Feed Composition Differences Resulting from Organic and Conventional Farming Practices Affect Physiological Parameters in Wistar Rats-Results from a Factorial, Two-Generation Dietary Intervention Trial
Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
506358
Sixth Framework Programme
6046137305
Ministry of Education of the Czech Republic
no grant number
Sheepdrove Trust
PubMed
33530419
PubMed Central
PMC7911726
DOI
10.3390/nu13020377
PII: nu13020377
Knihovny.cz E-zdroje
- Klíčová slova
- cadmium, conventional feed, hormonal balance, immune system responsiveness, mineral fertilizer, organic feed, pesticides, rat physiology,
- MeSH
- biopotraviny * MeSH
- dieta * MeSH
- draslík MeSH
- dusík MeSH
- farmy MeSH
- fenotyp MeSH
- fosfor MeSH
- hnůj MeSH
- kadmium MeSH
- krmivo pro zvířata analýza MeSH
- krysa rodu Rattus MeSH
- lidé MeSH
- pesticidy MeSH
- pěstování plodin * MeSH
- potkani Wistar MeSH
- přijímání potravy MeSH
- průmyslová hnojiva MeSH
- zemědělské plodiny chemie MeSH
- zemědělství metody MeSH
- zvířata MeSH
- Check Tag
- krysa rodu Rattus MeSH
- lidé MeSH
- mužské pohlaví MeSH
- ženské pohlaví MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- Geografické názvy
- Spojené království MeSH
- Názvy látek
- draslík MeSH
- dusík MeSH
- fosfor MeSH
- hnůj MeSH
- kadmium MeSH
- pesticidy MeSH
- průmyslová hnojiva MeSH
Recent human cohort studies reported positive associations between organic food consumption and a lower incidence of obesity, cancer, and several other diseases. However, there are very few animal and human dietary intervention studies that provide supporting evidence or a mechanistic understanding of these associations. Here we report results from a two-generation, dietary intervention study with male Wistar rats to identify the effects of feeds made from organic and conventional crops on growth, hormonal, and immune system parameters that are known to affect the risk of a number of chronic, non-communicable diseases in animals and humans. A 2 × 2 factorial design was used to separate the effects of contrasting crop protection methods (use or non-use of synthetic chemical pesticides) and fertilizers (mineral nitrogen, phosphorus and potassium (NPK) fertilizers vs. manure use) applied in conventional and organic crop production. Conventional, pesticide-based crop protection resulted in significantly lower fiber, polyphenol, flavonoid, and lutein, but higher lipid, aldicarb, and diquat concentrations in animal feeds. Conventional, mineral NPK-based fertilization resulted in significantly lower polyphenol, but higher cadmium and protein concentrations in feeds. Feed composition differences resulting from the use of pesticides and/or mineral NPK-fertilizer had a significant effect on feed intake, weight gain, plasma hormone, and immunoglobulin concentrations, and lymphocyte proliferation in both generations of rats and in the second generation also on the body weight at weaning. Results suggest that relatively small changes in dietary intakes of (a) protein, lipids, and fiber, (b) toxic and/or endocrine-disrupting pesticides and metals, and (c) polyphenols and other antioxidants (resulting from pesticide and/or mineral NPK-fertilizer use) had complex and often interactive effects on endocrine, immune systems and growth parameters in rats. However, the physiological responses to contrasting feed composition/intake profiles differed substantially between the first and second generations of rats. This may indicate epigenetic programming and/or the generation of "adaptive" phenotypes and should be investigated further.
Department of Animal Physiology Faculty of Biology University of Warsaw 02 096 Warsaw Poland
Department of Haematology Oslo University Hospital 0424 Oslo Norway
Department of Nutrition Institute of Basic Medical Sciences University of Oslo 0372 Oslo Norway
Faculty of Engineering and Natural Sciences Sabanci University 34956 Istanbul Turkey
Human Nutrition Research Centre Institute of Cellular Medicine Newcastle upon Tyne NE2 4HH UK
NatMed Southern Cross University Military Rd Lismore NSW 2480 Australia
SCU Plant Science Southern Cross University Military Rd Lismore NSW 2480 Australia
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Barański M., Średnicka-Tober D., Volakakis N., Seal C., Sanderson R., Stewart G.B., Benbrook C., Biavati B., Markellou E., Giotis C., et al. Higher antioxidant and lower cadmium concentrations and lower incidence of pesticide residues in organically grown crops: A systematic literature review and meta-analyses. Br. J. Nutr. 2014;112:794–811. doi: 10.1017/S0007114514001366. PubMed DOI PMC
