Factors Influencing Readmission after Curative Gastrectomy for Gastric Cancer Rima Ahmad, MBBS, Benjamin H Schmidt, MD, David W Rattner, MD, FACS, John T Mullen, MD, FACS The incidence of, and associated risk factors for, readmission after potentially curative gastrectomy for patients with gastric cancer has not been well studied. We sought to determine the 30-day readmission rate as well as the potential risk factors for readmission at our institution in patients undergoing gastrectomy for gastric cancer with curative intent. STUDY DESIGN: We performed a retrospective analysis of all patients undergoing potentially curative gastrectomy for gastric cancer from1995 to 2011. The 30-day hospital readmission rate was determined, and potential clinicopathologic risk factors for readmission were examined. RESULTS: Readmission to the hospital within 30 days occurred in 14.6% (61 of 418) of patients, including 6 patients who were readmitted more than once. The most common reasons for readmission included nutritional difficulties (n ¼12, 20%), intra-abdominal fluid collections (n ¼ 11, 18%), and small bowel obstruction (n ¼ 6, 10%). Factors associated with a higher 30-day readmission rate included type of resection (total gastrectomy, 23% vs subtotal gastrectomy, 13% vs esophagogastrectomy, 9%, p ¼ 0.016), pre-existing cardiovascular disease (17%, p ¼ 0.05), and history of a major postoperative complication (24%, p < 0.001). Factors not associated with a higher readmission rate included advanced age, preexisting pulmonary disease, T or N stage, extent of lymph node dissection, receipt of neoadjuvant chemotherapy or radiotherapy, length of stay of the index hospitalization, and destination and level of support on discharge. CONCLUSIONS: Readmission after potentially curative gastrectomy for gastric cancer is common. Patients with pre-existing cardiovascular disease, those who suffer major postoperative complications, and those undergoing total gastric resections are at especially high risk for readmission, and strategies designed to support these high-risk patients on discharge are warranted. (J Am Coll Surg 2014;218:1215e1222.  2014 by the American College of Surgeons)

BACKGROUND:

Since the Affordable Care Act of 2010 mandated creation of the Hospital Readmissions Reduction Program, which requires the Centers for Medicare and Medicaid Services (CMS) to reduce payments to hospitals with excess readmissions, there has been much discussion about strategies to decrease the rate of readmissions. Furthermore, readmission can be associated with increased hospital-related inpatient morbidity and mortality,1 so lowering the rate of readmission has been proposed as an important quality metric.2 Most hospitals have focused on steps to increase Disclosure Information: Nothing to disclose. Presented at the New England Surgical Society 94th Annual Meeting, Hartford, CT, September 2013. Received October 18, 2013; Revised January 9, 2014; Accepted February 10, 2014. From the Department of Surgery, Massachusetts General Hospital, Boston, MA. Correspondence address: John T Mullen, MD, FACS, Department of Surgery, Massachusetts General Hospital, 55 Fruit St, Yawkey 7B, Boston, MA 02114. email: [email protected]

ª 2014 by the American College of Surgeons Published by Elsevier Inc.

coordination of care and communications between providers and patients as well as improve discharge planning, education, and follow-up for discharged patients. Measures such as these and others have been implemented on a large scale, yet all-cause readmission rates have only decreased from 16.0% in 2006 to 15.3% in 2011.3 Although many of the steps taken so far, such as reducing the rate of in-hospital complications and strengthening the transitions of care, are quite intuitive and are applicable to patients across a wide spectrum of diagnoses, there is a need to better understand at a more granular level the exact causes of readmission to allow for introduction of more targeted care strategies. In particular, efforts to reduce the rate of readmission for surgical patients must account for the vast differences among the various surgical procedures in terms of their unique risks and complications. Although there have been several studies that have reported on the rates of readmission after abdominal surgery in general,4 colorectal surgery,5 and hepatopancreato-biliary surgery,6 few data exist on readmission

