Transhiatal vs. Transthoracic Esophagectomy: A ...

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TTE 9.4%, p = 0.35) or 30-day mortality (THE 2.3% vs. TTE 2.5%, p ..... Khullar OV, Jiang R, Force SD, Pickens A, Sancheti MS, Ward K, ... SS, van der Peet DL.
J Gastrointest Surg DOI 10.1007/s11605-017-3572-1

ORIGINAL ARTICLE

Transhiatal vs. Transthoracic Esophagectomy: A NSQIP Analysis of Postoperative Outcomes and Risk Factors for Morbidity Francisco Schlottmann, MD 1

&

Paula D. Strassle, MSPH 1,2 & Marco G. Patti, MD 3

Received: 29 June 2017 / Accepted: 29 August 2017 # 2017 The Society for Surgery of the Alimentary Tract

Abstract Background Both transhiatal esophagectomy (THE) and transthoracic esophagectomy (TTE) are accepted procedures for esophageal resection. We aimed to compare postoperative outcomes between these procedures and identify risk factors for morbidity. Methods A retrospective analysis was performed using the American College of Surgeons National Surgical Quality Improvement Program database. Adult patients who underwent THE or TTE between 2005 and 2014 were included. Postoperative morbidity, length of stay, and 30-day mortality were compared. Multivariable logistic regression was used to determine risk factors for complications, and likelihood ratio tests were used to assess whether the effect of each risk factor was different across THE and TTE. Results A total of 4053 patients were included, 2362 (58.3%) underwent TTE and 1691 (41.7%) underwent THE. TTE was associated with higher incidences of postoperative pneumonia and bleeding requiring transfusion. THE had higher incidences of superficial wound infection, deep wound infection, urinary tract infection, and sepsis. There were no significant differences in occurrence of anastomotic leak (THE 7.6% vs. TTE 9.4%, p = 0.35) or 30-day mortality (THE 2.3% vs. TTE 2.5%, p = 0.63). Female gender, black race, hypertension, diabetes, chronic obstructive pulmonary disease, partially or fully dependent functional status, and an ASA score ≥ 3 were independently associated with postoperative complications. The impact of the risk factors on morbidity was similar across both procedures. Conclusions THE and TTE have similar incidence of anastomotic leak and 30-day mortality. The impact of gender, race, and patients’ comorbidities on postoperative complications is similar across both types of esophagectomy. Keywords Transhiatal esophagectomy . Transthoracic esophagectomy . Outcomes Francisco Schlottmann, MD, Paula Strassle, MSPH, and Marco G. Patti, MD, conceived the study and helped with literature search and writing of the manuscript. * Francisco Schlottmann, MD [email protected]

1

Department of Surgery and Center for Esophageal Diseases and Swallowing, University of North Carolina at Chapel Hill, 4030 Burnett Womack Building, 101 Manning Drive, CB 7081, Chapel Hill, NC 27599-7081, USA

2

Department of Epidemiology, Gillings School of Global Public Health, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA

3

Department of Medicine and Surgery, University of North Carolina, Chapel Hill, NC, USA

Introduction Although there has been a significant improvement in operative techniques and postoperative care, esophagectomy remains one of the most demanding surgical procedures with significant associated morbidity and mortality.1,2 The two main surgical techniques to remove the esophagus include a transthoracic (Ivor Lewis) esophagectomy (TTE) with a mediastinal anastomosis, and transhiatal esophagectomy (THE) with a cervical anastomosis. The transthoracic technique offers better visualization of the operative field, which allows more thorough dissection of the esophagus. However, this approach has often been

J Gastrointest Surg

linked to higher rates of postoperative morbidity and mortality.3–5 On the other hand, THE is often criticized because it does not adhere to the basic surgical principles of exposure and hemostasis. Consequently, the surgical approach is often decided based on surgeon preference. Besides the operative approach, which is an important consideration, patient’s characteristics may have a greater influence on postoperative complications.6,7 Thus, it is of paramount importance to tailor the operation to the individual patient, based on specific patient’s factors that may contribute to major complications. We aimed to compare surgical outcomes between THE and TTE, and identify patient’s risk factors for postoperative complications for both procedures in a large multi-hospital cohort.

