Timing of rehabilitation and occurrence of pressure ulcers in patients with cervical spinal cord injuries

doi:10.21203/rs.3.rs-4624133/v1

Study design: A retrospective cohort study using a nationwide Japanese inpatient database.

Objectives: To investigate the association between the timing of rehabilitation interventions and the occurrence of pressure ulcers in hospitalized patients with cervical spinal cord injuries between 2010 and 2022 in a real-world clinical setting.

Setting: We used the Diagnosis Procedure Combination database, a nationwide Japanese inpatient database.

Methods: We included patients with cervical spinal cord injury who underwent spinal surgery within 3 days of admission between July 2010 and March 2022. We defined rehabilitation within 2 days of surgery as early rehabilitation and ≥3 days of surgery as non-early rehabilitation. The primary outcome was treating severe pressure ulcers ≥4 days after admission, and the secondary outcomes were length of hospital stay, hospitalization costs, and in-hospital mortality. Propensity score inverse probability of treatment weighting was conducted to compare the outcomes between the early and non-early rehabilitation groups.

Results: We identified 5,162 eligible patients, 3,434 (66.1%) of whom underwent early rehabilitation. After weighting, the occurrence of treating severe pressure ulcers showed no significant difference between the early and non-early rehabilitation groups (odds ratio [OR], 1.30; 95% confidence interval [CI], 0.79–2.12; P=0.297). The early rehabilitation group had lower total hospitalization costs (difference, –3.2%; 95% CI, –6.1% to 0.0%; P=0.043) and shorter length of hospital stay (difference, –4.5%; 95% CI, –8.4% to 0.0%; P=0.034) than the non-early rehabilitation group.

Conclusion: This study found no significant difference in the development of severe pressure ulcers between the early and non-early rehabilitation groups.

Health sciences/Diseases/Neurological disorders/Spinal cord diseases

Health sciences/Signs and symptoms/Skin manifestations

Pressure ulcers are a serious concern in patients with spinal cord injuries. These injuries impair motor, sensory, and autonomic functions, thereby increasing the risk of pressure ulcers [1, 2, 3, 4]. In total, 30–39% of patients with spinal cord injury develop pressure ulcers [5]. Moreover, the risk of developing pressure ulcers increases with higher levels of spinal cord injury, particularly with injuries at the cervical level, compared with that at the thoracic or lumbar levels [5].

Rehabilitation is crucial for preventing pressure ulcers in patients with spinal cord injuries. It aims to maximize bodily functions, preserve remaining functions, and enhance muscle strength for voluntary movement [6, 7]. Specifically, prolonged periods of immobility may compress the soft tissue between the bony prominence and external surface in patients with spinal cord injuries [8]. Poor physical activity increases the risk of pressure ulcers [4].

Although early intervention is commonly believed to be preferable [9, 10], few studies have thoroughly examined the timing of rehabilitation interventions for spinal cord injury. Although several studies have investigated the association between the timing of rehabilitation interventions and risk of pressure ulcers [10, 11], the results have been inconsistent, leaving the association unclear.

Therefore, this study aimed to investigate the association between the timing of rehabilitation interventions and the occurrence of pressure ulcers in patients with cervical spinal cord injuries in a real-world clinical setting.

Study Design and Data Source

We conducted a retrospective cohort study using the Diagnosis Procedure Combination database, a nationwide inpatient database of administrative claims and discharge abstracts in Japan. The details of the database are described elsewhere [12]. In short, the database includes approximately eight million inpatients annually from over 1,200 hospitals, corresponding to approximately 50% of all acute care admissions in Japan. The database includes data on age, sex, weight, height, smoking history, level of consciousness at admission, use of ambulance, discharge status, and Barthel Index at the time of admission or discharge. It also includes information on pressure ulcers. This database uses DESIGN-R to classify pressure ulcers [13]. The DESIGN-R evaluates pressure ulcers in terms of depth (D), exudate (E), size (S), inflammation/infection (I), granulation tissue (G), necrotic tissue (N), and pockets. The database includes the status of pressure ulcers at admission and discharge and treatment for severe pressure ulcers that reach the subcutaneous tissue (Design-R D3 or higher). The International Classification of Diseases and Related Health Problems 10th edition (ICD-10) codes are used to summarize the main diagnosis, admission precipitating diagnosis, resource-consuming diagnosis, comorbidities present at admission, and complications during hospitalization. It also includes information on date-stamped treatments, such as medications, procedures, and rehabilitation. Total hospitalization costs are also recorded.

