Cigarette smoking and risk of pressure ulcer in adult intensive care unit patients
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1 bs_bs_banner International Journal of Nursing Practice 2014; 20: RESEARCH PAPER Cigarette smoking and risk of pressure ulcer in adult intensive care unit patients Mohammad Nassaji MD Associate Professor, Department of Infectious Diseases, Fatemieh Hospital, Semnan University of Medical Science, Semnan, Iran Zahra Askari MD Assistant of Internal Medicine, Department of Internal Medicine, Fatemieh Hospital,Semnan University of Medical Science, Semnan, Iran Raheb Ghorbani PhD Associate professor, Department of Social Medicine, Faculty of Medicine, Semnan University of Medical Science, Semnan, Iran Accepted for publication March 2013 Nassaji M, Askari Z, Ghorbani R. International Journal of Nursing Practice 2014; 20: Cigarette smoking and risk of pressure ulcer in adult intensive care unit patients The objective of this study was to assess relationship between smoking, some other risk factors and ulcers development in intensive care unit. This prospective cohort study was performed in two university-affiliated hospitals. The sample consisted of adult male patients who were admitted to medical surgical intensive care units. All eligible patients were grouped according to their cigarette smoking status as smoker and non-smoker. The final sample included 160 smokers and 192 non-smokers. Pressure ulcer occurred in 62 smoker patients and 28 of non-smoker who showed significant difference. Also number of pack-year of cigarettes smoking showed significant association with ulcer development. Ulcer stage was significantly different between the two groups. Besides of smoking, age, length of stay, faecal incontinency, diabetes mellitus, anaemia and trauma were significantly associated with pressure ulcers. Our study showed significant association between smoking and development of pressure ulcers. Key words: adult, intensive care unit, pressure ulcers, risk factors, smoking. INTRODUCTION Pressure ulcer (PU) is a common and serious complication of multiple morbidity and lack of mobility in hospital. It is defined as an area of localized damage to the skin and underlying tissue usually over a bony prominence, caused by pressure, shear or friction, or a combination of these. 1 Correspondence: Mohammad Nassaji, Department of Infectious Diseases, Fatemieh Hospital, Semnan University of Medical Sciences, 17 Shahrivar Boulevard, Semnan , Iran. hnassaji@ yah00.com; mnzmohammad@gmail.com This research was supported by a research grant from the Semnan University of Medical Sciences. These ulcers are associated with an increased risk of infection, disability, high level of dependence, longer hospital stay and higher hospitalization costs. 2 Development of PU is complex and multifactorial. The most important pathologic event is the changes in the blood supply to dermal tissues that leads to decreased capillary blood flow and tissue ischaemia. These changes are ultimately responsible for necrosis of skin and subcutaneous tissue and formation of PU. 3 Several risk factors are associated with increased prevalence of PU including immobility, vascular diseases, neuropathies, nutritional status, urine and faecal incontinency, age, and chronic diseases such as diabetes mellitus. 4 doi: /ijn.12141
2 Smoking and pressure ulcer 419 Patients in intensive care units (ICUs) are at high risk for development of PUs because of severity of illness, haemodynamic instability, movement restriction for extended periods and use of sedative and analgesic drugs that decrease sensory perception. 5 The reported incidence of PU in critical care patients varies widely from 1% to 56% The first step in preventing PUs is determining the preventable risk factors. Consensus on some risk factors is lacking, and the significance of these factors is yet to be elucidated. Smoking is one of risk factors that has been suggested for the development of PU. 11 Smoking has been associated with significant effects on all systems of the body including skin. The currently available literature suggests that smoking exerts deleterious effects on both morphological and functional aspects of the microcirculation. The mechanisms of this action include compromised endothelial-dependent vasorelaxation, thickening of the walls of arterioles, platelet aggregation and endothelial cell dysfunction. 