Research ArticleClinical Studies

Prospective Randomized Trial of Early Postoperative Enteral and Total Parenteral Nutrition for Treating Esophageal Cancer

YOICHI HAMAI, JUN HIHARA, MANABU EMI, YUTA IBUKI, TOMOAKI KUROKAWA, TORU YOSHIKAWA, RYOSUKE HIROHATA, MANATO OHSAWA, NAO KITASAKI and MORIHITO OKADA
Anticancer Research December 2021, 41 (12) 6237-6246; DOI: https://doi.org/10.21873/anticanres.15444

Abstract

Background/Aim: Surgical stress significantly decreases serum diamine oxidase (DAO), a marker of intestinal mucosal maturation and integrity. This study aimed to determine the effects of postoperative enteral and total parenteral nutrition (EN and TPN, respectively) in patients with esophageal cancer. Patients and Methods: This prospective randomized trial compared serum DAO activities, nutritional states, trace elements and complications between patients who underwent esophagectomy and received EN or TPN for seven days thereafter. Results: Fifty-one patients were randomized to receive EN or TPN. The rates of change in serum DAO activity from the day before surgery were 0.79, 0.89 and 0.91 on postoperative days (POD) 1, 3 and 7, respectively, in the EN group, and 0.64, 0.76 and 1.06, respectively, in the TPN group, with no significant differences. Furthermore, the rates of changes in indicators of nutritional status, namely total protein, albumin, total cholesterol, trace element concentrations and infectious and non-infectious complications did not significantly differ between the groups. Conclusion: EN and/or TPN can be administered for early nutritional management until resumption of oral intake after esophagectomy according to the postoperative status of individual patients with esophageal cancer.

Key Words:

Esophageal cancer is the ninth most common cancer and the sixth most common cause of cancer-related death globally (1). Surgery is the best option for curative treatment of esophageal cancer, and it has recently become more standardized and centralized (1). However, esophageal surgery is still highly invasive compared with other types of gastroenterological surgery (2, 3) and patients undergoing esophagectomy are unable to take oral nutrition for several days after surgery. Therefore, enteral nutrition (EN) and/or parenteral nutrition (PN) have become routine nutritional management after surgery for patients with esophageal cancer (4). The starting date at which patients without postoperative complications after esophagectomy can tolerate oral nutrition is around postoperative day (POD) 7 (5). Therefore, postoperative nutritional management before resuming oral intake is particularly important for patients with esophageal cancer.

Stating EN soon after esophagectomy reduces the length of hospital stay (6-8), postoperative weight loss (9), postoperative morbidity (7-10) and rates of life-threatening complications (11). Therefore, early EN as perioperative care enhances the recovery of patients after surgery (ERAS) for esophageal cancer according to guidelines (3, 12). However, early EN does not confer any clinical benefit upon outcomes of esophagectomy such as the length of the hospital stay, morbidity, or mortality according to some studies (13-15). Others have not found a superior clinical benefit of postoperative early EN after esophagectomy over total parenteral nutrition (TPN) (16, 17), but have indicated that perioperative nutritional support with EN or TPN should be safe (16).

Diamine oxidase (DAO) histaminase contains copper and although it is found in various tissues, it is particularly active in the intestinal mucosa (18). It functions in the oxidative deamination of polyamines, which are essential for cell proliferation. Diamine oxidase thus plays a regulatory role in rapidly proliferating tissues such as bone marrow and intestinal mucosa (18-20). It is normally found at extremely low levels in the circulation and its basal serum level positively correlates with the maturity and integrity of the small intestinal mucosa (19-21). To the best of our knowledge, a randomized study has never evaluated whether serum DAO activity differs between nutritional management by EN and TPN after esophagectomy.

Therefore, this prospective randomized trial aimed to determine whether serum DAO activities, nutritional status, trace elements and postoperative complications differ between patients who receive EN and TPN from the early postoperative period after esophagectomy.

Patients and Methods

Eligibility and exclusion criteria. Patients were considered eligible to participate in the study if they met the following inclusion criteria: age of 20-80 years; histologically proven malignant neoplasm of the esophagus; scheduled for esophagectomy via thoracotomy or a thoracoscopic approach and gastric tube reconstruction; adequate bone marrow function (leucocytes 3,000-12,000/mm3; neutrophils ≥1,500/mm3; hemoglobin ≥9.5 g/dl, platelets ≥100,000/mm3); adequate renal function (creatinine ≤1.5 mg/dl); adequate liver function [bilirubin ≤1.5 mg/dl, aspartate transaminase (AST) and alanine transaminase (ALT) ≤60 IU/l, alkaline phosphatase ≤600 IU/l] and albumin ≥2.8 g/dl. All patients included in the study provided written informed consent to participate.

