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Dietary inflammatory index and non-Hodgkin lymphoma risk in an Italian case–control study

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Abstract

Background

While dietary factors have been shown to play an important etiologic role in non-Hodgkin lymphoma (NHL), little is known about the association between inflammatory properties of diet and NHL risk.

Methods

We explored the association between the dietary inflammatory index (DII) and NHL risk in a multicenter Italian case–control study conducted between 1999 and 2014. Cases were 536 subjects with incident, histologically confirmed NHL from three areas in Italy. Controls were 984 subjects admitted to the same network of hospitals as the cases for acute, nonmalignant conditions, unrelated to diet. DII scores were computed based on 30 nutrients and food items assessed using a reproducible and validated 78-item food-frequency questionnaire. Odds ratios (ORs) were estimated through logistic regression models adjusting for age, total energy intake, and other recognized confounding factors.

Results

Subjects in the highest quartile of DII scores (i.e., with the most pro-inflammatory diets) had a higher risk of NHL compared with subjects in the lowest quartile (i.e., with the most anti-inflammatory diets) (ORQuartile4vs1 1.61, 95% confidence interval CI 1.07–2.43; p-trend = 0.01). Stratified analyses produced stronger associations between DII and NHL among males (ORQuartile4vs1 2.14; 95% CI 1.25–3.67) with significant heterogeneity (p value = 0.02); when analyzed by histologic subtype, a significant association was observed with diffuse large B-cell lymphoma (ORQuartile4vs1 1.84; 95% CI 1.09–3.10).

Conclusion

A pro-inflammatory diet, as indicated by higher DII scores, is associated with elevated odds of NHL, especially among males.

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References

  1. Ferlay JSI, Ervik M, Dikshit R, Eser S, Mathers C, et al. (2013) GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11. Lyon, France

  2. Ferlay JBF, Steliarova-Foucher E, Forman D (2014) Cancer Incidence in Five Continents, CI5plus: IARC CancerBase No. 9. Lyon, France

  3. Charbonneau B, O’Connor HM, Wang AH, Liebow M, Thompson CA, Fredericksen ZS et al (2013) Trans fatty acid intake is associated with increased risk and n3 fatty acid intake with reduced risk of non-Hodgkin lymphoma. J Nutr 143(5):672–681

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Chiu BC, Kwon S, Evens AM, Surawicz T, Smith SM, Weisenburger DD (2011) Dietary intake of fruit and vegetables and risk of non-Hodgkin lymphoma. Cancer Causes Control 22(8):1183–1195

    Article  PubMed  Google Scholar 

  5. Lu D, Chen J, Jin J (2014) Vitamin D status and risk of non-Hodgkin lymphoma: a meta-analysis. Cancer Causes Control 25(11):1553–1563

    Article  PubMed  Google Scholar 

  6. Gu Y, Shore RE, Arslan AA, Koenig KL, Liu M, Ibrahim S et al (2010) Circulating cytokines and risk of B-cell non-Hodgkin lymphoma: a prospective study. Cancer Causes Control 21(8):1323–1333

    Article  PubMed  PubMed Central  Google Scholar 

  7. Rothman N, Skibola CF, Wang SS, Morgan G, Lan Q, Smith MT et al (2006) Genetic variation in TNF and IL10 and risk of non-Hodgkin lymphoma: a report from the InterLymph Consortium. Lancet Oncol 7(1):27–38

    Article  CAS  PubMed  Google Scholar 

  8. Saberi Hosnijeh F, Krop EJ, Scoccianti C, Krogh V, Palli D, Panico S et al (2010) Plasma cytokines and future risk of non-Hodgkin lymphoma (NHL): a case–control study nested in the Italian European Prospective Investigation into Cancer and Nutrition. Cancer Epidemiol Biomark Preven 19(6):1577–1584

    Article  CAS  Google Scholar 

  9. Shivappa N, Steck SE, Hurley TG, Hussey JR, Hebert JR (2014) Designing and developing a literature-derived, population-based dietary inflammatory index. Public Health Nutr 17(8):1689–1696

    Article  PubMed  Google Scholar 

  10. Shivappa N, Steck SE, Hurley TG, Hussey JR, Ma Y, Ockene IS et al (2014) A population-based dietary inflammatory index predicts levels of C-reactive protein in the Seasonal Variation of Blood Cholesterol Study (SEASONS). Public Health Nutr 17(8):1825–1833

    Article  PubMed  Google Scholar 

  11. Shivappa N, Hebert JR, Rietzschel ER, De Buyzere ML, Langlois M, Debruyne E et al (2015) Associations between dietary inflammatory index and inflammatory markers in the Asklepios Study. Br J Nutr 113(4):665–671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Tabung FK, Steck SE, Zhang J, Ma Y, Liese AD, Agalliu I et al (2015) Construct validation of the dietary inflammatory index among postmenopausal women. Ann Epidemiol 25(6):398–405

