Abstract
Critically ill patients are at high risk of developing pressure ulcers (PUs) and patients who develop PUs remain significantly longer in the intensive care unit (ICU) with significantly increased morbidity and mortality. Therefore, the identification of patients at truly increased risk is important. The aim of this study was to examine the association of low serum albumin present at admission in ICU patients with the onset of PUs. We conducted a retrospective cohort study on 610 patients who were admitted to intensive care unit. Level of serum albumin and other biochemical indices, recorded at the time of admission, were collected. We collected information about PU occurrence after admission and conducted a statistical analysis with biomarkers at ICU admission and during hospital stay. The incidence of PU in the ICUs was 31% and about 70% of patients with PUs had hypoalbuminemia at admission. The lowest values of serum albumin in patients with PUs were directly proportional to the severity of ulcers. In this study, we found a close association between serum albumin and PUs. In fact serum albumin was negatively correlated with PU and may be considered one of the independent determinants of PU occurrence in patients admitted to ICUs.
Keywords: Albumin, Intensive care unit, Pressure ulcer
Introduction
Pressure ulcers (PUs) are common among hospitalised patients of intensive care units (ICUs). ICU studies providing prevalence and incidence figures are scarce and their reported incidence in critical care patients varies widely from 1% to 56% 1, 2, 3, 4, 5, 6, 7. PU prevalence rate has been found to vary between 14% and 41% 1, 8, 9. Patients admitted to ICUs, who are sedated, ventilated and almost invariably confined to bed for long periods, are at particularly high risk of developing PUs 2, 9.
PUs are associated with negative patient‐outcomes in terms of pain, loss of function and independence, increased risk of infection and sepsis, and additional surgical procedures 2, 10.
PUs develop as a result of extrinsic and intrinsic factors. Main extrinsic factors are decreased tissue perfusion due to interface pressure, shearing forces, friction and moisture. Intrinsic factors are the nutritional status of the patient, patient age, immobility, incontinence, metabolic and circulatory factors and neurological disease; hypoalbuminemia is also suggested to increase frequency of PUs 11. In fact one study showed that 75% of patients with a serum albumin level below 35 g/l developed PUs compared to only 16% of patients with a higher serum albumin level 12.
As hypoalbuminemia is a frequent condition in patients admitted to ICUs, 13 the aim of this study is to verify the association between hypoalbuminemia and the occurrence of PUs in critically ill patients.
Information on PU risk factors in critically ill patients may be especially useful for the early and appropriate implementation of preventive measures.
Methods
This retrospective cohort study was conducted at the intensive care unit of University Magna Graecia of Catanzaro. Institutional Review Board (IRB) approval was obtained for this study.
All categories of ICU patients were included, such as surgical, internal medicine and cardiovascular.
In the period from 1st January 2000 to 31st December 2010, a total of 610 patients were admitted to ICU (males 380 [62·2%]; females 230 [37·8%]), age ranges: <20 years n = 2 (0·32%); 20–40 years n = 42 (6·8%); 40–60 years n = 203 (33·2%); 60–80 years n = 312 (51·1%); >80 years n = 51 (8·3%). Full demographics are shown in Table 1.
Table 1.
Demographics
| Variable | Whole study group |
|---|---|
| n (male/female) | 610 (380/230) |
| Age (year) | 70 ± 12 |
| Body mass index (kg/m2) | 30·3 ± 5·9 |
| SBP (mmHg) | 134 ± 17 |
| DBP (mmHg) | 83 ± 10 |
| Fasting glucose (mg/dl) | 180 ± 11 |
| Total cholesterol (mg/dl) | 202 ± 39 |
| High‐density lipoprotein (mg/dl) | 51 ± 14 |
| Triglycerides (mg/dl) | 128 ± 74 |
| Albuminemia (mg/dl) | 2·8 ± 1·6 |
| eGFR (ml/minute per 1·73 m2) | 35 ± 20 |
| EF%(Simpson) | 30 ± 20 |
eGFR, estimated glomerular filtration rate; EF%, ejection fraction percentage; DBP, diastolic blood pressure; SBP, systolic blood pressure.