Patients were considered ineligible to participate if they had a history of gastrectomy, active double cancer, comorbidities including liver, cardiac, mental, and autoimmune diseases, diabetes mellitus, contraindications to TPN and EN products, were pregnant or breast-feeding, or were deemed ineligible for this study by an investigator.

Study design. This prospective randomized study included 51 patients with esophageal cancer who were treated by esophagectomy followed by gastric tube reconstruction between November 2011 and January 2014. Figure 1 shows the study design. Eligible patients who agreed to participate were randomly assigned to EN (n=26) and TPN (n=25) groups. Caloric intake was similarly adjusted in both groups.

Figure 1.
Figure 1.

Study design. Eligible patients who agreed to participate in this study were randomly assigned in a 1:1 ratio to EN and TPN groups. RACOL®-NF was administered to the EN group from POD 1, and amounts were gradually increased to POD 7 [protocol for RACOL®-NF doses was changed (May 2013) to start from POD 2]. In the TPN group, ELNEOPA®-NF was administered from POD 1, and amounts were gradually increased to POD 7. Blood was collected before surgery, and on POD 1, 3 and 7. EN, Enteral nutrition; POD, postoperative day(s); TPN, total parenteral nutrition.

The EN group was started on 20 ml/kg/day of RACOL®-NF (Otsuka Pharmaceuticals Co., Ltd., Tokyo, Japan) on POD 1 and 2, increased to 25 ml/kg on POD 3, then to 30 ml/kg/day on POD 4-7. The amount of water was adjusted by injecting hot water into the feeding jejunostomy tube. We changed the protocol from May 2013 by administering RACOL®-NF during POD 2-7 (POD 2, 3 and 4-7: 20, 25, and 30 ml/kg/day), because slight chylothorax and chylous ascites developed when RACOL®-NF was started on POD 1.

We administered the TPN group with 20 ml/kg of ELNEOPA®-NF (Ohtsuka Pharmaceuticals Co. Ltd.) from POD 1 via a central venous catheter and increased the amount on POD 2 to 25 ml/kg, and on POD 3-7 to 30 ml/kg/day. The amount of water was adjusted by injecting normal saline into a central intravenous catheter.

We measured the concentrations of albumin, total protein, total cholesterol and trace elements as well as DAO activity in serum separated from blood collected before surgery and on POD 1, 3 and 7. The Institutional Review Board at Hiroshima University approved this study (approval number: RIN–254 and Clinical trial registration number: UMIN000004777).

Endpoints. The primary endpoint was differences in rates of changes in serum DAO activities between the EN and TPN groups based on the day before surgery through POD 1, 3 and 7, respectively. The integrity of the intestinal mucosa was evaluated by evaluating DAO.

Secondary endpoints were differences in change rates of nutritive value indexes including albumin, total protein, total cholesterol, and the trace elements iron (Fe), copper (Cu) and zinc (Zn) concentrations between the EN and TPN groups, based on levels on the day before surgery and on POD 1, 3 and 7. Differences in postoperative infectious and non-infectious complications between the EN and TPN groups were also evaluated. We defined postoperative infectious complications as anastomotic leakage, pneumonia, pyothorax, catheter infection and wound infection.

Neoadjuvant therapy and surgery. Patients with stage I tumors were surgically treated. Those with tumors of a higher stage received neoadjuvant therapy followed by surgery. The surgical procedure for all patients was transthoracic or thoracoscopic esophagectomy with at least two-field LN dissection (thoracic and abdominal fields). Esophageal cancer in the upper and middle thirds of the thoracic esophagus or LN metastasis in the superior mediastinum were treated by cervical lymphadenectomy (three-field LN dissection: cervical, thoracic and abdominal fields). The gastric tube was subsequently lifted via the posterior mediastinal, retrosternal or subcutaneous route for cervical anastomosis with the esophagus. Anesthesia was induced, then a central intravenous catheter was inserted into the subclavian veins of all patients for TPN. A feeding jejunostomy tube for EN was placed during surgery.

