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


Martin L, Lagergren P. Long-term weight change after oesophageal cancer surgery. B J Surg. 2009; 96 (11): 1,308-1,314.

PubMed ID: 19847871
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 investigate weight changes after esophageal cancer surgery and to determine whether pre-operative weight loss, sex, body mass index (BMI) at operation and mortality were associated with the risk of malnutrition.

Inclusion Criteria:
  • Patients diagnosed with esophageal or gastric cardia cancer who underwent esophagectomy with curative intent between April 2001 and December 2004 in Sweden
  • Tumor resection was complete both microscopically and macroscopically
  • Patients who were alive three years after surgery. (This criterion was not used for a separate mortality analysis.)
Exclusion Criteria:
  • Tumor resection was not complete both microscopically and macroscopically
  • Patients who died within three years. (This criterion was not used for a separate mortality analysis.)
Description of Study Protocol:


Almost all Swedish hospital departments (97.2%) involved in the investigation and treatment of patients with esophageal or cardia cancer participated. This collaboration enabled an almost complete data collection of approximately 90% of all patients who had surgery for esophageal cancer in Sweden.


Prospective cohort study.


Researchers collected data on height, weight, other patient characteristics and clinical data through questionnaires, case records and histopathological reports. 

Statistical Analysis

  • Logistic regression was used to estimate relative risks of malnutrition, expressed as ORs with 95% CI 
  • Malnutrition was considered as a dichotomous outcome (no, less than 15% weight loss; yes, 15% or more)
  • Adjustments for potential confounding were made in multivariable logistic regression models. Three models were considered:
    • A crude model without adjustment
    • A basic model adjusted for age, sex and tumor stage
    • A full model adjusted for histological type, tumor location, surgical approach, number of pre-defined surgical complications occurring within 30 days of surgery, co-morbidity, neoadjuvant treatment, BMI at operation and use of a nutritional catheter jejunostomy.
Data Collection Summary:

Timing of Measurements

  • The study was conducted between April 1, 2001 and January 31, 2008. Patients who underwent esophagectomy between April 2001 and December 2004 were followed until death or end of study
  • Data on weight changes were collected through written study-specific questionnaires focusing on height and weight just before operation, and weight at six months and three years after surgery
  • Clinical data were collected and evaluated according to a pre-defined study protocol (described in detail elsewhere).

Dependent Variables

Malnutrition (defined as weight loss 15% or more) between operation and six months later and between operation and three years later.

Independent Variables

  • Sex
  • Pre-operative weight loss (measured as the difference between average weight as an adult and weight at the time of operation; patients grouped into those with less than 10% or 10% or more weight loss)
  • BMI at operation (less than 25kg/m2 or 25kg/m2 or more) 
  • Mortality (patients who died within three years of surgery or those who survived at least three years).

Other Variables

Those listed under Statistical Analysis (adjustments for multivariable logistic regression models).

Description of Actual Data Sample:

Initial N

203 (162 males, 41 females); the separate mortality analysis included all 359 patients (three-year survivors and those who died between six months and three years) who responded to the six-month questionnaire. 

Attrition (Final N)

  • 176 (86.7%) included in the analysis at six months. 25 did not respond to the six-month questionnaire due to non-participation (two) or administrative errors (23). Two were excluded because weight data were missing.
  • 136 (67.0%) included in the analysis at three years; 65 did not respond to the questionnaire because of non-participation (four) or administrative errors (61). Two were excluded because data on height or weight were missing.


  • Less than 60 years: 27%
  • Between 60 and 69 years: 36%
  • 70 years or more: 38%.

Other Relevant Demographics

  • Adenocarcinoma was the dominating histological type
  • More than half (59.1%) has stage II or more advanced tumors
  • Only 6.4% received neoadjuvant treatment
  • A thoracoabdominal approach was used in most patients (80.8%), with stomach as the esophageal substitute (76.9%)
  • Some 44.8% had at least one complication within 30 days of surgery.


  • The mean BMI in the whole group was 25.7kg/m2 at the time of operation
  • Almost half (42.4%) were overweight or obese at the time of surgery, although 15.3% lost 10% or more of their body weight before operation
  • The mean weight loss from the average adult weight to the weight three years after operation was 10.8kg
  • 46 (33.8%) had weight loss of 15% or more during the three years after surgery.



