Association between Preoperative Exercise Tolerance and Unplanned Readmission in Patients with Pancreatic Cancer: A Retrospective Analysis

doi:10.21203/rs.3.rs-4875393/v1

Background

This study aimed to investigate the relationship between preoperative exercise tolerance and the likelihood of unplanned readmission in patients with pancreatic cancer. Despite advances in treatment, the incidence of postoperative complications following pancreatectomy remains high, leading to frequent hospital readmissions.

Methods

This retrospective analysis included 133 patients who underwent pancreatectomy between July 2019 and September 2022 and their preoperative exercise tolerance was assessed using the 6-min walk distance (6 MWD).

Results

The study found a 23.4% readmission rate within 1 year, with the median 6 MWD being significantly lower in readmitted patients than in those who were not readmitted (390.0 m versus 438.5 m; p < 0.01). A 6 MWD cut-off of 425 m was a strong predictor of readmission, with lower preoperative exercise tolerance associated with a higher risk of readmission.

Conclusions

Enhancing preoperative physical reserves through exercise therapy may reduce readmission rates and improve patient outcomes. Further research with larger sample sizes is required to confirm these findings.

preoperative exercise tolerance

unplanned readmission

pancreatic cancer

As the incidence of pancreatic cancer is projected to increase to 18.6/100 000 persons by 2050,¹ it is essential to address the related healthcare concerns. In Japan, the increase in age-adjusted mortality rates ranks first in both men and women.² Treatment for pancreatic cancer is selected on the basis of the pathological stage and overall condition (Performance Status: PS) of the patient and includes chemotherapy and surgical therapy. Neoadjuvant chemotherapy is currently administered for resectable pancreatic cancer, followed by surgical treatment.³ Pancreatectomy is a highly invasive and complex procedure that results in a postoperative complication rate of 10–50%,⁴ and often leads to prolonged hospitalization. The unexpected readmission rate within 30 days after pancreatectomy is reported to be 15–20%,^5,6 which is higher than that for esophageal cancer (10–13%)^7,8 and liver cancer (8%).⁹ Additionally, the readmission rate increases to 39% within 6 months¹⁰ and 53% within 1 year.¹¹ Unplanned readmissions have been linked to a range of factors, including postoperative complications,^5,10–12 age,^5,13 and operative time,¹⁴ which can negatively impact PS and affect long-term patient prognosis.¹⁵ Therefore, predicting the readmission risk preoperatively is crucial to improving patient outcomes. Preoperative knee extension strength, grip strength,¹⁶ and frailty¹⁷ are associated with survival rates in patients with pancreatic cancer, suggesting a link between preoperative physical function and midterm outcomes such as readmission. The 6-minute walk distance (6 MWD), which is an indicator of exercise tolerance, has been used to assess cardiopulmonary function.¹⁸ Moreover, the effects of resection, such as the decline in cardiopulmonary function and muscle strength, are well-documented,¹⁹ making it essential to evaluate the overall condition of patients before surgery and implement measures to enhance the physical reserve preoperatively if possible. To date, no studies have investigated the association between preoperative exercise tolerance and unplanned readmission in patients with pancreatic cancer. Therefore, this study aimed to explore this relationship.

Patients

In this retrospective study, which aimed to investigate the association between preoperative exercise tolerance and unplanned readmission in patients with pancreatic cancer, patient data were obtained from the medical records of 133 patients who underwent pancreatectomy between July 2019 and September 2022 at our hospital. Patients diagnosed with pancreatic cancer who underwent preoperative physical function assessments were selected. The exclusion criteria were diagnoses other than pancreatic cancer and missing data. The study end date was set at September 30, 2023. In accordance with the Declaration of Helsinki, an opt-out option was provided through our website and the study outline was made publicly available to provide patients with the opportunity to decline participation. The study was approved by the Institutional Review Board of Kitakyushu Municipal Medical Center (approval number: 202307003).