Criteria for inclusion of patients in this study were as follows: to have been hospitalized in one of the ICUs with a minimum stay of 24 hours, and not to have PU when admitted. Patients were assessed during their stay in the ICU and, after being discharged from this unit, were followed‐up until discharge from hospital or death. Collected details included socio‐demographic, clinical and hospitalization data and risk of PU. The following variables were studied: age, sex, length of ICU stay, length of hospital stay, co‐morbidity and chronic diseases. Patients admitted to the ICUs were mostly from the operating room (46·0%), followed by the emergency room (25·6%). The main reasons for hospitalization in the ICU were postoperative care period (50·0%) or respiratory diseases (22·9%). Characterisation of patients according to clinical and hospitalization data is shown in Table 2.
Table 2.
Hospitalization data
| Main diagnosis at ICU admission | n | % |
|---|---|---|
| Complicated cardiac surgery | 145 | 23·77 |
| Subarachnoid haemorrhage | 102 | 16·72 |
| Cardiogenic shock | 101 | 16·29 |
| Complicated neurosurgery | 81 | 13·27 |
| Exacerbated COPD | 61 | 10·00 |
| Polytrauma | 53 | 8· 68 |
| Adult respiratory distress syndrome | 43 | 7·04 |
| Haemorrhagic shock | 10 | 1·63 |
| Decompensated myasthenia gravis | 7 | 1·14 |
| Pancreatitis | 5 | 0·82 |
| Decompensated rheumatoid arthritis | 2 | 0· 32 |
ICU, intensive care unit; COPD, chronic obstructive pulmonary disease.
We reviewed the patients at admission to ICU for their clinical record levels of serum albumin and other biochemical indices, such as serum calcium, phosphate, triglycerides, total cholesterol lipoprotein, low‐density lipoprotein and high‐density lipoprotein.
Hypoalbuminemia was defined by serum albumin concentration lower than 3·3 g/dl.
We collected information about PU occurrence after admission.
For clinical classification and PU assessment, National Pressure Ulcer Advisory Panel's (NPUAP) Pressure Ulcer Stages/Categories were used 14.
Categorical variables were compared by χ 2 test. Unpaired t was used to compare differences of continuous variables between two groups (patient with PUs and patient without PUs). Assessment of the predictive discrimination of the various quantitative variables was made by using the receiver operating characteristic curve analysis. P < 0·05 was considered statistically significant. All analyses were performed using SPSS 12·0 for Windows.
Results
Mean length of ICU stay was 13·6 days (SD = 14; min. = 2, max. = 82), of which 40·5% stayed up to 7 days hospitalised in these units, followed by 25% who stayed between 8 and 14 days, whereas the mean length of hospital stay was 30·0 days (SD = 24·7; min. = 4 and max. = 115).
The incidence of PUs in the ICUs was 31% (189 out of 610 patients) (Table 3), of which the majority (61·38%) of cases was observed to appear in the first week of ICU stay (Table 4).
Table 3.
Frequency of PU during ICU stay
| NPUAP Pressure Ulcer Stages/Categories | Presence of PU | Albuminemia | |
|---|---|---|---|
| n (male/female) | % | ||
| Stage I | 19 (11/8) | 10·05 | 2·8 ± 0·4 |
| Stage II | 37 (21/16) | 19·58 | 2·6 ± 0·5 |
| Stage III | 105 (66/39) | 55·56 | 2·3 ± 0·4 |
| Stage IV | 28 (17/11) | 14·81 | 2·5 ± 0·5 |
| Total | 189 (115/74) | 100 | 2·5 ± 0·5 |
ICU, intensive care unit; PU, pressure ulcer; NPUAP, National Pressure Ulcer Advisory Panel.
Table 4.
Length of time until pressure ulcer
| Days | n | % |
|---|---|---|
| Until 7 | 116 | 61·38 |
| From 8 to 14 | 33 | 17·46 |
| From 15 to 21 | 19 | 10·05 |
| 22 or more | 21 | 11·11 |
| Total | 189 | 100 |
Analysis of quantitative variables divided by gender (Tables 5 and 6) showed that 67·82% of PUs in male patients and 71·68% in female patients were associated with hypoalbuminemia (P = 0·00001, OR = 2·08 for males and P =0·00001, OR = 5·0 in females). Diabetes mellitus II and congestive heart failure were also positively associated with the occurrence of PUs as shown in Tables 5 and 6.