Średnicka-Tober D., Barański M., Seal C., Sanderson R., Benbrook C., Steinshamn H., Gromadzka-Ostrowska J., Rembiałkowska E., Skwarło-Sońta K., Eyre M., et al. Composition differences between organic and conventional meat: A systematic literature review and meta-analysis. Br. J. Nutr. 2016;115:994–1011. doi: 10.1017/S0007114515005073. PubMed DOI PMC
Średnicka-Tober D., Barański M., Seal C.J., Sanderson R., Benbrook C., Steinshamn H., Gromadzka-Ostrowska J., Rembiałkowska E., Skwarło-Sońta K., Eyre M., et al. Higher PUFA and n-3 PUFA, conjugated linoleic acid, α-tocopherol and iron, but lower iodine and selenium concentrations in organic milk: A systematic literature review and meta- and redundancy analyses. Br. J. Nutr. 2016;115:1043–1060. doi: 10.1017/S0007114516000349. PubMed DOI PMC
Sander J.F., Heitefuss R. Suceptibility to Erysiphe graminis f.sp tritici and phenolic acid content of wheat as influenced by different levels of nitrogen fertilization. J. Phytopathol. 1998;146:495–507. doi: 10.1111/j.1439-0434.1998.tb04611.x. DOI
Cooper J., Sanderson R., Cakmak I., Ozturk L., Shotton P., Carmichael A., Haghighi R.S., Tetard-Jones C., Volakakis N., Eyre M., et al. Effect of organic and conventional crop rotation, fertilization, and crop protection practices on metal contents in wheat (Triticum aestivum) J. Agric. Food Chem. 2011;59:4715–4724. doi: 10.1021/jf104389m. PubMed DOI
Rempelos L., Almuayrifi A.M., Baranski M., Tetard-Jones C., Eyre M., Shotton P., Cakmak I., Ozturk L., Cooper J., Volakakis N., et al. Effects of agronomic management and climate on leaf phenolic profiles, disease severity and grain yield in organic and conventional wheat production systems. J. Agric. Food Chem. 2018;66:10369–10379. doi: 10.1021/acs.jafc.8b02626. PubMed DOI
Rempelos L., Almuayrifi M.S.B., Baranski M., Tetard-Jones C., Barkla B., Cakmak I., Ozturk L., Cooper J., Volakakis N., Hall G., et al. The effect of agronomic factors on crop health and performance of winter wheat varieties bred for the conventional and the low input farming sector. Field Crops Res. 2020;254:107822. doi: 10.1016/j.fcr.2020.107822. DOI
Baker B.P., Benbrook C.M., Groth E., 3rd, Benbrook K.L. Pesticide residues in conventional, integrated pest management (IPM)-grown and organic foods: Insights from three US data sets. Food Addit. Contam. 2002;19:427–446. doi: 10.1080/02652030110113799. PubMed DOI
Wang J., Hasanalieva G., Wood L., Anagnostopoulos C., Ampadogiannis G., Bempelou E., Kiousi M., Markellou E., Iversen P.O., Seal C., et al. Effect of wheat species (Triticum aestivum vs T. spelta), farming system (organic vs conventional) and flour type (wholegrain vs white) on composition of wheat flour—Results of a retail survey in the UK and Germany—3. Pesticide residue content. Food Chem. X. 2020:100089. doi: 10.1016/j.fochx.2020.100089. PubMed DOI PMC
Montonen J., Järvinen R., Knekt O., Reunanen A. Dietary antioxidant intake and risk of type 2 diabetes. Diabetes Care. 2004;27:362–366. doi: 10.2337/diacare.27.2.362. PubMed DOI
Abdali D., Samson S.E., Grover A.K. How effective are antioxidant supplements in obesity and diabetes. Med. Princ. Pract. 2015;24:201–215. doi: 10.1159/000375305. PubMed DOI PMC
Perez M.C., Knisley B.D., Crosby G.E., Zheng S., Barth M. Obesity prevalence and dietary intake of antioxidants in native American adolescents. IJPHS. 2016;5:222–227. doi: 10.11591/ijphs.v5i3.4788. DOI
Stenzel A.P., Carvalho R., Jesus P., Bull A., Pereira S., Soboya C., Ramalho A. Serum antioxidant associations with metabolic characteristics in metabolically healthy and unhealthy adolescents with severe obesity: An observational study. Nutrients. 2018;10:150. doi: 10.3390/nu10020150. PubMed DOI PMC
Pantavos A., Ruiter R., Feskens E.F., de Keyser C.E., Hofman A., Stricker B.H., Franco O.H., Kiefte-de Jong J.C. Total dietary antioxidant capacity, individual antioxidant intake and breast cancer risk: The Rotterdam study. Int. J. Cancer. 2014;136:2178–2186. doi: 10.1002/ijc.29249. PubMed DOI
Egnell M., Fassier P., Lécuyer L., Gonzales R., Zelek L., Vasson M.P., Hercberg S., Latino-Martel P., Galan P., Druesne-Pecollo N., et al. Antioxidant intake from diet and supplements and risk of digestive cancers in middle-aged adults: Results from the prospective NutriNet-Santé cohort. Br. J. Nutr. 2017;118:541–549. doi: 10.1017/S0007114517002392. PubMed DOI
