Serum Polychlorinated Biphenyls Increase and Oxidative Stress Decreases with a Protein-Pacing Caloric Restriction Diet in Obese Men and Women

Feng He, Li Zuo, Emery Ward, Paul J Arciero, Feng He, Li Zuo, Emery Ward, Paul J Arciero

Abstract

The purposes were to compare the effects of a: (1) 12-week P-CR weight loss (WL) diet (Phase 1) between obese men and women and; (2) 52-week modified P-CR (mP-CR) vs. heart healthy (HH) weight maintenance (WM) diet (Phase 2) on serum PCBs and oxidative stress biomarkers (thiobarbituric acid reactive substances, TBARS; total antioxidant capacity, TAC) in 40 obese participants (men, n = 21; women, n = 19). Participants received dietary counseling and monitoring of compliance. PCBs, TBARS, and TAC were assessed at weeks -1 (CON), 12 (WL), and 64 (WM). Following WL (Week 12), concomitant with reductions in TBARS (0.24 ± 0.15 vs. 0.18 ± 0.11 µM; p < 0.01), PCB serum concentrations (86.7 ± 45.6 vs. 115.6 ± 65.9 ng/g lipid; p < 0.01) and TAC (18.9 ± 2.6 vs. 19.9 ± 2.3 nmol/mL; p < 0.02) were increased similarly in men and women. At the end of WM (Week 64), a significant effect of time × group interaction was observed for % change in PCB 170 and 187; whereby mP-CR values were higher compared to HH (PCB170: 19.31% ± 26.48% vs. -6.61% ± 28.88%, p = 0.02; PCB187: -3.04% ± 17.78% vs. -21.4% ± 27.31%, p = 0.04). PCB changes were positively correlated with TBARS levels (r > 0.42, p < 0.05) and negatively correlated with body weight, fat mass, and abdominal fat (r < -0.46, p < 0.02). Our results support mobilization of stored PCBs as well as enhanced redox status following a 12-week P-CR WL diet. Additionally, a 52-week mP-CR WM diet demonstrated an advantage in preventing weight gain relapse accompanied by an increase in circulating PCBs compared to a traditional HH diet.

Keywords: caloric restriction; intermittent-fasting; oxidative stress; polychlorinated biphenyls (PCBs).

Conflict of interest statement

This study was supported by a grant from Isagenix International, LLC through an unrestricted research grant to Skidmore College and Paul J. Arciero. #13-086. Paul J. Arciero received honoraria for travel to present preliminary data from Isagenix International, Limited Liability Company (LLC). Paul J. Arciero is president and founder of PRISE LLC, a company marketing health and wellness solutions not related to any Isagenix products used in this study. There are no patents, products in development or marketed products to declare. All authors have no financial interests regarding the outcomes of this investigation. The funder had no roles in the study design, data collection and analysis, and decision to publish.

Figures

Figure 1
Figure 1
CONSORT of Participant Flow Chart.
Figure 2
Figure 2
Study Timeline.
Figure 3
Figure 3
Daily timing and meal content during Phase 1 (Weight Loss, WL; P-CR).
Figure 4
Figure 4
Total PCB concentration and body weight changes following Weight Loss Phase 1 (WL; P-CR, Weeks 0–12). * Significant difference compared to baseline (p < 0.01).
Figure 5
Figure 5
Percentage changes in PCB-170 (A) and PCB-187 (B) between mP-CR and HH groups following WM (Phase 2). * Significant group effect (mP-CR vs. HH; p < 0.05).

