RESEARCH ARTICLE


Hospital-acquired Pressure Ulcers in Trauma Patients: A Retrospective Study of 410 Patients at a Referral Trauma Center in the North of Iran



Mohammadreza Mobayen1, Samad Karkhah1, 2, Parisa Bagheri3, Alireza Feizkhah1, 4, Mahtab Taati Moghadam4, Hamideh Mohmmadnia5, Mahsa Sadeghi1, *
1 Burn and Regenerative Medicine Research Center, Guilan University of Medical Sciences, Rasht, Iran
2 Department of Medical-Surgical Nursing, School of Nursing and Midwifery, Guilan University of Medical Sciences, Rasht, Iran
3 Research Center for Health Information Management, Kashan University of Medical Sciences, Kashan, Iran
4 Student Research Committee, School of Medicine, Guilan University of Medical Sciences, Rasht, Iran
5 Guilan Road Trauma Research Center, Guilan University of Medical Sciences, Rasht, Iran


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Creative Commons License
© 2022 Mobayen et al.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: https://creativecommons.org/licenses/by/4.0/legalcode. This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

* Address correspondence to this author at the Burn and Regenerative Medicine Research Center, Guilan University of Medical Sciences, Rasht, Iran; E-mail: Mahsa_heris@yahoo.com


Abstract

Background:

Pressure ulcers (PUs) are among the most common chronic ulcers and complications of hospitalization.

Objective:

The present study aims to evaluate the prevalence of hospital-acquired PUs and their grades in trauma patients, comparing demographic characteristics, clinical features, and outcomes among patients without and with PUs referred to a trauma center in the North of Iran.

Methods:

In a retrospective study, 410 patients with trauma referred to a trauma center in the North of Iran were enrolled. Data were collected using a simple random sampling from March 2019 to September 2019.

Results:

The prevalence of PU in patients with trauma was 27.6%. Grade III (35.5%) and grade I (3.5%) wounds had the highest and lowest frequency of PU, respectively (P<0.001). The mean age of patients with PU was higher than patients without PU (61.73 vs. 47.71 years, P<0.001). The mean hemoglobin level of patients with PU was lower than patients without PU (9.93 vs. 12.25, P<0.001). PUs were more common in smokers compared to non-smokers (P<0.001), with a history of PU (P<0.001), a history of diabetes mellitus (P<0.001), and a history of hypertension (P<0.001). The mean length of stay in the hospital for patients with PU was higher than for patients without PU (13.02 vs. 5.54 days, P<0.001). 74.3% of people with PUs were completely immobile (P<0.001), and 60% of them had mild brain damage (GCS of 13 to 15). Also, the number of people with severe and moderate brain injury among PUs patients was 15% and 24.7%, respectively (P<0.001). Mobility, brain damage, Hemoglobin rate and smoking status were risk factors for pressure ulcers.

Conclusion:

Therefore, it is recommended that health managers and policymakers develop care and treatment plans by considering these risk factors.

Keywords: Pressure ulcer, Wounds, Injuries, Trauma nursing, Risk factors, Treatment.