Potential risk factors for complication were assessed using multivariable logistic regression. Models were adjusted for admit year, esophagectomy type, age, gender, race, hypertension, diabetes, chronic obstructive pulmonary disease (COPD), smoking, wound classification, and American Society of Anesthesiologists (ASA) classification. In addition to the covariates listed above, interaction terms between esophagectomy type and each covariate were included in the multivariable models so effect-measure modification could be assessed, using likelihood ratio tests. Patient age was modeled as quadratic variable as determined by functional form assessment and centered at 60 years old. All analyses were performed using SAS software version 9.4 (SAS Inc., Cary, NC). A p value < 0.05 was considered significant for all tests.

Methods Study Design and Population

Results A cohort of patients was identified using the American College of Surgeons (ACS) National Surgical Quality Improvement Program (NSQIP) database between January 1, 2005 and December 31, 2014. NSQIP is a risk-adjusted database comprised of over 500 hospitals that voluntarily submit patient demographic, preoperative risk factors, and 30-day postoperative outcome data as part of an ACS-sponsored initiative in quality improvement. Eligible patients were identified using Current Procedural Terminology (CPT) codes. Adult patients who underwent a primary procedure of THE (CPT 43107) or TTE (43117) were eligible for inclusion. Postoperative complications included superficial and deep wound surgical site infections, anastomosis leak (defined as organ site infection), pneumonia, pulmonary embolism/deep vein thromboembolism (PE/ DVT), unplanned intubation, > 48 h on ventilator, acute renal failure, urinary tract infection (UTI), cardiac complications (cardiac arrest and/or myocardial infarction), bleeding requiring transfusion, sepsis/septic shock, return to the OR, and 30-day mortality. A composite complication (i.e., at least one postoperative complication) and length of stay after surgery were also analyzed. Statistical Analyses Patient demographics and surgical characteristics were compared across esophagectomy type using chi-square and Student’s t tests where appropriate. Unadjusted, bivariate analyses of postoperative complications, length of stay, and 30day mortality were also assessed using chi-square and Student’s t tests. Patient demographics, stratified by complication status were compared using Fisher’s exact and Student’s t tests.

A total of 4053 patients were included; 2362 (58.3%) underwent TTE and 1691 (41.7%) underwent THE. There were no meaningful differences in age, presence of comorbidities, and functional status between patients undergoing TTE and THE (Table 1). The transthoracic approach was associated with significantly higher incidences of postoperative pneumonia (16.8 vs. 13.8%, p = 0.01) and bleeding requiring transfusion (15.4 vs. 11.6%, p < 0.001). THE had significantly higher incidences of superficial wound infection (10.2 vs. 4.7%, p < 0.001), deep wound infection (3.1 vs. 1.3%, p < 0.001), unplanned intubation (14.1 vs. 11.7%, p = 0.02), urinary tract infection (3.8 vs. 2.5%, p = 0.01), and sepsis (15.0 vs. 12.4%, p = 0.01). There were no significant differences in occurrence of anastomotic leak (THE 7.6% vs. TTE 9.4%, p = 0.35) or 30day mortality (THE 2.3% vs. TTE 2.5%, p = 0.63). The mean length of hospital stay was 14 days for both procedures (Table 2). Female gender (OR 1.33, 95% CI 1.11, 1.60, p = 0.003), black race (OR 1.59, 95% CI 1.03, 2.46, p = 0.04), hypertension (OR 1.17, 95% CI 1.00, 1.37, p = 0.05), diabetes (OR 1.74, 95% CI 1.29, 2.36, p = 0.0003), COPD (OR 1.87, 95% CI 1.39, 2.51, p < 0.0001), partially or fully dependent functional status (OR 2.71, 95% CI 1.29, 5.69, p = 0.008), and ASA score ≥ 3 (OR 1.37, 95% CI 1.13, 1.68, p = 0.002) were independently associated with postoperative complications (Table 3). The effect-measure modification analysis showed that the impact of each risk factor on postoperative morbidity was similar across both procedures (Table 4).