Table 5.
Statistic analysis of main clinical characteristics in male patients with pressure ulcers
| Variables | n (%) | P (0·05) | Odds ratio |
|---|---|---|---|
| Hypoalbuminemia | 78 (67·82) | 0·00001 | 2·08 |
| Diabetes mellitus II | 65 (56·52) | 0·0017 | 2·04 |
| Congestive heart failure | 60 (52·17) | 0·018 | 0·48 |
| Obesity | 46 (40·00) | 0·8 | 1·07 |
| Malnutrition | 64 (55·65) | 0·01 | 2 |
| CKD | 51 (44·34) | 0·3 | 1·26 |
CKD, chronic kidney disease.
Table 6.
Statistic analysis of main clinical characteristics in female patients with pressure ulcers
| Variables | n (%) | P (0·05) | Odds ratio |
|---|---|---|---|
| Hypoalbuminemia | 53 (71·62) | 0·00001 | 5 |
| Diabetes mellitus II | 48 (64·86) | 0·047 | 2·25 |
| Congestive heart failure | 48 (64·86) | 0·0047 | 2·25 |
| Obesity | 37 (50·00) | 0·018 | 2 |
| Malnutrition | 47 (63·51) | 0·04 | 2·25 |
| CKD | 31 (41·89) | 0·9 | 0·94 |
CKD, chronic kidney disease.
Albumin values were also lower for increasing ulcer stages as shown in Table 3.
Discussion
Critical care patients show peculiar characteristics due to the severity of their clinical conditions, association with complex therapies and the need for more frequent and rigorous surveillance and control. Thus, they are more exposed to invasive procedures and a greater need for handling, causing them to be more susceptible to complications and resulting in greater length of hospital stay 1. In ICUs, the demand for specialized care using complex technology is high, given the need and concern of the health team to prioritise the stabilisation of the patient's critical condition, thus causing procedures to maintain body health, including skin and emotional integrity and family bonds, to be compromised or hindered 2. In this context, whether because of the difficulty to perform preventive measures to maintain skin integrity or patient severity, the appearance of PU, a commonly occurring complication, is observed in critical patients who are hospitalised 3. As regards the appearance of PUs in patients admitted to ICUs, it is important to consider both the severity of their clinical condition and the nursing workload, as these aspects have direct implications for the quality of care provided to patients, quality of life of professionals and hospital costs 5, 6, 7, 8, 9, 10, 11, 12, 13.
Albumin is the most abundant visceral protein in the blood synthesized in the liver, and its levels are therefore considered to reflect protein synthesis and it also plays other physiologic roles, including the maintenance of oncotic pressure which may influence tissue tolerance 15.
In fact, oncotic pressure serves as the main driving pressure (together with hydration status) for vascular refill, and subsequent lowering of albumin levels may be responsible for decreasing skin perfusion 16.
A recent study on wound healing showed that in the management of patients in an acute care setting, PU healing was improved by providing protein supplements to keep serum albumin level greater than 2·8 g/dl 17.
Diminished circulating level of albumin is a common condition in seriously ill patients and a study reported that the frequency of hypoalbuminemia was 21% at the time of admission in this type of patients 18.
Results from this study revealed a high incidence of PU (31%) in patients admitted to ICUs.
In this study, there was a close association between serum albumin and PU: (i) serum albumin was negatively correlated with PU; (ii) serum albumin was one of the independent determinants of PU; (iii) in univariate correlation analysis, we found that PU was negatively associated with serum albumin, but positively correlated with diabetic status and congestive cardiac failure; (iv) marked hypoalbuminemia was correlated with more severe stages of ulcer.
Acknowledgements
This research received no funding. The authors have no conflict of interest to declare.