Ethics

This study was approved by the Institutional Review Board of the University of Tokyo. The need for informed consent was waived owing to data anonymity.

Study Population

We identified patients diagnosed with cervical spinal cord injury (ICD-10 code S141) in the main diagnosis, admission precipitating diagnosis, and resource-consuming diagnosis during hospitalization from July 2010 to March 2022. We excluded patients who (i) were aged < 18 years, (ii) did not undergo spinal surgery within 3 days of admission, (iii) did not undergo cerebrovascular rehabilitation during hospitalization, or (iv) had a history of pressure ulcers at admission. If patients were admitted more than once for cervical cord injury, only the first admission was included.

Exposure and Outcome

We defined rehabilitation within 2 days of surgery as early rehabilitation. Rehabilitation that started ≥ 3 days of surgery was defined as non-early rehabilitation. The national health insurance system in Japan covers the rehabilitation provided by physical and occupational therapists.

The primary outcome was the treatment of severe pressure ulcers (Design-R D3 or higher) on the fourth day of admission. The secondary outcomes were length of hospital stay, hospitalization costs, and in-hospital mortality.

Covariates

We extracted data on factors that could affect the development of pressure injuries from the database. Baseline measurements included age, sex, body mass index, Charlson Comorbidity Index score, smoking index, level of consciousness at admission, diabetes mellitus, use of ambulance, Barthel index items at admission [14], presence of suicide attempt, days from hospitalization to surgery, drug use within 3 days of admission (steroids, inotropes, gastrointestinal drugs, anticoagulants, anesthetics), respiratory management with tracheostomy and intubation within 3 days of admission, type of spinal cord injury (central, without radiographic evidence of trauma, with radiographic evidence of trauma or fracture), and hospital volume. Hospital volume was defined as the annual average number of patients with cervical spinal cord injury and categorized into < 24 patients, 24 to < 48 patients, and ≥ 48 patients annually.

Statistical Analyses

We used propensity score inverse probability of treatment weighting to compare outcomes between the early and non-early rehabilitation groups [15, 16]. A multivariate logistic regression model was applied to predict the propensity score of each patient to receive rehabilitation within 2 days postoperatively using the variables listed in Table 1 as independent variables. We adjusted for within-hospital clustering using generalized estimating equations. We calculated the absolute standardized differences in each variable in the unweighted and weighted cohorts to examine whether the weighting balanced the measured variables between groups. An absolute standardized difference of < 10% indicated a negligible imbalance between groups [15].