1. INTRODUCTION

Pressure ulcers (PUs) are among the most common chronic ulcers and complications of hospitalization [1, 2]. PU is a localized lesion on the skin or underlying tissue, which often occurs in hospitalized patients due to pressure or friction on areas of the body, especially bony prominences [3]. PUs based on severity can be classified into four stages: redness of the skin (stage 1), loss of epidermis (stage 2), and loss of fat, muscle, and bone (stages 3 and 4) [4]. PUs are often associated with high treatment expenses, a higher length of stay in the hospital, and a higher risk of infection and mortality for the patients [5-8]. Furthermore, PUs can be good indicators of the quality of patient care, as their incidence varies in different hospitals and health centers [9, 10]. These injuries are often a secondary diagnosis rather than the leading cause of hospitalization, and sadly, they are frequently overlooked by carers [11]. Patients hospitalized or confined to a bed or wheelchair are at high risk for PUs due to clinical instability and less mobility [1, 8, 12]. While other examples of contributing factors for PUs are age, comorbidities, length of stay in hospital, malnutrition, smoking, and prolonged mechanical ventilation [13-17]. The risk of death from a patient with a PU is 2 to 6 times higher than a patient with healthy skin [18]. Although the quality of the care provided has improved significantly in many nations in recent years, nevertheless, PUs remains a significant health challenge worldwide [19]. The prevalence of PUs is varied in different regions of the world [8]. In Iran, for instance, the prevalence of PUs is believed to be between 10 and 50% [19]. According to Akhkand and Karimian studies, the prevalence of PUs in intensive care units (ICUs) ranges between 3.6% and 45.7%, although a more recent study indicated that this rate could be as low as 19% [8, 20]. PUs can cause significant pain, increased risk of infection and sepsis, additional surgical procedures, prolongation of length of stay in the hospital, and imposing additional costs on the patient and the health care unit [8]. Patients with PU often suffer from compromised quality of life and emotional wellbeing [21]. On the other hand, the cost of treatment of PU is 2.5 times the cost of its prevention [22]. Hence, it is necessary to identify high-risk patients and related factors while taking appropriate preventive measures in order to prevent the negative clinical and economic outcomes of PUs [1]. Therefore, the present study aimed to assess the prevalence of hospital-acquired PUs and their grades in patients with trauma, comparison of demographic characteristics, clinical features, and clinical outcomes among patients without and with PUs, and mobility and brain damage among patients with PUs at a referral trauma center in the North of Iran.

2. MATERIALS AND METHODS

2.1. Study design and subjects

In a retrospective study, 410 trauma patients referred to a trauma center in the North of Iran were enrolled. Based on equation , using the ratio of 0.19 in the previous study [20], d=0.038 and =0.05, the minimum sample size was obtained in 410 cases. Data were collected using a simple random sampling from March 2019 to September 2019. The required number of samples was selected using the table of random numbers and the last three digits of patients' files code. Patients who were admitted for at least 24 hours without PUs were included. The Ethics Committee approved this Research of Guilan University of Medical Sciences (IR.GUMS.REC.1399.072).

2.2. Data Collection

Data such as age, sex, length of stay in the hospital, history of PU, degree of PU, smoking, diabetes mellitus (all types of diabetes), blood group, blood pressure, hemoglobin level, mobility, and Glasgow coma scale (GCS) was collected. Skin assessments are generally classified in accordance with the European PU Advisory Panel (EPUAP) classification system for PU as normal or indicative of PU stages (I-IV): I) non-branched erythema; II) loss of skin with partial-thickness; III) loss of full-thickness skin and IV) Loss of full-thickness tissue [23]. Furthermore, the extent of brain damage was estimated based on the GCS criterion (a criterion for determining loss of consciousness in people over five years old):

1. Mild injury (GCS of 13 to 15).

2. Moderate injury (GCS of 9 to 12).

3. Severe injury (GCS of 3 to 8).

2.3. Statistical Analysis

Quantitative and qualitative variables were presented using mean (standard deviation) and number (percentage). The normality of the data was assessed using the Kolmogorov-Smirnov test. Independent t-test and chi-square test were used to evaluate study variables. Multivariate linear regression was applied to identify independent predictors of PU. All probable risk factors were first tested; then, a regular set of independent statistically remarkable covariates were designed in a multivariable model through binary logistic regression, and all data were analyzed two-tailed. A p-value < 0.05 was assumed statistically considerable for the aims of this paper. SPSS® V24.0 statistical package was used for conducting all analyses.

