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ONC: Nutrition Status and Outcomes in Adult Oncology Patients (2013)


Antoun S, Rey A, Béal J, Montange F, Pressoir M, Vasson MP, Dupoiron D, Gourdiat-Borye A, Guillaume A, Maget B, Nitenberg G, Raynard B, Bachmann P. Nutritional risk factors in planned oncologic surgery: What clinical and biological parameters should be routinely used? World J Surg. 2009 Aug; 33(8): 1,633-1,640.

Study Design:
Prospective Cohort Study
B - Click here for explanation of classification scheme.
Quality Rating:
Neutral NEUTRAL: See Quality Criteria Checklist below.
Research Purpose:

To determine the most relevant nutritional parameters not only in terms of an association with surgical morbidity but also of practical routine feasibility for cancer patients undergoing planned major surgery of any type.

Inclusion Criteria:

Adult patients (no age identified) undergoing major cancer surgery, including:

  • Complex surgery for head and neck cancer (resection of oropharyngolaryngeal airways with or without reconstruction)
  • Esophageal and gastrointestinal surgery (resection of a segment of the digestive tract, esophagectomy, partial or total gastrectomy, colonic and rectal resections, reconstruction of bladder using the Bricker technique)
  • Pancreatic surgery
  • Extensive retroperitoneal surgery
  • Invasive surgery for gynecological cancers
  • Surgical resection of peritoneal carcinosis.
Exclusion Criteria:

Adult cancer patients:

  • Colioscopic procedure
  • Intraperitoneal hyperthermic chemotherapy for peritoneal carcinosis
  • Partial hepatectomy
  • Isolated bile duct surgery
  • Isolated urinary tract surgery
  • Minor head and neck surgery (cervical dissection, lymph node biopsy, thyroid surgery)
  • Surgery to other sites of malignancy: Sarcomas (breast, lung, limbs)
  • Emergency surgery.
Description of Study Protocol:


Patients in nine of 20 French cancer centers were recruited during a three-month period at their initial anesthesia consultation.


Prospective, observational, multi-center study.


Subjects underwent major cancer surgery.

Statistical Analysis

  • Values collected on the day before surgery were selected in all cases for correlation with surgical morbidity rates. Percentages were compared using the chi-squared test. Mean values were compared using the T-test.
  • A test was considered statistically significant if P<0.05.
  • Univariate analysis calculations were carried out using the Epi-info software. Receiver operating characteristic curves were used to investigate variations in the specificity and sensitivity of the different values.
  • Logistic regression was used for multivariate analysis of the different variables associated with major complications.
Data Collection Summary:

Timing of Measurements

  • Pre-anesthesia consultation: Clinical parameters and biological data
  • Weight: Routine (unspecified interval)
  • Data collected a day before surgery if:
    • Some data were not collected at inclusion
    • The time between the anesthesia consultation and the surgical procedure was more than 15 days
    • Initial malnutrition resulted in the introduction of pre-operative artificial nutrition
  • Prospectively collected data:
    • Score of the American Society of Anesthesiology
    • Number of red blood cell units transfused during surgery (transfusions given in the recovery room were taken into account)
    • Duration of the surgical procedure
  • Post-surgery:
    • Events that occurred during the first 30 days to assess morbidity and mortality
    • Average duration of stay was calculated from the overall hospital stay of all patients
    • For patients admitted to the intensive care unit of another hospital because of organ failure, the time spent in the ICU and in the follow-up surgical treatment 
    • If during this 30-day post-operative period the patient was re-admitted due to an undesirable effect, this effect was taken into account and considered a post-surgical complication.
  • The patient left the study either on being discharged from the hospital or after 30 days of follow-up
  • Excluded data:
    • Complications or other undesirable effects that occurred after the patient had been discharged
    • Complications that occurred after the 30-day post-operative period.

Dependent Variables

Clinical Outcomes

  • Minor infectious complications (mIC)
  • Major infectious complications (MIC)
  • Minor non-infectious complications (mNIC)
  • Major non-infectious complications (MNIC)
  • All complications (AC)
  • Hospital length of stay (LOS)
  • Mortality.