Table 1

Characteristics of patients before and after inverse probability of treatment weighting
	Before IPTW			After IPTW
Characteristics	Early rehabilitation (N = 3,434)	Non-early rehabilitation (N = 1,728)	SMD	Early rehabilitation (N = 3,434)	Non-early rehabilitation (N = 1,728)	SMD
Age, years, %
< 40	4.3%	5.7%	–0.07	4.5%	5.0%	–0.02
40–65	24.1%	23.4%	0.01	24.0%	24.6%	–0.01
> 65	71.7%	70.9%	0.02	71.5%	70.4%	0.02
Male ,%	76%	78%	–0.06	76%	77%	–0.01
Body mass index (kg/m²), %
< 18.5	8.1%	7.3%	0.03	7.8%	7.6%	0.01
18.5–22.4	35.7%	35.6%	0.00	35.4%	36.1%	–0.02
22.5–24.9	24.6%	25.4%	–0.02	24.5%	24.9%	–0.01
25.0–30.0	19.8%	20.8%	–0.03	20.0%	20.5%	–0.01
> 30.0	3.9%	3.9%	0.00	3.9%	3.7%	0.01
missing	8.0%	7.0%	0.04	8.4%	7.1%	0.05
Charlson Comorbidity Index score, %
0	70.6%	69.2%	0.03	69.3%	71.0%	–0.04
1	4.3%	4.5%	–0.01	4.4%	4.1%	0.02
2	21.6%	21.8%	–0.01	22.2%	21.0%	0.03
≥ 3	3.5%	4.6%	–0.05	4.1%	3.9%	0.01
Smoking history, %
None	53.7%	50.3%	0.07	52.4%	52.0%	0.01
Brinkman Index 1–399	7.6%	8.4%	–0.03	7.9%	8.0%	0.00
Brinkman Index 400–699	8.7%	7.3%	0.05	8.4%	7.5%	0.03
Brinkman Index 700–	11.5%	11.1%	0.01	11.5%	11.5%	0.00
missing	18.5%	22.8%	–0.11	19.7%	21.0%	–0.03
Days from hospitalization to surgery, %
0	53.1%	61.6%	–0.17	56.5%	55.1%	0.03
1	32.6%	28.3%	0.09	31.0%	31.2%	0.00
2	14.3%	10.1%	0.13	12.4%	13.7%	–0.04
Japan Coma Scale score at admission, %
Alert	74.1%	67.3%	0.15	73.3%	69.6%	0.08
Dizziness	19.4%	23.8%	–0.11	19.7%	22.7%	–0.07
Somnolence	4.3%	5.3%	–0.04	4.5%	5.0%	–0.02
Coma	2.2%	3.6%	–0.09	2.5%	2.7%	–0.01
Diabetes mellitus, %	19%	18%	0.00	19%	18%	0.03
Ambulance use, %	84%	87%	–0.10	85%	84%	0.01
Suicide attempt, %	58%	50%	0.15	55%	57%	–0.03
Drug use within 3 days of admission, %
Steroid	28.9%	27.8%	0.02	27.9%	29.0%	–0.02
Anesthetic	93.3%	90.6%	0.10	92.9%	91.7%	0.04
Cardiotonic	79.9%	82.3%	–0.06	81.1%	80.9%	0.01
Gastrointestinal	75.4%	83.0%	–0.19	78.0%	79.0%	–0.02
Anticoagulant	64.6%	68.1%	–0.07	64.2%	68.0%	–0.08
Procedures within 3 days of admission, %
Tracheostomy	2.0%	2.8%	–0.05	2.3%	2.4%	–0.01
Artificial ventilation in intubation	24.2%	38.1%	–0.30	28.4%	30.3%	–0.04
Type of spinal cord injury, %
Radiographic evidence of trauma or fracture	10.0%	15.2%	–0.16	11.8%	11.9%	–0.01
No radiographic evidence of trauma	5.3%	4.9%	0.02	5.0%	5.4%	–0.02
Central	8.6%	5.5%	0.12	7.5%	7.4%	0.00
Hospital volume, %
< 24	65.0%	62.8%	0.05	61.5%	68.1%	–0.14
24–48	21.6%	21.8%	–0.01	21.9%	20.9%	0.02
> 48	13.5%	15.4%	–0.06	16.6%	11.0%	0.16
Barthel Index at admission, %
Feeding
0	69.8%	71.9%	–0.05	70.7%	70.6%	0.00
5	6.4%	6.8%	–0.01	6.6%	6.8%	–0.01
10	15.1%	11.2%	0.12	13.9%	13.2%	0.02
45	8.7%	10.1%	–0.05	8.8%	9.5%	–0.02
Transferring
0	78.5%	80.3%	–0.05	79.7%	78.8%	0.02
5	1.7%	1.6%	0.02	1.7%	1.6%	0.01
10	3.6%	2.8%	0.04	3.3%	2.9%	0.02
15	11.5%	9.0%	0.08	10.4%	11.1%	–0.02
45	4.7%	6.3%	–0.07	4.8%	5.6%	–0.03
Grooming
0	81.4%	82.5%	–0.03	82.4%	81.2%	0.03
5	12.9%	9.8%	0.10	11.6%	12.2%	–0.02
45	5.7%	7.7%	–0.08	6.0%	6.6%	–0.03
Toilet use
0	78.3%	79.7%	–0.03	79.3%	78.6%	0.02
5	4.1%	3.9%	0.01	4.0%	3.5%	0.03
10	11.7%	9.0%	0.09	10.5%	11.3%	–0.03
45	5.9%	7.5%	–0.06	6.1%	6.5%	–0.02
Bathing
0	77.7%	79.5%	–0.04	78.8%	77.8%	0.03
5	11.2%	8.2%	0.10	9.9%	10.6%	–0.02
45	11.1%	12.3%	–0.04	11.3%	11.6%	–0.01
Mobility
0	77.4%	77.4%	0.00	78.1%	76.6%	0.04
5	1.2%	1.4%	–0.03	1.2%	1.4%	–0.02
10	1.7%	1.7%	0.00	1.7%	1.6%	0.01
15	10.8%	8.4%	0.08	9.7%	10.5%	–0.03
45	8.9%	10.9%	–0.07	9.2%	9.8%	–0.02
Climbing stairs
0	77.4%	77.0%	0.01	78.1%	76.5%	0.04
5	2.1%	2.3%	–0.01	2.2%	2.0%	0.01
10	10.8%	8.2%	0.09	9.6%	10.3%	–0.03
45	9.7%	12.5%	–0.09	10.2%	11.2%	–0.03
Dressing
0	79.7%	81.2%	–0.04	81.0%	79.9%	0.03
5	4.5%	4.0%	0.03	4.4%	3.9%	0.02
10	11.3%	8.4%	0.10	10.0%	10.8%	–0.02
45	4.4%	6.4%	–0.09	4.6%	5.5%	–0.04
Bowels
0	72.5%	75.5%	–0.07	74.1%	73.5%	0.01
5	3.8%	3.4%	0.02	3.8%	3.5%	0.02
10	16.8%	12.4%	0.12	15.1%	15.1%	0.00
45	6.9%	8.7%	–0.07	7.1%	7.9%	–0.03
Bladder
0	73.2%	76.1%	–0.07	74.7%	74.0%	0.02
5	3.8%	3.1%	0.04	3.6%	3.2%	0.02
10	16.6%	12.0%	0.13	14.8%	15.0%	0.00
45	6.4%	8.8%	–0.09	6.8%	7.8%	–0.04
IPTW, inverse probability of treatment weighting; SMD, standardized mean difference