J Gastrointest Surg Table 1 Distribution of patient and hospital characteristics among adult patients undergoing transhiatal esophagectomy or Ivor Lewis esophagectomy between 2005 and 2014, stratified by type

Gender, n (%) Male Female Age, mean (SD) Race, n (%) White Black Othera Comorbidities, n (%) Hypertension Diabetes COPD Smoking Functional status, n (%) Independent Partially or fully dependent Wound classification, n (%) Clean Clean/contaminated Contaminated or dirty/infected ASA classification, n (%) 1 or 2 3, 4, or 5

Transhiatal

Ivor Lewis

p value

1691 (41.7%)

2362 (58.3%)

1342 (79.5) 347 (20.5) 64 (10.5)

1933 (81.9) 428 (18.1) 63 (10.3)

0.05 – 0.01

1239 (94.5) 43 (3.3) 29 (2.2)

1936 (94.7) 70 (3.4) 39 (1.9)

0.84 0.82 0.54

859 (50.8) 98 (6.6) 133 (7.9) 425 (25.1)

1218 (51.6) 131 (6.2) 181 (7.7) 624 (26.4)

0.63 0.64 0.81 0.36

1658 (98.2) 30 (1.8)

2328 (98.6) 32 (1.4)

0.28 –

54 (3.2) 1.591 (94.1) 46 (2.7)

48 (2.0) 2198 (93.1) 116 (4.9)

0.02 0.19 0.0004

343 (20.3) 1347 (79.7)

425 (18.0) 1936 (82.0)

0.07 –

p-values < 0.05 are denoted in italic SD standard deviation, COPD chronic obstructive pulmonary disease, ASA American Society of Anesthesiologists a

Other race includes American Indian/Alaska native, Asian, and native Hawaiian/Pacific Islander

Discussion We aimed to compare postoperative outcomes and identify risk factors for morbidity for both types of esophagectomy. Table 2 Incidence of postoperative complications and length of stay among adults undergoing hernia repair, stratified by type

Postoperative complications, n (%) Superficial wound infection Deep wound infection Anastomosis leaka Pneumonia PE/DVT Unplanned intubation > 48 h on ventilator Renal failure Urinary tract infection Cardiac complications Bleeding requiring transfusion Sepsis Return to the OR Mortality Any complicationb, n (%) LOS after surgery, mean (SD)

We found that TTE was associated with a higher incidence of postoperative pneumonia and bleeding requiring transfusion, while THE had a higher incidence of wound infection and sepsis. Both procedures had similar incidence of anastomotic Transhiatal

Ivor Lewis

1691 (41.7%)

2362 (58.3%)

173 (10.2) 53 (3.1) 128 (7.6) 234 (13.8) 74 (4.4) 238 (14.1) 225 (13.3) 19 (1.1) 65 (3.8) 46 (2.7) 196 (11.6) 254 (15.0) 205 (12.1) 39 (2.3) 803 (47.5) 14 (12.9)

110 (4.7) 30 (1.3) 189 (9.4) 396 (16.8) 121 (5.1) 276 (11.7) 284 (12.0) 29 (1.2) 58 (2.5) 56 (2.4) 363 (15.4) 292 (12.4) 333 (14.1) 60 (2.5) 1102 (46.7) 14 (12.2)

p value

< 0.0001 < 0.0001 0.35 0.01 0.28 0.02 0.22 0.76 0.01 0.48 0.0006 0.01 0.07 0.63 0.60 0.93

p-values < 0.05 are denoted in italic PE/DVT pulmonary embolism/deep vein thromboembolism, SD standard deviation, OR operating room, LOS length of stay a