Nutritional Parameters

  • Weight Loss (WL) 10% or more
  • WL 15% or more
  • BMI less than 18.5
  • Patient-generated subjective global assessment (PG-SGA) level
  • Albumin less than 30g per L
  • Transthyretin less than 110g per L
  • Nutritional Risk Index (NRI).

Independent Variables

  • Major surgical procedure
  • Chemotherapy
  • Radiotherapy
  • Pre-surgical parenteral or enteral nutrition
  • Oral immune-enhancing nutrition
  • Oral nutrition supplements.

Control Variables

No controls, self serves as control for presence of morbidity or not based on pre-treatment data parameters.

Description of Actual Data Sample:

Initial N

275 (167 women, 108 men).


  • Average age: 57 years
  • Median: 58 years
  • Range: 17 to 86 years.

Tumor Sites

  • Head and neck cancer (N=68)
    • Oral Cavity (N=26)
    • Larynx (N=19)
    • Oropharynx (N=10)
    • Hypopharynx (N=8)
    • Nasopharynx (N=1)
    • Double site (N=4)
  • Gastrointestinal cancer (N=68)
    • Colon (N=20)
    • Rectum (N=24)
    • Stomach (N=8)
    • Esophagus (N=4)
    • Small intestine (N=4)
    • Double site (N=2)
    • Other (N=6)
  • Gynecological cancer (N=111)
    • Uterus (N=28)
    • Endometrium (N=21)
    • Ovary (N=62)
  • Other origins (N=28)
    • Retroperitoneum (N=3)
    • Pelvis (N=6)
    • Testis metastases (N=8)
    • Urinary tract (N=1)
    • Other site (N=10).


  • Adenocarcinoma (N=125)
  • Epidermoid carcinoma (N=91)
  • Rare benign tumors (N=18)
  • Other malignant varied histology (N=41).

Risk Associated Malnutrition and Nutritional Management

  Moderate Risk (5%<WL<10% and 83.5<NRI<97.5) High Risk (WL>10% and NRI<97.5) No Risk (According to WL and NRI)
No management 49 38  
Parenteral nutrition 1 1  
Enteral nutrition 2 2 3
Oral immune-enhancing nutrition 14 7 4
Nutritional supplement (without immune-enhancing nutrition) 3 3 1
Non-specified 2 2  
  • Recommendation for nutritional support were incorrectly followed at the centers that took part in the study, with only 35% nutritional management (22 of 71) when the risk was moderate and 28% (15 of 53) for high-risk patients.

Distribution of the 275 Patients Depending on Values of Various Nutritional Parameters

  Overweight or Weight Gain No Evidence of Malnutrition Moderate Malnutrition Severe Malnutrition

Variation in weight

N=270, 98%

Weight gain


Stable weight






BMI (kg/m2)

N=273, 99%










N=196, 71%









N=212, 77%


Alb≤35g per L


Alb ≤ 30g per L



N=212, 77%

*N=243, 88%












N=169, 61%


≤150mg per L


≤110mg per L


 WL and BMI based Nutritional Status and the Type of Surgery

  Head and Neck (%) Esophagus, Stomach, Small Intestine (%) Colon, Rectum (%) Pancrease, Peritoneum (%) Gynecologic (%)
Frequency of WL>10% 24 27 19 20 18
BMI≤18.5 18 8 5 20 7
18.5<BMI<25 49 52 50 30 52
25≤BMI<30 23 36 27 40 27
BMI≥30 10 4 18 10 14



Summary of Results:

Key Findings

Morbidity and Mortality of Study Population (%)

mIC MIC mNIC MNIC Major Complications (MNIC and MIC) Any Complication Deaths
28.4% 12.7% 24.7% 22.2% 28.4% 52% 1
  • More than one in four patients (28.4%) had a major complication
  • More than one in two patients (52%) had a complication
  • Mortality was not significant with less than 0.01% of population.

Statistical Significance (P) of Correlations Between Nutritional Parameters and Morbidity

  MIC MNIC MIC +MNIC AC Duration of Hospital Stay Sample Size
WL 10% or more 0.02 NS NS NS <0.05 N=55
WL 15% or more <0.001 NS 0.03 NS <0.001 N=28
BMI less than 18.5 NS 0.04 NS 0.04 NS N=27
PG-SGA level 0.04 NS 0.03 0.006 <0.001 N=67
Albumin less than 30g per L <0.001 <0.005 <0.001 0.04 <0.001 N=17
Transthyretin less than 110g per L NS NS NS NS NS N=12
NRI <0.001 NS <0.005 0.05 =0.001 N=87 (N=106)

*NS not significant, AC all complications. Values given in italics include the data collected during the anesthesia consultation immediately before surgery.