A generalized linear model was used to estimate the association between early rehabilitation and primary or secondary outcomes in the weighted population. The significance level threshold was set at P value < 0.05. All statistical analyses were performed using STATA version 18.0.

Sensitivity Analyses

For the sensitivity analyses, we changed the outcome definition and performed the same analysis. Pressure ulcers were redefined as (i) those diagnosed with ICD-10 code L890–899 (pressure ulcers) as complications during hospitalization and (ii) those requiring medication for pressure ulcers after the fourth day of admission.

We identified 75,161 hospitalized patients with cervical spinal cord injury. After applying the inclusion and exclusion criteria, 5,162 patients were included in this study (Fig. 1). Of those, 3,434 (66.1%) were included in the early rehabilitation group.

Table 1 shows a comparison of the characteristics of the early and non-early rehabilitation groups. Thirteen of the 31 baseline covariates had standardized differences > 10%. After applying inverse probability of treatment weighting, the patient characteristics were well-balanced between the two groups. Propensity score distribution was also balanced (Figures S1–S2).

Table 2 shows the outcomes of the weighted cohorts. After inverse probability of treatment weighting, the occurrence of treating severe pressure ulcers after the fourth day of admission showed no significant difference in the early and non-early rehabilitation groups (1.7% vs. 1.6%; odds ratio, 1.30; 95% confidence interval [CI], 0.79–2.12; P = 0.297). The early rehabilitation group had lower total hospitalization costs (difference, − 3.2%; 95% CI, − 6.1–0.0%; P = 0.043) and shorter length of hospital stay (difference, − 4.5%; 95% CI, − 8.4–0.0%; P = 0.034) than the non-early rehabilitation group. In-hospital mortality was not significantly different between the two groups (odds ratio, 1.04; 95% CI, 0.76–1.43; P = 0.775).