Measurement of serum diamine oxidase levels. Blood samples were collected early in the morning of the day before surgery and on POD 1, 3 and 7; they were placed in tubes containing heparin and were then separated by centrifugation (1,000 rpm for 15 min) for serum sampling. The activities of DAO were assessed in serum samples stored at –80°C using enzyme-linked immunosorbent assay (ELISA) kits (Immundiagnostik AG, Bensheim, Germany).

Statistical analysis. Categorical and continuous variables were analyzed using χ2 and unpaired t-tests, respectively. Values with p<0.05 were considered statistically significant. All data were statistically analyzed using SPSS software version 27 (IBM Corporation, Armonk, NY, USA).

Results

Patient characteristics. The CONSORT diagram details the flow chart (Figure 2). Fifty-one patients were randomized to receive EN (n=26) or TPN (n=25). We excluded 7 patients from the EN group during the early postoperative period, because they developed very slight chylothorax or chylous ascites from POD 1, and RACOL®-NF was immediately discontinued. Therefore, we changed the RACOL®-NF protocol to start from POD 2 in May 2013.

Figure 2.
Figure 2.

CONSORT diagram. Fifty-one patients were randomized to EN or TPN group (n=26 and 25, respectively). Seven patients of the EN group were excluded during the early postoperative period, because of very slight chylothorax or chylous ascites due to early EN administration on POD 1. One patient in TPN group was excluded, because the central venous catheter could not be inserted after induction of anesthesia. Three others were excluded within the early postoperative period due to an infected central venous catheter that was removed as it might have been associated with persistent fever. Forty patients who could tolerate TPN or EN until POD 7 were analyzed per-protocol (PP), and postoperative complications in all enrolled patients were analyzed per intention-to-treat (ITT).

One patient in the TPN group was excluded, because a central venous catheter could not be inserted after the induction of anesthesia. Three patients were excluded during the early postoperative period because of infected central venous catheters possibly associated with persistent fever, and these were removed.

Postoperative complications were evaluated in all patients in an intention-to-treat analysis. Forty patients who tolerated TPN or EN until POD 7 were analyzed per-protocol. Table I shows that the clinical characteristics of the patients did not significantly differ between the EN and TPN groups due to the random allocation.

View this table:
Table I.

Characteristics of the patients.

Serum DAO activity. Rates of change in serum DAO activity compared with levels on the day before surgery were 0.79±0.36, 0.89±0.54 and 0.91±0.44 on POD 1, 3 and 7, respectively, in the EN group; 0.64±0.33, 0.76±0.37 and 1.06±0.48, respectively, in the TPN group. These values did not significantly differ on POD 1, 3, 7 between the EN and TPN groups. Although the DAO activities decreased to POD 1 in both groups, they returned almost to preoperative levels by POD 7 (Figure 3A).

Figure 3.
Figure 3.

Rates of change in serum DAO activity. Rates of change in serum DAO activity in patients (A) managed by EN or TPN, (B) with or without neoadjuvant therapy, and (C), after surgery via open thoracotomy or thoracoscopy. Each value was analyzed using unpaired t-test.

Rates of change in serum DAO activities on POD 1, 3, 7 did not significantly differ between patients with and without neoadjuvant therapy, although DAO activities on POD 1 and 3 were lower in the patients with, than without neoadjuvant therapy (Figure 3B), and did not differ between those who underwent open thoracotomy and thoracoscopy (Figure 3C).

Changes in nutritive indexes. The rates of change in total protein were 0.68±0.07, 0.74±0.06 and 0.85±0.07 on POD 1, 3 and 7, respectively, in the EN group, and 0.67±0.05, 0.74±0.07 and 0.81±0.08 respectively, in the TPN group (Figure 4A). The rates of change in albumin were 0.70±0.10, 0.66±0.08 and 0.72±0.02 on POD 1, 3 and 7, respectively, in the EN group, and 0.68±0.08, 0.64±0.08 and 0.68±0.07, respectively, in the TPN group (Figure 4B). The rates of changes in total cholesterol were 0.57±0.13, 0.68±0.11 and 0.78±0.09 on POD 1, 3 and 7, respectively, in the EN group, and 0.61±0.10, 0.68±0.13 and 0.67±0.14 on POD 1, 3 and 7, respectively, in the TPN group (Figure 4C). Rates of changes in the nutritive indexes of total protein, albumin, and total cholesterol did not significantly differ between the EN and TPN groups on POD 1, 3, 7 (Figure 4A-C).