Defined as either an organ space infection or dehiscence

b

At least one postoperative complication (compared to no complications)

J Gastrointest Surg Table 3 Crude and adjusted odds ratio of risk factors on postoperative complications among patients undergoing transhiatal or Ivor Lewis esophagectomy

Adjusteda

Crude

Gender Male Female Age, 10-year increase Race White Black Other Comorbiditiesb Hypertension Diabetes COPD Smoking Functional status Independent Partially or fully dependent Wound classification Clean Clean/contaminated Contaminated or dirty/infected ASA classification 1 or 2 3, 4, or 5

OR (95% CI)

p value

OR (95% CI)

p value

ref 1.30 (1.11, 1.52) 1.12 (1.06, 1.19)

– < 0.0001 0.0001

ref 1.33 (1.11, 1.60) 1.07 (0.99, 1.15)

– 0.003 0.11

ref 1.59 (1.09, 2.32) 1.04 (0.64, 1.69)

– 0.02 0.87

ref 1.59 (1.03, 2.46) 1.04 (0.61, 1.78)

– 0.04 0.88

1.31 (1.16, 1.48) 1.76 (1.34, 2.32) 1.98 (1.56, 2.52) 1.15 (1.00, 1.32)

< 0.0001 < 0.0001 < 0.0001 0.06

1.17 (1.00, 1.37) 1.74 (1.29, 2.36) 1.87 (1.39, 2.51) 1.07 (0.90, 1.28)

0.05 0.0003 < 0.0001 0.45

ref 3.95 (2.17, 7.18)

– < 0.0001

ref 2.71 (1.29, 5.69)

– 0.008

ref 0.76 (0.51, 1.13) 1.51 (0.91, 2.50)

– 0.18 0.11

ref 0.78 (0.49, 1.16) 1.39 (0.80, 2.43)

– 0.19 0.25

ref 1.56 (1.33, 1.83)

– < 0.0001

ref 1.37 (1.13, 1.68)

– 0.002

p-values < 0.05 are denoted in italic OR odds ratio, CI confidence interval, ref reference, COPD chronic obstructive pulmonary disease, ASA American Society of Anesthesiologists a

Models were adjusted for gender, age, race, comorbidities, functional status, wound classification, ASA classification, admit year, and esophagectomy type; age was modeled as a linear variable and centered at 60

b

Patients with each specific comorbidity were compared to patients without the comorbidity (i.e., yes vs. no [ref])

leak and 30-day mortality. Female gender, black race, and patient’s comorbidities were associated with postoperative complications in both types of esophagectomy. In 1946, a British surgeon called Ivor Lewis described a new technique for esophageal resection, which consisted in mobilizing the stomach by laparotomy, dissecting the esophagus through a r i gh t t ho r ac oto m y, an d pe r f o r m i ng a t ho r ac i c esophagogastrostomy.8 In 1978, Orringer and Sloan9 promoted the transhiatal esophagectomy considering that a blunt dissection without thoracotomy was safe and better tolerated than the traditional combined transthoracic and abdominal operation. The debate regarding the influence of the operative approach on surgical complications is still open in the twenty-first century. A randomized controlled trial performed in the Netherlands showed that THE was associated with fewer pulmonary complications and shorter length of hospital stay, but there was no significant difference in in-hospital mortality.4 The follow-up study of the same cohort revealed that the 5-year survival for THE and TTE was 34 and 36%, respectively (p = 0.71).10 However, patients with a limited number of positive lymph nodes in the resection seemed to benefit from a TTE, showing an ongoing trend towards a better 5-year survival.10 Boshier et al.11 performed a meta-analysis including 52 studies and reported that the transthoracic group had

