A Retrospective Study Using the Pressure Ulcer Scale for Healing (PUSH) Tool to Examine Factors Affecting Stage II Pressure Ulcer Healing in a Korean Acute Care Hospital

Stage II pressure ulcers (PUs) should be managed promptly and appropriately in order to prevent complications. To identify the factors affecting Stage II PU healing and optimize care, the electronic medical records of patients with a Stage II PU in an acute care hospital were examined.   Patient and ulcer characteristics as well as nutritional assessment variables were retrieved, and ulcer variables were used to calculate Pressure Ulcer Scale for Healing (PUSH) scores. The effect of all variables on healing status (healed versus nonhealed) and change in PUSH score for healing rate were compared. Records of 309 Stage II PUs from 155 patients (mean age 61.2 ± 15.2 [range 5–89] years, 182 [58.9%] male) were retrieved and analyzed. Of those, 221 healed and 88 were documented as not healed at the end of the study. The variables that were significantly different between patients with PUs that did and did not heal were: major diagnosis (P = 0.001), peripheral arterial disease (P = 0.007), smoking (P = 0.048), serum albumin (<2.5 g/dL) (P = 0.002), antidepressant use (P = 0.035), vitamin use (P = 0.006), history of surgery (P <0.001), PU size (P = 0.003), Malnutrition Universal Screening Tool (MUST) score (P = 0.020), Braden scale score (P = 0.003), and mean arterial pressure (MAP, mm Hg) (P = 0.026). The Cox proportional hazard model showed a significant positive difference in PUSH score change —indicative of healing — when pressure-redistribution surfaces were used (P <0.001, HR = 2.317), PU size was small (3.0 cm², P = 0.006, HR = 1.670), MAP (within a range of 52–112 mm Hg) was higher P = 0.010, HR = 1.016), and patients were provided multivitamins (P = 0.037, HR=1.431). The results of this study suggest strategies for healing Stage II PUs in the acute care setting should include early recognition of lower-stage PUs, the provision of static pressure-redistribution surfaces and multivitamins, and maintaining higher MAP may facilitate healing and prevent deterioration. Further prospective research is warranted to verify the effect of these interventions.

Epidemiological data¹ from 1982 to 1999 show pressure ulcer (PU) incidence may have decreased slightly, but PUs continue to occur despite improved understanding, increased regulatory oversight, and improvements in technologies available for PU prevention. An observational study² among patients in Veterans Administration long-term care facilities from 1990 to 1997 indicates the incidence of PUs increased slightly, and the persistence of PU incidence seems related to various factors, including patient condition (multiple comorbidities, sicker/older population, and the existence of unavoidable PUs), medical device-related events, and health system issues (eg, staff issues and training with PU prevention program).³ Therefore the treatment of PUs remains as important an issue as the prevention of PU.

According to Gardner et al’s⁴ 2005 prospective study, Stage II PUs (ie, partial-thickness skin damage with erosion in epidermis) accounted for the largest share (69%) of PUs in acute care hospitals; in 2010, Park and Kim⁵ reported in their retrospective study that Stage II PUs accounted for 87.7%. Timely and aggressive intervention is needed to prevent these wounds from progressing to Stage III or Stage IV PUs.⁶ Cost of treatment related to stage is another consideration. According to a 2011 survey by Dealey et al⁷ in the United Kingdom, cost estimates to treat Stage I, Stage II, Stage III, and Stage IV PUs were £1213.58, £4398.79, £7232.93, and £8782.85, respectively. In 2009, Padula et al⁸ reported the daily cost of treatment for hospital-acquired Stage III and Stage IV PUs compared to Stage I and Stage II in the United States. The costs for treatment of Stage I and Stage II versus Stage III and Stage IV were $2,770.54 and $5,622.98 per day, respectively, providing additional incentive to focus on factors that affect Stage II PU healing.