Figure 4.
Figure 4.

Rates of change in nutritive value indexes. Rates of change in (A) total protein, (B) albumin, and (C) total cholesterol in patients managed by EN or TPN. Each value was analyzed using unpaired t-test.

Changes in trace elements. The rates at which Fe changed were 0.19±0.14, 0.50±0.37 and 0.47±0.29 on POD 1, 3 and 7, respectively, in the EN group, and 0.16±0.13, 0.42±0.28 and 0.37±0.27 on POD 1, 3 and 7, respectively, in the TPN group (Figure 5A). The rates of change in Cu, were 0.61±0.12, 0.79±0.27 and 1.01±0.22 on POD 1, 3 and 7, respectively in the EN group, and 0.57±0.22, 0.88±0.14 and 0.95±0.32, respectively, in the TPN group (Figure 5B). The rates of changes in total cholesterol were 0.40±0.11, 0.56±0.16 and 0.93±0.15 on POD 1, 3 and 7, respectively, in the EN group, and 0.40±0.09, 0.61±0.15 and 0.89±0.15 on POD 1, 3 and 7, respectively, in the TPN group (Figure 5C). The rates at which concentrations of Fe, Cu and Zn concentrations changed did not significantly differ between the EN and TPN groups on POD 1, 3, 7 (Figure 5A-C).

Figure 5.
Figure 5.

Rates of change in trace elements. Rates of change in (A) Fe, (B) Cu, and (C) Zn in patients managed by EN or TPN. Each value was analyzed using unpaired t-test. Cu, Copper; Fe, iron; Zn, zinc.

Postoperative complications. The differences of postoperative infectious and non-infectious complications between EN and TPN groups were evaluated in all enrolled all patients (n=51) as intent-to-treat analysis (Table II). Infectious complications developed in 10 (38.5%) and 14 (56.0%) patients in the EN and TPN groups, respectively (p=0.21). Non-infectious complications developed in 11 (44.0%) and 11 (42.3%) patients in the EN and TPN groups, respectively (p=0.90). These complications did not significantly differ between the two groups, although slightly more infectious complications developed in patients given TPN than EN.

View this table:
Table II.

Postoperative complications.

Discussion

Patients with surgically-treated esophageal cancer cannot intake oral nutrition for several postoperative days. Therefore, EN and/or PN are essentially needed for routine nutritional management after surgery. The introduction of early EN for perioperative care is beneficial in patients undergoing surgery for esophageal cancer according to ERAS guidelines (3, 12), but differences in serum DAO activities between nutritional managements by EN and TPN after esophagectomy have never been evaluated in a randomized study. Therefore, the present, prospective randomized trial compared DAO activities, nutritional indicators, trace elements and postoperative complications between patients with esophageal cancer who received EN and TPN during the early postoperative period until oral intake was resumed. This study found no significant differences in the above factors between the EN and TPN groups.

Diamine oxidase is normally abundant in the intestinal mucosa, kidneys, and placenta of humans and other mammals, and the intestinal mucosa is the prime source of serum DAO (19-22). Serum levels of this enzyme activity closely reflect the maturity and integrity of the intestinal mucosa; serum enzyme activity increases as the rat intestinal mucosa differentiates and contains increasing amounts of enzyme and decreases as the adult rat mucosa is progressively damaged (19). The small intestinal mucosa contains the most DAO activity in humans. Serum DAO activity might be a good marker of intestinal mucosal maturation and integrity (19-22). Human DAO can be reliably and accurately quantified in various biological fluids using ELISAs (18).

Surgical stress influences intestinal integrity after esophagectomy for esophageal cancer, and serum DAO activity was obviously decreased in such patients (23). A comparison of DAO activity between patients with gastric cancer who received postoperative nutrition with EN and TPN found decreased DAO activity in both groups after total gastrectomy and recovery within 1 week in the EN, but not in the TPN group (24). Furthermore, in another study, elderly patients with esophageal or cardiac cancers were divided into EN or PN groups based on nutrition support modes. The early postoperative EN could more effectively improve nutritional status and postoperative intestinal permeability assessed as serum DAO activity and protect the intestinal mucosal barrier (25). The present study did not find significant differences in serum DAO activities between the EN and TPN groups. Although the DAO activities decreased to POD 1 levels in both groups, they returned almost to preoperative levels. Although surgical stress temporarily influences postoperative intestinal integrity and permeability, the subsequent amount of change of DAO activity might also be influenced depending on the status of each patient and types of gastrointestinal tract diseases, operative procedures, as well as enteral and parenteral nutrients.