Brantsæter A.L., Haugen M., Samuelsen S.O., Torjusen H., Trogstad L., Alexander J., Magnus P., Meltzer H.M. A dietary pattern characterized by high intake of vegetables, fruits, and vegetable oils is associated with reduced risk of preeclampsia in nulliparous pregnant norwegian women. J. Nutr. 2009;139:1162–1168. doi: 10.3945/jn.109.104968. PubMed DOI PMC
Patel S., Murray C.S., Woodcock A., Simpson A., Custovic A. Dietary antioxidant intake, allergic sensitisation and allergic diseases in young children. Allergy. 2009;64:1766–1772. doi: 10.1111/j.1398-9995.2009.02099.x. PubMed DOI
Kao Y.-H., Hiipakka R.A., Liao S. modulation of endocrine systems and food intake by green tea epigallocatechin gallate. Endocrinology. 2000;141:980–987. doi: 10.1210/endo.141.3.7368. PubMed DOI
Alavanja M.C.R., Hoppin J.A., Kamel F. Health effects of chronic pesticide exposure: Cancer and neurotoxicity. Annu. Rev. Public Health. 2004;25:155–197. doi: 10.1146/annurev.publhealth.25.101802.123020. PubMed DOI
Bassil K.L., Vakil C., Sanborn M., Cole D.C., Kaur J.S., Kerr K.J. Cancer health effects of pesticides. Can. Fam. Physician. 2007;53:1704–1711. PubMed PMC
Mnif W., Hassine A.I.H., Bouaziz A., Bartegi A., Thomas O., Roig B. Effect of endocrine disruptor pesticides: A review. Int. J. Environ. Res. Public Health. 2011;8:2265–2303. doi: 10.3390/ijerph8062265. PubMed DOI PMC
Rocheleau C.M., Romitti P.A., Dennis L.K. Pesticides and hypospadias: A meta-analysis. J. Pediatr. Urol. 2009;5:17–24. doi: 10.1016/j.jpurol.2008.08.006. PubMed DOI PMC
Guyton K.Z., Loomis D., Grosse Y., Ghissassi F.E., Benbrahim-Tallaa L., Guha N., Scoccianti C., Mattock H., Straif K. Carcinogenicity of tetrachlorvinphos, parathion, malathion, diazinon, and glyphosate. Lancet Oncol. 2015;16:490–491. doi: 10.1016/S1470-2045(15)70134-8. PubMed DOI
Petrakis D., Vassilopoulou L., Mamoulakis C., Psycharakis C., Anifantaki A., Sifakis S., Docea A.O., Tsiaoussis J., Makrigiannakis A., Tsatsakis A.M. Endocrine disruptors leading to obesity and related diseases. Int. J. Environ. Res. Public Health. 2017;14:1282. doi: 10.3390/ijerph14101282. PubMed DOI PMC
Chiu Y.H., Afeiche M.C., Gaskins A.J., Williams P.L., Petrozza J.C., Tanrikut C., Hauser R., Chavarro J.E. Fruit and vegetable intake and their pesticide residues in relation to semen quality among men from a fertility clinic. Hum. Reprod. 2018;30:1342–1351. doi: 10.1093/humrep/dev064. PubMed DOI PMC
Chiu Y.H., Williams P.L., Gillman M.W., Gaskins A.J., Mínguez-Alarcón L., Souter I., Toth T.L., Ford J.B., Hauser R., Chavarro J.E. Association between pesticide residue intake from consumption of fruits and vegetables and pregnancy outcomes among women undergoing infertility treatment with assisted reproductive technology. JAMA Intern. Med. 2018;178:17–26. doi: 10.1001/jamainternmed.2017.5038. PubMed DOI PMC
Mokarizadeh A., Faryabi M.R., Rezvanfar M.A., Abdollahi M. A comprehensive review of pesticides and the immune dysregulation: Mechanisms, evidence and consequences. Toxicol. Mech. Methods. 2015;25:258–278. doi: 10.3109/15376516.2015.1020182. PubMed DOI
Hamilton D., Ambrus A., Dieterle R., Felsot A., Harris C., Petersen B., Racke K., Wong S.-S., Gonzalez R., Tanaka K., et al. Pesticide residues in food—Acute dietary exposure. Pest Manag. Sci. 2004;60:311–339. doi: 10.1002/ps.865. PubMed DOI
Winter C.K. Chronic dietary exposure to pesticide residues in the United States. Int. J. Food Contam. 2015;2:11. doi: 10.1186/s40550-015-0018-y. DOI
Markantonis M., van der Velde-Koerts T., Graven C., Te Biesebeek J.D., Zeilmaker M., Rietveld A.G., Ossendorp B.C. Assessment of occupational and dietary exposure to pesticide residues. EFSA J. 2018;16:e16087. doi: 10.2903/j.efsa.2018.e16087. PubMed DOI PMC
Heindel J.J., vom Saal F.S. Role of nutrition and environmental endocrine disrupting chemicals during the prerinatal period on the aetiology of obesity. Mol. Cell. Endocrinol. 2009;304:90–96. doi: 10.1016/j.mce.2009.02.025. PubMed DOI
Schug T.T., Janesick A., Blumberg B., Heindel J.J. Endocrine Disrupting Chemicals and Disease Susceptibility. J. Steroid Biochem. Mol. Biol. 2011;127:204–215. doi: 10.1016/j.jsbmb.2011.08.007. PubMed DOI PMC
Yang O., Kim H.L., Weon J.I., Seo Y.R. Endocrine-disrupting chemicals: Review of toxicological mechanisms using molecular pathway analysis. J. Cancer Prev. 2015;20:12–24. doi: 10.15430/JCP.2015.20.1.12. PubMed DOI PMC
Xin F., Susiarjo M., Bartolomei M.S. Multigenerational and transgenerational effects of endocrine disrupting chemicals: A role for altered epigenetic regulation? Semin. Cell Dev. Biol. 2015;43:66–75. doi: 10.1016/j.semcdb.2015.05.008. PubMed DOI PMC
Satarug S., Moore M.R. Adverse Health Effects of Chronic Exposure to Low-Level Cadmium in Foodstuffs and Cigarette Smoke. Environ. Health Perspect. 2004;112:1099–1103. doi: 10.1289/ehp.6751. PubMed DOI PMC