Measurement of exercise tolerance

Preoperative exercise tolerance was assessed by measuring the 6 MWD. The 6 MWD was measured under maximal effort according to the American Thoracic Society.²⁰

Measurement items

The variables included age, sex, body mass index, Brinkman index score, geriatric nutritional risk index, clinical frailty scale (CFS),²¹ preoperative neoadjuvant chemotherapy, length of hospital stay after surgery, cancer stage,²² Charlson Comorbidity Index score, and Clavien–Dindo classification. Complications were categorized on the basis of grade II or higher level.²³ Surgical factors included the surgical procedure, operative time, total fluid volume, blood loss volume, and blood transfusion. Preoperative physical function was assessed by measuring grip strength and knee extensor strength. Knee extension muscle strength was measured using a handheld dynamometer (#Tas F-1; Anima Co., Ltd., Tokyo, Japan). Measurements were conducted with the patient in a sitting position, with the knee positioned at approximately 90° of flexion. The dynamometer force pad was positioned proximal to the ankle joint to measure the force produced during quadriceps muscle contraction. Grip strength was measured twice on each side using a digital grip strength meter (TKK 5101, grip-D; Takei Scientific Instruments Co., Ltd., Tokyo, Japan) with the patient in the standing position, and the maximum value was adopted. Muscle strength varies with body size; therefore, the measurement results were divided by body weight to normalize the body size.²⁴ The preoperative blood data included hemoglobin, serum total protein, and serum albumin levels.

Statistical analyses

Data are presented as the median (interquartile range) regardless of whether it is normally distributed. Initially, the Shapiro–Wilk test was performed to check for normality. Patients were classified into two groups on the basis of whether they were readmitted within 1 year. Each variable was compared using a two-sample t-test, Mann–Whitney U test, and χ² test.

A receiver operating characteristic (ROC) curve was plotted, and the cut-off value, sensitivity, specificity, and area under the curve (AUC) for the 6 MWD were determined.

Log-rank tests and Kaplan–Meier analyses were performed, with the endpoint defined as the number of days until unplanned readmission within 1 year. Cox proportional hazards analysis was conducted with readmission as the dependent variable, the 6 MWD as the explanatory variable, and factors reported in previous studies as covariates.

All statistical analyses were performed using EZR, version 1.55²⁵ (Saitama Medical Center, Jichi Medical University, Saitama, Japan).

Basic patient characteristics

Table 1 shows the basic characteristics of the 94 patients. There were 43 males and 51 females with a median age of 72 (interquartile range, 69–77) years. The readmission rates were 22 (23.4%) within 1 year and 43 (45.7%) during the study period. The causes of readmission within 1 year included cholangitis (n = 4), septic shock (n = 3), liver abscess (n = 2), peritoneal dissemination, hypoglycemia, pancreaticojejunostomy stenosis, ulcer at the gastrojejunal anastomosis, common bile duct stone, pneumonia, hemorrhagic anemia, hyperammonemia, peripheral dizziness, urinary tract infection, bilateral hydronephrosis, fatigue, and anorexia.

Table 1

Preoperative characteristics of the study patients
Age, y	72.0 (69.3–77.0)
Male/female sex, n (%)	43 (45.7)/51 (54.3)
BMI (kg/m²)	22.3 (20.5–24.1)
GNRI	94.8 (89.6–101.4)
Brinkmann index	45 (0–761.3)
Procedure, PD/DP/LDP/TP (%)	50 (53.2)/39 (41.5)/2 (2.1)/3 (3.2)
Stage, 0/I/II/III/IV (%)	2 (2.1)/5 (5.3)/83 (88.3)/1 (1.1)/3 (3.2)
NAC, n (%)	80 (85.1)

Values are reported as the median (interquartile range) or number of patients (percentage).