    Article  PubMed  PubMed Central  Google Scholar 

  13. Zamora-Ros R, Shivappa N, Steck SE, Canzian F, Landi S, Alonso MH et al (2015) Dietary inflammatory index and inflammatory gene interactions in relation to colorectal cancer risk in the Bellvitge colorectal cancer case–control study. Genes Nutr 10(1):447

    Article  PubMed  Google Scholar 

  14. Shivappa N, Zucchetto A, Montella M, Serraino D, Steck SE, La Vecchia C et al (2015) Inflammatory potential of diet and risk of colorectal cancer: a case-control study from Italy. Br J Nutr 114(1):152–158

    Article  CAS  PubMed  Google Scholar 

  15. Tabung FK, Steck SE, Ma Y, Liese AD, Zhang J, Caan B et al (2015) The association between dietary inflammatory index and risk of colorectal cancer among postmenopausal women: results from the Women’s Health Initiative. Cancer Causes Control 26(3):399–408

    Article  PubMed  Google Scholar 

  16. Wirth MD, Shivappa N, Steck SE, Hurley TG, Hebert JR (2015) The dietary inflammatory index is associated with colorectal cancer in the National Institutes of Health-American Association of Retired Persons Diet and Health Study. Br J Nutr 113(11):1819–1827

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Shivappa N, Prizment AE, Blair CK, Jacobs DR Jr, Steck SE, Hebert JR (2014) Dietary inflammatory index and risk of colorectal cancer in the Iowa Women’s Health Study. Cancer Epidemiol Biomark Prev 23(11):2383–2392

    Article  CAS  Google Scholar 

  18. Garcia-Arellano A, Ramallal R, Ruiz-Canela M, Salas-Salvado J, Corella D, Shivappa N et al (2015) Dietary inflammatory index and incidence of cardiovascular disease in the PREDIMED Study. Nutrients 7(6):4124–4138

    Article  PubMed  PubMed Central  Google Scholar 

  19. Ramallal R, Toledo E, Martinez-Gonzalez MA, Hernandez-Hernandez A, Garcia-Arellano A, Shivappa N et al (2015) Dietary inflammatory index and incidence of cardiovascular disease in the SUN cohort. PLoS ONE 10(9):e0135221

    Article  PubMed  PubMed Central  Google Scholar 

  20. Shivappa N, Hebert JR, Polesel J, Zucchetto A, Crispo A, Montella M et al (2015) Inflammatory potential of diet and risk for hepatocellular cancer in a case–control study from Italy. Br J Nutr 11:1–8

    Google Scholar 

  21. Shivappa N, Zucchetto A, Serraino D, Rossi M, La Vecchia C, Hebert JR (2015) Dietary inflammatory index and risk of esophageal squamous cell cancer in a case-control study from Italy. Cancer Causes Control 26(10):1439–1447

    Article  PubMed  Google Scholar 

  22. Shivappa N, Hébert JR, Zucchetto A, Montella M, Serraino D, La Vecchia C et al (2015) Dietary inflammatory index and endometrial cancer risk in an Italian case–control study. Br J Nutr 115:1–9

    Google Scholar 

  23. Talamini R, Montella M, Crovatto M, Dal Maso L, Crispo A, Negri E et al (2004) Non-Hodgkin’s lymphoma and hepatitis C virus: a case-control study from northern and southern Italy. Int J Cancer 110(3):380–385

    Article  CAS  PubMed  Google Scholar 

  24. Taborelli M, Polesel J, Montella M, Libra M, Tedeschi R, Battiston M et al (2016) Hepatitis B and C viruses and risk of non-Hodgkin lymphoma: a case-control study in Italy. Infect Ag Cancer 11:27

    Article  Google Scholar 

  25. Gnagnarella P, Parpinel M, Salvini S, Franceschi S, Palli D, Boyle P (2004) The update of the Italian Food Composition Database. J Food Compos Anal 17(3–4):509–522

    Article  Google Scholar 

  26. Decarli A, Franceschi S, Ferraroni M, Gnagnarella P, Parpinel MT, La Vecchia C et al (1996) Validation of a food-frequency questionnaire to assess dietary intakes in cancer studies in Italy. Results for specific nutrients. Ann Epidemiol 6(2):110–118

    Article  CAS  PubMed  Google Scholar 

  27. Franceschi S, Negri E, Salvini S, Decarli A, Ferraroni M, Filiberti R et al (1993) Reproducibility of an Italian food frequency questionnaire for cancer studies: results for specific food items. Eur J Cancer 29A(16):2298–2305