3. RESULTS

3.1. Participants

A total of 410 patients with trauma participated in the present study. Of the participants, 53.7% were male, 24.1% were smokers, 23.7% had a history of diabetes mellitus, and 31% had a history of hypertension. The mean age, hemoglobin level, and length of stay in the hospital were 51.57 (SD=24.67), 11.61 (SD=2.26), and 7.60 (SD=9.83), respectively (Table 1).

3.2. Prevalence of PU and its Grades in Patients with Trauma

The prevalence of PU in patients with trauma was 27.6%. Grade III (35.5%) and grade I (3.5%) wounds had the highest and lowest frequency of PU, respectively (P<0.001). The frequency of PUs grades in patients with PU is shown in Fig. (1).

3.3. Comparison of Demographic Characteristics, Clinical Features, and Clinical Outcomes among Patients without and with PUs

As presented in Table 1, the mean age of patients with PU was higher than patients without PU (61.73 vs. 47.71 years, P<0.001). The mean hemoglobin level of patients with PU was lower than patients without PU (9.93 vs. 12.25, P<0.001). Also, PU was more common in males than females (P=0.888), smokers compared to non-smokers (P<0.001), with a history of PU (P<0.001), with a history of diabetes mellitus (P<0.001), and with a history of hypertension (P<0.001). The mean length of stay in the hospital for patients with PU was higher than for patients without PU (13.02 vs. 5.54 days, P<0.001).

Fig. (1). Frequency of PU grades in patients with trauma.

Table 1. Comparison of demographic characteristics, clinical features, and clinical outcomes among patients without and with PUs (n=410).
Total (n=410) Patients without PUs (n=297) Patients with PUs (n=113) P-value
Demographic Characteristics
Gender 0.888
Male 220 (53.7) 160 (53.9) 60 (53.0)
Female 190 (46.3) 137 (46.1) 53 (47.0)
Age 51.57 (SD=24.67) 47.71 (SD=25.23) 61.73 (SD=19.90) <0.001
Smoking <0.001
Yes 99 (24.1) 55 (18.5) 44 (39.0)
No 311 (75.9) 242 (81.5) 69 (61.0)
Blood Groups 0.340
A+ 106 (25.9) 85 (28.6) 21 (18.6)
A- 27 (6.6) 18 (6.1) 9 (8.0)
B+ 68 (16.6) 46 (15.5) 22 (19.5)
B- 22 (5.4) 14 (4.7) 8 (7.1)
AB+ 19 (4.6) 13 (4.4) 6 (5.3)
AB- 8 (2.0) 5 (1.7) 3 (2.6)
O+ 125 (30.5) 94 (31.6) 31 (27.4)
O- 35 (8.5) 22 (7.4) 13 (11.5)
Clinical Features
A history of PU <0.001
Yes 66 (16.1) 0 (0) 66 (34.5)
No 344 (83.9) 297 (100) 47 (65.5)
A history of diabetes mellitus <0.001
Yes 97 (23.7) 58 (19.5) 39 (34.5)
No 313 (76.3) 239 (80.5) 74 (65.5)
A history of hypertension <0.001
Yes 127 (31.0) 80 (27.0) 47 (41.5)
No 283 (69.0) 217 (73.0) 66 (58.5)
Hemoglobin rate 11.61 (SD=2.26) 12.25 (SD=2.09) 9.93 (SD=1.79) <0.001
Clinical Outcome
Length of stay in hospital (days) 7.60 (SD=9.83) 5.54 (SD=5.72) 13.02 (SD=15.01) <0.001
Abbreviations: SD: Standard Deviation; PUs: Pressure Ulcers.
Data are presented as number (percentage) and mean (standard deviation).

3.4. Mobility and Brain Damage among Patients with PUs

74.3% of people with PUs were completely immobile (P<0.001) (Table 2), and 60% of them had mild brain damage (GCS of 13 to 15). Also, the number of people with severe and moderate brain injury among PUs patients was 15% and 24.7%, respectively (P<0.001) (Table 3).