BMI: body mass index, GNRI: geriatric nutritional risk index, PD: pancreatoduodenectomy, DP: distal pancreatectomy, LDP: laparoscopic distal pancreatectomy, TP: total pancreatectomy, NAC: neoadjuvant chemotherapy

Comparison of factors between readmission and non-readmission groups

The results of the comparison between the readmission and non-readmission groups are presented in Table 2. The preoperative 6 MWD was significantly lower in the readmission group than in the non-readmission group (390.0 m versus [vs.] 438.5 m; p < 0.01). Significant differences were found in CFS scores [3 (3–4) vs. 3 (1–3); p = 0.047], operative time (356.5 minutes vs. 298.5 minutes; p = 0.015), total transfusion volume (3527 mL vs. 2653 mL; p < 0.001), blood transfusion status [7 (31.8%) vs. 3 (4.2%); p < 0.01], and preoperative hemoglobin (10.5 g/dL vs. 11.5 g/dL p = 0.026) between the readmission and non-readmission groups.

Table２. Comparison of factors between groups with and without readmission

Variable	Readmission (n=22)	Without readmission (n=72)	p-value
Age (y)	72.0 (68.0–77.5)	72.5 (69.8–77.0)	0.484
Male/female sex, n (%)	10 (45.5) /12 (54.5)	41 (56.9) / 31 (43.1)	0.464
BMI (kg/m²)	21.89 (20.1–23.9)	22.43 (20.9–24.2)	0.495
GNRI	94.0 (88.4–102.3)	96.0 (90.7–101.3)
Brinkman index	152 (0–787.5)	0 (0–731.3)	0.411
NAC, n (%)	20 (90.9)	60 (83.3)	0.508
CCI, n (%)			0.305
Low	4 (18.2)	21 (29.2)
Medium	16 (72.7)	43 (59.7)
High	2 (9.1)	8 (11.1)
Cancer stage, n (%)			0.405
0	0	2
IA	0	4
IB	1	0
IIA	13	31
IIB	7	32
III	0	1
IV	2	1
Complications, n (%)	8 (36.4)	20 (27.8)	0.438
LOS (days)	20.0 (15.3–29.8)	21.0 (17.0–26.5)	0.858
Grip strength (%)	0.39 (0.31–0.49)	0.43 (0.36–0.48)	0.634
KES (N/kg)	2.69 (2.49–3.10)	3.10 (2.43–4.18)	0.25
６MWD (m)	390.0 (356.3–424.3)	438.5 (398.6–480.0)	<0.01
Clinical frailty scale score	3 (3–4)	3 (1–3)	0.047
Surgical procedure PD/DP/LDP/TP, n (%)	14 (63.6)/8 (36.4)/ 0(0)/ 0(0)	36 (50.0)/31 (43.1)/2 (2.8)/3 (4.2)	0.729
Operative time (min)	356.5 (303.8–458.3)	298.5 (224.8–377.0)	0.015
Infusion volume (mL)	3527.5 (2778.8–4863.8)	2653.0 (2002.5–3602.5)	<0.01
Blood loss (mL)	445 (220–1061.3)	240 (137.5–411.3)	0.011
Hb level (g/dL)	10.5 (9.5–11.7)	11.5 (10.6–12.2)	0.026
TP level (g/dL)	6.15 (5.9–6.8)	6.3 (6.0–6.6)	0.626
Alb level (g/dL)	3.6 (3.0–3.8)	3.6 (3.2–3.8)	0.456

Values are reported as the median (interquartile range) or number of patients (percentage).

BMI: body mass index, PD: pancreatoduodenectomy, GNRI: Geriatric Nutritional Risk Index, DP: distal pancreatectomy, NAC: neoadjuvant chemotherapy, LDP: laparoscopic distal pancreatectomy, CCI: Charlson Comorbidity Index, TP: total pancreatectomy, LOS: length of hospital stay, Hb: hemoglobin, KES: knee extension strength, TP: serum total protein, 6 MWD: 6-min walk distance, Alb: serum albumin

Insert Table 2 near here.

Cut-off value of 6 MWD associated with readmission

The cut-off value of the 6 MWD for readmission is shown in Fig. 1. The cut-off value in the ROC curve was 425 m (AUC: 0.747, sensitivity 63.9%, specificity 77.3%, 95% confidence interval [CI]: [0.632–0.862]).