We evaluated whether rates at which the nutritive indexes, namely albumin, total protein, total cholesterol, and trace element concentrations changed between the EN and TPN groups and found no significant differences in any of them. RACOL®-NF and ELNEOPA®-NF both include enough calories, trace elements and multivitamins that postoperative patients need. Although all nutritive indexes were decreased to POD 1, they increased to about 80% of preoperative levels in both groups.

Although Cu and Zn decreased on POD 1, they recovered almost to preoperative levels on POD 7 in both groups. On the other hand, Fe increased to only ~40% of preoperative levels by POD 7 in both groups. A previous study of sequential perioperative changes in the nutritional and immune status of patients after esophageal cancer surgery also found that the deterioration in serum iron was most severe by POD 3 (26). Other than iron-related parameters, all measured nutritional parameters returned to preoperative levels within 2-3 weeks after surgery. However, serum levels of iron returned to normal after more than 1 month. Therefore, postoperative iron and protein supplementation might be needed for 1-3 months to prevent an iron deficiency.

Early EN initiated after esophagectomy reduced the length of the hospital stay (6-8), postoperative weight loss (9), postoperative morbidity (8-10), and the rate of life-threatening complications (11). On the other hand, early EN did not generate any evidence or confer any clinical benefits upon the length of hospital stays, morbidity, and mortality after esophagectomy (13-15). Although postoperative complications also did not significantly differ between the groups, infectious complications, especially catheter infection, developed slightly more often in the TPN group. Therefore, catheter infection should be carefully monitored in patients who are administered with TPN via a central venous catheter. Furthermore, the very slight chylothorax and chylous ascites that developed when EN was administered from POD 1 indicated that EN administered from POD 1 might confer the risk of developing these states. Therefore, EN containing fat might be appropriate to administer from day 2 after esophagectomy.

Although we compared patients who received EN and TPN until POD 7, estimation over a longer period should be applied for postoperative nutritional management in patients with esophageal cancer. Enteral nutrition is needed for patients who are forced to fast over the long term due to postoperative anastomotic leakage (27), and to improve nutritional status during long postoperative periods even after discharge (28). Therefore, EN is essential for postoperative management of esophageal cancer. On the other hand, TPN might be also needed to conservatively manage patients who develop postoperative chylothorax (29). Thus, TPN and EN should be appropriately administered for short- and long-term postoperative nutritional management according to the status of individual patients with esophageal cancer because each might confer specific advantages.

In conclusion, the change of serum DAO activity, nutritional state, trace elements and postoperative complications were similar in the EN and TPN groups within 7 days after esophagectomy. Thus, either TPN and/or EN can be administered for the early postoperative nutritional management of individual patients with esophageal cancer according to their status.

Footnotes

  • Authors’ Contributions

    YH drafted the article. ME, YI, TK, TY, RH, MO and NK contributed to patient care. YH performed the literature search. JH and MO participated in the critical revision of the article. All Authors read and approved the final article.

  • Conflicts of Interest

    The Authors have no commercial support or conflicts of interest to disclose in relation to this study.

  • Received July 10, 2021.
  • Revision received August 23, 2021.
  • Accepted August 30, 2021.

