Skip to main content
Erschienen in: Annals of Hematology 6/2017

24.12.2016 | Review Article

Carotenoid intake and risk of non-Hodgkin lymphoma: a systematic review and dose-response meta-analysis of observational studies

verfasst von: Feifei Chen, Jiyi Hu, Ping Liu, Jing Li, Zheng Wei, Peng Liu

Erschienen in: Annals of Hematology | Ausgabe 6/2017

Einloggen, um Zugang zu erhalten

Abstract

Carotenoids may play a protective role in the development of non-Hodgkin lymphoma (NHL), but findings from epidemiological studies on the associations between carotenoid intake and NHL risk are inconsistent. We therefore performed a meta-analysis to systemically evaluate the associations. Eligible studies were identified by a search of PubMed, Web of Science, Embase, and article reference lists. We pooled risk estimates from individual studies using a random-effect model to quantify the associations between intakes of specific carotenoids and NHL risk. A total of 10 (7 case-control and 3 cohort) studies met our inclusion criteria. In the highest versus lowest analyses, intakes of alpha-carotene, beta-carotene, and lutein/zeaxanthin, but not lycopene or beta-cryptoxanthin, were associated with a significant reduced risk of NHL. The estimated summary relative risks (95% confidence intervals) for alpha-carotene, beta-carotene, and lutein/zeaxanthin were 0.87 (0.78–0.97), 0.80 (0.68–0.94), and 0.82 (0.69–0.97), respectively. Subgroup analyses showed that evidence supporting these protective associations was mostly based on studies with a case-control design. In addition, intakes of alpha-carotene and beta-carotene were associated with a significant decreased risk of diffuse large B-cell lymphoma, but not follicular lymphoma or small lymphocytic lymphoma/chronic lymphocytic leukemia. There was a significant inverse dose-response relationship between alpha-carotene intake and NHL risk (13% lower risk per 1000 μg/day increment of intake). In conclusion, our findings suggest that higher intakes of alpha-carotene, beta-carotene, and lutein/zeaxanthin might protect against NHL development. Further cohort studies with a control of plausible confounding are needed to confirm these associations.
Literatur
2.
Zurück zum Zitat Besson H, Brennan P, Becker N, Nieters A, De Sanjose S, Font R, Maynadie M, Foretova L, Cocco PL, Staines A, Vornanen M, Boffetta P (2006) Tobacco smoking, alcohol drinking and non-Hodgkin’s lymphoma: a European multicenter case-control study (Epilymph). Int J Cancer J Int du cancer 119(4):901–908. doi:10.1002/ijc.21913 CrossRef Besson H, Brennan P, Becker N, Nieters A, De Sanjose S, Font R, Maynadie M, Foretova L, Cocco PL, Staines A, Vornanen M, Boffetta P (2006) Tobacco smoking, alcohol drinking and non-Hodgkin’s lymphoma: a European multicenter case-control study (Epilymph). Int J Cancer J Int du cancer 119(4):901–908. doi:10.​1002/​ijc.​21913 CrossRef
3.
Zurück zum Zitat Gapstur SM, Diver WR, McCullough ML, Teras LR, Thun MJ, Patel AV (2012) Alcohol intake and the incidence of non-Hodgkin lymphoid neoplasms in the cancer prevention study II nutrition cohort. Am J Epidemiol 176(1):60–69. doi:10.1093/aje/kwr497 CrossRefPubMed Gapstur SM, Diver WR, McCullough ML, Teras LR, Thun MJ, Patel AV (2012) Alcohol intake and the incidence of non-Hodgkin lymphoid neoplasms in the cancer prevention study II nutrition cohort. Am J Epidemiol 176(1):60–69. doi:10.​1093/​aje/​kwr497 CrossRefPubMed