significantly more respiratory complications and early postoperative mortality, whereas anastomotic leak was significantly higher after THE. Khullar and colleagues12 utilized the Surveillance, Epidemiology, and End Results-Medicare linked database and found that TTE and THE had similar complication rates (46.75 vs. 50.8%), operative mortality (7.9 vs. 7.1%), and 90-day re-admission rates (30.5 vs. 32.5%). Concordantly, Connors et al.13 utilizing the National Inpatient Sample found that overall morbidity, in-hospital mortality, and length of hospital stay were similar between transthoracic and transhiatal esophagectomies. We found that TTE was associated with a higher incidence of postoperative pneumonia and bleeding requiring transfusion, while THE had a higher incidence of wound infection and sepsis. Unfortunately, details about the complexity of cases (disease variables, previous abdominal or thoracic surgery, etc.) are not provided by NSQIP, therefore introducing confounders in our study. Anastomotic leak is the most feared complication and remains the Achilles’ heel of esophageal resection. When it occurs, it severely impacts on morbidity with increases rates of re-operation, re-admission, and 30-day mortality.14,15 Previous studies have shown lower anastomotic leak rates after TTE, as compared to THE.11,16,17 In our analysis, there

J Gastrointest Surg Table 4 Adjusted odds ratio of risk factors on postoperative complications, stratified by transhiatal and Ivor Lewis esophagectomy

Gender, n (%) Male Female Age, 10-year increase Race White Black Other Comorbiditiesc Hypertension Diabetes COPD Smoking Functional status Independent Partially or fully dependent Wound classification Clean Clean/contaminated Contaminated or dirty/infected ASA classification 1 or 2 3, 4, or 5

p valueb

Transhiatal

Ivor Lewis

OR (95% CI)a

OR (95% CI)a

ref 1.42 (1.06, 1.89) 1.09 (0.96, 1.24)

ref 1.27 (1.00, 1.63) 1.05 (0.95, 1.16)

0.58 – 0.65

ref 1.29 (0.64, 2.59) 1.27 (0.56, 2.89)

ref 1.82 (1.05, 3.18) 0.91 (0.45, 1.85)

0.61 – –

1.02 (0.79, 1.32) 1.87 (1.16, 3.04) 2.11 (1.31, 3.40) 1.31 (0.90, 1.63)

1.27 (1.04, 1.55) 1.68 (1.13, 2.48) 1.70 (1.16, 2.47) 1.00 (0.80, 1.25)

0.18 0.73 0.49 0.30

ref 4.00 (1.10, 14.49)

ref 2.20 (0.87, 5.58)

0.46 –

ref 1.00 (0.54, 1.83) 1.14 (0.48, 2.75)

ref 0.57 (0.30, 1.07) 1.33 (0.62, 2.85)

0.10 – –

ref 1.43 (1.04, 1.96)

ref 1.35 (1.05, 1.75)

0.80 –

OR odds ratio, CI confidence interval, ref reference, COPD chronic obstructive pulmonary disease, ASA American Society of Anesthesiologists a

Models were adjusted for gender, age, race, comorbidities, functional status, wound classification, ASA classification, admit year, esophagectomy type, and interaction between procedure type and each potential risk factor; age was modeled as a linear variable and centered at 60

b A likelihood ratio test was used to assess whether the effect of each risk factor (e.g., gender) on complications was significantly different across surgery type; a p value < 0.05 was considered significant c

Patients with each specific comorbidity were compared to patients without the comorbidity (i.e., yes vs. no [ref])

were no significant differences in occurrence of anastomotic leak (THE 7.6% vs. TTE 9.4%, p = 0.35). These results, however, are limited by the definition of anastomotic leak as an organ/space surgical site infection. Unfortunately, there is no Banastomotic leak^ or Banastomotic dehiscence^ code using the NSQIP database. Although an organ/space surgical site infection seems to represent fairly an anastomotic leak, this definition has not been clinically validated and coding errors can occur. In addition, some patients with anastomotic leaks in the neck may have been coded as wound infections, therefore underestimating leak rates after THE. Many advocates of the transhiatal approach have historically argued that thoracic leaks are associated with higher morbidity and mortality than cervical leaks.18 Interestingly, we found that the incidence of 30-day mortality was similar between the two techniques (THE 2.3% vs. TTE 2.5%), and – significantly lower than previous reports.19 21 Advancements in surgical technique and perioperative care, dedicated anesthetic teams, high dependency units, and interventional radiology-placed drains certainly contributed to the reduction of mortality over time. Unfortunately, we were unable to identify minimally invasive and robotic cases in NSQIP based on CPT codes. It is