Lugon-Moulin N., Ryan L., Donini P., Rossi L. Cadmium content of phosphorus fertilizers used for tobacco production. Agron. Sustain. Dev. 2006;26:151–155. doi: 10.1051/agro:2006010. DOI
Henson M.C., Chedrese P.J. Endocrine disruption by cadmium, a common environmental toxicant with paradoxical effects on reproduction. Exp. Biol. Med. 2004;229:383–392. doi: 10.1177/153537020422900506. PubMed DOI
Borello P., Giardino A. Lead and cadmium at very low doses affect in vitro immune response of human lymphocytes. Environ. Res. 1991;55:165–177. doi: 10.1016/S0013-9351(05)80173-2. PubMed DOI
Hemdan N.Y., Emmrich F., Sack U., Wichmann G., Lehmann J., Adham K., Lehmann I. The in vitro immune modulation by cadmium depends on the way of cell activation. Toxicology. 2006;222:37–45. doi: 10.1016/j.tox.2006.01.026. PubMed DOI
Gerhard I., Waibel S., Daniel V., Runnebaum B. Impact of heavy metals on hormonal and immunological factors in women with repeated miscarriages. Hum. Reprod. Update. 1998;4:301–309. doi: 10.1093/humupd/4.3.301. PubMed DOI
Porter W.P., Jaeger J.W., Carlson I.H. Endocrine, immune and behavioral effects of aldicarb (carbamate), atrazine (triazine) and nitrate (fertilizer) mixtures at groundwater concentrations. Toxicol. Ind. Health. 1999;15:133–151. doi: 10.1191/074823399678846691. PubMed DOI
Goel A., Chauhan D.P., Dhawan D.K. Protective effects of Zinc in chlorpyriphos induced hapatoxicity: A biochemical and trace elemental study. Biol. Trace Elem. Res. 2000;74:171–183. doi: 10.1385/BTER:74:2:171. PubMed DOI
Hazarika A., Sarkar S.N., Hajare S., Kataria M., Malik J.K. Influence of malathion pretreatment on the toxicity of anilofos in male rats: A biochemical interaction study. Toxicology. 2003;185:1–8. doi: 10.1016/S0300-483X(02)00574-7. PubMed DOI
Kortenkamp A. Ten years of mixing cocktails: A review of combination effects of endocrine-disrupting chemicals. Environ. Health Perspect. 2007;115:98–105. doi: 10.1289/ehp.9357. PubMed DOI PMC
Astiz M., de Alaniz M.J.T., Marra C.A. Antioxidant defence system in rats simultaneously intoxicated with agrochemicals. Environ. Toxicol. Pharmacol. 2009;28:465–473. doi: 10.1016/j.etap.2009.07.009. PubMed DOI
Bradbury K.E., Balkwill A., Spencer E.A., Roddam A.W., Reeves G.K., Green J., Key T.J., Beral V., Pirie K. Organic food consumption and the incidence of cancer in a large prospective study of women in the United Kingdom. Br. J. Cancer. 2014;110:2321–2326. doi: 10.1038/bjc.2014.148. PubMed DOI PMC
Christensen J.S., Asklund C., Skakkebaek N.E., Jorgensen N., Andersen H.R., Jorgensen T.M., Olsen L.H., Hoyer A.P., Moesgaard J., Thorup J., et al. Association between organic dietary choice during pregnancy and hypospadias in offspring: A study of mothers of 306 boys operated on for hypospadias. J. Urol. 2013;189:1077–1082. doi: 10.1016/j.juro.2012.09.116. PubMed DOI
Torjusen H., Brantsæter A.L., Haugen M., Alexander J., Bakketeig L.S., Lieblein G., Stigum H., Næs T., Swartz J., Holmboe-Ottesen G., et al. Reduced risk of pre-eclampsia with organic vegetable consumption: Results from the prospective Norwegian Mother and Child Cohort Study. BMJ Open. 2014;4 doi: 10.1136/bmjopen-2014-006143. PubMed DOI PMC
Brantsæter A.L., Torjusen H., Meltzer H.M., Papadopoulou E., Hoppin J.A., Alexander J., Lieblein G., Roos G., Holten J.M., Swartz J., et al. Organic food consumption during pregnancy and hypospadias and cryptorchidism at birth: The Norwegian Mother and Child Cohort Study (MoBa) Environ. Health Perspect. 2016;124:357–364. doi: 10.1289/ehp.1409518. PubMed DOI PMC
Kesse-Guyot E., Baudry J., Assmann K.E., Galan P., Hercberg S., Lairon D. Prospective association between consumption frequency of organic food and body weight change, risk of overweight or obesity: Results from the NutriNet-Santé Study. Br. J. Nutr. 2017;117:325–334. doi: 10.1017/S0007114517000058. PubMed DOI
Baudry J., Lelong H., Adriouch S., Julia C., Allès B., Hercberg S., Touvier M., Lairon D., Galan P., Kesse-Guyot E. Association between organic food consumption and metabolic syndrome: Cross-sectional results from the NutriNet-Santé study. Eur. J. Nutr. 2018;57:2477–2488. doi: 10.1007/s00394-017-1520-1. PubMed DOI
Baudry J., Assmann K.E., Touvier M., Allès B., Seconda L., Latino-Martel P., Ezzedine K., Galan P., Hercberg S., Lairon D., et al. Association of frequency of organic food consumption with cancer risk Findings from the NutriNet-Sante prospective cohort Study. JAMA Intern. Med. 2018;178:1597–1606. doi: 10.1001/jamainternmed.2018.4357. PubMed DOI PMC