4.
Zurück zum Zitat Fallah M, Kharazmi E, Pukkala E, Tretli S, Olsen JH, Tryggvadottir L, Sundquist K, Hemminki K (2015) Familial risk of non-Hodgkin lymphoma by sex, relationship, age at diagnosis and histology: a joint study from five Nordic countries. Leukemia 30(2):373–378. doi:10.1038/leu.2015.272 CrossRefPubMed Fallah M, Kharazmi E, Pukkala E, Tretli S, Olsen JH, Tryggvadottir L, Sundquist K, Hemminki K (2015) Familial risk of non-Hodgkin lymphoma by sex, relationship, age at diagnosis and histology: a joint study from five Nordic countries. Leukemia 30(2):373–378. doi:10.​1038/​leu.​2015.​272 CrossRefPubMed
6.
Zurück zum Zitat Chen GC, Lv DB, Pang Z, Liu QF (2013) Fruits and vegetables consumption and risk of non-Hodgkin’s lymphoma: a meta-analysis of observational studies. Int J Cancer J Int du Cancer 133(1):190–200. doi:10.1002/ijc.27992 CrossRef Chen GC, Lv DB, Pang Z, Liu QF (2013) Fruits and vegetables consumption and risk of non-Hodgkin’s lymphoma: a meta-analysis of observational studies. Int J Cancer J Int du Cancer 133(1):190–200. doi:10.​1002/​ijc.​27992 CrossRef
7.
Zurück zum Zitat Maiani G, Caston MJ, Catasta G, Toti E, Cambrodon IG, Bysted A, Granado-Lorencio F, Olmedilla-Alonso B, Knuthsen P, Valoti M, Bohm V, Mayer-Miebach E, Behsnilian D, Schlemmer U (2009) Carotenoids: actual knowledge on food sources, intakes, stability and bioavailability and their protective role in humans. Mol Nutr Food Res 53(Suppl 2):S194–S218. doi:10.1002/mnfr.200800053 CrossRefPubMed Maiani G, Caston MJ, Catasta G, Toti E, Cambrodon IG, Bysted A, Granado-Lorencio F, Olmedilla-Alonso B, Knuthsen P, Valoti M, Bohm V, Mayer-Miebach E, Behsnilian D, Schlemmer U (2009) Carotenoids: actual knowledge on food sources, intakes, stability and bioavailability and their protective role in humans. Mol Nutr Food Res 53(Suppl 2):S194–S218. doi:10.​1002/​mnfr.​200800053 CrossRefPubMed
9.
Zurück zum Zitat Zhang SM, Hunter DJ, Rosner BA, Giovannucci EL, Colditz GA, Speizer FE, Willett WC (2000) Intakes of fruits, vegetables, and related nutrients and the risk of non-Hodgkin’s lymphoma among women. Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 9(5):477–485 Zhang SM, Hunter DJ, Rosner BA, Giovannucci EL, Colditz GA, Speizer FE, Willett WC (2000) Intakes of fruits, vegetables, and related nutrients and the risk of non-Hodgkin’s lymphoma among women. Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 9(5):477–485
10.
Zurück zum Zitat Zheng T, Holford TR, Leaderer B, Zhang Y, Zahm SH, Flynn S, Tallini G, Zhang B, Zhou K, Owens PH, Lan Q, Rothman N, Boyle P (2004) Diet and nutrient intakes and risk of non-Hodgkin’s lymphoma in Connecticut women. Am J Epidemiol 159(5):454–466CrossRefPubMed Zheng T, Holford TR, Leaderer B, Zhang Y, Zahm SH, Flynn S, Tallini G, Zhang B, Zhou K, Owens PH, Lan Q, Rothman N, Boyle P (2004) Diet and nutrient intakes and risk of non-Hodgkin’s lymphoma in Connecticut women. Am J Epidemiol 159(5):454–466CrossRefPubMed
11.