Cox proportional hazards analysis with days to readmission as the end point

The relationship between the preoperative 6 MWD and readmission is presented in Fig. 2 and Table 3. The Kaplan–Meier curve revealed a significant difference in readmission rates between the group with 6 MWD > 425 m compared with the group with 6 MWD < 425 m (60.5% vs. 90.2%; p < 0.05). In the Cox proportional hazards analysis, a 6 MWD < 425 m was significantly associated with the risk of readmission within 1 year (hazard ratio: 5.41, 95% CI: 1.928–15.21; p < 0.01).

Table 3. Association of 6 MWD with unplanned hospital admissions within 1 year

	Model 1		Model 2		Model 3
	HR (95% CI)	p-value	HR (95% CI)	p-value	HR (95% CI)	p -value
6 MWD ≥425 m	Reference		Reference		Reference
6 MWD < 425 m	5.591(1.989–15.71)	< 0.01	5.465(1.931–15.46)	< 0.01	5.416 (1.928–15.21)	< 0.01
Age	0.958 (0.899–1.02)	0.179	0.956(0.897–1.019)	0.169	0.956 (0.897–1.017)	0.155
Complications			1.188(0.488–2.896)	0.705	1.494 (0.604–3.696)	0.385
Operation time					1.006 (1.00–1.01)	< 0.01
Model 1: adjusted for age, Model 2: adjusted for the variable in Model 1 and complications, Model 3: adjusted for variables in Model 2 and the operation time

This study aimed to examine the association between preoperative exercise tolerance and unscheduled readmissions in patients with pancreatic cancer. A 6 MWD cut-off of 425 m was identified, and patients with a preoperative 6 MWD <425 m exhibited a higher risk of readmission.

The readmission rate within 1 year in this study was 23.4%, which is less than half of the rate of 53%–59% reported in previous studies.^11,13 Several studies have reported 30-day readmission rates ranging from 11%–19%.^5-6,12 In this study, the average time to readmission was 140 days, with no (0%) patients readmitted within 30 days and seven (31.8%) readmitted within 90 days. This may be because the average length of hospital stay in other countries is reported to be approximately 7 days,¹² which is significantly shorter than the average of 21 days observed in this study. The shorter hospital stay may have resulted in a higher rate of postoperative complications after discharge, leading to early readmission. Early readmission within 30 days is associated with postoperative complications and may be preventable. Furthermore, readmission within 1 year may be linked to disease progression,¹¹ and hence it is crucial to investigate its association with survival.

The 6-min walk test is a simple tool that is used to assess cardiopulmonary function and is widely applied in clinical settings in cancer patients, as well as in individuals with respiratory and cardiovascular diseases. This test measures the use of oxygen by the muscles and the activity of the oxygen-carrying systems of the entire body.²⁶ The preoperative exercise capacity was used to estimate the physiological reserve available postoperatively by loading the entire oxygen delivery system.²⁷ A longer 6 MWD was moderately associated with higher maximum oxygen uptake capacity and better physical function.²⁸ However, the precise mechanisms linking preoperative exercise tolerance to readmission remain unclear. Low preoperative exercise tolerance can lead to further postoperative cardiorespiratory and muscular weakness¹⁹ due to reduced muscle mass and tissue fragility,²⁹ and may contribute to readmission due to postoperative complications. The 6 MWD cut-off calculated in this study may be useful as a predictor of future readmission.

In the multivariate analysis, operative time was also associated with readmission. The operative time was significantly longer in the readmission group than in the non-readmission group (356.5 minutes vs. 298.5 minutes; p=0.004). The total transfusion volume and number of intraoperative blood transfusions were also significantly different. Pancreatectomy is inherently a longer operation owing to its invasive nature and the complex surgical maneuvers required. The cardiac output increases to compensate for tissue hypoxia during severe surgical stress.³⁰ However, patients with low physical reserve are unable to cope with tissue oxygen deprivation and dysfunction during the immediate postoperative period. The body's compensatory response to prolonged surgical stress cannot be maintained, thereby leading to postoperative complications.³¹ Nevertheless, no significant difference in postoperative complications were identified in this study (13.9% vs. 31.8%, p=0.109); however, complications tended to be more common in the readmission group. These factors should be clarified further by conducting studies with larger cohorts.