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after gastrectomy. Kim and colleagues7 reported a 7.5% 30-day readmission rate for patients with early gastric cancer undergoing subtotal gastrectomy at a single institution in Korea. However, the processes of care in the hospital and on discharge may vary significantly in Korea compared with the United States, so their experience may not be easily applied to the US. The only report from the US detailing the readmission rate after gastrectomy was published by Goodney and associates8 in 2003; they reported a 16.6% rate of readmission after gastrectomy for patients in the Medicare population. This study was limited by considering only 1 population of patients (those covered by Medicare) undergoing gastrectomy and by its lack of granular detail; the authors used a national database such that the true causes of readmission could not be ascertained. Accordingly, we sought to examine the 30-day readmission rate for patients undergoing potentially curative gastrectomy for gastric cancer at our institution in order to gain more detailed insight into the processes that led to readmission to the hospital. We sought to determine the risk factors for readmission and, in particular, to identify those factors on which we could potentially intervene to prevent readmission.

reasons for readmission, but the most significant problem that was cited as the reason for readmission was recorded. A broad panel of clinicopathologic factors that might influence the risk of readmission was examined. Among these were demographic and clinical characteristics, such as age, sex, pre-existing comorbidities, and receipt of neoadjuvant chemotherapy and/or radiotherapy. Cardiovascular comorbidities included conditions such as hypertension, coronary artery disease, and arrhythmias. Similarly, pulmonary comorbidities included such conditions as asthma, COPD, and interstitial lung disease. The lengths of the index admission and the out-of-hospital interval were noted for each patient. Data concerning the destination and the level of supportive services that each patient received on discharge from the index admission were also recorded. Patients were divided into 3 categories: those who received full-time support in a rehabilitation facility, those who were discharged to home with home services (eg, visiting nurse or home physical therapy services), and those who were discharged to home without services. Operative details were examined, including the extent of resection (esophagogastrectomy vs total gastrectomy vs subtotal gastrectomy) and the extent of lymph node dissection (D1 vs D2). All postoperative complications during the index hospitalization and within 30 days of the surgical procedure, including those identified in the outpatient setting, were recorded, and major complications were defined as those meeting the criterion of grade II or higher according to the Clavien-Dindo classification.9 In order to allow for a meaningful analysis, we only recorded whether or not a patient suffered any event that met these criteria during their index admission or within 30 days of discharge, regardless of the number of events or their exact severity level. We also examined a number of pathologic characteristics such as TNM stage, tumor grade, and the presence of perineural and venous invasion to determine whether any of these factors influenced the rate of readmission. Univariate comparisons were assessed using the chi-square test or Student’s independent t-test, where appropriate. Multivariate logistic regression models were constructed to explore the association of covariates with readmission. Overall survival (OS) was defined as death due to any cause and was estimated using the Cox proportional hazards model. All statistical analyses were performed using SPSS version 22.0 (SPSS).

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METHODS We conducted a retrospective review of our institutional database of all patients with gastric cancer who underwent resection with curative intent from 1995 to 2011. Patients undergoing gastrectomy with palliative intent and those who died within 30 days of the procedure were excluded from the study. Readmission was defined as admission to the inpatient service within 30 days of discharge from the index hospitalization for resection. The period of 30 days was chosen in part because this is the time interval that CMS uses to define a readmission in their Hospital Readmissions Reduction Program, and in part because the 30-day readmission rate has long been the standard rate reported in previous studies, allowing for comparison of our outcomes with those from other studies examining similar outcomes. An emergency room visit was not counted as a readmission unless the visit resulted in a subsequent inpatient hospitalization. Furthermore, readmissions to hospitals outside of the Massachusetts General Hospital (MGH)/Partners network could not be comprehensively captured, though it is our policy to encourage physicians at neighboring facilities to transfer their postoperative patients to MGH for further care, and these physicians are typically eager to do so. Discharge summaries were used to document the dates and the reasons for readmission. At least 1 primary reason for readmission was determined for each patient. Patients may have had multiple

RESULTS A total of 419 patients underwent curative intent gastrectomy for gastric cancer and met the inclusion criteria. Demographic and clinical characteristics of these patients are presented in Table 1. The median patient age was 68

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Table 1.