Zurück zum Zitat Chang ET, Balter KM, Torrang A, Smedby KE, Melbye M, Sundstrom C, Glimelius B, Adami H-O (2006) Nutrient intake and risk of non-Hodgkin’s lymphoma. Am J Epidemiol 164(12):1222–1232. doi:10.1093/aje/kwj330 CrossRefPubMed Chang ET, Balter KM, Torrang A, Smedby KE, Melbye M, Sundstrom C, Glimelius B, Adami H-O (2006) Nutrient intake and risk of non-Hodgkin’s lymphoma. Am J Epidemiol 164(12):1222–1232. doi:10.​1093/​aje/​kwj330 CrossRefPubMed
12.
Zurück zum Zitat Kelemen LE, Cerhan JR, Lim U, Davis S, Cozen W, Schenk M, Colt J, Hartge P, Ward MH (2006) Vegetables, fruit, and antioxidant-related nutrients and risk of non-Hodgkin lymphoma: a National Cancer Institute-surveillance, epidemiology, and end results population-based case-control study. Am J Clin Nutr 83(6):1401–1410PubMed Kelemen LE, Cerhan JR, Lim U, Davis S, Cozen W, Schenk M, Colt J, Hartge P, Ward MH (2006) Vegetables, fruit, and antioxidant-related nutrients and risk of non-Hodgkin lymphoma: a National Cancer Institute-surveillance, epidemiology, and end results population-based case-control study. Am J Clin Nutr 83(6):1401–1410PubMed
13.
Zurück zum Zitat Polesel J, Talamini R, Montella M, Parpinel M, Dal Maso L, Crispo A, Crovatto M, Spina M, La Vecchia C, Franceschi S (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):713–718CrossRefPubMed Polesel J, Talamini R, Montella M, Parpinel M, Dal Maso L, Crispo A, Crovatto M, Spina M, La Vecchia C, Franceschi S (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):713–718CrossRefPubMed
14.
Zurück zum Zitat Thompson CA, Habermann TM, Wang AH, Vierkant RA, Folsom AR, Ross JA, Cerhan JR (2010) Antioxidant intake from fruits, vegetables and other sources and risk of non-Hodgkin’s lymphoma: the Iowa women’s health study. Int J Cancer 126(4):992–1003. doi:10.1002/ijc.24830 PubMedPubMedCentral Thompson CA, Habermann TM, Wang AH, Vierkant RA, Folsom AR, Ross JA, Cerhan JR (2010) Antioxidant intake from fruits, vegetables and other sources and risk of non-Hodgkin’s lymphoma: the Iowa women’s health study. Int J Cancer 126(4):992–1003. doi:10.​1002/​ijc.​24830 PubMedPubMedCentral
15.
16.
Zurück zum Zitat Holtan SG, O’Connor HM, Fredericksen ZS, Liebow M, Thompson CA, Macon WR, Micallef IN, Wang AH, Slager SL, Habermann TM, Call TG, Cerhan JR (2012) Food-frequency questionnaire-based estimates of total antioxidant capacity and risk of non-Hodgkin lymphoma. Int J Cancer 131(5):1158–1168. doi:10.1002/ijc.26491 CrossRefPubMed Holtan SG, O’Connor HM, Fredericksen ZS, Liebow M, Thompson CA, Macon WR, Micallef IN, Wang AH, Slager SL, Habermann TM, Call TG, Cerhan JR (2012) Food-frequency questionnaire-based estimates of total antioxidant capacity and risk of non-Hodgkin lymphoma. Int J Cancer 131(5):1158–1168. doi:10.​1002/​ijc.​26491 CrossRefPubMed
17.
Zurück zum Zitat Kabat GC, Kim MY, Wactawski-Wende J, Shikany JM, Vitolins MZ, Rohan TE (2012) Intake of antioxidant nutrients and risk of non-Hodgkin’s lymphoma in the Women’s Health Initiative. Nutr Cancer-an Int J 64(2):245–254. doi:10.1080/01635581.2012.642454 CrossRef Kabat GC, Kim MY, Wactawski-Wende J, Shikany JM, Vitolins MZ, Rohan TE (2012) Intake of antioxidant nutrients and risk of non-Hodgkin’s lymphoma in the Women’s Health Initiative. Nutr Cancer-an Int J 64(2):245–254. doi:10.​1080/​01635581.​2012.​642454 CrossRef
18.