Various instruments are available to assess patient risk for PUs, PU status, and likelihood to heal. The Braden Scale, which evaluates a patient’s risk of developing PUs, assesses six parameters with total score range from 6 to 23 — the lower the score, higher the risk. The National Pressure Ulcer Advisory Panel (NPUAP) and European Pressure Ulcer Advisory Panel (EPUAP)⁹ instrument is commonly used to classify PU stages. The Malnutrition Universal Screening Tool¹⁰ (MUST) identifies patients malnourished or at risk of malnutrition. A MUST score of 0 indicates a low risk of under nutrition, a score of 1 indicates medium risk, and a score of 2 or more points indicates high risk. However, the relationship between these variables and Stage II PU healing is not clear, hampering the development of evidence-based intervention strategies and guidelines for treating Stage II PU in various healthcare settings.⁵ The Pressure Ulcer Scale for Healing (PUSH) Tool¹¹ is a validated instrument that comprises three subscale scores used to assess PU healing: 1) ulcer size (scored on a scale of 0 to 10 points), 2) exudate (scored on a scale of 0 to 3 points), and 3) type of the tissue (scored on a scale of 0 to 4 points). The three subscale scores are added to generate a cumulative wound status score. A cumulative score of 17 indicates poorest PU status and a score of 0 indicates the best possible status.

A retrospective study was conducted to evaluate the effect of patient, ulcer, and environmental factors on Stage II PU healing. The specific aims of this study were to 1) compare the healing of Stage II PUs according to patient characteristics, PU characteristics, and nursing interventions; and 2) determine factors affecting Stage II PU healing.

Patients and setting. The electronic medical records (EMR) of persons with a Stage II PU hospitalized in an acute care facility in Seoul, Korea, from March 2010 through February 2011 and who no longer required treatment because of complete healing of their ulcers or discharge from hospital were analyzed. All patients regardless of age or comorbidities with a Stage II PU were included; patients with Stage III or higher PU, no follow-up data for final PUSH score, and other missing data were excluded (see Figure 1).

Variables.
Survey instrument. The author determined factors affecting PU healing based on a comprehensive literature review. The literature was searched and reviewed for pressure ulcer and wound healing in the PubMed, CINAHL, and the Cochrane Library databases. Patient characteristics, nursing care, and PU status variables were considered.

The first version of the factor list contained 36 variables. The content validity of the list-based questionnaire was determined by two wound, ostomy and continence (WOC) nurses. The content validity index (CVI) is 4-point scale where 4 = highly relevant, 3 = quite relevant, 2 = somewhat relevant, and 1 = not relevant. Each questionnaire item received a CVI score of 0 to 0.75; as verification criteria of content validity,¹² scores <0.75 were excluded — ie, application of restraints, chemotherapy, consultation with a WOC nurse, consultation with nutritionist, PU-related nursing diagnosis, PU-related nursing records, attending caregiver, and infection. A pilot study then was conducted involving four patients with Stage II PU assessed by five primary wound care nurses (PWNs) — ie, nurses who have completed middle-level wound care courses and are under the supervision of WOC nurses in their institutional units — to determine the usability of the instrument, and final modifications were made accordingly. The final questionnaire included 26 variables: 21 items related to patient characteristic and five to PU characteristics (see Table 1A, 1B). Intraclass correlation of PUSH scores on four Stage II PU cases among the PWNs was 0.926.

Data from patient EMRs from the author’s acute care facility were searched for information on the factors identified, along with Braden Scale scores, NPUAP ulcer stage, and MUST scores (the latter calculated from patient data). Subsequently, all PU data were used to provide the various characteristics, including three items (wound size, exudate amount, and tissue type) for the PUSH Tool, used with permission from the NPUAP (per facility policy) for calculating PUSH score of each patient as the dependent study variable.¹² PUSH instrument results were assessed by five PWNs. PU healing was operationally defined as a completely healed, closed ulcer.

Data analysis. The estimated sample size was 152 patients, determined using 5% significance level and a power of 80%, given an anticipated dropout rate of 10%, and reported proportion for Stage II PU (including ulcers documented on admission or hospital-acquired based on 1-year data) of 85%.⁵

General and PU characteristics of participants were summarized using percentile, mean value, and standard deviation; χ^²-test and independent t-test were applied to compare healing versus nonhealing ulcers. The degree of PU healing (proportions healed) was examined using Kaplan-Meier survival analysis. All ulcers were analyzed independently; many patients had more than one ulcer.