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Clinicopathologic Characteristics of the Patients

Characteristic

Median age, y Sex, n (%) Male Female Pre-existing comorbidities, n (%) Cardiovascular Pulmonary Type of resection, n (%) Total gastrectomy Subtotal gastrectomy Esophagogastrectomy Neoadjuvant therapy, n (%) Chemotherapy Radiotherapy Extent of node dissection, n (%) D0 D1 D2 D3 D4 Pathologic T stage, n (%) T0 T1 T2 T3 T4 Pathologic N stage, n (%) N0 N1 N2 N3

Data

68 272 (64.9) 146 (34.8) 210 (50.1) 34 (8.1) 124 (29.6) 159 (37.9) 129 (30.8) 108 49 1 132 283 2 1

(25.8) (11.7) (0.6) (29.9) (67.5) (1.3) (0.6)

8 80 124 166 41

(1.9) (19.0) (29.6) (39.6) (9.8)

170 131 71 46

(40.6) (31.2) (16.9) (11.0)

years, and the majority of patients (64.9%) were male. Sixty-one patients were readmitted within 30 days of index discharge, for an overall readmission rate of 14.6%. The median length of stay of the index hospitalization was 9 days, and the median time to readmission was also 9 days. There were 5 patients who were readmitted twice within the initial 30-day period, and 1 patient was readmitted 3 times. The causes of readmission were diverse and are summarized in Table 2. The single leading cause of readmission was nutritional difficulty, which occurred in 13 (21.3%) of the 61 patients. Patients were defined to have “nutritional difficulty” if they were unable to meet their nutritional needs due to inadequate intake and/or intolerance of oral and/or enteral feedings, typically manifested by nausea, vomiting, and/or early satiety. In the majority of patients (11 of 13), the cause of the nutritional

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Table 2. Causes of Readmission in 61 Patients after Gastrectomy for Gastric Cancer Cause of readmission

n

Nutritional difficulty Intra-abdominal fluid collection Small bowel obstruction Anastomotic leak Clostridium difficile colitis Chest pain Pleural effusion Abdominal pain Fever Gastrointestinal hemorrhage Jejunostomy tube site infection Pneumonia Anxiety Arrhythmia Decubitus ulcer Deep venous thrombosis Electrolyte abnormality PICC line infection Sepsis Transient ischemic attack Urinary retention

13 11 6 3 3 3 3 2 2 2 2 2 1 1 1 1 1 1 1 1 1

PICC, peripherally inserted central venous catheter.

difficulty was deemed to be a functional obstruction of the gastrointestinal tract, such as delayed gastric emptying or Roux limb stasis. Two patients had nutritional difficulties due to mechanical gastric outlet obstruction. Patients who had nutritional difficulty due to a small bowel obstruction were said to be readmitted with a small bowel obstruction and not “nutritional difficulty.” A single value of serum albumin within 1 month before surgery was used as a marker of preoperative nutritional status. These data were available for 11 of the 13 patients who were readmitted with nutritional difficulty, and all 11 patients had serum albumin levels in the normal range, with a median value of 4.0 g/dL (range 3.5 g/dL to 4.5 g/dL). Patients who were readmitted with nutritional difficulty were more likely to have received preoperative chemotherapy (6.5% vs 1.9%, p ¼ 0.019) or radiotherapy (12.2% vs 1.9%, p < 0.001). All patients readmitted for nutritional difficulty were meeting their nutritional needs via oral and/or enteral feedings at the time of discharge. Four of these patients were initially discharged to a rehabilitation facility, and 4 were discharged home with visiting nurse services. The remaining patients were evaluated by case managers and were deemed suitable to be discharged home without services. On readmission, most of these patients were managed conservatively; however, 2 patients were taken to the operating room for

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balloon dilation of an anastomotic stricture, and 1 patient underwent percutaneous endoscopic gastrostomy tube placement for delayed gastric emptying. Seven of the patients who were readmitted for nutritional compromise had feeding jejunostomy tubes that were placed at the time of operation, and 1 patient had a pre-existing jejunostomy tube that had been placed before initiation of neoadjuvant therapy. These patients presented with malnutrition despite the presence of an indwelling jejunostomy tube. The presence of a jejunostomy tube did not increase the out of hospital interval significantly (13 days compared with 9 days, p ¼ 0.431). Although patients without jejunostomy tubes all left the hospital on oral diets, those with feeding tubes left on either oral diets or tube feeds with an advancing oral plan. Three of these patients developed intolerance to their tube feeds at home, despite initially tolerating them during their index admission, and 1 patient’s jejunostomy tube became clogged before adequate transition to oral nutrition. The remaining patients were discharged entirely on oral intake, their jejunostomy tubes being left in place but not used. On readmission, these patients were managed by titration of their tube feedings with whatever level of oral intake they tolerated, so that when combined, their total caloric needs were met. Data for discharge destination and services on discharge were available for 374 (89%) of the patients in our cohort. In total, 73 patients (19.5%) were discharged to a rehabilitation hospital, 125 (33.4%) were discharged to home with support services, and the remaining 176 (47.1%) patients were discharged to home without services (Table 3). The destination and level of support provided to patients on discharge did not significantly affect the likelihood of