Table 2. Comparison of mobility among patients without and with PUs (n=410).
Total (n=410) Patients without PUs (n=297) Patients with PUs (n=113) P-value
Mobility
Motionless 134 (32.7) 50 (16.8) 84 (74.3)
High restrictions on movement 37 (9.0) 12 (4.0) 25 (22.1) <0.001
Mild restriction in movement 39 (9.5) 35 (11.7) 4 (3.5)
No restrictions on movement 200 (48.8) 200 (67.3) 0
Abbreviations: SD: Standard Deviation; PUs: Pressure Ulcers.
Data are presented as number (percentage) and mean (standard deviation).
Table 3. Comparison of brain damage in patients without and with PUs (n=410).
Total (n=410) Patients without PUs (n=297) Patients with PUs (n=113)
Brain damage
Mild injury (GCS of 13 to 15) 333 (81.2) 265 (89.2) 68 (60.0)
Moderate injury (GCS of 9 to 12) 47 (11.5) 19 (6.3) 28 (24.7)
Severe injury (GCS of 3 to 8) 30 (7.3) 13 (4.3) 17 (15.0)
Abbreviations: SD: Standard Deviation; PUs: Pressure Ulcers; GCS: Glasgow Coma Scale.
Data are presented as number (percentage).

3.5. Risk Factors Associated with the Occurrence of Pressure Ulcers

All independent variables were analyzed in binary logistic regression with the dependent variable to analyze their association. Among those variables, mobility, brain damage, Hemoglobin rate and smoking status were found to be significant in binary logistic regression and then taken into multivariate analysis (Table 4). For instance, smokers were 3.4 times more likely to develop PU compared to patients who were non-smokers.

Table 4. Association between some selected variables and pressure ulcer.
Variable B Exp(B) 95% CI P-value
Smoking status 1.225 3.404 (1.596,7.263) .002
Hemoglobin rate -.385 .680 (0.576,0.803) <,001
Brain damage .168 1.183 (1.065,1.314) .002
Mobility -1.675 .187 (0.125,0.280) <,001
Constant 4.288 72.844 - <,001