Independent variables with a P value <0.05 were analyzed with simple Cox regression; the healing variables noted in literature to be important were analyzed from the patient records with multiple Cox regression.

The statistical software PASW Statistics 18 (SPSS Inc, Chicago, IL) was used for all calculations.

From the records of 205 patients with PUs screened, 29 patients had Stage III or greater ulcers and were excluded; 21 additional patients were excluded due to no follow-up data for final PUSH score and other missing data. Ultimately, data from 155 patients (mean age 61.2 ± 15.2 [range 5–89] years, 182 [58.9%] male) with 309 Stage II PUs were analyzed (see Figure 1).

Patient and PU characteristics. The most common major diagnoses were neurovascular disease (104, 33.7%), musculoskeletal disease (52, 16.8%), cancer (48, 15.5%), diabetes (72, 23.3%), and peripheral arterial disease (10, 3.2%). Mean arterial pressure (MAP) was 87.7 mm Hg. The majority of participants (253, 81.9%) were continent; 41 (13.3%) were smokers. Hemoglobin level was >12 g/dL in 186 patients (60.2%); 236 (76.4%) had an albumin level >2.5 g/dL. Antidepressants were used by 41 patients (13.3%), and 99 (32.0%) were taking oral and/or IV multivitamins. PU locations included the trunk (163, 52.8%) and extremities (145, 47.2%). Most PUs (238, 77%) were <3 cm² in size. Due to their medical conditions, 86 patients (27.8%) did not receive regular repositioning. Average MUST score was 1.06, and average Braden Scale score was 14.05 (see Table 1A, 1B). Almost all (96.4%) patients’ PUs were treated with moist dressing. Among all PUs, 50% healed in 14 days. The 30-day and 60-day healing rates were 79.5±2.7% and 90.6±2.4%, respectively (see Figure 2). Two hundred, twenty-one (221, 71.5%) PUs healed within the study period; 88 did not heal.

Comparison of variables between healing and nonhealing group (see Table 2). The variables that were significantly different between patients with PUs that did and did not heal were: major diagnosis (P = 0.001), peripheral arterial disease (P = 0.007), smoking (P = 0.048), serum albumin (<2.5 g/dL) (P = 0.002), antidepressant use (P = 0.035), vitamin use (P = 0.006), history of surgery (P <0.001), PU size at baseline (P = 0.003), MUST score (P = 0.020), Braden Scale score (P = 0.003), and MAP (mm Hg) (P = 0.026).

Factors influencing healing. Variables that were statistically significantly different (P <0.05) between ulcers that did and did not heal at the end of the study included major diagnosis, peripheral arterial disease, smoking, serum albumin (<2.5 g/dL), antidepressants, multivitamin use, surgery, PU size, MUST score, Braden Scale score, and MAP (mm Hg) (see Table 2). Change in PUSH scores are shown in Table 3. Statistically significant differences included a history of surgery (P = 0.03), use of a pressure-redistribution surface (P <0.001), small wound size at baseline (≤3.0 cm², P = 0.014), and low MUST score (P = 0.003).

Subsequently, independent variables with P <0.05 (see Table 3) including valuable variables for healing (according to the literature search) were analyzed because certain factors affect each other in practice (see Table 4). The variables showing significant difference in degree of healing were a history of surgery (P = 0.030), use of a pressure-redistribution surface (P <0.001), wound size ≤3.0 cm² (P = 0.014), and MUST score (P = 0.003) (see Table 3).

Patients who were provided pressure-redistribution surfaces had a change in PUSH score 2.317 times higher for complete healing than persons who did not use pressure-redistribution devices (P <0.001, hazard ratio [HR] = 2.317). The healing rate in PUs ≤3.0 cm² was 1.67 times higher than in ulcers >3.0 cm² (P = 0.006, HR = 1.670).

Patients provided multivitamins had a change in PUSH score 1.431 times higher than patients who did not take multivitamins (P = 0.037, HR = 1.431). A one-point increase in MAP increased the change in PUSH score 1.016 times (P = 0.010, HR = 1.016). Thus, the HR in PUSH score change were the use of a pressure-redistribution surface, PU size, use of multivitamins, and MAP (see Table 4).