Other Findings

  • Median duration of the surgical procedure was 255 minutes and 26% of patients required a blood transfusion
  • Procedures lasting longer than four hours (P<0.001) and amount of red blood cell units transfused (P=0.03) was found statistically linked to major complications when tested in multi-variate analysis
  • No correlation with the ASA score (American Society of Anesthesiology).
Author Conclusion:

The prediction of not only major infectious but also major non-infectious complications seemed less accurate with anthropometric features and clinical score than with albumin levels less than 30g per L. With albumin level being the only variable found statistically linked to major complications in the multi-variable analysis, collecting these data before surgery is mandatory. Recognition of severe malnutrition was most often not associated with an implementation of nutrition care or participial nutrition when required.

Funding Source:
University/Hospital: Institute Gustave Roussy, Inter CLAN Centers Research Lutte Contre Concer
Reviewer Comments:
  • The correlation between albumin, duration of operation for four hours or more, and units of blood transfused to all forms of morbidity validates that importance of hemodynamic stability for post-operative outcomes
  • The aim of the study was for evaluation of nutritional parameters, not hemodynamic stability. The multivariate analysis does not study the significance of nutritional management parameters when risk is identified by standardized scores.
  • The study indicates that recommendations for nutritional support were incorrectly followed at the centers due to 35% nutritional management of moderate-risk and 28% for high-risk patients. These statistics excluded PG-SGA scores identified at-risk patients for reasons unknown but most likely due to the sample size of N=67 (34.2%).
  • Although anthropometrics were not of significance, data analysis limits feasibility of considering PG-SGA and NRI scores due to limited data collection and lack of analysis from the author. This leaves a discussion open for nutritional management pre-operatively for reducing hemodynamic instability.
  • The author fails to discuss the correlation between the standardized scores and albumin levels to identify whether or not the scores validated albumin levels as a risk stratification measure
  • Albumin less than 30g per L sample size was the smallest at N=17 allowing for greater correlation between morbidity. This could be a limitation of the study and make the data statistically significant but clinically insignificant.
  • No co-morbidities of population were indicated or explained in inclusion and exclusion criteria
  • Medication or treatment interventions and their potential to cause infectious complications not considered such as central or peripheral venous lines and respiratory treatments if necessary.
Quality Criteria Checklist: Primary Research
Relevance Questions
  1. Would implementing the studied intervention or procedure (if found successful) result in improved outcomes for the patients/clients/population group? (Not Applicable for some epidemiological studies) Yes
  2. Did the authors study an outcome (dependent variable) or topic that the patients/clients/population group would care about? Yes
  3. Is the focus of the intervention or procedure (independent variable) or topic of study a common issue of concern to dieteticspractice? Yes
  4. Is the intervention or procedure feasible? (NA for some epidemiological studies) Yes
Validity Questions
1. Was the research question clearly stated? Yes
  1.1. Was (were) the specific intervention(s) or procedure(s) [independent variable(s)] identified? Yes
  1.2. Was (were) the outcome(s) [dependent variable(s)] clearly indicated? Yes
  1.3. Were the target population and setting specified? Yes
2. Was the selection of study subjects/patients free from bias? Yes
  2.1. Were inclusion/exclusion criteria specified (e.g., risk, point in disease progression, diagnostic or prognosis criteria), and with sufficient detail and without omitting criteria critical to the study? Yes
  2.2. Were criteria applied equally to all study groups? Yes
  2.3. Were health, demographics, and other characteristics of subjects described? Yes
  2.4. Were the subjects/patients a representative sample of the relevant population? Yes
3. Were study groups comparable? Yes
  3.1. Was the method of assigning subjects/patients to groups described and unbiased? (Method of randomization identified if RCT) Yes
  3.2. Were distribution of disease status, prognostic factors, and other factors (e.g., demographics) similar across study groups at baseline? No
  3.3. Were concurrent controls or comparisons used? (Concurrent preferred over historical control or comparison groups.) Yes