References
- 1. Allman RM, Laprade CA, Noel LB, Walker JM, Moorer CA, Dear MR, Smith CR. Pressure sores among hospitalized patients. Ann Intern Med 1986;105:337–42. [DOI] [PubMed] [Google Scholar]
- 2. Keller BPJA, Wille J, Ramshorst BV, van der Werken C. Pressure ulcers in intensive care patients: a review of risk and prevention. Intensive Care Med 2002;28:1379–88. [DOI] [PubMed] [Google Scholar]
- 3. Boyle M, Green M. Pressure sores in intensive care: defining their incidence and associated factors and assessing the utility of two pressure sore risk assessment tools. Aust Crit Care 2001;14:24–30. [DOI] [PubMed] [Google Scholar]
- 4. Jiricka MK, Ryan P, Carvalho MA, Bukvich J. Pressure ulcer risk factors in an ICU population. Am J Crit Care 1995;4:361–7. [PubMed] [Google Scholar]
- 5. 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. [DOI] [PubMed] [Google Scholar]
- 6. Perneger TV, Helliot C, Raë AC, Borst F, Gaspoz JM. Hospital‐acquired pressure ulcers. Risk factors and use of preventive devices. Arch Intern Med 1998;158:1940–5. [DOI] [PubMed] [Google Scholar]
- 7. Manzano F, Navarro MJ, Roldan D, Moral MA, Leyva I, Guerrero C, Sanchez MA, Colmenero M, Fernández‐Mondejar E; Granada UPP Group. Pressure ulcer incidence and risk factor in ventiled intensive care patients. J Clin Care 2010;25:469–76. [DOI] [PubMed] [Google Scholar]
- 8. O’Dea K. Prevalence of pressure damage in hospital patients in the UK. J Wound Care 1993;2:221–5. [DOI] [PubMed] [Google Scholar]
- 9. Bours GJJW, De Laat E, Halfens RJG, Lubbers M. Prevalence, risk factors and prevention of pressure ulcers in Dutch intensive care units. 2001;27:1599–1605. [DOI] [PubMed] [Google Scholar]
- 10. Jiricka MK, Ryan P, Carvalho MA, Bukvich J. Pressure ulcer risk factors in an ICU population. Am J Crit Care 1995;4:361–7. [PubMed] [Google Scholar]
- 11. Terekeci H, Kucukardali Y, Top C, Onem Y, Celik S, Öktenli C. Risk assessment study of the pressure ulcers in intensive care unit patients. Eur J Intern Med 2009;394–7. [DOI] [PubMed] [Google Scholar]
- 12. Holmes R, Macchiano K, Jhangiani SS, Agarwal NR, Savino JA. Nutrition know‐how. Combating pressure sores – nutritionally. Am J Nurs 1987;87:1301–3. [PubMed] [Google Scholar]
- 13. Neel DR, McClave S, Martindale R. Hypoalbuminemia in the perioperative period: clinical significance and management options. Best Pract Res Clin Anaesthesiol 2011;25:395–400. [DOI] [PubMed] [Google Scholar]
- 14. Black J, Baharestani M, Cuddigan J, Dorner B, Edsberg L, Langemo D, Posthauer ME, Ratliff C, Taler G; National Pressure Ulcer Advisory Panel. National pressure ulcer advisory panel's updated pressure ulcer staging system. Dermatol Nurs 2007;19:343–9. [PubMed] [Google Scholar]
- 15. Iizaka S, Sanada H, Matsui Y, Furue M, Tachibana T, Nakayama T, Sugama J, Furuta K, Tachi M, Tokunaga K, Miyachi Y. Serum albumin level is a limited nutritional marker for predicting wound healing in patients with pressure ulcer: two multicenter prospective cohort studies. Clin Nutr 2011;30:738–45. [DOI] [PubMed] [Google Scholar]
- 16. Mistrík E, Dusilová‐Sulková S, Bláha V, Sobotka L. Plasma albumin levels correlate with decreased microcirculation and the development of skin defects in hemodialyzed patients. Nutrition 2010;26:880–5. [DOI] [PubMed] [Google Scholar]
- 17. Sung YH, Park KH. Factors affecting the healing of pressure ulcers in a Korean acute care hospital. J Wound Ostomy Continence Nurs 2011;38:38–45. [DOI] [PubMed] [Google Scholar]
- 18. Herrmann FR, Safran C, Levkoff SE, Minaker KL. Serum albumin level on admission as a predictor of death, length of stay, and readmission. Arch Intern Med 1992;152:125–30. [PubMed] [Google Scholar]