In this retrospective study involving 155 patients in acute care settings with 309 Stage II PUs, the following variables were significantly more frequently documented in patients who did compared to those who did not heal: peripheral arterial disease, smoking, serum albumin (<2.5 g/dL), antidepressant use, multivitamin use, history of surgery (P <0.001), PU size at baseline, MUST score, Braden Scale score, and MAP (mm Hg). Similarly, average change in PUSH scores indicative of healing were significantly greater in ulcers of patients where pressure-redistribution surfaces were used, PU size was small, MAP (within a range of 52–112 mm Hg) was higher, and multivitamins were provided.

Patient characteristics. Age is a major factor in PU occurrence and healing. In a review article, Pittman¹³ found as the skin ages, the density of fibroblasts is affected by the molecular structure of senescent cells. Multiple researchers have demonstrated that age influences PU healing.^14,15 By contrast, Kramer and Kearney⁶ found no significant differences in healing, and in the current retrospective study patient age also did not significantly affect healing status. This may be because Stage II PUs heal comparatively quickly compared to Stage III and Stage IV PUs.

Although diabetes mellitus can exacerbate vascular pathologies related to both arterial and venous insufficiencies and delay healing of PUs,¹⁶ the current analysis revealed no difference in healing Stage II PUs between persons with and without diabetes.

Among the major diagnoses of the study patients, neurovascular disease was the most prevalent (104, 33.7%). In the study, comparing patients with a healed compared to a nonhealed ulcer, a major diagnosis of cardiovascular or respiratory diseases was significantly more common in the nonhealed patient group.

The majority of patients (66.7%) had a history of surgery, which may have increased their risk of developing a PU.¹⁷ However, no significant difference was noted in treatment based on the principal diagnosis. In a randomized, controlled comparative study by Thomas et al,¹⁸ patients who had surgery could not move well, exhibited expansion of blood vessels due to anesthetic, and had decreased blood flow over bony prominences. Vasoconstriction, damaging to the immune response, and hemostasis due to hypothermia caused by PU occurrence, increases the incidence of infection and concentration of norepinephrine, disrupting wound healing. However, in the current study, surgery was not associated with change in PUSH score or PU healing.

In one study, the recurrence rate of PUs was 13% to 15% in PU patients¹⁷; however, 21% of new ulcers occurred in locations different from the existing/original ulcer. In the current study, 51 (16.5%) had a history of PUs, but that did not affect PU outcome.

A retrospective study⁶ involving 106 patients with PUs at a long-term care facility found that fecal and urinary incontinence were associated with PU healing. In that study, patients with urinary incontinence had larger changes in PUSH scores than the group of patients without urinary incontinence or with an indwelling catheter. The authors hypothesized that enhanced nursing attention required for incontinence management may have resulted in more frequent repositioning and turning and more frequent assessment of the topical dressing, leading to better PU outcomes. Contrary to the current author’s expectation, PU healing was not significantly affected by incontinence in this study, perhaps because a Stage II PU is a limited-depth wound.

Nutritional status. Three indicators of nutritional status were evaluated: hemoglobin, serum albumin,^2,19 and MUST score, none of which was associated with PU healing in this study. Hemoglobin transports oxygen to the peripheral tissues and is important for PU healing.^14,19 However, in this study, no significant differences were seen between groups with hemoglobin level >12 g/dL and below 12 g/dL. Because Stage II PUs are partial-thickness wounds, their healing may not be influenced by hemoglobin level.

The WOCN Society¹⁷ reported serum albumin level below 2.8 g/dL may be indicative of malnutrition, which would negatively influence PU healing. In a retrospective study²⁰ of acute care patients with 326 PUs, patients with serum albumin levels >2.8 g/dL had larger PUSH score changes when compared to patients with lower albumin levels. Similarly, in a prospective study of 150 tube-fed patients with Stage III and Stage IV PUs in a long-term, acute care facility, Pompeo²¹ found protein, known to be helpful for the healing of PUs,^22,23 is critical for wound healing. However, a retrospective cohort study²³ of 1,241 patients with Stage II PUs at a long-term care facility showed protein was not a significant factor, results supported by the current that also involved small, partial-thickness wounds.

