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ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

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Review Article

NAFLD at the Interface of the Mother-Infant Dyad

Author(s): ">Sara Bertrando* and ">Pietro Vajro*

Volume 26, Issue 10, 2020

Page: [1119 - 1125] Pages: 7

DOI: 10.2174/1381612826666200122153055

Price: $65

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Abstract

This review aims to focus the links existing between several aspects of the mother-child dyad in the intricate playground of obesity and Metabolic Syndrome (MetS), including its hepatic component, the Non- Alcoholic Fatty Liver Disease (NAFLD). In recent years human and animal model studies have shown that dietary interventions in mothers and offspring can be successful in reducing the risk of NAFLD development. Evidences also concern the new concept of a real intergenerational transmission of predisposition to metabolic disorders. Certain genes, such as SIRT1 and PNPLA3, and some epigenetic modifications, including micro RNAs function, seem to be responsible for fetal reprogramming in the setting of maternal obesity. These modifiers appear to be potential therapeutic targets to reduce the risk of future metabolic dysfunctions.

Controlling antepartum hyperglycemia, preventing gestational diabetes, and avoiding excessive weight gain during pregnancy can help reduce the relentless epidemic of childhood obesity and NAFLD. Also, the composition of the intestinal microbiota seems to be related to the development of metabolic disorders in the offspring. Several studies show that breastfed infants have a microbial signature different from formula-fed infants. Much interestingly, prolonged breastfeeding is beneficial not only for the newborn and his health in adult life, but also for the mothers’ health. Maternal benefits include reducing the risk of developing chronic diseases, such as diabetes mellitus, myocardial infarction and NAFLD as well.

In conclusion, all above mechanisms appear to intervene synergistically and may act as modifiable risk factors for infant and mother NAFLD.

Keywords: Breastfeeding, gut microbiota, maternal health benefits, metabolic syndrome, non-alcoholic fatty liver disease, hyperglycemia.