worth to mention, however, that minimally invasive esophagectomy (MIE) has shown to be associated with better perioperative outcomes.22,23 In addition, MIE appears to produce similar oncologic survival outcomes to those to open esophagectomy.24,25 These results support the use of minimally invasive techniques in the treatment of esophageal cancer. Identifying specific factors that contribute to postoperative complications after esophagectomy might help predicting the morbidity associated with this procedure. We identified multiple risk factors for morbidity after esophagectomy: female gender, black race, hypertension, diabetes, COPD, partially or fully dependent functional status, and ASA score ≥ 3. Functional status and ASA score, as surrogates for medical comorbidities, have previously been associated with morbidity after esophagectomy.7,26 Given that pulmonary problems are the most common complications after esophagectomy, it is intuitive that COPD leads to worse outcomes. Diabetes is a chronic debilitating disease that has also been linked to poor outcomes after esophagectomy.27,28 In fact, Dhungel et al.28 reported that diabetes was the strongest independent predictor of major complications following esophagectomy. It is unclear why women had higher incidence of complications in our analysis. The finding that black race was

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associated with morbidity is also remarkable. It is possible that other unmeasured comorbidities, observed with greater frequency in the African-American population, will explain the higher morbidity on these patients. Interestingly, Rodgers et al.29 also found that women had 1.5-fold increase in the odds of death, and black patients had double the odds of death after esophagectomy. These findings suggest that the impact of gender and race on postoperative outcomes following esophagectomy needs further investigation. The inability to determine the tumor location or histologic type may have also acted as a confounder. Mid or upper thoracic tumors are typically squamous cell carcinomas (SCC), and these patients usually have alcohol abuse and smoking history and are more prone to complications.30 In addition, although the overall burden of SCC in the USA is low, SCC is significantly more common in African-Americans than their Caucasian counterparts.31–33 To our knowledge, this is the first study that compares the impact of the risk factors on postoperative morbidity between the two types of esophagectomy. The likelihood ratio tests, which assess whether the effect of each risk factor on complications is significantly different between both procedures, showed that the impact of all risk factors on postoperative morbidity was similar across THE and TTE. Thus, our results suggest that patient’s risk factors should not determine the type of esophagectomy. This is particularly important, for example, for patients with pulmonary comorbidities such as COPD that have been historically considered to have a higher risk of morbidity after a transthoracic esophagectomy. This retrospective study has several limitations. As with all large database analyses, the study was limited by the variables collected. It is unknown why patients were selected for either THE or TTE, but it is likely multifactorial, involving disease variables, patient factors, and physician’s preference. Currently, there are no codes for minimally invasive surgery, making this variable inaccessible to this large dataset. In addition, NSQIP measures short-term outcomes and patients are followed for up to 30 days only. Thus, the incidences of complications and mortality are likely underestimated. Lastly, because participation in NSQIP is voluntary, results may not be generalizable to all hospitals performing esophageal surgery. Besides these limitations, NSQIP is a nationally validated database specifically designed for surgical outcomes with a large sample of esophageal resections from different hospital categories in the USA, which added unique advantages to our study.

dependent functional status, and an ASA score ≥ 3 were associated with postoperative complications. As the impact of the risk factors on morbidity was similar across both procedures, patient’s characteristics should not determine the type of esophagectomy. Compliance with Ethical Standards Conflict of Interest The authors declare that they have no conflict of interest.

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Conclusions Our study showed that TTE and THE had similar incidence of anastomotic leak and 30-day mortality. Female gender, black race, hypertension, diabetes, COPD, partially or fully

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