4. DISCUSSION

This study showed that, generally, the prevalence of PU in patients with trauma was 27.6%. Meanwhile, Grade III (35.5%) and grade I (3.5%) wounds had the highest and lowest frequency of PU, respectively. The mean age of patients with PU was higher than patients without PU. The mean hemoglobin level of patients with PU was lower than patients without PU. PU was more common in males than females, smokers compared to non-smokers, with a history of PU, diabetes mellitus, and hypertension. The mean length of stay in the hospital of patients with PU was higher than patients without PU. 74.3% of people with PUs were completely immobile, and 60% had mild brain damage (GCS of 13 to 15). Also, the number of people with severe and moderate brain injury among PUs patients was 15% and 24.7%, respectively. In the present study, PU was observed in 27.6% of patients with trauma. Furthermore, the prevalence of PU varies in previous studies in different countries. The prevalence of PU in Saudi Arabia [24], Greece [25], Spain [7, 26], Turkey [27], Brazil [28, 29], Norway [23], and Iran [30] was 39.3%, 29.6%, 8.1 to 16%, 15.5%, 11 to 13.6%, 14.9%, and 13.4%, respectively. Differences in findings may be caused by the diversity in the features of the study population, data collection processes, inclusion criteria, and various methods of prevention and control of PU in hospitals [1]. Sample heterogeneity may also affect the prevalence of PU and identified risk factors [23]. Consistent with the present study, previous evidence from Norway [23], Iran [31], Saudi Arabia [24], Portugal [32], Greece [7], Brazil [28, 33], and the United States [34], as well as findings from three review studies showed that prolonged length of stay in the hospital was related with an increased risk of PUs [13, 15, 16]. During a prolonged stay in bed, the patient's tissues remain immobile and pressured, which leads to an increased risk of PUs [1]. One study in Iran showed that PUs in cases with muscle paralysis is five times higher than in others. These patients are at a higher risk of PU due to decreased mobility, increased pressure on the underlying tissues, and tissue necrosis [35]. Also, another study in Iran showed that trauma is a significant risk factor for PUs. Because long-term immobility and increased pressure on an area of the body in trauma patients can lead to the development of PUs [31]. Based on the results of this study, age has been identified as one of the risk factors for PU in patients with trauma, which was concordant with previous evidence from Iran [30, 31], Norway [36], Greece [7], Brazil [28], Portugal [32], and the United States [34]. Meanwhile, factors such as decreased mobility, tissue tolerance, skin vessels, and pain perception could also contribute to an increased risk of PU in older people [15, 31]. Nevertheless, two systematic studies have shown that there is inconsistency in the evidence. Factors such as medical complexity, iatrogenic skin lesions, and the presence of underlying disease in older people may affect findings, and lead to varied results [23]. Grade III and IV ulcers had the highest frequency of PU (34.5%), which was consistent with the results of previous evidence from China [37], Belgium [38], Portugal [32], Norway [36], and Iran [20, 31]. Preventive measures taken by hospital staff can reduce PU progression in the first stage, resulting in a lower incidence of grade III and IV wounds [31]. Consistent with the present study results, two studies have also identified smoking as a predisposing factor for patients with PUs [31, 35]. Nicotine in cigarettes prevents the distribution of prostacyclin and causes the capillaries on the skin's surface to contract. Consequentially, the amount of oxidized blood in the tissues is reduced. Also, carbon monoxide and hydrogen cyanide can hinder the healing process of the wound [31]. This study emphasized that diabetic patients are at a higher risk for PU. Previous studies from Iran [31, 35, 39], Norway [36], Greece [7], and a review study [15, 17] have also reported an association between diabetes and PU. Due to the higher prevalence of diabetes in older people, diabetes may be a confounding factor in analyzing the relationship between age and PUs. However, in the current data analysis, both diabetes and older age have been reported as independent risk factors for PUs [23]. Results of this study implicated that there was a significant relationship between hypertension and hemoglobin levels with PUs. People with hypertension and lower hemoglobin levels were more prone to PUs. Consistent with the present study results, previous studies from Iran [40], and India showed a direct correlation between hemoglobin level and PU development in hospitalized patients [41]. Also, two studies [40, 42] showed a direct correlation between hypertension (systolic blood pressure above 130) and PUs [42]. When the risk of developing a PU is established, individual prevention strategies must be implemented. It is recommended that health managers and policymakers develop care and treatment plans with the risk factors associated with PUs in mind. As nurses have a central role in preventing and managing under-pressure areas, they should also be able to identify the risk factors associated with developing PU and take adequate measures to provide appropriate care. Also, based on the components affecting PUs mentioned in this study, software packages for predicting or preventing pressure ulcers can be designed as a PU reduction strategy.

4.1. Limitations

This study had several limitations: it was conducted only in a single center, which may affect the generalizability of the findings of this study; also, no hypotheses were developed before the study. Thus, extreme caution is recommended for interpreting the statistical significance of this study.

4.2. Implications for Nursing Management

Nursing care has a significant impact on developing and preventing pressure ulcers. The results of this study can be considered in the development of nursing management programs. Nurses should be able to assess the risk of developing PU in patients using evidence-based methods or assessment and predictive tools and be aware of the risk factors that increase the likelihood of developing these lesions. It is also recommended that nurses classify PU development or severity patients according to clinical conditions and related risk factors and then take appropriate preventive measures. Controlling blood sugar and blood pressure, monitoring the hemoglobin and nutrition of patients, moving the patient or using a wavy mattress, timely treatment of burn wounds, and infection control should be an essential part of nursing care interventions for patients at PU risk.