Table 2

Association between early rehabilitation and outcomes after inverse probability of treatment weighting
	Early rehabilitation (N = 3,434)	Non-early rehabilitation (N = 1,728)	Odds ratio	95% CI	P
Primary outcome
Treatment of severe pressure ulcers	1.7%	1.6%	1.30	(0.79–2.12)	0.297
Secondary outcome
In-hospital mortality	3.4%	3.9%	1.04	(0.76–1.43)	0.775
			%difference	95% CI	P
Length of hospital stay, median	33 days	37 days	–4.5	(–8.4 to 0.0)	0.034
Hospital cost, median	27,183 dollars	31,317 dollars	–3.2	(–6.1 to 0.0)	0.043
CI, confidence interval

In the sensitivity analyses, the early rehabilitation group had a lower proportion of patients who used medications to treat pressure ulcers after the fourth day of admission than the non-early rehabilitation group. No other outcomes showed significant differences between the two groups.

In this study, we used a large national inpatient database to examine the association between early rehabilitation and development of pressure ulcers in patients with cervical spinal cord injuries. There was no significant association between early rehabilitation intervention within 2 days after surgery and the occurrence of severe pressure ulcers. Furthermore, early rehabilitation was not associated with in-hospital mortality but was significantly associated with lower total hospital costs and shorter length of hospital stay.

Common risk factors for pressure ulcers include activity, mobility, perfusion, and skin conditions. These factors interact with each other and influence the development of pressure ulcers [4]. Although some studies have investigated the risk factors specific to spinal cord injury [17], few have investigated the association between the timing of rehabilitation and outcomes, showing inconsistent results [10, 11]. In this study, we used a large database to examine the association between early rehabilitation and development of pressure ulcers.

In this study, there was no significant difference in the development of severe pressure ulcers, regardless of the timing of rehabilitation. Early rehabilitation may increase the time required for shear and friction forces to occur during bed up and movement [18, 19]. In addition, pressure is applied to the supporting surface of the body, which differs from that when lying down. Exercise is also assumed to increase blood flow throughout the body [20]. We hypothesized that these factors offset each other and that there was no noticeable difference in the occurrence of pressure ulcers.

In the sensitivity analysis, the early rehabilitation group had a lower proportion of patients who used medications to treat pressure ulcers after the fourth day of admission than did the non-early rehabilitation group. These results suggest that early rehabilitation may positively affect the occurrence of mild-to-moderate pressure ulcers.

The results of our study suggest that early rehabilitation is unlikely to negatively affect the development of pressure ulcers. Therefore, considering functional and mental recovery [21–23], it may be advisable to initiate rehabilitation early without concerns about increasing pressure ulcers.

This study has some limitations. First, because it had a retrospective observational design, the decision to perform early rehabilitation was left to the discretion of each physician. It is possible that the severity and instability of the spinal cord injury itself influenced the decision to undergo early rehabilitation. Second, there may have been some unmeasured confounders. The database does not contain detailed information on the severity of spinal cord injuries (e.g., level of neurological damage or assessment based on the American Spinal Injury Association classification), vital signs, or blood test results. In addition, data on exercise intensity during rehabilitation or rehabilitation procedures were lacking. Third, this study used treatment of severe pressure ulcers as an outcome. However, similar information is not available for patients with mild pressure ulcers. The definition of the outcome may have high specificity but low sensitivity. However, we performed sensitivity analyses to change the definition of pressure ulcers. The results of the sensitivity analyses were consistent with those of the main analysis.

In conclusion, this study, using a nationwide inpatient database, found no significant differences in the development of severe pressure ulcers between the early and non-early rehabilitation groups.

Data Availability Statement

The data analyzed in the present study are not publicly available for ethical reasons but are available from the corresponding author upon request.

Ethical Approval

This study was approved by the Institutional Review Board of the University of Tokyo (approval number: 3501-[3]) and was conducted in accordance with the Declaration of Helsinki. The obligation to obtain informed consent was waived because of data anonymity.

Competing Interests

The authors declare no competing interests.

Funding

This work was supported by grants from the Ministry of Health, Labour and Welfare, Japan (23AA2007 and 22AA2003).

Author Contributions

RY and YS conceived the concept and design of the study. RY and SA compiled and synthesized the data. RY and YM performed the statistical analyses. YH supervised the study. All authors participated in the interpretation of the results and writing of the report and approved the final version of the manuscript.

Acknowledgements

None

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There is no duality of interest

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Timing of rehabilitation and occurrence of pressure ulcers in patients with cervical spinal cord injuries

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