Vigar V., Myers S., Oliver C., Arellano J., Robinson S., Leifert C. A Systematic Review of Organic Versus Conventional Food Consumption: Is There a Measurable Benefit on Human Health? Nutrients. 2020;12:7. doi: 10.3390/nu12010007. PubMed DOI PMC
Alm J.S., Swartz J., Lilja G., Scheynius A., Pershagen G. Atopy in children of families with an anthroposophic lifestyle. Lancet. 1999;353:1485–1488. doi: 10.1016/S0140-6736(98)09344-1. PubMed DOI
Flöistrup H., Swartz J., Bergström A., Michaels K.M., Pershagen G. Allergic disease and sensitization in Steiner school children. J. Allergy Clin. Immunol. 2006;117:59–66. doi: 10.1016/j.jaci.2005.09.039. PubMed DOI
Kesse-Guyot E., Peneau S., Mejean C., de Edelenyi F.S., Galan P., Hercberg S., Lairon D. Profiles of organic food consumers in a large sample of French Adults: Results from the Nutrinet-Santé cohort study. PLoS ONE. 2013;8:e76998. doi: 10.1371/journal.pone.0076998. PubMed DOI PMC
Baudry J., Méjean C., Allès B., Péneau S., Touvier M., Hercberg S., Lairon D., Galan P., Kesse-Guyot E. Contribution of organic food to the diet in a large sample of French adults (the NutriNet-Santé Cohort Study) Nutrients. 2015;7:8615–8632. doi: 10.3390/nu7105417. PubMed DOI PMC
Baudry J., Allès B., Péneau S., Touvier M., Méjean C., Hercberg S., Galan P., Lairon D., Kesse-Guyot E. Dietary intakes and diet quality according to levels of organic food consumption by French adults: Cross-sectional findings from the NutriNet-Santé Cohort Study. Public Health Nutr. 2017;20:638–648. doi: 10.1017/S1368980016002718. PubMed DOI PMC
Srednicka-Tober D., Barański M., Gromadzka-Ostrowska J., Skwarło-Sońta K., Rembiałkowska E., Hajslova J., Schulzova V., Çakmak I., Öztürk L., Królikowski T., et al. Effect of crop protection and fertilization regimes used in organic and conventional production systems on feed composition and physiological parameters in rats. J. Agric. Food Chem. 2013;61:1017–1029. doi: 10.1021/jf303978n. PubMed DOI
Wang J., Chatzidimitriou E., Wood L., Hasanalieva G., Markellou E., Iversen P.O., Seal C., Baranski M., Vigar V., Ernst L., et al. Effect of wheat species (Triticum aestivum vs. T. spelta), farming system (organic vs conventional) and flour type (wholegrain vs white) on composition of wheat flour—Results of a retail survey in the UK and Germany—2. Antioxidant activity, and phenolic and mineral content. Food Chem. X. 2020;6:100091. doi: 10.1016/j.fochx.2020.100091. PubMed DOI PMC
Palmer M.W., Cooper J., Tétard-Jones C., Średnicka-Tober D., Barański M., Eyre M., Shotton P.N., Volakakis N., Cakmak I., Ozturk L., et al. The influence of organic and conventional fertilisation and crop protection practices, preceding crop, harvest year and weather conditions on yield and quality of potato (Solanum tuberosum) in a long-term management trial. Eur. J. Agron. 2013;49:83–92. doi: 10.1016/j.eja.2013.03.004. DOI
Dunn G.A., Bale T.L. Maternal high-fat diet effects on third-generation female body size via the paternal lineage. Endocrinology. 2011;152:2228–2236. doi: 10.1210/en.2010-1461. PubMed DOI PMC
Parlee S.D., MacDougald O.A. Maternal nutrition and risk of obesity in offspring: The Trojan horse of developmental plasticity. Biochim. Biophys. Acta Mol. Basis Dis. 2014;1842:495–506. doi: 10.1016/j.bbadis.2013.07.007. PubMed DOI PMC
Alavian-Ghavanni A., Rüegg J. Understanding epigenetic effects of endocrine disrupting chemicals: From mechanism to novel test methods. Basic Clin. Pharmacol. Toxicol. 2018;122:38–45. doi: 10.1111/bcpt.12878. PubMed DOI
Wang S., Moustaid-Moussa N., Chen L., Mo H., Shastri A., Su R., Bapat P., Kwun I., Shen C.-L. Novel insights of dietary polyphenols and obesity. J. Nutr. Biochem. 2014;25:1–18. doi: 10.1016/j.jnutbio.2013.09.001. PubMed DOI PMC
Tinkov A.A., Filippini T., Ajsuvakova O.P., Aaseth J., Gluhcheva Y.G., Ivanova J.M., Bjørklund G., Skalnaya M.G., Gatiatulina E.R., Popova E.V., et al. The role of cadmium in obesity and diabetes. Sci. Total Environ. 2017;601:741–755. doi: 10.1016/j.scitotenv.2017.05.224. PubMed DOI
Tian Y., Liu Y., Zhou Y., Liu Y., Lü G., Zheng X., Xu D. Effect of aldicarb exposure on cellular immunity and antioxidant capacity in Kunming mice. Health. 2015;7:830–837. doi: 10.4236/health.2015.77098. DOI
NRC . Nutrient Requirements of Laboratory Animals. 4th ed. The National Academies Press; Washington, DC, USA: 1995. PubMed
AOAC . Official Methods of Analysis of the Association of Official Analytical Chemists. 15th ed. Association of Official Analytical Chemists; Washington, DC, USA: 1990.
