Adherence to Mediterranean Diet and Risk of Pancreatic Cancer: Systematic Review and Meta-Analysis
Abstract
:1. Introduction
2. Materials and Methods
2.1. Search Strategy and Data Source
2.2. Inclusion/Exclusion Criteria
2.3. Selection Process and Data Extraction
2.4. Strategy for Data Synthesis
2.5. Critical Appraisal
2.6. Statistical Analysis
2.7. Sensitivity and Subgroup Analysis
3. Results
3.1. Literature Search
3.2. Main Characteristics of Included Articles
3.3. Characteristics of the Studied Populations
3.4. Mediterranean Diet and Scores Used to Assess Adherence Thereto
3.5. Critical Appraisal Results
3.6. Results of Meta-Analysis
3.7. Sensitivity Analyses
3.8. Subgroup Analyses
4. Discussion
4.1. Data Interpretation
4.2. Potential Biological Mechanisms
4.3. Strengths and Limitations
4.4. Implications for Public Health Policies and Practice
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Database | Syntax |
---|---|
PubMed/MEDLINE | (((“tumor*” [Title/Abstract] OR “tumour*” [Title/Abstract] OR “cancer*” [Title/Abstract] OR “neoplasm*” [Title/Abstract] OR “malignanc*” [Title/Abstract] OR “neoplastic” [Title/Abstract]) AND (“pancreas” [Title/Abstract] OR “pancreatic” [Title/Abstract])) OR “pancreatic neoplasms” [MeSH Terms]) AND (“diet, mediterranean” [MeSH Terms] OR (“Mediterranean” [Title/Abstract] AND (“diet” [Title/Abstract] OR “diets” [Title/Abstract] OR “dietary pattern” [Title/Abstract] OR “dietary patterns” [Title/Abstract] OR “dietary” [Title/Abstract] OR “dietary adherence” [Title/Abstract] OR “dietary score” [Title/Abstract] OR “dietary scores” [Title/Abstract] OR “dietary index” [Title/Abstract] OR “dietary intervention” [Title/Abstract] OR “dietary behaviour” [Title/Abstract] OR “dietary behavior” [Title/Abstract]))) |
Scopus | ((TITLE-ABS-KEY (pancreatic OR pancreas) AND TITLE-ABS-KEY (neoplasm OR cancer OR tumor OR tumour OR malignanc*))) AND ((TITLE-ABS-KEY (mediterranean) AND TITLE-ABS-KEY (diet OR dietary OR pattern OR intervention OR behavior OR behaviour OR index OR score OR adherence))) |
EMBASE | (‘mediterranean diet’/exp OR ((diet* OR dietary OR score* OR intervention* OR ‘behavior’/exp OR behavior OR ‘behaviour’/exp OR behaviour OR ‘index’/exp OR index OR ‘adherence’/exp OR adherence) AND (‘mediterranean’/exp OR mediterranean OR meddiet))) AND (‘pancreas cancer’/exp OR ((‘pancreas’/exp OR pancreas OR pancreatic) AND (neoplasm* OR cancer* OR malignan* OR tumor* OR tumour*))) |
Search Strategy | Details |
---|---|
Inclusion criteria | P: adults ≥ 18 years (both female and male) I/E: higher adherence to Mediterranean diet C: lowest or no adherence to Mediterranean diet or adherence to other dietary patterns O: pancreatic cancer risk S: all original study types (both observational and trial-based) |
Exclusion criteria | P: people < 18 years old I/E: other diets, dietary patterns, dietary supplementation, single food or food components or micro/macro-nutrients intake C: study assessing the effect of other diets, dietary patterns, dietary supplementation, single food or food components or micro/macro-nutrients intake O: other outcomes or data combined for pancreatic cancer with other gastrointestinal cancers. S: non-original papers, paper without data, articles not published as peer-reviewed in international journals |
Language | English |
Time filter | No filter (from inception) |
Databases | PubMed/Medline; EMBASE, Scopus |