readmission (p ¼ 0.134), even when stratified by the type of surgical resection. Furthermore, the likelihood of readmission for nutritional difficulty, in particular, was not affected by the level of support on discharge (p ¼ 0.820). Several factors were associated with a significantly increased risk of readmission after curative intent gastrectomy (Table 4). Patients with pre-existing cardiovascular disease were more likely to be readmitted (p ¼ 0.05). However, advanced age and pre-existing pulmonary disease did not predict an increased risk of readmission. The extent of resection strongly correlated with the risk of readmission; patients undergoing a total gastrectomy had a readmission rate of 23% compared with 13% and 9% for those who underwent a subtotal gastrectomy and an esophagogastrectomy, respectively (p ¼ 0.016). There was no significant difference in the readmission rate between patients undergoing subtotal gastrectomy and esophagogastrectomy (p ¼ 0.38). The extent of lymph node dissection (D1 vs D2) also did not influence the rate of readmission (p ¼ 0.40). Not unexpectedly, patients who suffered a major postoperative complication were significantly more likely to be readmitted than those whose postoperative course was without a major complication (24% vs 9%, p < 0.01). Surprisingly, the median length of stay of the index admission did not have a significant impact on the rate of readmission (p ¼ 0.32). A number of pathologic factors were also analyzed to determine if the tumor biology or the extent of disease affected the risk of readmission. Though pathologic T stage and N stage showed no correlation with the likelihood of readmission (p ¼ 0.15 and p ¼ 0.32, respectively), the histologic factors of venous invasion (22.8% vs 12.6%, p ¼ 0.02) and perineural invasion (20% vs 9.9%,

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Table 3. Level of Support on Discharge from the Hospital by Type of Gastric Resection (Data Available for 374 of 419 Patients)

Extent of resection

Total gastrectomy Readmitted (n ¼ 28) Not readmitted (n ¼ 84) Subtotal gastrectomy Readmitted (n ¼ 20) Not readmitted (n ¼ 122) Esophagogastrectomy Readmitted (n ¼ 12) Not readmitted (n ¼ 108) All patients Readmitted (n ¼ 60) Not readmitted (n ¼ 314)

Discharge to a rehabilitation hospital

Level of support on discharge, % Discharge home with services

Discharge home with no services

p Value

0.092 36 17

32 36

32 47

15 16

35 29

50 55

25 22

42 36

33 42

0.844

0.856

0.214 27 18

35 33

38 49

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Table 4. Logistic Regression Analysis of Factors Associated with Readmission Within 30 Days of Discharge from Index Admission Risk factor

Sex Cardiovascular comorbidity Pulmonary comorbidity Major postoperative complication Length of stay of index hospitalization >10 d Neoadjuvant chemotherapy Neoadjuvant radiation therapy Extent of resection (vs total gastrectomy) Subtotal gastrectomy Esophagogastrectomy D1 vs D2 node dissection Pathologic T stage (vs T1 disease) T1 T2 T3 T4 Pathologic N stage (vs N0 disease) N0 N1 N2 N3 Histologic grade (vs well differentiated) Moderately differentiated Poorly differentiated Undifferentiated Perineural invasion Lymphovascular invasion Venous invasion

Odds ratio

1.33 1.83* 1.55 3.07* 1.43 1.17 0.93 1.00 0.49* 0.35* 1.24 1.00 1.25 2.30 2.49 1.00 1.46 1.85 2.00 1.00 0.65 1.14 1.00 2.27* 1.49 2.04*

Univariate 95% CI

p Value

Odds ratio

(0.73, (1.00, (0.62, (1.78, (0.84, (0.67, (0.74,

0.337 0.050* 0.361

Factors influencing readmission after curative gastrectomy for gastric cancer.

The incidence of, and associated risk factors for, readmission after potentially curative gastrectomy for patients with gastric cancer has not been we...
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