12 In addition, collagen synthesis and the deposition of mature collagen in the extracellular matrix are reduced by smoking. This phenomenon leads to an imbalance between biosynthesis and degradation of dermal proteins. On the other hand, smoking can also cause delayed wound healing secondary to decreased blood flow. 13 Few studies have been published about the relationship between smoking and the incidence of PU in ICU patients and most studies conducted on non-icu patients. Several of these studies have found a relationship between smoking and PU, whereas additional studies have not found a similar relationship The objective of this study was to determine the effect of smoking and some other risk factors on the incidence of PU in adult male patients hospitalized at ICU. MATERIALS AND METHODS This prospective cohort study was conducted in ICUs (20 medical surgical beds) in the two university-affiliated hospitals in Semnan province (Iran) from July 2011 to March All adult male patients admitted to the ICU who met the inclusion criteria were included in this study. Patients were included if they were male, 18 years or older, stayed for > 24 h in ICU and were free of PUs on admission. Because smoking rate between women is very low in our community, we did not include women in the study. Patients were excluded if they had a PU at the time of admission to the ICU, died during the study before development of PU, not evaluated within 24 h after admission and if admitted to ICU from other services of the hospital. The study was approved by the Research and Ethical Committee of the Semnan University of Medical Science. Informed written consent was obtained from all patients (where possible) or from their family in the cases of the unconscious patients. All eligible patients were grouped according to their cigarette smoking status as smoker (cases) and non-smoker (control). Smoking data were obtained from the patient and/or family. Subjects were defined as cigarette smokers if they had smoked five or more cigarettes per day for at least 6 months. Pack-year smoking (average number of packs of cigarettes smoked per day multiplied by the total number of years of smoking) was calculated. Undetermined, intermittent and ex-smoker were excluded. The following data were prospectively gathered in the first day of admission for each subject: age, body mass index (BMI), reason of hospitalization, haemoglobin level, level of consciousness, faecal incontinence, history of diabetes mellitus and hypertension. BMI was derived from the height and weight recorded for all patients admitted to the hospital. Patients level of consciousness was assessed by Glasgow Coma Scale (GCS) that routinely used in these wards. Patients had been classified according to the GCS into mild (13 15), moderate (9 12) and severe ( 8). Diabetes mellitus was defined as self-reported (or family reported) history of diabetes mellitus, use of oral hypoglycaemic agents or insulin. Hypertension was defined as self-reported history of hypertension and/or use of antihypertensive medications. Incontinence status was defined based on the observation of skin moisture and soiling with stool during the skin assessment. Urinary incontinence is not usually a problem in ICU because most patients have a bladder catheter and not included in our study. PU screening was performed to all patients within the first day of admission. The skin of each patient was assessed daily by one physician-researcher to identify the presence and stage of PU. PUs were classified into four stages according to the European Pressure Ulcer Advisory Panel staging bedsore. 22 A patient was considered to acquired PU if the ulcer was documented after admission in the ICU as a stage I or greater. PU stage I was defined if the skin was intact but showed a persistent
3 420 M Nassaji et al. erythematous area that did not blanch when it is pressed with a finger. The number of days from the ICU admission to the formation of PU was also registered. Patients were evaluated until PU onset or until ICU discharge or death in the group without PUs. During the study period, routine protocols for prevention of PUs were in place in both ICUs. Preventive measures included turning patients every 2 h, alternating pressure mattress and the use of support surfaces. Data were analysed by one sample Kolmogorov Smirnov test, χ 2 test, Mann Whitney U-test, Student s t-test and logistic regression using SPSS software (version 16.0, SPSS Inc., Chicago, IL, USA). RESULTS Of the 2046 patients admitted to both ICU during the study period, 352 patients met the inclusion criteria. This final sample was included 160 smokers and 192 non-smokers and evaluated for development of PU. Mean (± standard deviation (SD) ) age of patients was 55.7 (± 20.3) years and control 48.8 (± 24.7) years (P < 0.001). Mean (± SD) BMI of smoker was 24.1 (± 2.7) and for non-smokers was 24.0 (± 2.30) with no significant difference (P = 0.357). Clinical characteristics of the subjects are summarized in Table 1. Table 1 Clinical characteristics of study patients Smoker Non-smoker P-value Length of ICU stay, 11.0 ± ± days (Mean ± SD) Reason of admission n (%) Trauma 86 (53.8) 104 (54.2) Postsurgical 30 (18.8) 35 (18.2) CVA 13 (8.1) 16 (8.3) Unconsciousness 13 (8.1) 10 (5.2) Others 31 (19.4) 37 (19.3) Anaemia n (%) 93 (58.1) 107 (55.7) Diabetes mellitus n (%) 24 (12.5) 10 (5.2) Hypertension n (%) 21 (13.1) 24 (12.5) Faecal incontinency n (%) 64 (40) 38 (19.8) < Level of consciousness n (%) Mild 103 (64.4) 143 (74.5) Moderate 31 (19.4) 24 (12.5) Sever 26 (16.2) 25 (13) Cerebrovascular accident. Overall, 90 (25.6%) of patients admitted to ICUs developed PU. PUs occurred in 62 smoker patients (38.8%) and 28 (14.6%) of non-smoker that showed significant difference (P < 0.001). Also, PU development was significantly associated with pack-year of smoking (P < 0.003). Ulcer stages in two groups are shown in Table 2. Most ulcers were stage I. No patient developed a stage IV ulcer. Ulcer stage was significantly different between two groups (P = 0.003). Patients with PU were more likely to be older (P = 0.001), have higher BMI (P = 0.029), diabetes mellitus (P < 0.001), hypertension (P = 0.006), anaemia (P = 0.007), faecal incontinency (P < 0.001), lower GCS (P < 0.001) trauma (P < 0.001) and longer duration of hospitalization (P < 0.001). Logistic regression analysis showed that development of a PU was significantly associated with smoking pack-year, age, length of ICU stay, faecal incontinency, diabetes mellitus, trauma and anaemia (Table 3). DISCUSSION PU represents one of the main complications among critical patients. It is generally burdensome to treat, results in complication and prolonged hospital stay and increases financial burden. Accurate identification of risk factors and patient who might be at risk is a prerequisite for determining and implementation of appropriate strategies to prevent PUs after admission to the hospital. The results of this study revealed that the overall PU incidence in intensive care settings was 25.6%. Other studies have shown varying incidences. These widely varied reported incidences of PUs in critically ill patients are due to differences in population characteristics, Table 2 Distribution of pressure ulcer stage in smoker and nonsmoker patients Ulcer stage Smoker Non-smoker n % n % I II III IV Total
4 Smoking and pressure ulcer 421 Table 3 Logistic regression analysis results for the associations between variables and pressure ulcer Variables β Coefficient SE (β) P-value Odds ratio (OR) 95% CI for OR Age < Length of ICU stay < Faecal incontinency Diabetes mellitus Anaemia Smoking Trauma < Constant CI, confidence interval. inclusion criteria, different preventive methods implemented and data collection methods. Some studies reported similar or higher incidence when compared with our finding. 14,17,23 25 A lower incidence than our study was reported by other investigators. 10,26 28 Some of the aforementioned studies that reported lower incidence did not include stage I ulcers. A low incidence might also reflect a good application of preventive measures and or a high proportion of low-risk patients. This study supports other studies, which revealed that the highest PU prevalence rates were found for PUs stage I. 6,26,29 Having the majority of the PUs to be stage I is assumed to be due to the effect of the PU preventive measures implemented in the ICUs. In addition, the patients included have had younger age when compared with most previous studies. We found significant differences in PU incidence among the smoker and non-smoker in our study (P < 0.001). Our analysis also revealed that the higher number of cigarette smoking significantly was associated with the risk of PU (P < 0.001). Smoking has a vasoconstrictive effect on the capillaries at the dermal level, which diminishes the amount of oxygenated blood reaching the tissues. This effect mostly is mediated by nicotine. Nicotine inhibits the release of prostacyclin and thus causes vasoconstriction in skin. On the other hand, components of cigarette smoke, especially carbon monoxide, and hydrogen cyanide interfere with the processes involved in wound healing. 30 This significant association between smoking and development of PUs is consistent with some previous studies that have found a relationship between smoking and PUs. In one study on 105 ICU patients, smoking was significantly associated with PU. 14 In a another study in an ICU on immobilized patients, smoking was significantly associated with PU. 31 In a prospective cohort study that was conducted in two ICUs on 235 patients, results showed that cigarette smoking has a significant association with PUs. 17 Krause et al. in a study on 650 individuals with spinal cord injury found evidence that cigarette smoking is significantly associated with the risk of PU. 15 In a retrospective study of 176 spinal cord injured patients, PU incidence rates were more than fourfold higher in the smoker than in the non-smoker. 32 In a large study, persons with spinal cord injury who smoked a pack of cigarettes or more per day were 2.82 times more common to develop PU than non-smokers. 16 However, some previous research reported that smoking had no correlation with PU development In Rodriguez et al. s study although there was an association between smoking and PU development, this factor did not reach statistical significance. 33 Most of these studies that not confirmed this association were conducted on non-icu patients. Another finding in our study was that the ulcer stage was significantly difference between two groups (P = 0.003). Smoker patients have had higher stage of PU when compared with non-smoker. The result shows that more pack-years of smoking had significant association with higher incidence and more extensive pressure sores. Six other variables that were independently associated with risk of PU were age, duration of hospitalization, faecal incontinency, diabetes mellitus, anaemia and trauma.