Author, Year [Ref.] | Country | Study Period | Study Design | Population Characteristics | Tool Used for Dietary Assessment | Mediterranesn Score Used | Diagnostic Assessment | Outcome Definition | Cancer Type | Funds | CoI |
---|---|---|---|---|---|---|---|---|---|---|---|
Bodèn, 2019 [33] | Sweden | 1990–2016; 15 y FU | CO | Male and female from the VIP | three versions of validated FFQs (84-items, 64-items and 66-items) | aMDS | Swedish Cancer Registry | Cases were defined based on ICD-10 codes as the first incident of primary malignancy via annual linkage | All types | yes | yes |
Bosetti, 2013 [34] | Italy | 1983–1992 first study and 1992–2008 second study | CC | Cases: subjects with pancreatic cancer (without history of previous cancers) admitted to hospitals in the province of Milan Control: subjects admitted to the same network of hospitals as the cases for a wide spectrum of acute, non-neoplastic conditions Matching ratio 2:1, based on age, sex and study centre | structured questionnaire, simplified dietary section (14 selected indicator foods); and validated and reproducible food frequency questionnaire (78 items) | a priori MDS MDPI MAI | n.s. | Incident cases of pancreatic cancer newly admitted to the hospital | n.s. | yes | n.a. |
Juliàn-Serrano, 2022 [35] | USA | 1995–2011; 15 y FU | CO | NIH–AARP | validated self-administered semiquantitative 124-item FFQ | aMED | Social Security Administration Death Master File | Cases were defined based on ICD-10 codes as the first incident of primary adenocarcinoma via annual linkage | excluding endocrine tumours, sarcomas and lymphomas | n.a. | no |
Luu, 2021 [36] | Singapore | 1993–2015; 25 y FU | CO | Singapore Chinese Health Study | validated semiquantitative 165-FFQ | aMED | Singapore Cancer Registry and the Singapore Birth and Death Registry | Incident cases of pancreatic cancer were identified via annual linkage | excluding neuroendocrine pancreatic cancer | yes | no |
Molina-Montes, 2017 [37] | 23 centres in 10 European countries# | From ‘90 s to 2004–2008 °; 11 y FU | CO | Male and female from the EPIC cohort | country-specific validated dietary questionnaires (FFQ, diet history, and semiquantitative FFQ) | arMED score | cancer registries and national mortality registries | Incident cancer cases identified via annual linkage | only including exocrine adenocarcinomas | n.a. | no |
Rosato, 2015 [38] | Italy | 1992–2008; | CC | Cases: subjects with pancreatic cancer (without history of previous cancers) admitted to hospitals in the province of Milan and Pordenone Control: subjects admitted to the same network of hospitals as the cases for a wide spectrum of acute, non-neoplastic conditions Matching ratio 2:1, based on age, sex and study centre | 78-item FFQ | a priori MDS | Histological or cytological confirmation (179 patients), ultrasound and/or tomography. | Incident cases of pancreatic cancer newly admitted to the hospital | excluding endocrine pancreatic cancer | yes | no |
Schulpen, 2018 [39] | The Netherlands | 1986–2006 NLCS and 1993–2014 EPIC-NL; 10 y FU | CO | NLCS and EPIC-NL | validated, self-administered, semiquantitative FFQs (number of items n.s.) | aMED modified MDS (for both scores a non-alcohol score was also estimated) | Netherlands Cancer Registry and nationwide Dutch Pathology Registry | Cases were defined based on ICD-10 codes as the first incident of primary malignancy via annual linkage | excluding endocrine pancreatic cancer | yes | no |