References

  1. ↵
    1. Smyth EC,
    2. Lagergren J,
    3. Fitzgerald RC,
    4. Lordick F,
    5. Shah MA,
    6. Lagergren P and
    7. Cunningham D
    : Oesophageal cancer. Nat Rev Dis Primers 3: 17048, 2017. PMID: 28748917. DOI: 10.1038/nrdp.2017.48
    OpenUrlCrossRefPubMed
  2. ↵
    1. Chevallay M,
    2. Jung M,
    3. Chon SH,
    4. Takeda FR,
    5. Akiyama J and
    6. Mönig S
    : Esophageal cancer surgery: review of complications and their management. Ann N Y Acad Sci 1482(1): 146–162, 2020. PMID: 32935342. DOI: 10.1111/nyas.14492
    OpenUrlCrossRefPubMed
  3. ↵
    1. Low DE,
    2. Allum W,
    3. De Manzoni G,
    4. Ferri L,
    5. Immanuel A,
    6. Kuppusamy M,
    7. Law S,
    8. Lindblad M,
    9. Maynard N,
    10. Neal J,
    11. Pramesh CS,
    12. Scott M,
    13. Mark Smithers B,
    14. Addor V and
    15. Ljungqvist O
    : Guidelines for perioperative care in esophagectomy: Enhanced recovery after surgery (ERAS®) society recommendations. World J Surg 43(2): 299–330, 2019. PMID: 30276441. DOI: 10.1007/s00268-018-4786-4
    OpenUrlCrossRefPubMed
  4. ↵
    1. Zheng R,
    2. Devin CL,
    3. Pucci MJ,
    4. Berger AC,
    5. Rosato EL and
    6. Palazzo F
    : Optimal timing and route of nutritional support after esophagectomy: A review of the literature. World J Gastroenterol 25(31): 4427–4436, 2019. PMID: 31496622. DOI: 10.3748/wjg.v25.i31.4427
    OpenUrlCrossRefPubMed
  5. ↵
    1. Li X,
    2. Yan S,
    3. Ma Y,
    4. Li S,
    5. Wang Y,
    6. Wang X,
    7. Wang Y,
    8. Wang J,
    9. Lv C,
    10. Yang Y and
    11. Wu N
    : Impact of early oral feeding on anastomotic leakage rate after esophagectomy: a systematic review and meta-analysis. World J Surg 44(8): 2709–2718, 2020. PMID: 32227277. DOI: 10.1007/s00268-020-05489-z
    OpenUrlCrossRefPubMed
  6. ↵
    1. Gabor S,
    2. Renner H,
    3. Matzi V,
    4. Ratzenhofer B,
    5. Lindenmann J,
    6. Sankin O,
    7. Pinter H,
    8. Maier A,
    9. Smolle J and
    10. Smolle-Jüttner FM
    : Early enteral feeding compared with parenteral nutrition after oesophageal or oesophagogastric resection and reconstruction. Br J Nutr 93(4): 509–513, 2005. PMID: 15946413. DOI: 10.1079/bjn20041383
    OpenUrlCrossRefPubMed
  7. ↵
    1. Han H,
    2. Pan M,
    3. Tao Y,
    4. Liu R,
    5. Huang Z,
    6. Piccolo K,
    7. Zhong C and
    8. Liu R
    : Early enteral nutrition is associated with faster post-esophagectomy recovery in chinese esophageal cancer patients: a retrospective cohort study. Nutr Cancer 70(2): 221–228, 2018. PMID: 29313724. DOI: 10.1080/01635581.2018.1412477
    OpenUrlCrossRefPubMed
  8. ↵
    1. Wang G,
    2. Chen H,
    3. Liu J,
    4. Ma Y and
    5. Jia H
    : A comparison of postoperative early enteral nutrition with delayed enteral nutrition in patients with esophageal cancer. Nutrients 7(6): 4308–4317, 2015. PMID: 26043031. DOI: 10.3390/nu7064308
    OpenUrlCrossRefPubMed
  9. ↵
    1. Takesue T,
    2. Takeuchi H,
    3. Ogura M,
    4. Fukuda K,
    5. Nakamura R,
    6. Takahashi T,
    7. Wada N,
    8. Kawakubo H and
    9. Kitagawa Y
    : A prospective randomized trial of enteral nutrition after thoracoscopic esophagectomy for esophageal cancer. Ann Surg Oncol 22 Suppl 3: S802–S809, 2015. PMID: 26219242. DOI: 10.1245/s10434-015-4767-x
    OpenUrlCrossRefPubMed
  10. ↵
    1. Yu HM,
    2. Tang CW,
    3. Feng WM,
    4. Chen QQ,
    5. Xu YQ and
    6. Bao Y