Measuring prealbumin (10–40 mg/dL) and total albumin (6–8 g/dL) is recommended for adults.²⁴ Serum albumin and prealbumin are useful in assessing the overall status of the patient but have no significant association with nutritional status.²⁵

Vitamins. Patients who received multivitamins showed higher healing rate than patients who did not. Vitamins are essential nutrients to maintain health, some of which, such as vitamin C, are known to be essential for wound healing. A review article²⁶ has shown vitamin deficiency can delay wound healing. The International Pressure Ulcer Treatment Guideline⁹ from NPUAP and EPUAP recommends vitamin supplementation for patients whose dietary intake is insufficient with B level strength of evidence. Participants in the current study had a medium risk of malnutrition (MUST score 1.06), and many were not able to absorb vitamins from normal regular diet. Despite the lack of a positive relationship between vitamin intake and wound healing in a randomized, controlled trial,²⁷ vitamins still seem important for PU healing in patients whose nutrition is insufficient. In the current study, the PUs of the patients who were administered vitamins showed had a higher healing rate than patients who did not receive vitamins.

A retrospective cohort study²⁸ of long-term care patients showed adequate nutritional support is a strong predictor of Stage III and Stage IV PU healing; an experimental design (randomly assigned convenience sample) study²⁹ of long-term care, geriatric patients where healing was assessed using the PUSH tool found effective management of Stage I and Stage II PU involves the optimization of nutrition, pressure relief, treatment of underlying medical conditions, and excellent local wound care. The current study did not show a relationship between MUST score and Stage II PU healing. The NPUAP and EPUAP guideline⁹ states the MUST score influences chronic wound healing. A possible explanation for the varied findings is that a Stage II PU is does not involve extensive amounts of tissue and heals in relatively short period of time. In addition, the current study was conducted in an acute care facility where nutritional deficiencies on admission were addressed immediately, so malnutrition was resolved rapidly and nutritional status was not an issue.

Antidepressant use. Horn et al’s¹⁵ evaluation of 1,524 patients in long-term care facilities found PU incidence was significantly lower among patients on antidepressant drugs (P = 0.027). Bivariate analysis indicated a statistically significant relationship between antidepressant use and PU healing, but this association was not confirmed on multivariate analysis.

Amitriptyline is a tricyclic antidepressant used for behavior disorders and peripheral vasodilator effect³⁰; improving blood flow is useful for PU healing. However, an experimental study³¹ found amitriptyline ineffective as part of the treatment of full-thickness wounds. In the current study, antidepressants did not influence healing.

MAP. The association between higher MAP and PU healing in the current study is consistent with the findings of Kramer and Kearney,⁶ who reported MAP predicted a 5% increase in the degree of PU healing rate.

Sung and Park²⁰ found maintaining MAP is necessary to promote PU healing. One possible explanation may be that PU healing is facilitated by the normal supply of oxygen, important cells, and nutrients when MAP is maintained above a certain level, because the oxygen that affects PU treatment and nutrient supply depends on blood circulation. The normal range of MAP is 70–110 mm Hg, and the lower limit of MAP to sustain the organs of the average person is 60 mm Hg. However, Pender and Frazier³² argued in their descriptive, correlational study that MAP and arterial blood gas analysis provide too little information about the actual oxygen diffusion status in tissue and cannot determine influence on PU healing.

Nursing interventions.
Repositioning. Regular turning and repositioning is commonly used as a preventive intervention and is an important component of PU prevention.¹⁶ Regular position change was graded A in strength of evidence for PU prevention³³ and treatment, but patient condition and mattress also are considerations.³⁴ In this study, repositioning was found to be a significant factor of healing versus nonhealing at the end of the study and/or change in PUSH score, regardless of the mattress.

In this study, the use of a pressure-redistribution surface was the most important, independent factor related to healing Stage II PUs, consistent with the finding of Park and Kim. The importance of pressure-redistribution surface use has mostly been emphasized for the prevention of PUs.^11,35

In many cases, a small Stage I or Stage II PU can be offloaded easily with repositioning.²⁹ In a randomized, controlled trial,³⁶ alternating-pressure overlays were compared to alternating-pressure mattress replacement in 113 patients with Stage I and Stage II PUs. No significant differences were found between the two groups for median healing time reported. The NPUAP⁹ supports use of powered pressure-redistribution surface to manage Stage III and Stage IV PUs, but overlays are sufficient for Stage I and Stage II. The mattress and overlay used in the current study are nonpowered pressure-redistribution surface, findings consistent with those recommendations.