4.3. Recommendations for Future Research

It is recommended that more clinical intervention studies be conducted, focusing on PU-related factors. Other possible factors affecting PU, such as body temperature, nutrition, albumin level, and infection, should also be considered in future studies.

CONCLUSION

Overall, the prevalence of PU in patients with trauma was 27.6%. Also, risk factors for hospital-acquired PUs included age, smoking, a history of PU, diabetes mellitus, hypertension, mean hemoglobin, and burn grade. The mean length of stay in the hospital for patients with PU was higher than for patients without PU. 74.3% of people with PUs were completely immobile, whilst this figure was only 60% for those who had mild brain damage. Also, the number of people with severe and moderate brain injury among PUs patients was 15% and 24.7%, respectively. Therefore, it is recommended that health managers and policymakers develop care and treatment plans by considering these risk factors.

LIST OF ABBREVIATIONS

PU = Pressure Ulcers
ICUs = Intensive Care Units
GCS = Glasgow Coma Scale
EPUAP = European PU Advisory Panel

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

The Ethics Committee approved this Research of Guilan University of Medical Sciences (IR.GUMS.REC.1399.072).

HUMAN AND ANIMAL RIGHTS

No animals were used in this research. All procedures performed in studies involving human participants were in accordance with the ethical standards of institutional and/or research committee and with the 1975 Declaration of Helsinki, as revised in 2013.

CONSENT FOR PUBLICATION

All data were obtained from patients during their hospitalization period, so the regional ethical committee waived the need for informed consent.

STANDARDS OF REPORTING

STROBE guidelines were followed.

AVAILABILITY OF DATA AND MATERIALS

The datasets are available from the corresponding author [M.S] upon reasonable request.

FUNDING

None.

CONFLICT OF INTEREST

The authors declare no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENTS

We sincerely thank Mojdeh Esmailzadeh and Armin Fazeli Masuleh, who participated in the preparation of the final version of the article.