    Article  CAS  PubMed  Google Scholar 

  28. Franceschi S, Barbone F, Negri E, Decarli A, Ferraroni M, Filiberti R et al (1995) Reproducibility of an Italian food frequency questionnaire for cancer studies. Results for specific nutrients. Ann Epidemiol 5(1):69–75

    Article  CAS  PubMed  Google Scholar 

  29. Sette S, Le Donne C, Piccinelli R, Mistura L, Ferrari M, Leclercq C et al (2013) The third National Food Consumption Survey, INRAN-SCAI 2005-06: major dietary sources of nutrients in Italy. Int J Food Sci Nutr 64(8):1014–1021

    Article  CAS  PubMed  Google Scholar 

  30. Talamini R, Polesel J, Montella M, Dal Maso L, Crovatto M, Crispo A et al (2006) Food groups and risk of non-Hodgkin lymphoma: a multicenter, case-control study in Italy. Int J Cancer 118(11):2871–2876

    Article  CAS  PubMed  Google Scholar 

  31. Polesel J, Talamini R, Montella M, Parpinel M, Dal Maso L, Crispo A et al (2006) Linoleic acid, vitamin D and other nutrient intakes in the risk of non-Hodgkin lymphoma: an Italian case-control study. Ann Oncol 17(4):713–718

    Article  CAS  PubMed  Google Scholar 

  32. Polesel J, Dal Maso L, La Vecchia C, Montella M, Spina M, Crispo A et al (2007) Dietary folate, alcohol consumption, and risk of non-Hodgkin lymphoma. Nutr Cancer 57(2):146–150

    Article  CAS  PubMed  Google Scholar 

  33. Holtan SG, O’Connor HM, Fredericksen ZS, Liebow M, Thompson CA, Macon WR et al (2012) Food-frequency questionnaire-based estimates of total antioxidant capacity and risk of non-Hodgkin lymphoma. Int J Cancer 131(5):1158–1168

    Article  CAS  PubMed  Google Scholar 

  34. Purdue MP, Lan Q, Bagni R, Hocking WG, Baris D, Reding DJ et al (2011) Prediagnostic serum levels of cytokines and other immune markers and risk of non-Hodgkin lymphoma. Can Res 71(14):4898–4907

    Article  CAS  Google Scholar 

Download references

Funding

This study was supported by the Italian Association for the Research on Cancer (AIRC; Grant #10447) and Italian Foundation for Research on Cancer. Drs. Shivappa and Hébert were supported by grant number R44DK103377 from the United States National Institute of Diabetes and Digestive and Kidney Diseases.

Author information

Authors and Affiliations

  1. Cancer Prevention and Control Program, University of South Carolina, Columbia, SC, 29208, USA

    Nitin Shivappa & James R. Hébert

  2. Department of Epidemiology and Biostatistics, Arnold School of Public Health, University of South Carolina, Columbia, SC, 29208, USA

    Nitin Shivappa & James R. Hébert

  3. Connecting Health Innovations LLC, Columbia, SC, 29201, USA

    Nitin Shivappa & James R. Hébert

  4. Unit of Cancer Epidemiology, CRO Aviano National Cancer Institute, Aviano, PN, Italy

    Martina Taborelli, Antonella Zucchetto, Diego Serraino & Jerry Polesel

  5. Dipartimento di Epidemiologia, ‘Fondazione G. Pascale’ Istituto Nazionale Tumori, Naples, Italy

    Maurizio Montella, Anna Crispo & Maria Grimaldi

  6. Department of Biomedical and Biotechnological Sciences (Biometec), University of Catania, Catania, Italy

    Massimo Libra

  7. Italy Department of Clinical Sciences and Community Health, Università degli Studi di Milano, Milan, Italy

    Carlo La Vecchia

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  1. Nitin Shivappa
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  2. James R. Hébert
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  3. Martina Taborelli
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  4. Maurizio Montella
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  11. Jerry Polesel
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Corresponding author

Correspondence to Nitin Shivappa.

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Conflict of interest

Though this is not thought to represent a conflict, Dr. James R. Hébert wishes to disclose that he owns controlling interest in Connecting Health Innovations LLC (CHI), a company planning to license the right to his invention of the dietary inflammatory index (DII) from the University of South Carolina in order to develop computer and smart phone applications for patient counseling and dietary intervention in clinical settings. Dr. Nitin Shivappa is an employee of CHI.

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Shivappa, N., Hébert, J.R., Taborelli, M. et al. Dietary inflammatory index and non-Hodgkin lymphoma risk in an Italian case–control study. Cancer Causes Control 28, 791–799 (2017). https://doi.org/10.1007/s10552-017-0905-z

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  • DOI: https://doi.org/10.1007/s10552-017-0905-z

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