References

    1. Clifton P.M., Bastiaans K., Keogh J.B. High protein diets decrease total and abdominal fat and improve CVD risk profile in overweight and obese men and women with elevated triacylglycerol. Nutr. Metab. Cardiovasc. Dis. 2009;19:548–554. doi: 10.1016/j.numecd.2008.10.006.
    1. Kelishadi R., Hashemi M., Mohammadifard N., Asgary S., Khavarian N. Association of changes in oxidative and proinflammatory states with changes in vascular function after a lifestyle modification trial among obese children. Clin. Chem. 2008;54:147–153. doi: 10.1373/clinchem.2007.089953.
    1. Klempel M.C., Kroeger C.M., Bhutani S., Trepanowski J.F., Varady K.A. Intermittent fasting combined with calorie restriction is effective for weight loss and cardio-protection in obese women. Nutr. J. 2012;11:98. doi: 10.1186/1475-2891-11-98.
    1. Arciero P.J., Ormsbee M.J., Gentile C.L., Nindl B.C., Brestoff J.R., Ruby M. Increased protein intake and meal frequency reduces abdominal fat during energy balance and energy deficit. Obesity. 2013;21:1357–1366. doi: 10.1002/oby.20296.
    1. Due A., Toubro S., Skov A.R., Astrup A. Effect of normal-fat diets, either medium or high in protein, on body weight in overweight subjects: A randomised 1-year trial. Int. J. Obes. 2004;28:1283–1290. doi: 10.1038/sj.ijo.0802767.
    1. Arciero P.J., Edmonds R., He F., Ward E., Gumpricht E., Mohr A., Ormsbee M.J., Astrup A. Protein-pacing caloric-restriction enhances body composition similarly in obese men and women during weight loss and sustains efficacy during long-term weight maintenance. Nutrients. 2016;8 doi: 10.3390/nu8080476.
    1. Skov A.R., Toubro S., Ronn B., Holm L., Astrup A. Randomized trial on protein vs. carbohydrate in ad libitum fat reduced diet for the treatment of obesity. Int. J. Obes. 1999;23:528–536. doi: 10.1038/sj.ijo.0800867.
    1. Larsen T.M., Dalskov S.M., van Baak M., Jebb S.A., Papadaki A., Pfeiffer A.F., Martinez J.A., Handjieva-Darlenska T., Kunesova M., Pihlsgard M., et al. Diets with high or low protein content and glycemic index for weight-loss maintenance. N. Engl. J. Med. 2010;363:2102–2113. doi: 10.1056/NEJMoa1007137.
    1. Zuo L., He F., Tinsley G.M., Pannell B.K., Ward E., Arciero P.J. Comparison of high-protein, intermittent fasting low-calorie diet and heart healthy diet for vascular health of the obese. Front. Physiol. 2016;7:350. doi: 10.3389/fphys.2016.00350.
    1. Despres J.P., Couillard C., Gagnon J., Bergeron J., Leon A.S., Rao D.C., Skinner J.S., Wilmore J.H., Bouchard C. Race, visceral adipose tissue, plasma lipids, and lipoprotein lipase activity in men and women—The health, risk factors, exercise training, and genetics (heritage) family study. Arterioscler. Thromb. Vasc. 2000;20:1932–1938. doi: 10.1161/01.ATV.20.8.1932.
    1. Dirinck E.L., Dirtu A.C., Govindan M., Covaci A., Jorens P.G., van Gaal L.F. Endocrine-disrupting polychlorinated biphenyls in metabolically healthy and unhealthy obese subjects before and after weight loss: Difference at the start but not at the finish. Am. J. Clin. Nutr. 2016;103:989–998. doi: 10.3945/ajcn.115.119081.
    1. Roos V., Ronn M., Salihovic S., Lind L., van Bavel B., Kullberg J., Johansson L., Ahlstrom H., Lind P.M. Circulating levels of persistent organic pollutants in relation to visceral and subcutaneous adipose tissue by abdominal MRI. Obesity. 2013;21:413–418. doi: 10.1002/oby.20267.
    1. Dirtu A.C., Dirinck E., Malarvannan G., Neels H., van Gaal L., Jorens P.G., Covaci A. Dynamics of organohalogenated contaminants in human serum from obese individuals during one year of weight loss treatment. Environ. Sci. Technol. 2013;47:12441–12449. doi: 10.1021/es400657t.
    1. Kim M.J., Marchand P., Henegar C., Antignac J.P., Alili R., Poitou C., Bouillot J.L., Basdevant A., Le Bizec B., Barouki R., et al. Fate and complex pathogenic effects of dioxins and polychlorinated biphenyls in obese subjects before and after drastic weight loss. Environ. Health Perspect. 2011;119:377–383. doi: 10.1289/ehp.1002848.