REFERENCES

[1] Zarei E, Madarshahian E, Nikkhah A, Khodakarim S. Incidence of pressure ulcers in intensive care units and direct costs of treatment: Evidence from Iran. J Tissue Viability 2019; 28(2): 70-4.
[2] Ghazanfari MJ, Karkhah S, Maroufizadeh S, et al. Knowledge, attitude, and practice of Iranian critical care nurses related to prevention of pressure ulcers: A multicenter cross-sectional study. J Tissue Viability 2022; 31(2): 326-31.
[3] Rafiei H, Abdar ME, Iranmanesh S, Lalegani H, Safdari A, Dehkordi AH. Knowledge about pressure ulcer prevention, classification and management: A survey of registered nurses working with trauma patients in the emergency department. Int J Orthop Trauma Nurs 2014; 18(3): 135-42.
[4] Martin D, Albensi L, Van Haute S, et al. Healthy skin wins: A glowing pressure ulcer prevention program that can guide evidence-based practice. Worldviews Evid Based Nurs 2017; 14(6): 473-83.
[5] Wong AL, Walia GS, Bello R, Aquino CS, Sacks JM. Pressure ulcer prevalence and perceptions on prevention: A hospital-wide survey of health professionals. J Wound Care 2018; 27(Sup4): S29-35.
[6] Tubaishat A, Anthony D, Saleh M. Pressure ulcers in Jordan: A point prevalence study. J Tissue Viability 2011; 20(1): 14-9.
[7] Manzano F, Navarro MJ, Roldán D, et al. Pressure ulcer incidence and risk factors in ventilated intensive care patients. J Crit Care 2010; 25(3): 469-76.
[8] Akhkand SS, Seidi J, Ebadi A, Gheshlagh RG. Prevalence of pressure ulcer in Iran’s intensive care units: A systematic review and meta-analysis. Nurs Pract Today 2020; 7(1): 12-20.
[9] Usher K, Woods C, Brown J, et al. Australian nursing students’ knowledge and attitudes towards pressure injury prevention: A cross-sectional study. Int J Nurs Stud 2018; 81: 14-20.
[10] Hommel A, Gunningberg L, Idvall E, Bååth C. Successful factors to prevent pressure ulcers - an interview study. J Clin Nurs 2017; 26(1-2): 182-9.
[11] Zaratkiewicz S, Whitney JD, Lowe JR, Taylor S, O’Donnell F, Minton-Foltz P. Development and implementation of a hospital-acquired pressure ulcer incidence tracking system and algorithm. J Healthc Qual 2010; 32(6): 44-51.
[12] Schoonhoven L, Grobbee DE, Donders AR, et al. Prediction of pressure ulcer development in hospitalized patients: A tool for risk assessment. Qual Saf Health Care 2006; 15(1): 65-70.
[13] Alderden J, Rondinelli J, Pepper G, Cummins M, Whitney J. Risk factors for pressure injuries among critical care patients: A systematic review. Int J Nurs Stud 2017; 71: 97-114.
[14] Shahin ESM, Dassen T, Halfens RJG. Pressure ulcer prevalence and incidence in intensive care patients: A literature review. Nurs Crit Care 2008; 13(2): 71-9.
[15] Lima SM, González MMI, Carrasco CFM, Lima RJS. Risk factors for pressure ulcer development in Intensive Care Units: A systematic review. Med Intensiva 2017; 41(6): 339-46.
[16] Cox J. Pressure injury risk factors in adult critical care patients: A review of the literature. Ostomy Wound Manage 2017; 63(11): 30-43.
[17] Coleman S, Gorecki C, Nelson EA, et al. Patient risk factors for pressure ulcer development: Systematic review. Int J Nurs Stud 2013; 50(7): 974-1003.
[18] McInerney JA. Reducing hospital-acquired pressure ulcer prevalence through a focused prevention program. Adv Skin Wound Care 2008; 21(2): 75-8.
[19] Azimian J, Dehghan NN, Pourkhaleghi E, Ansari M. Transdermal wound oxygen therapy on pressure ulcer healing: A single-blind multi-center randomized controlled trial. Iran Red Crescent Med J 2015; 17(11): e20211.
[20] Karimian M, Sarokhani D, Sarokhani M, Sayehmiri K, Mortazavi Tabatabai SA. Prevalence of bedsore in Iran: A systematic review and meta-analysis. J Maz Univ Med Sci 2016; 26(136): 202-10.
[21] Moore ZE, Cowman S. Repositioning for treating pressure ulcers. Cochrane Database Syst Rev 2015; 1: CD006898.
[22] Nuru N, Zewdu F, Amsalu S, Mehretie Y. Knowledge and practice of nurses towards prevention of pressure ulcer and associated factors in Gondar University Hospital, Northwest Ethiopia. BMC Nurs 2015; 14(1): 34.