Tognon, 2012 [40] | Sweden | 1990–2008;18 y FU | CO | VIP | three versions of FFQ (2 × 84-items and 65-items), only one validated | mMDS | Swedish national cause-of-death registry | Deaths were defined based on ICD-10 codes via record linkage | excluding in situ and benign PC | n.a. | no |
Author, Year [Ref.] | Total Sample | Attrition * | Sex | Age: Mean and/or Range | MDS Categories | Effect Size (95% CI) | Adjustment | QS/9 |
---|---|---|---|---|---|---|---|---|
Bodèn, 2019 [33] | Ca: 223 Co: 100,881 | 63% | Ca: F = 107 Co: F = 51,001 | 40–60 y | Tertiles range n.s. | Total sample: HR = 0.90 (0.76–1.07) Male: HR = 1.01 (0.80–1.28) Female: HR = 0.80 (0.63–1.02) | EI, BMI, smoking, PA, and education | 8 |
Bosetti, 2013 [34] | Ca: 688 Ct: 2204 | 5% | Ca: F = 285 Co: F = 715 | 56 (18–84) y | MDPI high ≥ 65.5 | Total sample: OR 0.44 (0.27–0.73) | centre, age, sex, year of interview, education, BMI, smoking, alcohol, history of T2D | 9 |
MAI high ≥ 2.48 | Total sample OR 0.68 (0.42–1.11) | |||||||
a priori MDS high ≥ 6 points | Total sample: OR = 0.48 (0.35–0.67) Male: OR = 0.84 (0.78–0.91) Female: OR = 0.87 (0.79–0.97) | |||||||
Juliàn-Serrano, 2022 [35] | Ca: 3137 Co: 535,824 | 5.4% | Ca: F = n.a. Co: F = 220,044 | 50–71 y | Quintiles, Q1 = 2.5; Q5 = 7.4 | Total sample: HR = 0.82 (0.73–0.93) Male: HR = 0.97 (0.95–1.00) Female: HR = 0.76 (0.63–0.92) | age at baseline, sex ^, smoking, BMI, T2D, EI | 9 |
Luu, 2021 [36] | Ca: 311 Co: 61,321 | 3% | Ca: F = 149 Co: F = n.a. | 45–74 y | Quintiles range n.s. | Total sample: HR = 0.57 (0.38–0.85) Male: HR = 0.43 (0.24–0.75) Female: HR = 0.79 (0.45–1.39) | age, sex ^, dialect, year of enrolment, education, smoking, smoking pack-years, coffee drinking, EI, BMI, T2D | 9 |
Molina-Montes, 2017 [37] | Ca: 865 Co: 477,309 | 2% | Ca: F = 469 Co: F = 335,060 | 51.5 y | low (0–5 points), medium (6–9 points) high (10–16 points) | Total sample: HR = 0.99 (0.77–1.26) Male: HR = 1.00 (0.68–1.49) Female: HR = 0.99 (0.72–1.37) | EI, BMI, smoking status and intensity, alcohol, T2D | 9 |
Rosato, 2015 [38] | Ca: 326 Ct: 652 | 0% | Ca: F = 152 Ct: F = 304 | 63 (34–80) y | low (≤3 points), medium (4–5 points) high (≥6 points) | Total sample: OR = 0.57 (0.34–0.95) | sex, age, study centre, education, BMI, smoking, alcohol, T2D, EI | 9 |
Schulpen, 2018 [39] | Ca: 311 Co: 61,321 | 14% | Ca: F = 149 Co: F = 28,275 | 45–74 y | aMED: low (0–3 points), medium (4–5 points) high (6–9 points) | Male: HR = 0.70 (0.44–1.12) Female: HR = 1.18 (0.80–1.75) | age, smoking status, smoking frequency, smoking duration, BMI, EI, alcohol, T2D, family history of pancreatic cancer, education, nonoccupational PA | 9 |
mMDS: low (0–3 points), medium (4–5 points) high (6–8 points) | Male: HR = 0.66 (0.40–1.10) Female: HR = 0.94 (0.63–1.40) | |||||||
Tognon, 2012 [40] | Ca: 92 Co: 77,151 | Ca: F = 45 Co: F = 39,605 | 30–60 y | high > 4 points | Total sample: HR = 0.82 (0.72–0.94) Male: HR = 0.82 (0.68–0.99) Female: HR = 0.83 (0.69–1.00) | age, obesity, smoking status, education, PA | 9 |
Scale Type | Food Items Included in the Scale | ||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
Vegetables 1 | Legumes | Fruit 2 | Cereals 3 | Fish 4 | Healthy 5 Fats | Alcohol | Meat and Meat Products | Dairy Products | Added Sugars | Score System | Score Range | Ref. | |
