice surgical intensive care unit. Am Surg 2007;73:1215-7.
19. Terekeci H, Kucukardali Y, Top C, Onem Y, Celik S, Oktenli C. Risk assessment study of the pressure ulcers in intensive care unit patients. Eur J Intern Med 2009;20:394-7.
20. Nijs N, Toppets A, Defloor T, Bernaerts K, Milisen K, Van Den Berghe G. Incidence and risk factors for pressure ulcers in the intensive care unit. J Clin Nurs 2009;18:1258-66.
21. Schneider LA, Korber A, Grabbe S, Dissemond J. Influence of pH on wound-healing: a new perspective for wound-therapy? Arch Dermatol Res 2007;298:413-20.
22. Junkin J, Selekof JL. Prevalence of incontinence and associated skin injury in the acute care inpatient. J Wound Ostomy Continence Nurs 2007;34:260-9.
23. Grey JE, Harding KG, Enoch S. Pressure ulcers. BMJ 2006;332:472-5.
24. Zimmerman JE, Kramer AA, McNair DS, Malila FM. Acute Physiology and Chronic Health Evaluation (APACHE) IV: hospital mortality assessment for today’s critically ill patients. Crit Care Med 2006;34:1297-1310.
25. Bergstrom N, Braden BJ, Laguzza A, Holman V. The Braden Scale for Predicting Pressure Sore Risk. Nurs Res 1987;36:205-10.
26. Black J, Baharestani MM, Cuddigan J, et al. National Pressure Ulcer Advisory Panel’s updated pressure ulcer staging system. Adv Skin Wound Care 2007;20:269-74.
27. Health Quality Ontario. Pressure ulcer prevention: an evidence-based analysis. Ont Health Technol Assess Ser 2009;9(2):1-104.
28. Afessa B, Gajic O, Keegan MT. Severity of illness and organ failure assessment in adult intensive care units. Crit Care Clin 2007;23:639-58.
29. Brinkman S, Bakhshi-Raiez F, Abu-Hanna A, et al. External validation of Acute Physiology and Chronic Health Evaluation IV
in Dutch intensive care units and comparison with Acute Physiology and Chronic Health Evaluation II and Simplified Acute Physiology Score II. J Crit Care 2011;26(1):105. e111-108.
30. Kramer AA, Yi J, Zimmerman JE. Independent validation of APACHE IV ICU length of stay prediction. Crit Care Med 2006;34(12):A127.
31. Braden BJ, Bergstrom N. Clinical utility of the Braden Scale for Predicting Pressure Sore Risk. Decubitus 1989;2(3):44-46, 50-41.
32. Hyun S, Vermillion B, Newton C, et al. Predictive validity of the Braden Scale for patients in intensive care units. Am J Crit Care 2013;22:514-20.
33. Wolverton CL, Hobbs LA, Beeson T, et al. Nosocomial pressure ulcer rates in critical care: performance improvement project. J Nurs Care Qual 2005;20:56-62.
34. Du B, An Y, Kang Y, et al. Characteristics of critically ill patients in ICUs in mainland China. Crit Care Med 2013;41:84-92.
35. Villar J, Kacmarek RM. Modern critical care medicine from China: an ancient civilization. Crit Care Med 2013;41:343-5.
36. Sun B, Ma L, Liu X, Gao X, Ni L. Development of neonatal respiratory and intensive care: Chinese perspectives. Neonatology 2012;101:77-82.
37. Cremasco MF, Wenzel F, Zanei SS, Whitaker IY. Pressure ulcers in the intensive care unit: the relationship between nursing workload, illness severity and pressure ulcer risk. J Clin Nurs 2013;22:2183-91.
38. Manzano F, Navarro MJ, Roldán D, et al. Pressure ulcer incidence and risk factors in ventilated intensive care patients. J Crit Care 2010;25:469-76.
39. Ülker Efteli E, Yapucu Günes Ü. A prospective, descriptive study of risk factors related to pressure ulcer development among patients in intensive care units. Ostomy Wound Manage 2013;59(7):22-7.
40. Pokorny ME, Koldjeski D, Swanson M. Skin care intervention for patients having cardiac surgery. Am J Critical Care 2003;12:535-44.
41. Shahin ES, Dassen T, Halfens RJ. Pressure ulcer prevalence in intensive care patients: a cross-sectional study. J Eval Clin Pract 2008;14:563-8.