Lauridsen C., Yong C., Halekoh U., Bügel S.H., Brandt K., Christensen L.P., Jørgensen H. Rats show differences in some biomarkers of health when eating diets based on ingredients produced with three different cultivation strategies. J. Sci. Food Agric. 2008;88:720–732. doi: 10.1002/jsfa.3142. DOI
Harris R.B., Kelso E.W., Flatt W.P., Grill H.J., Bartness T.J. Testosterone replacement does not normalize carcass composition in chronically decerebrate male rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2009;296:1687–1694. doi: 10.1152/ajpregu.00019.2009. PubMed DOI PMC
Kanashiro-Takeuchi R.M., Tziomalos K., Takeuchi L.M., Treuer A.V., Lamirault G., Dulce R., Hurtado M., Song Y., Block N.L., Rick F., et al. Cardioprotective effects of growth hormone-releasing hormone agonist after myocardial infarction. Proc. Natl. Acad. Sci. USA. 2010;107:2604–2609. doi: 10.1073/pnas.0914138107. PubMed DOI PMC
Pinheiro J.C., Bates D.M. Mixed-Effects Models in S and S-PLUS. Springer; New York, NY, USA: 2000.
Crawley M.J. The R Book. John Wiley & Sons, Ltd.; Chichester, UK: 2007.
Ter Braak C.J.F., Smilauer P. CANOCO Reference Manual and User’s Guide to Canoco for Windows: Software for Canonical Community Ordination. Centre for Biometry; Wageningen, The Netherlands: 1998. Version 4.
Hasanaliyeva G., Chatzidimitrou E., Wang J., Baranski M., Volakakis N., Seal C., Rosa E.A.S., Iversen P.O., Vigar V., Barkla B., et al. Effects of Production Region, Production Systems and Grape Type/Variety on Nutritional Quality Parameters of Table Grapes; Results from a UK Retail Survey. Foods. 2020;9:1874. doi: 10.3390/foods9121874. PubMed DOI PMC
Lueck L., Schmidt C.S., Cooper J.M., Shotton P.N., Hajslova J., Schulzova V., Leifert C. Effect of organic, low-input and conventional production systems on pesticide and growth regulator residues in wheat, potato and cabbage. In: Niggli U., Leifert C., Alfoeldi T., Lueck L., Willer H., editors. Improving Sustainability in Organic and Low Input Food Production Systems, Proceedings of the 3rd International Congress of the European Integrated Project Quality Low Input Food (QLIF), University of Hohenheim, Stuttgart, Germany, 20–23 March 2007. FiBL; Frick, Switzerland: 2007. [(accessed on 1 January 2021)]. pp. 96–99. Available online: https://www.researchgate.net/publication/255421475_Effect_of_organic_low-input_and_conventional_production_systems_on_pesticide_and_growth_regulator_residues_in_wheat_potato_and_cabbage.
Wootton-Beard P., Ryan L. Improving public health? The role of antioxidant-rich fruit and vegetable beverages. Food Res. Int. 2011;44:3135–3148. doi: 10.1016/j.foodres.2011.09.015. DOI
Wang H.J., Liu Z.P., Jia X.D., Chen H., Tan Y.J. Endocrine disruption of cadmium in rats using the OECD enhanced TG 407 test system. Biomed. Environ. Sci. 2014;27:950–959. doi: 10.3967/bes2014.135. PubMed DOI
Abbaspour N., Hurrell R., Kelishadi R. Review in iron and its importance for human health. J. Res. Med. Sci. 2014;19:164–174. PubMed PMC
Rose M.S., Crabtree H.C., Fletcher K., Wyatt I. Biochemical effects of diquat and paraquat. Disturbance of the control of corticosteroid synthesis in rat adrenal and subsequent effects on the control of liver glycogen utilization. Biochem. J. 1974;138:437–443. doi: 10.1042/bj1380437. PubMed DOI PMC
Marth E., Jelovcan S., Kleinhappl B., Gutschi A., Barth S. The effect of heavy metals on the immune system at low concentrations. Int. J. Occup. Environ. Health. 2001;14:375–386. PubMed
McKinlay R., Plant J.A., Bell J.N.B., Voulvoulis N. Endocrine disrupting pesticides: Implications for risk assessment. Environ. Int. 2008;34:168–183. doi: 10.1016/j.envint.2007.07.013. PubMed DOI
Grün F., Blumberg B. Endocrine disrupters as obesogens. Mol. Cell Endocrinol. 2009;304:19–29. doi: 10.1016/j.mce.2009.02.018. PubMed DOI PMC
Multigner L., Kadhel P., Pascal M., Huc-Terki F., Kercret H., Massart C., Janky E., Auger J., Jégou B. Parallel assessment of male reproductive function in workers and wild rats exposed to pesticides in banana planta-tions in Guadeloupe. Environ. Health. 2008;7:1–10. doi: 10.1186/1476-069X-7-40. PubMed DOI PMC
Hughes D.A. Dietary antioxidants and human immune function. Nutr. Bulletin. 2008;25:35–41. doi: 10.1046/j.1467-3010.2000.00016.x. DOI