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[1]
Julvez J, Guxens M, Carsin AE, et al. A cohort study on full breastfeeding and child neuropsychological development: the role of maternal social, psychological, and nutritional factors. Dev Med Child Neurol 2014; 56(2): 148-56.
[http://dx.doi.org/10.1111/dmcn.12282] [PMID: 24116864]
[2]
Brumbaugh DE, Friedman JE. Developmental origins of nonalcoholic fatty liver disease. Pediatr Res 2014; 75(1-2): 140-7.
[http://dx.doi.org/10.1038/pr.2013.193] [PMID: 24192698]
[3]
Feldstein AE, Charatcharoenwitthaya P, Treeprasertsuk S, Benson JT, Enders FB, Angulo P. The natural history of non-alcoholic fatty liver disease in children: a follow-up study for up to 20 years. Gut 2009; 58(11): 1538-44.
[http://dx.doi.org/10.1136/gut.2008.171280] [PMID: 19625277]
[4]
Schwimmer JB, McGreal N, Deutsch R, Finegold MJ, Lavine JE. Influence of gender, race, and ethnicity on suspected fatty liver in obese adolescents. Pediatrics 2005; 115(5): e561-5.
[http://dx.doi.org/10.1542/peds.2004-1832] [PMID: 15867021]
[5]
Wesolowski SR, Kasmi KC, Jonscher KR, Friedman JE. Developmental origins of NAFLD: a womb with a clue. Nat Rev Gastroenterol Hepatol 2017; 14(2): 81-96.
[http://dx.doi.org/10.1038/nrgastro.2016.160] [PMID: 27780972]
[6]
Lomas-Soria C, Reyes-Castro LA, Rodríguez-González GL, et al. Maternal obesity has sex-dependent effects on insulin, glucose and lipid metabolism and the liver transcriptome in young adult rat offspring. J Physiol 2018; 596(19): 4611-28.
[http://dx.doi.org/10.1113/JP276372] [PMID: 29972240]
[7]
Bayol SA, Simbi BH, Fowkes RC, Stickland NC. A maternal “junk food” diet in pregnancy and lactation promotes nonalcoholic Fatty liver disease in rat offspring. Endocrinology 2010; 151(4): 1451-61.
[http://dx.doi.org/10.1210/en.2009-1192] [PMID: 20207831]
[8]
Drake AJ, Reynolds RM. Impact of maternal obesity on offspring obesity and cardiometabolic disease risk. Reproduction 2010; 140(3): 387-98.
[http://dx.doi.org/10.1530/REP-10-0077] [PMID: 20562299]
[9]
Bringhenti I, Ornellas F, Martins MA, Mandarim-de-Lacerda CA, Aguila MB. Early hepatic insult in the offspring of obese maternal mice. Nutr Res 2015; 35(2): 136-45.
[http://dx.doi.org/10.1016/j.nutres.2014.11.006] [PMID: 25582085]
[10]
Oben JA, Mouralidarane A, Samuelsson AM, et al. Maternal obesity during pregnancy and lactation programs the development of offspring non-alcoholic fatty liver disease in mice. J Hepatol 2010; 52(6): 913-20.
[http://dx.doi.org/10.1016/j.jhep.2009.12.042] [PMID: 20413174]
[11]
Zhou L, Liu D, Wang Z, Dong H, Xu X, Zhou S. Establishment and comparison of juvenile female mouse models of nonalcoholic fatty liver disease and nonalcoholic steatohepatitis. Gastroenterol Res Pract 2018; 2018: 8929620
[http://dx.doi.org/10.1155/2018/8929620] [PMID: 30158971]
[12]
Simpson J, Smith AD, Fraser A, et al. Cord blood adipokines and lipids and adolescent nonalcoholic fatty liver disease. J Clin Endocrinol Metab 2016; 101(12): 4661-8.
[http://dx.doi.org/10.1210/jc.2016-2604] [PMID: 27648968]
[13]
Dumolt JH, Browne RW, Patel MS, Rideout TC. Malprogramming of hepatic lipid metabolism due to excessive early cholesterol exposure in adult progeny. Mol Nutr Food Res 2019; 63(2): e1800563
[http://dx.doi.org/10.1002/mnfr.201800563] [PMID: 30447138]
[14]
Aerts L, Van Assche FA. Animal evidence for the transgenerational development of diabetes mellitus. Int J Biochem Cell Biol 2006; 38(5-6): 894-903.
[http://dx.doi.org/10.1016/j.biocel.2005.07.006] [PMID: 16118061]
[15]
Brumbaugh DE, Tearse P, Cree-Green M, et al. Intrahepatic fat is increased in the neonatal offspring of obese women with gestational diabetes. J Pediatr 2013; 162(5): 930-6.e1.
[http://dx.doi.org/10.1016/j.jpeds.2012.11.017] [PMID: 23260099]
[16]
Patel S, Lawlor DA, Callaway M, Macdonald-Wallis C, Sattar N, Fraser A. Association of maternal diabetes/glycosuria and pre-pregnancy body mass index with offspring indicators of non-alcoholic fatty liver disease. BMC Pediatr 2016; 16: 47.