    1. Arrebola J.P., Cuellar M., Claure E., Quevedo M., Antelo S.R., Mutch E., Ramirez E., Fernandez M.F., Olea N., Mercado L.A. Concentrations of organochlorine pesticides and polychlorinated biphenyls in human serum and adipose tissue from bolivia. Environ. Res. 2012;112:40–47. doi: 10.1016/j.envres.2011.10.006.
    1. Fernandez-Gonzalez R., Yebra-Pimentel I., Martinez-Carballo E., Simal-Gandara J. A critical review about human exposure to polychlorinated Dibenzo-p-Dioxins (PCDDs), polychlorinated dibenzofurans (PCDFs) and polychlorinated biphenyls (PCBs) through foods. Crit. Rev. Food Sci. 2015;55:1590–1617. doi: 10.1080/10408398.2012.710279.
    1. Charlier C., Desaive C., Plomteux G. Human exposure to endocrine disrupters: Consequences of gastroplasty on plasma concentration of toxic pollutants. Int. J. Obes. Relat. Metab. Disord. 2002;26:1465–1468. doi: 10.1038/sj.ijo.0802144.
    1. Golden R.J., Noller K.L., Titus-Ernstoff L., Kaufman R.H., Mittendorf R., Stillman R., Reese E.A. Environmental endocrine modulators and human health: An assessment of the biological evidence. Crit. Rev. Toxicol. 1998;28:109–227. doi: 10.1080/10408449891344191.
    1. Safe S.H. Polychlorinated biphenyls (PCBs): Environmental impact, biochemical and toxic responses, and implications for risk assessment. Crit. Rev. Toxicol. 1994;24:87–149. doi: 10.3109/10408449409049308.
    1. Imbeault P., Tremblay A., Simoneau J.A., Joanisse D.R. Weight loss-induced rise in plasma pollutant is associated with reduced skeletal muscle oxidative capacity. Am. J. Physiol. Endocrinol. Metab. 2002;282:E574–E579. doi: 10.1152/ajpendo.00394.2001.
    1. Meagher E.A., FitzGerald G.A. Indices of lipid peroxidation in vivo: Strengths and limitations. Free Radic. Biol. Med. 2000;28:1745–1750. doi: 10.1016/S0891-5849(00)00232-X.
    1. Ben Mansour R., Gargouri B., Bouaziz M., Elloumi N., Belhadj Jilani I., Ghrabi Z., Lassoued S. Antioxidant activity of ethanolic extract of inflorescence of ormenis africana in vitro and in cell cultures. Lipids Health Dis. 2011;10:78. doi: 10.1186/1476-511X-10-78.
    1. Enseleit F., Sudano I., Periat D., Winnik S., Wolfrum M., Flammer A.J., Frohlich G.M., Kaiser P., Hirt A., Haile S.R., et al. Effects of pycnogenol on endothelial function in patients with stable coronary artery disease: A double-blind, randomized, placebo-controlled, cross-over study. Eur. Heart J. 2012;33:1589–1597. doi: 10.1093/eurheartj/ehr482.
    1. Imbeault P., Chevrier J., Dewailly E., Ayotte P., Despres J.P., Tremblay A., Mauriege P. Increase in plasma pollutant levels in response to weight loss in humans is related to in vitro subcutaneous adipocyte basal lipolysis. Int. J. Obes. Relat. Metab. Disord. 2001;25:1585–1591. doi: 10.1038/sj.ijo.0801817.
    1. Chevrier J., Dewailly E., Ayotte P., Mauriege P., Despres J.P., Tremblay A. Body weight loss increases plasma and adipose tissue concentrations of potentially toxic pollutants in obese individuals. Int. J. Obes. Relat. Metab. Disord. 2000;24:1272–1278. doi: 10.1038/sj.ijo.0801380.
    1. Dirinck E., Dirtu A.C., Jorens P.G., Malarvannan G., Covaci A., Van Gaal L.F. Pivotal role for the visceral fat compartment in the release of persistent organic pollutants during weight loss. J. Clin. Endocrinol. Metab. 2015;100:4463–4471. doi: 10.1210/jc.2015-2571.
    1. Mullerova D., Matejkova D., Dvorakova J., Muller L., Rosmus J., Kovarova K. Persistent organochlorine pollutants in obese women after diet induced weight loss: Five years follow up study. Cent. Eur. J. Public Health. 2015;23:214–217.
    1. Cheikh Rouhou M., Karelis A.D., St-Pierre D.H., Lamontagne L. Adverse effects of weight loss: Are persistent organic pollutants a potential culprit? Diabetes Metab. 2016;42:215–223. doi: 10.1016/j.diabet.2016.05.009.
    1. De Roos A.J., Ulrich C.M., Sjodin A., McTiernan A. Adiposity, body composition, and weight change in relation to organochlorine pollutant plasma concentrations. J. Expo. Sci. Environ. Epidemiol. 2012;22:617–624. doi: 10.1038/jes.2012.43.
    1. Hue O., Marcotte J., Berrigan F., Simoneau M., Dore J., Marceau P., Marceau S., Tremblay A., Teasdale N. Increased plasma levels of toxic pollutants accompanying weight loss induced by hypocaloric diet or by bariatric surgery. Obes. Surg. 2006;16:1145–1154. doi: 10.1381/096089206778392356.