    : Early enteral nutrition versus parenteral nutrition after resection of esophageal cancer: a retrospective analysis. Indian J Surg 79(1): 13–18, 2017. PMID: 28331260. DOI: 10.1007/s12262-015-1420-7
    OpenUrlCrossRefPubMed
  11. ↵
    1. Fujita T,
    2. Daiko H and
    3. Nishimura M
    : Early enteral nutrition reduces the rate of life-threatening complications after thoracic esophagectomy in patients with esophageal cancer. Eur Surg Res 48(2): 79–84, 2012. PMID: 22377820. DOI: 10.1159/000336574
    OpenUrlCrossRefPubMed
  12. ↵
    1. Ashok A,
    2. Niyogi D,
    3. Ranganathan P,
    4. Tandon S,
    5. Bhaskar M,
    6. Karimundackal G,
    7. Jiwnani S,
    8. Shetmahajan M and
    9. Pramesh CS
    : The enhanced recovery after surgery (ERAS) protocol to promote recovery following esophageal cancer resection. Surg Today 50(4): 323–334, 2020. PMID: 32048046. DOI: 10.1007/s00595-020-01956-1
    OpenUrlCrossRefPubMed
  13. ↵
    1. Klevebro F,
    2. Johar A,
    3. Lagergren J and
    4. Lagergren P
    : Outcomes of nutritional jejunostomy in the curative treatment of esophageal cancer. Dis Esophagus 32(7): doy113, 2019. PMID: 30496419. DOI: 10.1093/dote/doy113
    OpenUrlCrossRefPubMed
    1. Wheble GA,
    2. Benson RA and
    3. Khan OA
    : Is routine postoperative enteral feeding after oesophagectomy worthwhile? Interact Cardiovasc Thorac Surg 15(4): 709–712, 2012. PMID: 22753430. DOI: 10.1093/icvts/ivs221
    OpenUrlCrossRefPubMed
  15. ↵
    1. Aiko S,
    2. Yoshizumi Y,
    3. Matsuyama T,
    4. Sugiura Y and
    5. Maehara T
    : Influences of thoracic duct blockage on early enteral nutrition for patients who underwent esophageal cancer surgery. Jpn J Thorac Cardiovasc Surg 51(7): 263–271, 2003. PMID: 12892455. DOI: 10.1007/BF02719376
    OpenUrlCrossRefPubMed
  16. ↵
    1. Seike J,
    2. Tangoku A,
    3. Yuasa Y,
    4. Okitsu H,
    5. Kawakami Y and
    6. Sumitomo M
    : The effect of nutritional support on the immune function in the acute postoperative period after esophageal cancer surgery: total parenteral nutrition versus enteral nutrition. J Med Invest 58(1-2): 75–80, 2011. PMID: 21372490. DOI: 10.2152/jmi.58.75
    OpenUrlCrossRefPubMed
  17. ↵
    1. Page RD,
    2. Oo AY,
    3. Russell GN and
    4. Pennefather SH
    : Intravenous hydration versus naso-jejunal enteral feeding after esophagectomy: a randomised study. Eur J Cardiothorac Surg 22(5): 666–672, 2002. PMID: 12414028. DOI: 10.1016/s1010-7940(02)00489-x
    OpenUrlCrossRefPubMed
  18. ↵
    1. Boehm T,
    2. Pils S,
    3. Gludovacz E,
    4. Szoelloesi H,
    5. Petroczi K,
    6. Majdic O,
    7. Quaroni A,
    8. Borth N,
    9. Valent P and
    10. Jilma B
    : Quantification of human diamine oxidase. Clin Biochem 50(7-8): 444–451, 2017. PMID: 28041932. DOI: 10.1016/j.clinbiochem.2016.12.011
    OpenUrlCrossRefPubMed
  19. ↵
    1. Wolvekamp MC and
    2. de Bruin RW
    : Diamine oxidase: an overview of historical, biochemical and functional aspects. Dig Dis 12(1): 2–14, 1994. PMID: 8200121. DOI: 10.1159/000171432
    OpenUrlCrossRefPubMed
  20. ↵
    1. Luk GD,
    2. Bayless TM and
    3. Baylin SB
    : Diamine oxidase (histaminase). A circulating marker for rat intestinal mucosal maturation and integrity. J Clin Invest 66(1): 66–70, 1980. PMID: 6772669. DOI: 10.1172/JCI109836
    OpenUrlCrossRefPubMed
  21. ↵
    1. Fukudome I,
    2. Kobayashi M,
    3. Dabanaka K,
    4. Maeda H,
    5. Okamoto K,
    6. Okabayashi T,
    7. Baba R,
    8. Kumagai N,
    9. Oba K,