[23] Børsting TE, Tvedt CR, Skogestad IJ, Granheim TI, Gay CL, Lerdal A. Prevalence of pressure ulcer and associated risk factors in middle- and older-aged medical inpatients in Norway. J Clin Nurs 2018; 27(3-4): e535-43.
[24] Tayyib N, Coyer F, Lewis P. Saudi Arabian adult intensive care unit pressure ulcer incidence and risk factors: A prospective cohort study. Int Wound J 2016; 13(5): 912-9.
[25] Apostolopoulou E, Tselebis A, Terzis K, Kamarinou E, Lambropoulos I, Kalliakmanis A. Pressure ulcer incidence and risk factors in ventilated intensive care patients. Health Sci J 2014; 8(3): 333.
[26] González-Méndez MI, Lima-Serrano M, Martín-Castaño C, Alonso-Araujo I, Lima-Rodríguez JS. Incidence and risk factors associated with the development of pressure ulcers in an intensive care unit. J Clin Nurs 2018; 27(5-6): 1028-37.
[27] Karayurt Ö, Akyol Ö, Kiliçaslan N, et al. The incidence of pressure ulcer in patients on mechanical ventilation andeffects of selected risk factors on pressure ulcer development. Turk J Med Sci 2016; 46(5): 1314-22.
[28] Campanili TCGF, Santos VL, Strazzieri-Pulido KC, Thomaz PB, Nogueira PC. Incidence of pressure ulcers in cardiopulmonary intensive care unit patients. Rev Esc Enferm USP 2015; 49(Spec No): 7-14.
[29] Becker D, Tozo TC, Batista SS, et al. Pressure ulcers in ICU patients: Incidence and clinical and epidemiological features: A multicenter study in southern Brazil. Intensive Crit Care Nurs 2017; 42: 55-61.
[30] Iranmanesh S, Rafiei H, Sabzevari S. Relationship between Braden scale score and pressure ulcer development in patients admitted in trauma intensive care unit. Int Wound J 2012; 9(3): 248-52.
[31] Nassaji M, Askari Z, Ghorbani R. Cigarette smoking and risk of pressure ulcer in adult intensive care unit patients. Int J Nurs Pract 2014; 20(4): 418-23.
[32] Sardo PMG, Simões CSO, Alvarelhão JJM, et al. Analyses of pressure ulcer incidence in inpatient setting in a Portuguese hospital. J Tissue Viability 2016; 25(4): 209-15.
[33] de Almeida Medeiros AB, da Conceição Dias Fernandes MI, de Sá Tinôco JD, Cossi MS, de Oliveira Lopes MV, de Carvalho Lira ALB. Predictors of pressure ulcer risk in adult intensive care patients: A retrospective case-control study. Intensive Crit Care Nurs 2018; 45: 6-10.
[34] Cox J. Predictors of pressure ulcers in adult critical care patients. Am J Crit Care 2011; 20(5): 364-75.
[35] Akbari SA, Doshmanghir L, Neghahban Z, Ghiasipour M, Beheshtizavareh Z. Rate of pressure ulcers in intensive units and general wards of Iranian hospitals and methods for their detection. Iran J Public Health 2014; 43(6): 787-92.
[36] Bredesen IM, Bjøro K, Gunningberg L, Hofoss D. The prevalence, prevention and multilevel variance of pressure ulcers in Norwegian hospitals: A cross-sectional study. Int J Nurs Stud 2015; 52(1): 149-56.
[37] Jiang Q, Li X, Qu X, et al. The incidence, risk factors and characteristics of pressure ulcers in hospitalized patients in China. Int J Clin Exp Pathol 2014; 7(5): 2587-94.
[38] Demarré L, Verhaeghe S, Annemans L, Van Hecke A, Grypdonck M, Beeckman D. The cost of pressure ulcer prevention and treatment in hospitals and nursing homes in Flanders: A cost-of-illness study. Int J Nurs Stud 2015; 52(7): 1166-79.
[39] Rafiei H. Incidence of pressure ulcer in patients who were admitted to open heart cardiac surgery intensive care unit. Int J Epidemiol Res 2016; 3(1): 12-8.
[40] Mogarehi M, Zarif Sanaiey N. Pressure sore incidence and risk factors in patients admitted in medical, surgical and orthopedic wards in affiliated hospitals of Shiraz University of medical sciences. Iran J Nurs 2003; 16(34): 8-13.
[41] Dhandapani M, Dhandapani S, Agarwal M, Mahapatra AK. Pressure ulcer in patients with severe traumatic brain injury: Significant factors and association with neurological outcome. J Clin Nurs 2014; 23(7-8): 1114-9.
[42] Azevedo Macena MS, Costa Silva RS, Dias Fernandes MIDC, Almeida Medeiros AB, Batista Lúcio KD, Carvalho Lira ALB. Pressure ulcer risk evaluation in critical patients: Clinical and social characteristics. Open Nurs J 2017; 11(1): 91-7.