Zurück zum Zitat Greenland S (1987) Quantitative methods in the review of epidemiologic literature. Epidemiol Rev 9:1–30CrossRefPubMed Greenland S (1987) Quantitative methods in the review of epidemiologic literature. Epidemiol Rev 9:1–30CrossRefPubMed
19.
Zurück zum Zitat DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188CrossRefPubMed DerSimonian R, Laird N (1986) Meta-analysis in clinical trials. Control Clin Trials 7(3):177–188CrossRefPubMed
21.
22.
Zurück zum Zitat Greenland S, Longnecker MP (1992) Methods for trend estimation from summarized dose-response data, with applications to meta-analysis. Am J Epidemiol 135(11):1301–1309CrossRefPubMed Greenland S, Longnecker MP (1992) Methods for trend estimation from summarized dose-response data, with applications to meta-analysis. Am J Epidemiol 135(11):1301–1309CrossRefPubMed
23.
Zurück zum Zitat Orsini N, Bellocco R, Greenland S (2006) Generalized least squares for trend estimation of summarized dose-response data. Stata J 6:40–57 Orsini N, Bellocco R, Greenland S (2006) Generalized least squares for trend estimation of summarized dose-response data. Stata J 6:40–57
26.
27.
Zurück zum Zitat Lan Q, Zheng T, Shen M, Zhang Y, Wang SS, Zahm SH, Holford TR, Leaderer B, Boyle P, Chanock S (2007) Genetic polymorphisms in the oxidative stress pathway and susceptibility to non-Hodgkin lymphoma. Hum Genet 121(2):161–168. doi:10.1007/s00439-006-0288-9 CrossRefPubMed Lan Q, Zheng T, Shen M, Zhang Y, Wang SS, Zahm SH, Holford TR, Leaderer B, Boyle P, Chanock S (2007) Genetic polymorphisms in the oxidative stress pathway and susceptibility to non-Hodgkin lymphoma. Hum Genet 121(2):161–168. doi:10.​1007/​s00439-006-0288-9 CrossRefPubMed
28.
Zurück zum Zitat Wang SS, Davis S, Cerhan JR, Hartge P, Severson RK, Cozen W, Lan Q, Welch R, Chanock SJ, Rothman N (2006) Polymorphisms in oxidative stress genes and risk for non-Hodgkin lymphoma. Carcinogenesis 27(9):1828–1834. doi:10.1093/carcin/bgl013 CrossRefPubMed Wang SS, Davis S, Cerhan JR, Hartge P, Severson RK, Cozen W, Lan Q, Welch R, Chanock SJ, Rothman N (2006) Polymorphisms in oxidative stress genes and risk for non-Hodgkin lymphoma. Carcinogenesis 27(9):1828–1834. doi:10.​1093/​carcin/​bgl013 CrossRefPubMed
30.
Zurück zum Zitat Jang SH, Lim JW, Kim H (2009) Beta-carotene inhibits Helicobacter pylori-induced expression of inducible nitric oxide synthase and cyclooxygenase-2 in human gastric epithelial AGS cells. J Physiol Pharmacol: Off J Polish Physiol Soc 60(Suppl 7):131–137 Jang SH, Lim JW, Kim H (2009) Beta-carotene inhibits Helicobacter pylori-induced expression of inducible nitric oxide synthase and cyclooxygenase-2 in human gastric epithelial AGS cells. J Physiol Pharmacol: Off J Polish Physiol Soc 60(Suppl 7):131–137
31.
Zurück zum Zitat Zhang X, Spiegelman D, Baglietto L, Bernstein L, Boggs DA, van den Brandt PA, Buring JE, Gapstur SM, Giles GG, Giovannucci E, Goodman G, Hankinson SE, Helzlsouer KJ, Horn-Ross PL, Inoue M, Jung S, Khudyakov P, Larsson SC, Lof M, McCullough ML, Miller AB, Neuhouser ML, Palmer JR, Park Y, Robien K, Rohan TE, Ross JA, Schouten LJ, Shikany JM, Tsugane S, Visvanathan K, Weiderpass E, Wolk A, Willett WC, Zhang SM, Ziegler RG, Smith-Warner SA (2012) Carotenoid intakes and risk of breast cancer defined by estrogen receptor and progesterone receptor status: a