  3.4. If cohort study or cross-sectional study, were groups comparable on important confounding factors and/or were preexisting differences accounted for by using appropriate adjustments in statistical analysis? Yes
  3.5. If case control study, were potential confounding factors comparable for cases and controls? (If case series or trial with subjects serving as own control, this criterion is not applicable.) N/A
  3.6. If diagnostic test, was there an independent blind comparison with an appropriate reference standard (e.g., "gold standard")? N/A
4. Was method of handling withdrawals described? No
  4.1. Were follow-up methods described and the same for all groups? No
  4.2. Was the number, characteristics of withdrawals (i.e., dropouts, lost to follow up, attrition rate) and/or response rate (cross-sectional studies) described for each group? (Follow up goal for a strong study is 80%.) No
  4.3. Were all enrolled subjects/patients (in the original sample) accounted for? No
  4.4. Were reasons for withdrawals similar across groups? No
  4.5. If diagnostic test, was decision to perform reference test not dependent on results of test under study? N/A
5. Was blinding used to prevent introduction of bias? No
  5.1. In intervention study, were subjects, clinicians/practitioners, and investigators blinded to treatment group, as appropriate? No
  5.2. Were data collectors blinded for outcomes assessment? (If outcome is measured using an objective test, such as a lab value, this criterion is assumed to be met.) No
  5.3. In cohort study or cross-sectional study, were measurements of outcomes and risk factors blinded? No
  5.4. In case control study, was case definition explicit and case ascertainment not influenced by exposure status? N/A
  5.5. In diagnostic study, were test results blinded to patient history and other test results? N/A
6. Were intervention/therapeutic regimens/exposure factor or procedure and any comparison(s) described in detail? Were interveningfactors described? Yes
  6.1. In RCT or other intervention trial, were protocols described for all regimens studied? N/A
  6.2. In observational study, were interventions, study settings, and clinicians/provider described? Yes
  6.3. Was the intensity and duration of the intervention or exposure factor sufficient to produce a meaningful effect? Yes
  6.4. Was the amount of exposure and, if relevant, subject/patient compliance measured? N/A
  6.5. Were co-interventions (e.g., ancillary treatments, other therapies) described? Yes
  6.6. Were extra or unplanned treatments described? Yes
  6.7. Was the information for 6.4, 6.5, and 6.6 assessed the same way for all groups? Yes
  6.8. In diagnostic study, were details of test administration and replication sufficient? N/A
7. Were outcomes clearly defined and the measurements valid and reliable? Yes
  7.1. Were primary and secondary endpoints described and relevant to the question? Yes
  7.2. Were nutrition measures appropriate to question and outcomes of concern? Yes
  7.3. Was the period of follow-up long enough for important outcome(s) to occur? Yes
  7.4. Were the observations and measurements based on standard, valid, and reliable data collection instruments/tests/procedures? Yes
  7.5. Was the measurement of effect at an appropriate level of precision? No
  7.6. Were other factors accounted for (measured) that could affect outcomes? Yes
  7.7. Were the measurements conducted consistently across groups? Yes
8. Was the statistical analysis appropriate for the study design and type of outcome indicators? Yes
  8.1. Were statistical analyses adequately described and the results reported appropriately? Yes
  8.2. Were correct statistical tests used and assumptions of test not violated? Yes
  8.3. Were statistics reported with levels of significance and/or confidence intervals? Yes
  8.4. Was "intent to treat" analysis of outcomes done (and as appropriate, was there an analysis of outcomes for those maximally exposed or a dose-response analysis)? N/A
  8.5. Were adequate adjustments made for effects of confounding factors that might have affected the outcomes (e.g., multivariate analyses)? Yes
  8.6. Was clinical significance as well as statistical significance reported? No
  8.7. If negative findings, was a power calculation reported to address type 2 error? N/A
9. Are conclusions supported by results with biases and limitations taken into consideration? No
  9.1. Is there a discussion of findings? Yes
  9.2. Are biases and study limitations identified and discussed? No
10. Is bias due to study's funding or sponsorship unlikely? Yes
  10.1. Were sources of funding and investigators' affiliations described? Yes
  10.2. Was the study free from apparent conflict of interest? Yes