Chen L., Qu G., Sun X., Zhang S., Wang L., Sang N., Du Y., Liu J., Sijin L. Characterization of the inter-action between cadmium and chlorpyrifos with integrative techniques in incurring synergistic hepatoxicity. PLoS ONE. 2013;8:e59553. doi: 10.1371/journal.pone.0059553. PubMed DOI PMC
Langhans W. Food components in health promotion and disease prevention. J. Agric. Food Chem. 2018;66:2287–2294. doi: 10.1021/acs.jafc.7b02121. PubMed DOI
Myers M.G., Jr., Leibel R.L., Seeley R.J., Schwartz M.W. Obesity and leptin resistance: Distinguishing cause from effect. Trends Endocrinol. Metab. 2010;21:643–651. doi: 10.1016/j.tem.2010.08.002. PubMed DOI PMC
Maurer A., Chen Q., McPherson C., Rainer R.A. Changes in satiety hormones and expression of genes involved in glucose and lipid metabolism in rats weaned onto diets high in fibre or protein reflect susceptibility to increased fat mass in adulthood. J. Physiol. 2009;587:679–691. doi: 10.1113/jphysiol.2008.161844. PubMed DOI PMC
Zhang R., Jiao J., Zhang W., Zhang Z., Zhang W., Qin L.-Q., Han S.-F. Effects of cereal fiber on leptin resistance and sensitivity in C57BL/6J mice fed a high-fat/cholesterol diet. Food Nutr. Res. 2016;60:31690. doi: 10.3402/fnr.v60.31690. PubMed DOI PMC
Nishijo M., Nakagawa H., Honda R., Tanebe K., Saito S., Teranishi H., Tawara K. Effects of maternal exposure to cadmium on pregnancy outcome and breast milk. Occup. Environ. Med. 2002;59:394–397. doi: 10.1136/oem.59.6.394. PubMed DOI PMC
Rebelo F.M., Caldas E.D. Arsenic, lead, mercury and cadmium: Toxicity, levels in breast milk and the risks for breastfed infants. Environ. Res. 2016;151:671–688. doi: 10.1016/j.envres.2016.08.027. PubMed DOI
Coutinho A.E., Chapman K.E. The anti-inflammatory and immunosuppressive effects of glucocorticoids, recent developments and mechanistic insights. Mol. Cell. Endocrinol. 2011;335:2–13. doi: 10.1016/j.mce.2010.04.005. PubMed DOI PMC
Blalock J.E. Shared ligands and receptors as a molecular mechanism for communication between the immune and neuroendocrine systems. Ann. N. Y. Acad Sci. 1994;741:292–298. doi: 10.1111/j.1749-6632.1994.tb23112.x. PubMed DOI
Procaccini C., Pucino V., De Rosa V., Marone G., Matarese G. Neuro-endocrine networks controlling immune system in health and disease. Front. Immunol. 2014;5:143. doi: 10.3389/fimmu.2014.00143. PubMed DOI PMC
Considine R.V., Sinha M.K., Heiman M.L., Kriauciunas A., Stephens T.W., Nyce M.R., Ohannesian J.P., Marco C.C., McKee L.J., Bauer T.L., et al. Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N. Engl. J. Med. 1996;334:292–295. doi: 10.1056/NEJM199602013340503. PubMed DOI
Wallace A.M., McMahon A.D., Packard C.J., Kelly A., Shepherd J., Gaw A., Sattar N. Plasma Leptin and the Risk of Cardiovascular Disease in the West of Scotland Coronary. Circulation. 2001;104:3052–3056. doi: 10.1161/hc5001.101061. PubMed DOI
Hamer M., Chida Y. Intake of fruit, vegetable, and antioxidants and risk of type 2 diabetes: Systematic review and meta-analysis. J. Hypertens. 2007;25:2361–2369. doi: 10.1097/HJH.0b013e3282efc214. PubMed DOI
Kadota A., Hozawa A., Okamura T., Kadowak T., Makmaura K., Murakami Y., Hayakawa T., Kita Y., Okayama A., Nakamura Y., et al. Relationship between metabolic risk factor clustering and cardiovascular Mortality stratified by high blood Glucose and obesity NIPPON DATA90, 1990–2000. Diabetes Care. 2007;30:1533–1538. doi: 10.2337/dc06-2074. PubMed DOI
Symonds M.E., Sebert S., Budge H. The obesity epidemic: From the environment to epigenetics—Not simply a response to dietary manipulation in a thermoneutral environment. Front. Genet. 2011;2:24. doi: 10.3389/fgene.2011.00024. PubMed DOI PMC
Ribaroff G.A., Wastnedge E., Drake A.J., Sharpe R.M., Chambers T.J.G. Animal models of maternal high fat diet exposure and effects on metabolism in offspring: A meta-regression analysis. Obes. Rev. 2017;18:673–686. doi: 10.1111/obr.12524. PubMed DOI PMC
Kohmura Y.K., Kanayama N., Muramatsu K., Tamura N., Yaguchi C., Uchida T., Suzuki K., Sugihara K., Aoe S., Sasaki T., et al. association between body weight at weaning and remodeling in the subcutaneous adipose tissue of obese adult mice with undernourishment in utero. Reprod. Sci. 2013;20:813–827. doi: 10.1177/1933719112466300. PubMed DOI PMC
Doo M., Kim Y. The consumption of dietary antioxidant vitamins modifies the risk of obesity among Korean men with short sleep Duration. Nutrients. 2017;9:780. doi: 10.3390/nu9070780. PubMed DOI PMC