    10. Fujita M and
    11. Hanazaki K
    : Diamine oxidase as a marker of intestinal mucosal injury and the effect of soluble dietary fiber on gastrointestinal tract toxicity after intravenous 5-fluorouracil treatment in rats. Med Mol Morphol 47(2): 100–107, 2014. PMID: 24005798. DOI: 10.1007/s00795-013-0055-7
    OpenUrlCrossRefPubMed
  22. ↵
    1. D’Agostino L,
    2. Ciacci C,
    3. Daniele B,
    4. Barone MV,
    5. Sollazzo R and
    6. Mazzacca G
    : Plasma diamine oxidase (DAO) and heparin. Dig Dis Sci 29(11): 1070–1071, 1984. PMID: 6435979. DOI: 10.1007/BF01311264
    OpenUrlCrossRefPubMed
  23. ↵
    1. Sato N,
    2. Oyamatsu M,
    3. Koyama Y,
    4. Tamiya Y and
    5. Hatakeyama K
    : Differences in gut integrity following abdominal surgery according to the magnitude of the surgical stress. Int Surg 85(1): 30–33, 2000. PMID: 10817428.
    OpenUrlPubMed
  24. ↵
    1. Kamei H,
    2. Hachisuka T,
    3. Nakao M and
    4. Takagi K
    : Quick recovery of serum diamine oxidase activity in patients undergoing total gastrectomy by oral enteral nutrition. Am J Surg 189(1): 38–43, 2005. PMID: 15701488. DOI: 10.1016/j.amjsurg.2004.03.015
    OpenUrlCrossRefPubMed
  25. ↵
    1. Yu G,
    2. Chen G,
    3. Huang B,
    4. Shao W and
    5. Zeng G
    : Effect of early enteral nutrition on postoperative nutritional status and immune function in elderly patients with esophageal cancer or cardiac cancer. Chin J Cancer Res 25(3): 299–305, 2013. PMID: 23825906. DOI: 10.3978/j.issn.1000-9604.2013.06.01
    OpenUrlCrossRefPubMed
  26. ↵
    1. Wang LS,
    2. Lin HY,
    3. Chang CJ,
    4. Fahn HJ,
    5. Huang MH and
    6. Lin CF
    : Effects of en bloc esophagectomy on nutritional and immune status in patients with esophageal carcinoma. J Surg Oncol 67(2): 90–98, 1998. PMID: 9486779. DOI: 10.1002/(sici)1096-9098(199802)67:2<90::aid-jso4>3.0.co;2-g
    OpenUrlCrossRefPubMed
  27. ↵
    1. Fabbi M,
    2. Hagens ERC,
    3. van Berge Henegouwen MI and
    4. Gisbertz SS
    : Anastomotic leakage after esophagectomy for esophageal cancer: definitions, diagnostics, and treatment. Dis Esophagus 34(1): doaa039, 2021. PMID: 32476017. DOI: 10.1093/dote/doaa039
    OpenUrlCrossRefPubMed
  28. ↵
    1. Wu Z,
    2. Wu M,
    3. Wang Q,
    4. Zhan T,
    5. Wang L,
    6. Pan S and
    7. Chen G
    : Home enteral nutrition after minimally invasive esophagectomy can improve quality of life and reduce the risk of malnutrition. Asia Pac J Clin Nutr 27(1): 129–136, 2018. PMID: 29222890. DOI: 10.6133/apjcn.032017.22
    OpenUrlCrossRefPubMed
  29. ↵
    1. Brinkmann S,
    2. Schroeder W,
    3. Junggeburth K,
    4. Gutschow CA,
    5. Bludau M,
    6. Hoelscher AH and
    7. Leers JM
    : Incidence and management of chylothorax after Ivor Lewis esophagectomy for cancer of the esophagus. J Thorac Cardiovasc Surg 151(5): 1398–1404, 2016. PMID: 26936011. DOI: 10.1016/j.jtcvs.2016.01.030
    OpenUrlCrossRefPubMed
Back to top

In this issue

Print
Download PDF
Article Alerts
Email Article
Citation Tools
Reprints and Permissions
Prospective Randomized Trial of Early Postoperative Enteral and Total Parenteral Nutrition for Treating Esophageal Cancer
YOICHI HAMAI, JUN HIHARA, MANABU EMI, YUTA IBUKI, TOMOAKI KUROKAWA, TORU YOSHIKAWA, RYOSUKE HIROHATA, MANATO OHSAWA, NAO KITASAKI, MORIHITO OKADA
Anticancer Research Dec 2021, 41 (12) 6237-6246; DOI: 10.21873/anticanres.15444
Twitter logo Facebook logo Mendeley logo

Jump to section

Keywords