aMDS | x | x | x | x | x | x | x | x | x | - | 1 point if consumption is above */below’ their sex and FFQ-specific median; for alcohol, 1 point if consumption < 50 g/day | 0–8 | [33] |
A priori MDS | x | x | x | x | x | x | x | x | x | - | 1 point if consumption is above */below’ their sex and FFQ-specific median | 0–9 | [34,38] |
MDPI | x | x | x | x | x | x | x | x | - | adding up the standardised residuals of the regression of cereals+ fruit+ vegetables+ legumes+ moderate alcohol+ MUFA/SFA ratio on total calories, and subtracting those of milk and meat | 0–100% | [34] | |
MAI | x | x | x | x | x | x | x | x | x | x | dividing the sum of the intake of bread+ cereals+ fruit+ vegetables+ legumes+ potatoes+ fish+ red wine+ vegetable oils as a percentage of total energy by the sum of milk+ cheese+ meat+ eggs+ animal fats and margarines+ sweet beverages+ cakes+ pies+ cookies+ sugar | 0–44 | [34] |
aMED | x | x | x | x | x | x | x | x | - | - | 1 point if consumption is above */below’ their study population’s specific median | 0–9 | [35,36] |
arMED | x | x | x | x | x | x | - | x | x | - | A score from 0 to 2 is assigned according to the first, second or third quartile of consumption, respectively (for vegetables, fruits, legumes, fish and cereals); for olive oil, a maximum score of 2 is assigned if consumption is above the median; a score from 0 to 2 is assigned according to the third, second or first quartile of consumption, respectively (for dairy and meat products) | 0–16 | [37] |
mMDS | x | - | x | x | x | x | x | x | x | - | 1 point if consumption is above */below’ their sex and FFQ-specific median; for alcohol 1 point if consumption < 50 g/day | 0–8 | [40] |
non-alcohol mMDS | x | - | x | x | x | x | - | x | x | - | 1 point if consumption is above */below’ their sex and FFQ-specific median | 0–7 | [39] |
non-alcohol aMED | x | x | x | x | x | x | - | x | - | - | 1 point if consumption is above */below’ their sex and FFQ-specific median | 0–8 | [39] |
Summary Statistics | Publication Bias | ||||||
---|---|---|---|---|---|---|---|
Analysis | Studies Included [Ref.] | No. of Participants | df | HR (95% CI); p-Value | I2; p-Value | Intercept’; p-Value | Estimated a ES; p-Value |
Overall analysis (both male and female) ^ | Boden (aMDS), Bosetti (a priori), Juliàn-Serrano (aMED), Luu (aMED), Molina-Montes (arMED), Rosato (a priori), Schulpen (aMED), Tognon (mMED) | 1,301,320 | 8 * | FE: 0.82 (0.76–0.88); p < 0.001 | 65.48%; p = 0.003 | −1.24, p = 0.331 | FE: 0.84 (0.79–0.90); p < 0.001 |
RE: 0.78 (0.68–0.90); p = 0.001 | RE: 0.84 (0.73–0.97); p = 0.017 | ||||||
Overall analysis (both male and female) $ | Boden (aMDS), Bosetti (a priori), Juliàn-Serrano (aMED), Luu (aMED), Molina-Montes (arMED), Rosato (a priori), Schulpen (mMED), Tognon (mMED) | 1,301,320 | 8 * | FE: 0.81 (0.76–0.87); p < 0.001 | 60.90%; p = 0.009 | −1.57; p = 0.171 | FE: 0.84 (0.78–0.90); p < 0.001 |
RE: 0.77 (0.68–0.88); p < 0.001 | RE: 0.83 (0.71–0.96); p = 0.014 | ||||||
Excluding mortality data | Boden (aMDS), Bosetti (a priori), Juliàn-Serrano (aMED), Luu (aMED), Molina-Montes (arMED), Rosato (a priori), Schulpen (aMED) | 1,224,007 | 7 * | FE: 0.81 (0.75–0.88); p < 0.001 | 69.79%; p = 0.002 | −1.36; p = 0.351 | FE: 0.81 (0.75–0.88); p < 0.001 |
RE: 0.77 (0.64–0.92); p = 0.004 | RE: 0.86 (0.79–0.92); p < 0.001 | ||||||