Summary of Results:

Key Findings

  • Female sex was associated with a non-significantly increased risk of malnutrition within 6 months after surgery (OR 1.78), but not at 3 years (OR 0.85).
  • Among patients with preoperative weight loss ≥10%, the risk of malnutrition was decreased at both the 6-month and 3-year follow-up.
  • Overweight patients (BMI≥25 kg/m2) had an almost fivefold increase in the risk of malnutrition at both 6 months and 3 years.
Odds Ratio for Post-operative
Weight Loss 15% or More
Six Months (N=176)
Three Years (N=136)
Sex Male




1.78 (0.69, 4.65)

0.85 (0.24, 2.98)

Pre-operative weight loss (%) Less than 10



10 or more

0.33 (0.08, 1.30)

0.54 (0.12,2.44)

BMI at operation (kg/m2) Less than 25



25 or more

4.90 (2.27, 10.59)1

4.60 (1.80, 11.78)2

Values in parentheses are 95% confidence intervals. 1P<0.001, 2P=0.001.

  • Death within three years after surgery was not associated with an increased risk of malnutrition six months after operation.
Number of Patients
Odds Ratio for Post-operative
Weight Loss 15% or More
Basic Model
Multivariable Model
Survived three or more years
Died within three years
1.20 (0.74, 1.95)
1.11 (0.64, 1.94)
  • Generally, results from the crude and basic analyses did not show any material differences from those obtained with the full model.

Other Findings

  • The whole group of 203 patients who survived at least three years did have a small amount of pre-operative weight loss. This weight loss was appreciable during the first six months after surgery and continued for three years.
  • Patients with a BMI 20 or more at the time of surgery showed considerable weight loss during the first six months, whereas those with a lower BMI at operation gained in body weight after surgery
  • Post-operative weight loss within six months of surgery was less pronounced among the patients who lost the most weight before operation. Both groups continued to lose weight up to three years.
  • Weight changes followed a similar pattern in men and women.


Author Conclusion:
  • Weight loss after esophageal cancer surgery continues for at least three years after operation. Post-operative weight loss was more pronounced among overweight patients, but was similar between men and women and between survivors and those who died within three years of surgery.
  • Patients with more pre-operative weight loss might have a decreased risk of weight loss at both six months and three years after operation, although the results were not statistically significant
  • Post-operative malnutrition negatively influences the chance of survival, as well as efficiency of treatment. Nutritional advice from dietitians has been shown to decrease weight loss. Dietitians should be involved in the management of patients with weight loss after esophageal cancer surgery.
Funding Source:
Reviewer Comments:
  • An advantage is the population-based design, which reduces selection bias
  • Data were collected from a comprehensive national Swedish organization for research, described in detail elsewhere. Assumed little bias due to nature of the variables studied. Unsure if blinding was used.
  • Response rate at three-year follow up slightly low (67%)
  • About four times more males than females at baseline; unsure of ratio at follow-ups
  • A source of error is that some patients, especially those who are overweight, might deliberately choose to lose weight, independent of the effect of the surgery
  • Use of weight loss cut-off of 15% to define malnutrition was based on previous research. Biochemical or hematological markers of malnutrition were not available.
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) N/A
  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) N/A
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? ???
  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? ???
  3.3. Were concurrent controls or comparisons used? (Concurrent preferred over historical control or comparison groups.) No
  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? Yes
  4.1. Were follow-up methods described and the same for all groups? Yes
  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%.) Yes
  4.3. Were all enrolled subjects/patients (in the original sample) accounted for? Yes
  4.4. Were reasons for withdrawals similar across groups? N/A
  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? ???
  5.1. In intervention study, were subjects, clinicians/practitioners, and investigators blinded to treatment group, as appropriate? N/A
  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.) Yes
  5.3. In cohort study or cross-sectional study, were measurements of outcomes and risk factors blinded? ???
  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? ???
  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? N/A
  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? ???
  7.5. Was the measurement of effect at an appropriate level of precision? Yes
  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? Yes
  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? Yes
  9.1. Is there a discussion of findings? Yes
  9.2. Are biases and study limitations identified and discussed? Yes
10. Is bias due to study's funding or sponsorship unlikely? ???
  10.1. Were sources of funding and investigators' affiliations described? No
  10.2. Was the study free from apparent conflict of interest? ???