5 422 M Nassaji et al. The results of this study confirmed other studies stating that older age was a potential risk factor in PU. 23,24,34 36 Older patients have more risk factor for development of PU including decreased activity and mobility, diminished tissue tolerance, decreased vascularization of skin, decreased pain perception and increased risk of comorbidities. In contrast, there are some studies that did not find age to have association with PU development. 10,33,36 39 The results of this study support the results of other studies that revealed longer ICU stay has been associated with a greater risk of PU. 10,24 26,34 In our study, 96.7% of all PU developed in patients who had more than 7 days hospitalization in ICU. In contrast to our finding, other investigators found no relationship between the duration of hospitalization and PU development. 14,17,37,39 The majority of studies have reported that the risk for PU is higher in patients with diabetes mellitus. 9,23,27,40 Our study supported this relationship. This finding was not consistent in all of the studies in which these relationships were tested. 6,18,21,34 A statistically significant difference was found in the patients for PU development according to their faecal incontinency. These data coincide with literature findings, which reveal higher PU incidence levels in patients with bowel incontinency. 8,14,25,31 A moist environment and maceration, which can be caused by faecal and urinary incontinence in long time, was proposed to cause disturbance in skin integrity and increase the risk of PU development. By contrast, Sayar et al. reported in their study that there was no significant relationship between incontinency and PU development. 26 In another study, bowel incontinency was not a significant risk factor for development of PU. 21 Anaemia has been shown in some studies to have an effect on PU development. 25,29,34,36 In our study, also, anaemia was significantly associated with development of PU. Anaemia can cause decrease in the tissue oxygenation and impair regeneration. However, there are studies that have not found anaemia to have significant effect on PU development. 26,31,34 Our study had some limitations. First, the BMI of most patients was calculated from previous weight and height measurements. Second, we did not include nutritional status of patients. Third, the study was based only in male patients. Finally, we cannot rule out that some PUs are due to associated comorbidities rather than directly related to smoke. CONCLUSION Our study showed significant association between smoking and development of PU as well as its severity. Advising to quit smoking can be undertaken as an important part for reduction of PUs. Future researches especially with larger sample size and with targeting the smoking as an important risk factor in relation to PU development are recommended. ACKNOWLEDGEMENT This research was supported by a research grant from the Semnan University of Medical Sciences. REFERENCES 1 Grey JE, Harding KG, Enoch S. Pressure ulcers. BMJ (Clinical Research Ed.) 2006; 332: Wake WT. Pressure ulcers: What clinicians need to know. The Permanente Journal 2010; 14: Hanson D, Langemo DK, Anderson J, Thompson P, Hunter S. Friction and shear considerations in pressure ulcer development. Advances in Skin and Wound Care 2010; 23: Anders J, Heinemann A, Leffmann C, Leutenegger M, Pröfener F, von Renteln-Kruse W. Decubitus ulcers: Pathophysiology and primary prevention. Deutsches Ärzteblatt International 2010; 107: Shahin ES, Dassen T, Halfens RJ. Pressure ulcer prevalence and incidence in intensive care patients: A literature review. Nursing in Critical Care 2008; 13: Perneger TV, Héliot C, Raë AC, Borst F, Gaspoz JM. Hospital-acquired pressure ulcers: Risk factors and use of preventive devices. Archives of Internal Medicine 1998; 158: Manzano F, Navarro MJ, Roldán D et al. Granada UPP Group. Pressure ulcer incidence and risk factors in ventilated intensive care patients. Journal of Critical Care 2010; 25: Shahin ES, Dassen T, Halfens RJ. Pressure ulcer prevalence in intensive care patients: A cross-sectional study. Journal of Evaluation in Clinical Practice 2008; 14: Keller BPJA, Wille J, van Ramshorst B, van der Werken C. Pressure ulcers in intensive care patients: A review of risk and prevention. Intensive Care Medicine 2002; 28: 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 Medicine 1998; 24: Lyder CH. Pressure ulcer prevention and management. JAMA: The Journal of the American Medical Association 2003; 289:
6 Smoking and pressure ulcer Lehr HA. Microcirculatory dysfunction induced by cigarette smoking. Microcirculation 2000; 7: Thomsen SF, Sørensen LT. Smoking and skin disease. Skin Therapy Letter 2010; 15: Suriadi, Sanada H, Sugama J et al. Risk factors in the development of pressure ulcers in an intensive care unit in Pontianak, Indonesia. International Wound Journal 2007; 4: Krause JS, Vines CL, Farley TL, Sniezek J, Coker J. An exploratory study of pressure ulcers after spinal cord injury: Relationship to protective behaviors and risk factors. Archives of Physical Medicine and Rehabilitation 2001; 82: Saunders LL, Krause JS. Personality and behavioral predictors of pressure ulcer history. Topics in Spinal Cord Injury Rehabilitation 2010; 16: Suriadi, Sanada H, Sugama J, Thigpen B, Subuh M. Development of a new risk assessment scale for predicting pressure ulcers in an intensive care unit. Nursing in Critical Care 2008; 13: Jiricka MK, Ryan P, Carvalho MA, Bukvich J. Pressure ulcer risk factors in an ICU population. American Journal of Critical Care 1995; 4: Noble M, Voegeli D, Clough CF. A comparison of cutaneous vascular responses to transient pressure loading in smokers and nonsmokers. Journal of Rehabilitation Research and Development 2003; 40: Lloyd EE, Baker F. An examination of variables in spinal cord injury patients with pressure sores. SCI Nursing 1986; 3: Rabadi MH, Vincent AS. Do vascular risk factors contribute to the prevalence of pressure ulcer in veterans with spinal cord injury? The Journal of Spinal Cord Medicine 2011; 34: European Pressure Ulcer Advisory Panel [homepage on the Internet]. United Kingdom. Pressure Ulcer Treatment Guidelines Available from URL: Accessed 1 July Slowikowski GC, Funk M. Factors associated with pressure ulcers in patients in a surgical intensive care unit. Journal of Wound, Ostomy, and Continence Nursing 2010; 37: Bours GJ, De Laat E, Halfens RJ, Lubbers M. Prevalence, risk factors and prevention of pressure ulcers in Dutch intensive care units. Results of a cross-sectional survey. Intensive Care Medicine 2001; 27: Theaker C, Mannan M, Ives N, Soni N. Risk factors for pressure sores in the critically ill. Anaesthesia 2000; 55: Sayar S, Turgut S, Doğan H et al. Incidence of pressure ulcers in intensive care unit patients at risk according to the Waterlow scale and factors influencing the development of pressure ulcers. Journal of Clinical Nursing 2009; 18: Senturan L, Karabacack U, Ozdilek S et al. The relationship among pressure ulcers, oxygenation, and perfusion in mechanically ventilated patients in an intensive care unit. Journal of Wound, Ostomy, and Continence Nursing 2009; 36: Cox J. Predictors of pressure ulcers in adult critical care patients. American Journal of Critical Care 2011; 20: Williams DF, Stotts NA, Nelson K. Patients with existing pressure ulcers admitted to acute care. Journal of Wound, Ostomy, and Continence Nursing 2000; 27: Ortiz A, Grando SA. Smoking and the skin. International Journal of Dermatology 2012; 51: Cakmak SK, Gül U, Ozer S, Yiğit Z, Gönü M. Risk factors for pressure ulcers. Advances in Skin and Wound Care 2009; 22: Niazi ZB, Slalzberg CA, Byrne DW, Viehbeck M. Recurrence of initial pressure ulcer in persons with spinal cord injuries. Advances in Wound Care 1997; 10: Rodriguez GP, Garber SL. Prospective study of pressure ulcer risk in spinal cord injury patients. Paraplegia 1994; 34: Terekeci H, Kucukardali Y, Top C, Onem Y, Celik S, Oktenli C. Risk assessment study of the pressure ulcers in intensive care unit patients. European Journal of Internal Medicine 2009; 20: Eachempati SR, Hydo LJ, Barie PS. Factors influencing the development of decubitus ulcers in critically ill surgical patients. Critical Care Medicine 2001; 29: Nixon J, Cranny G, Iglesias C et al. Randomised, controlled trial of alternating pressure mattresses compared with alternating pressure overlays for the prevention of pressure ulcers: PRESSURE (pressure relieving support surfaces) trial. BMJ (Clinical Research Ed.) 2006; 332: Fife C, Otto G, Capsuto EG et al. Incidence of pressure ulcers in a neurologic intensive care unit. Critical Care Medicine 2001; 29: Scarlatti KC, Michel JL, Gamba MA, de Gutiérrez MG. Pressure ulcers in surgery patients: Incidence and associated factors. Revista Da Escola De Enfermagem Da USP2011; 45: Frankel H, Sperry J, Kaplan L. Risk factors for pressure ulcer development in a best practice surgical intensive care unit. The American Surgeon 2007; 73: Tschannen D, Bates O, Talsma A, Guo Y. Patient-specific and surgical characteristics in the development of pressure ulcers. American Journal of Critical Care 2012; 21:
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