    1. Matsuda M., Shimomura I. Increased oxidative stress in obesity: Implications for metabolic syndrome, diabetes, hypertension, dyslipidemia, atherosclerosis, and cancer. Obes. Res. Clin. Pract. 2013;7:e330–e341. doi: 10.1016/j.orcp.2013.05.004.
    1. Li Q.Q., Loganath A., Chong Y.S., Tan J., Obbard J.P. Persistent organic pollutants and adverse health effects in humans. J. Toxicol. Environ. Health A. 2006;69:1987–2005.
    1. Faroon O.M., Keith S., Jones D., de Rosa C. Effects of polychlorinated biphenyls on development and reproduction. Toxicol. Ind. Health. 2001;17:63–93. doi: 10.1191/0748233701th097oa.
    1. Faroon O.M., Keith S., Jones D., de Rosa C. Carcinogenic effects of polychlorinated biphenyls. Toxicol. Ind. Health. 2001;17:41–62. doi: 10.1191/0748233701th098oa.
    1. Ghosh S., Mitra P.S., Loffredo C.A., Trnovec T., Murinova L., Sovcikova E., Ghimbovschi S., Zang S., Hoffman E.P., Dutta S.K. Transcriptional profiling and biological pathway analysis of human equivalence PCB exposure in vitro: Indicator of disease and disorder development in humans. Environ. Res. 2015;138:202–216. doi: 10.1016/j.envres.2014.12.031.
    1. Ghosh S., Zang S., Mitra P.S., Ghimbovschi S., Hoffman E.P., Dutta S.K. Global gene expression and ingenuity biological functions analysis on PCBs 153 and 138 induced human PBMC in vitro reveals differential mode(s) of action in developing toxicities. Environ. Int. 2011;37:838–857. doi: 10.1016/j.envint.2011.02.010.
    1. Mitra P.S., Ghosh S., Zang S., Sonneborn D., Hertz-Picciotto I., Trnovec T., Palkovicova L., Sovcikova E., Ghimbovschi S., Hoffman E.P., et al. Analysis of the toxicogenomic effects of exposure to persistent organic pollutants (pops) in Slovakian girls: Correlations between gene expression and disease risk. Environ. Int. 2012;39:188–199. doi: 10.1016/j.envint.2011.09.003.
    1. Krishnamoorthy G., Venkataraman P., Arunkumar A., Vignesh R.C., Aruldhas M.M., Arunakaran J. Ameliorative effect of vitamins (alpha-tocopherol and ascorbic acid) on PCB (aroclor 1254) induced oxidative stress in rat epididymal sperm. Reprod. Toxicol. 2007;23:239–245. doi: 10.1016/j.reprotox.2006.12.004.
    1. Selvakumar K., Bavithra S., Ganesh L., Krishnamoorthy G., Venkataraman P., Arunakaran J. Polychlorinated biphenyls induced oxidative stress mediated neurodegeneration in hippocampus and behavioral changes of adult rats: Anxiolytic-like effects of quercetin. Toxicol. Lett. 2013;222:45–54. doi: 10.1016/j.toxlet.2013.06.237.
    1. Selvakumar K., Bavithra S., Krishnamoorthy G., Venkataraman P., Arunakaran J. Polychlorinated biphenyls-induced oxidative stress on rat hippocampus: A neuroprotective role of quercetin. Sci. World J. 2012;2012:980314. doi: 10.1100/2012/980314.
    1. Selvakumar K., Bavithra S., Suganthi M., Benson C.S., Elumalai P., Arunkumar R., Krishnamoorthy G., Venkataraman P., Arunakaran J. Protective role of quercetin on pcbs-induced oxidative stress and apoptosis in hippocampus of adult rats. Neurochem. Res. 2012;37:708–721. doi: 10.1007/s11064-011-0661-5.
    1. Sridevi N., Venkataraman P., Senthilkumar K., Krishnamoorthy G., Arunakaran J. Oxidative stress modulates membrane bound atpases in brain regions of PCB (aroclor 1254) exposed rats: Protective role of alpha-tocopherol. Biomed. Pharm. 2007;61:435–440. doi: 10.1016/j.biopha.2007.03.003.
    1. Venkataraman P., Krishnamoorthy G., Vengatesh G., Srinivasan N., Aruldhas M.M., Arunakaran J. Protective role of melatonin on PCB (aroclor 1254) induced oxidative stress and changes in acetylcholine esterase and membrane bound atpases in cerebellum, cerebral cortex and hippocampus of adult rat brain. Int. J. Dev. Neurosci. 2008;26:585–591. doi: 10.1016/j.ijdevneu.2008.05.002.
    1. Venkataraman P., Muthuvel R., Krishnamoorthy G., Arunkumar A., Sridhar M., Srinivasan N., Balasubramanian K., Aruldhas M.M., Arunakaran J. PCB (aroclor 1254) enhances oxidative damage in rat brain regions: Protective role of ascorbic acid. Neurotoxicology. 2007;28:490–498. doi: 10.1016/j.neuro.2006.11.002.

Source: PubMed

스폰서 및 공동 작업자

건강 상태

약물 개입

3
구독하다