Tang M. Protein Intake during the First Two Years of Life and Its Association with Growth and Risk of Overweight. Int. J. Environ. Res. Public Health. 2018;8:1742. doi: 10.3390/ijerph15081742. PubMed DOI PMC
Sarkies P. Molecular mechanisms of epigenetic inheritance: Possible evolutionary implications. Semin. Cell Dev. Biol. 2020;97:106–115. doi: 10.1016/j.semcdb.2019.06.005. PubMed DOI PMC
Dupont C., Armant D.R., Brenner C.A. Epigenetics: Definition, mechanisms and clinical perspective. Semin. Reprod. Med. 2009;27:351–357. doi: 10.1055/s-0029-1237423. PubMed DOI PMC
Plunk E.C., Richards S.M. Epigenetic modifications due to environment, ageing, nutrition, and endocrine disrupting chemicals and their effects on the endocrine system. Int. J. Endocrinol. 2020;2020:9251980. doi: 10.1155/2020/9251980. PubMed DOI PMC
Holliday R. Epigenetics: A historical overview. Epigenetics. 2006;1:76–80. doi: 10.4161/epi.1.2.2762. PubMed DOI
Kaufman P.D., Rando O.J. Chromatin as a potential carrier of heritable information. Curr. Opin. Cell Biol. 2010;22:284–290. doi: 10.1016/j.ceb.2010.02.002. PubMed DOI PMC
Bühler M. RNA turnover and chromatin-dependent gene silencing. Chromosoma. 2009;118:141–151. doi: 10.1007/s00412-008-0195-z. PubMed DOI
Harvey Z.H., Chen Y., Jarosz D.F. Protein-based inheritance: Epigenetics beyond the chromosome. Mol. Cell. 2018;69:195–202. doi: 10.1016/j.molcel.2017.10.030. PubMed DOI PMC
Milagro F.I., Mansego M.L., De Miguel C., Martínez J.A. Dietary factors, epigenetic modifications and obesity outcomes: Progresses and perspectives. Mol. Asp. Med. 2013;34:782–812. doi: 10.1016/j.mam.2012.06.010. PubMed DOI
Amarasekera M., Prescott S.L., Palmer D.J. Nutrition in early life, immune-programming and allergies. Asian Pac. J. Allergy Immunol. 2013;31:175–182. PubMed
Yong S.-B., Wu C.C., Wang L., Yang K. Influence and mechanisms of maternal and infant diets on the development of childhood asthma. Pediatrics Neonatol. 2013;54:5–11. doi: 10.1016/j.pedneo.2012.12.009. PubMed DOI
Bishop K.S., Ferguson L.R. The interaction between epigenetics, nutrition and the development of cancer. Nutrients. 2015;7:922–948. doi: 10.3390/nu7020922. PubMed DOI PMC
Topart C., Werner E., Arimondo P.B. Wandering along the epigenetic timeline. Clin. Epigenetics. 2020;12:97. doi: 10.1186/s13148-020-00893-7. PubMed DOI PMC
Choi S.-W., Friso S. Epigenetics: A new bridge between nutrition and health. Adv. Nutr. 2010;1:8–16. doi: 10.3945/an.110.1004. PubMed DOI PMC
Tryndyak V.P., Ross S.A., Beland F.A., Pogribny I.P. Down-regulation of the microRNAs miR-34a, miR-127, and miR-200b in rat liver during hepatocarcinogenesis induced by a methyl-deficient diet. Mol. Carcinog. 2009;48:479–487. doi: 10.1002/mc.20484. PubMed DOI
Gerhauser C. Impact of dietary gut microbial metabolites on the epigenome. Philos. Trans. R. Soc. B Biol. Sci. 2018;373:20170359. doi: 10.1098/rstb.2017.0359. PubMed DOI PMC
Fang M., Chen D., Yang C.S. Dietary polyphenols may affect DNA methylation. J. Nutr. 2007;137:223–228. doi: 10.1093/jn/137.1.223S. PubMed DOI
Wang L.-S., Arnold M., Huang Y.-W., Sardo C., Seguin C., Martin E., Huang T.H.-M., Riedl K., Schwartz S., Frankel W., et al. Modulation of genetic and epigenetic biomarkers of colorectal cancer in humans by black raspberries: A phase I pilot study. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 2011;17:598–610. doi: 10.1158/1078-0432.CCR-10-1260. PubMed DOI PMC
Pudenz M., Roth K., Gerhauser C. Impact of soy isoflavones on the epigenome in cancer prevention. Nutrients. 2014;6:4218–4272. doi: 10.3390/nu6104218. PubMed DOI PMC
Lascano S., Lopez M., Arimondo P.B. Natural products and chemical biology tools: Alternatives to target epigenetic mechanisms in cancers. Chem. Rec. 2018;18:1854–1876. doi: 10.1002/tcr.201800133. PubMed DOI
Donley N. The USA lags behind other agricultural nations in banning harmful pesticides. Environ. Health. 2019;18:1–12. doi: 10.1186/s12940-019-0488-0. PubMed DOI PMC
King A.J.F. The use of animal models in diabetes research. Br. J. Pharmacol. 2012;166:877–894. doi: 10.1111/j.1476-5381.2012.01911.x. PubMed DOI PMC
Buettner R., Schölmerich D., Bollheimer L.C. High-fat diets: Modelling the metabolic disorders of human obesity in rodents. Obesity. 2007;15:798–808. doi: 10.1038/oby.2007.608. PubMed DOI
Lutz T.A., Woods S.C. Overview of animal models for obesity. Curr. Protoc. Pharmacol. 2012;58:5–61. doi: 10.1002/0471141755.ph0561s58. PubMed DOI PMC