pooled analysis of 18 prospective cohort studies. Am J Clin Nutr 95(3):713–725. doi:10.3945/ajcn.111.014415 CrossRefPubMedPubMedCentral Zhang X, Spiegelman D, Baglietto L, Bernstein L, Boggs DA, van den Brandt PA, Buring JE, Gapstur SM, Giles GG, Giovannucci E, Goodman G, Hankinson SE, Helzlsouer KJ, Horn-Ross PL, Inoue M, Jung S, Khudyakov P, Larsson SC, Lof M, McCullough ML, Miller AB, Neuhouser ML, Palmer JR, Park Y, Robien K, Rohan TE, Ross JA, Schouten LJ, Shikany JM, Tsugane S, Visvanathan K, Weiderpass E, Wolk A, Willett WC, Zhang SM, Ziegler RG, Smith-Warner SA (2012) Carotenoid intakes and risk of breast cancer defined by estrogen receptor and progesterone receptor status: a pooled analysis of 18 prospective cohort studies. Am J Clin Nutr 95(3):713–725. doi:10.​3945/​ajcn.​111.​014415 CrossRefPubMedPubMedCentral
32.
Zurück zum Zitat Mannisto S, Smith-Warner SA, Spiegelman D, Albanes D, Anderson K, van den Brandt PA, Cerhan JR, Colditz G, Feskanich D, Freudenheim JL, Giovannucci E, Goldbohm RA, Graham S, Miller AB, Rohan TE, Virtamo J, Willett WC, Hunter DJ (2004) Dietary carotenoids and risk of lung cancer in a pooled analysis of seven cohort studies. Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 13(1):40–48CrossRef Mannisto S, Smith-Warner SA, Spiegelman D, Albanes D, Anderson K, van den Brandt PA, Cerhan JR, Colditz G, Feskanich D, Freudenheim JL, Giovannucci E, Goldbohm RA, Graham S, Miller AB, Rohan TE, Virtamo J, Willett WC, Hunter DJ (2004) Dietary carotenoids and risk of lung cancer in a pooled analysis of seven cohort studies. Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 13(1):40–48CrossRef
35.
36.
Zurück zum Zitat Basu M, Banerjee A, Bhattacharya UK, Bishayee A, Chatterjee M (2000) Beta-carotene prolongs survival, decreases lipid peroxidation and enhances glutathione status in transplantable murine lymphoma. Phytomedicine : Int J Phytother Phytopharmacology 7(2):151–159. doi:10.1016/S0944-7113(00)80088-4 CrossRef Basu M, Banerjee A, Bhattacharya UK, Bishayee A, Chatterjee M (2000) Beta-carotene prolongs survival, decreases lipid peroxidation and enhances glutathione status in transplantable murine lymphoma. Phytomedicine : Int J Phytother Phytopharmacology 7(2):151–159. doi:10.​1016/​S0944-7113(00)80088-4 CrossRef
37.
Zurück zum Zitat Molnar J, Gyemant N, Mucsi I, Molnar A, Szabo M, Kortvelyesi T, Varga A, Molnar P, Toth G (2004) Modulation of multidrug resistance and apoptosis of cancer cells by selected carotenoids. In vivo 18(2):237–244PubMed Molnar J, Gyemant N, Mucsi I, Molnar A, Szabo M, Kortvelyesi T, Varga A, Molnar P, Toth G (2004) Modulation of multidrug resistance and apoptosis of cancer cells by selected carotenoids. In vivo 18(2):237–244PubMed
Metadaten
Titel
Carotenoid intake and risk of non-Hodgkin lymphoma: a systematic review and dose-response meta-analysis of observational studies
verfasst von
Feifei Chen
Jiyi Hu
Ping Liu
Jing Li
Zheng Wei
Peng Liu
Publikationsdatum
24.12.2016
Verlag
Springer Berlin Heidelberg
Erschienen in
Annals of Hematology / Ausgabe 6/2017
Print ISSN: 0939-5555
Elektronische ISSN: 1432-0584
DOI
https://doi.org/10.1007/s00277-016-2898-1

Weitere Artikel der Ausgabe 6/2017

Annals of Hematology 6/2017 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.