Dressing. A review³⁷ showed moist dressings decrease the days to complete healing and pain scores when compared with nonmoist dressings. In a retrospective chart review³⁸ including patients 50 years of age or older, Stage II PUs managed with a hydrocolloid dressing healed faster than those managed with wet-to-dry dressing. The NPUAP/EPUAP guideline, while indicating differences in each material, notes the effectiveness of moist dressings for healing with C-level strength of evidence. In the current study, 94.6% of patients used moist dressings; thus, the sample of patients in the dry dressing group may have been too small to find significant differences.

PU characteristics. PUs on the sacrum and buttocks have been found to be slower to heal than ulcers on other portions of the body.³⁹ In Bergstorm et al’s retrospective cohort study,²³ Stage II PU healing on the body and limbs was 59 days and 41 days, respectively, implying PUs on limbs heal faster than those on the body. When considering superficial thickness wounds, one may assume they are subject to less pressure than wounds other parts of the body, but there is no difference in their treatment.

The current study showed the proportion of small ulcers (3.0 cm²) healed at the end of the study was significantly higher than the proportion of larger ulcers, and smaller ulcer size was an independent factor in change in PUSH score, consistent with previous studies such as Gardner et al.⁴ Bergstorm et al²³ also reported PU <1 cm² in size heal five times faster than PUs >4.0 cm² and 3.5 times faster than PUs >1 cm² and <4.0 cm². In addition, no significant difference was found in healing status per stage, location, and length of healing, but according to PUSH factors, smaller wounds heal faster.

A number of study limitations suggest the results should be interpreted with caution. First, several possible explanations for the large unexplained variables in healing can be offered. Variables collected retrospectively from the EMR may not be as reliable as prospectively collected data. Second, a number of variables such as the use of a convenience sample that would have been useful to predict healing were not available for retrieval. Third, the time interval chosen to observe evidence of healing may not have fully reflected the effect of the factors measured, because patients may have healed after the study was concluded. Even though the changes in their PUSH score contributed to the survival analysis curve, the ultimate outcome may not be accurately reflected in the healed versus nonhealed comparisons. Finally, findings in a single acute hospital may indicate the effects of facility-specific factors influencing healing that are not readily apparent, such as knowledge and skills of caregivers and/or the number of staff. Also, although serum prealbumin may predict malnutrition outcomes, the author’s facility does not check this factor routinely, so these data were not available.

A retrospective chart review of patients with Stage II PUs was conducted to evaluate ulcer outcomes — operationalized as healed versus nonhealed — and factors that may affect healing as reflected in a change in PUSH score. The study showed that small ulcer size (3.0 cm²), higher MAP, and providing a pressure-redistribution surface and multivitamins positively affected healing of Stage II PUs in an acute care setting. A Stage II PU has limited tissue damage and heals in a pattern similar to an acute wound, so it is possible for these wounds to heal quickly and predictably. The author suggests strategies for Stage II PU healing in acute care setting should include expedient recognition of lower stage PUs and prevention of PU progression to higher stage; use of a pressure-redistribution surface; maintaining higher MAP; and providing multivitamins. Prospective studies are needed to confirm these findings.

The author thanks J. M. Hwang, RN, for the statistical analysis; J. H. Park, BSN, RN, CWON, and K. M. Kwon, MSN, RN, for participating in the expert group; and the five PWNs/RNs at Samsung Medical Center for assisting with data collection.

Dr. Park is Director, Samsung Medical Center International Wound Ostomy Continence Nursing Educational Program, Department of Nursing, Samsung Medical Center, Seoul, South Korea.

Please address correspondence to: Kyung Hee Park, PhD, RN, CWOCN, KGNP, WOC Office, 5th Floor, Annex Building, 81, Irwonro, Gangnam-gu, Samsung Medical Center, Seoul 135-719, Korea; email: khparksmc@skku.edu.