The CFS also differed significantly between the readmission and non-readmission groups [3 (1–3) vs. 3 (3–4); p=0.047]. Although the median CFS score for both groups was 3, the readmission group had a higher proportion of individuals with CFS ≥4.³² We have previously reported an association between preoperative frailty and postoperative complications in patients with pancreatic cancer.²⁹ In general, frailty is characterized by a combination of factors such as loss of mobility, muscle strength, muscle mass, and poor nutritional status.³³ These factors reduce physiological reserves and increase vulnerability to acute stress.³⁴ Preoperative frailty may have affected post-discharge complications, leading to readmission due to tissue fragility. Therefore, detailed frailty assessments should be conducted in future studies.

The most common cause of readmission was cholangitis, which occurred in four cases (18%). Cholangitis is common not only in the early postoperative period but also during the late postoperative period after discharge and return to the community.³⁵ The late-onset rate ranges from 18% to 21%,^35-36 which is similar to the rate observed in this study (18.2%). Complications were not clearly related to exercise tolerance because of the influence of surgical procedures. However, it is crucial to improve physical reserve during the preoperative period to enhance the ability to tolerate treatment and prevent PS loss and muscle weakness due to re-hospitalization.

This study has several limitations. First, this was a single-center retrospective study with a small sample size, which limits the generalizability of our findings. Second, the general condition of the patients at the time of discharge may also be a potential factor affecting readmission; however, because this study focused on preoperative and intraoperative findings, the variable postoperative courses of patients was not adequately captured. Prospective studies with larger cohorts are required in the future to address these issues.

Invasive pancreatectomy may be associated with unfavorable outcomes in patients with low physical reserve. Therefore, preoperative exercise tolerance could be an important predictor of patient prognosis. In future, exercise therapy intervention during preoperative chemotherapy, preoperative exercise instruction, and surgery with increased reserve capacity may aid in improving the medium-term prognosis of patients with regard to re-hospitalization.

PS, Performance Status; 6 MWD, 6-min walk distance; CFS, clinical frailty scale; ROC, receiver operating characteristic; AUC, area under the curve; CI, confidence interval; vs., versus

Ethics approval and consent to participate

In accordance with the Declaration of Helsinki, an opt-out option was provided through our website and the study outline was made publicly available to provide patients with the opportunity to decline participation. The study was approved by the Institutional Review Board of Kitakyushu Municipal Medical Center (approval number: 202307003).

Consent for publication

Not applicable.

Availability of data and materials

The datasets generated and/or analyzed during the current study are not publicly available due to ethical and data security reasons (e.g., potential for identification of individual patients) but are available from the corresponding author on reasonable request.

Competing interests

The authors declare that they have no competing interests.

Funding

The authors declare that no funds, grants, or other support was received during the preparation of this manuscript.

Authors’ contributions

OM and NA collected the data. OM analyzed and organized the data and wrote the manuscript. KS, NK, and KS assisted in revising the manuscript and are accountable for all aspects of the work. All authors read and approved the final manuscript.

Acknowledgments

We would like to thank Editage (www.editage.jp) for English language editing.

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No competing interests reported.

Association between Preoperative Exercise Tolerance and Unplanned Readmission in Patients with Pancreatic Cancer: A Retrospective Analysis

Status:

Version 1

Abstract

Background

Methods

Results

Conclusions

Figures

Background

Methods

Patients

Measurement of exercise tolerance

Measurement items

Statistical analyses

Results

Basic patient characteristics

Comparison of factors between readmission and non-readmission groups

Cut-off value of 6 MWD associated with readmission

Cox proportional hazards analysis with days to readmission as the end point

Discussion

Conclusions

Abbreviations

Declarations

References

Additional Declarations

Status:

Version 1