Excluding potential overlapping cohorts (both male and female) | Boden (aMDS), Bosetti (a priori), Juliàn-Serrano (aMED), Luu (aMED), Molina-Montes (arMED), Schulpen (aMED) | 1,223,009 | 6 * | FE: 0.82 (0.76–0.89); p < 0.001 | 70.94%; p = 0.002 | −1.04; p = 0.550 | FE: 0.87 (0.80–0.94); p < 0.001 |
RE: 0.79 (0.66–0.95); p = 0.001 | RE: 0.80 (0.68–0.93); p < 0.004 | ||||||
Only studies using validated FFQ | Juliàn-Serrano (aMED), Luu (aMED), Molina-Montes (arMED), Schulpen (aMED) | 1,119,103 | 4 * | FE: 0.84 (0.76–0.93); p = 0.001 | 55.10%; p = 0.063 | −0.04; p = 0.979 | FE: 0.86 (0.78–0.95); p = 0.002 |
RE: 0.84 (0.70–1.02); p = 0.084 | RE: 0.90 (0.73–1.12); p = 0.342 | ||||||
Diagnosis based on record linkage + | Boden (aMDS), Juliàn-Serrano (aMED), Luu (aMED), Molina-Montes (arMED), Schulpen (aMED) | 1,220,207 | 5 * | FE: 0.86 (0.78–0.93); p < 0.001 | 46.64%; p = 0.095 | −0.10; p = 0.947 | FE: 0.86 (0.78–0.93); p < 0.001 |
RE: 0.86 (0.75–0.99); p = 0.033 | RE: 0.90 (0.77–1.05); p = 0.176 | ||||||
Only studies conducted in Europe | Boden (aMDS), Bosetti (a priori), Molina-Montes (arMED), Schulpen (aMED) | 622,506 | 4 * | FE: 0.85 (0.76–0.96); p = 0.009 | 76.57%; p = 0.002 | −1.46; p = 0.652 | FE: 0.85 (0.76–0.96); p = 0.009 |
RE: 0.82 (0.62–1.08); p= 0.152 | RE: 0.82 (0.62–1.08); p = 0.152 | ||||||
Subgroup analyses | |||||||
Including only male | Boden (aMDS), Bosetti (a priori), Juliàn-Serrano (aMED), Luu (aMED), Molina-Montes (arMED), Schulpen (aMED) | 585,430 | 5 | FE: 0.95 (0.93–0.98); p < 0.001 | 76.82%; p = 0.001 | −1.45; p = 0.206 | FE: 0.96 (0.93–0.98); p < 0.001 |
RE: 0.89 (0.78–1.01); p = 0.061 | RE: 0.91 (0.80–1.05); p = 0.197 | ||||||
Including only female | Boden (aMDS), Bosetti (a priori), Juliàn-Serrano (aMED), Luu (aMED), Molina-Montes (arMED), Schulpen (aMED) | 698,960 | 5 | FE: 0.86 (0.80–0.93); p < 0.001 | 14.94%; p = 0.318 | 0.41; p = 0.698 | FE: 0.86 (0.80–0.93); p < 0.001 |
RE: 0.86 (0.79–0.95); p = 0.002 | RE: 0.86 (0.79–0.95); p = 0.002 | ||||||
Cancer type (excluding endocrine PC) | Juliàn-Serrano (aMED), Luu (aMED), Rosato (a priori), Schulpen (aMED) | 641,907 | 4 * | FE: 0.80 (0.72–0.89); p < 0.001 | 56.68%; p = 0.056 | −0.85; p = 0.556 | FE: 0.81 (0.73–0.90); p < 0.001 |
RE: 0.76 (0.60–0.96); p = 0.021 | RE: 0.80 (0.64–1.00); p = 0.050 |
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Nucci, D.; Nardi, M.; Cinnirella, A.; Campagnoli, E.; Maffeo, M.; Perrone, P.M.; Shishmintseva, V.; Grosso, F.M.; Castrofino, A.; Castaldi, S.; et al. Adherence to Mediterranean Diet and Risk of Pancreatic Cancer: Systematic Review and Meta-Analysis. Int. J. Environ. Res. Public Health 2023, 20, 2403. https://doi.org/10.3390/ijerph20032403
Nucci D, Nardi M, Cinnirella A, Campagnoli E, Maffeo M, Perrone PM, Shishmintseva V, Grosso FM, Castrofino A, Castaldi S, et al. Adherence to Mediterranean Diet and Risk of Pancreatic Cancer: Systematic Review and Meta-Analysis. International Journal of Environmental Research and Public Health. 2023; 20(3):2403. https://doi.org/10.3390/ijerph20032403
Chicago/Turabian StyleNucci, Daniele, Mariateresa Nardi, Andrea Cinnirella, Emanuela Campagnoli, Manuel Maffeo, Pier Mario Perrone, Viktoriia Shishmintseva, Francesca Maria Grosso, Ambra Castrofino, Silvana Castaldi, and et al. 2023. "Adherence to Mediterranean Diet and Risk of Pancreatic Cancer: Systematic Review and Meta-Analysis" International Journal of Environmental Research and Public Health 20, no. 3: 2403. https://doi.org/10.3390/ijerph20032403