[http://dx.doi.org/10.1186/s12887-016-0585-y] [PMID: 27036545]
[17]
Bedogni G, De Matteis G, Fabrizi M, et al. Association of bright liver with the PNPLA3 I148M gene variant in 1-year-old toddlers. J Clin Endocrinol Metab 2019; 104(6): 2163-70.
[http://dx.doi.org/10.1210/jc.2018-01998] [PMID: 30649436]
[18]
Nguyen LT, Chen H, Zaky A, Pollock C, Saad S. SIRT1 overexpression attenuates offspring metabolic and liver disorders as a result of maternal high-fat feeding. J Physiol 2019; 597(2): 467-80.
[http://dx.doi.org/10.1113/JP276957] [PMID: 30381838]
[19]
Sun C, Fan JG, Qiao L. Potential epigenetic mechanism in non-alcoholic Fatty liver disease. Int J Mol Sci 2015; 16(3): 5161-79.
[http://dx.doi.org/10.3390/ijms16035161] [PMID: 25751727]
[20]
Shakibapour N, Dehghani Sani F, Beigoli S, Sadeghian H, Chamani J. Multi-spectroscopic and molecular modeling studies to reveal the interaction between propyl acridone and calf thymus DNA in the presence of histone H1: binary and ternary approaches. J Biomol Struct Dyn 2019; 37(2): 359-71.
[http://dx.doi.org/10.1080/07391102.2018.1427629] [PMID: 29338579]
[21]
Maloyan A, Muralimanoharan S, Huffman S, et al. Identification and comparative analyses of myocardial miRNAs involved in the fetal response to maternal obesity. Physiol Genomics 2013; 45(19): 889-900.
[http://dx.doi.org/10.1152/physiolgenomics.00050.2013] [PMID: 23922128]
[22]
Puppala S, Li C, Glenn JP, et al. Primate fetal hepatic responses to maternal obesity: epigenetic signaling pathways and lipid accumulation. J Physiol 2019; 597: 467-80.
[23]
de Paula Simino LA, de Fante T, Figueiredo Fontana M, et al. Lipid overload during gestation and lactation can independently alter lipid homeostasis in offspring and promote metabolic impairment after new challenge to high-fat diet. Nutr Metab (Lond) 2017; 14: 16.
[http://dx.doi.org/10.1186/s12986-017-0168-4] [PMID: 28239403]
[24]
Gutierrez Sanchez LH, Tomita K, Guo Q, et al. Perinatal nutritional reprogramming of the epigenome promotes subsequent development of nonalcoholic steatohepatitis. Hepatol Commun 2018; 2(12): 1493-512.
[http://dx.doi.org/10.1002/hep4.1265] [PMID: 30556038]
[25]
Devarajan A, Rajasekaran NS, Valburg C, Ganapathy E, Bindra S, Freije WA. Maternal perinatal calorie restriction temporally regulates the hepatic autophagy and redox status in male rat. Free Radic Biol Med 2019; 130: 592-600.
[http://dx.doi.org/10.1016/j.freeradbiomed.2018.09.029] [PMID: 30248445]
[26]
Anatolitou F. Human milk benefits and breastfeeding. JPNIM 2012; 1: 11-8.
[27]
Paolella G, Vajro P. Childhood obesity, breastfeeding, intestinal microbiota and early exposure to antibiotics. What Is the Link? JAMA Pediatr 2016; 170(8): 735-7.
[http://dx.doi.org/10.1001/jamapediatrics.2016.0964] [PMID: 27294594]
[28]
Hunsberger M, Lanfer A, Reeske A, et al. Infant feeding practices and prevalence of obesity in eight European countries - the IDEFICS study. Public Health Nutr 2013; 16(2): 219-27.
[http://dx.doi.org/10.1017/S1368980012003850] [PMID: 22916704]
[29]
Casazza K, Fontaine KR, Astrup A, et al. Myths, presumptions, and facts about obesity. N Engl J Med 2013; 368(5): 446-54.
[http://dx.doi.org/10.1056/NEJMsa1208051] [PMID: 23363498]
[30]
Li R, Fein SB, Grummer-Strawn LM. Do infants fed from bottles lack self-regulation of milk intake compared with directly breastfed infants? Pediatrics 2010; 125(6): e1386-93.
[http://dx.doi.org/10.1542/peds.2009-2549] [PMID: 20457676]
[31]
Güngör D, Nadaud P, LaPergola CC, et al. Infant milk-feeding practices and diabetes outcomes in offspring: a systematic review. Am J Clin Nutr 2019; 109(Supplement_7): 817S-37.
[http://dx.doi.org/10.1093/ajcn/nqy311] [PMID: 30982877]
[32]
Dentin R, Benhamed F, Pégorier JP, et al. Polyunsaturated fatty acids suppress glycolytic and lipogenic genes through the inhibition of ChREBP nuclear protein translocation. J Clin Invest 2005; 115(10): 2843-54.
[http://dx.doi.org/10.1172/JCI25256] [PMID: 16184193]
[33]
Nobili V, Bedogni G, Alisi A, et al. A protective effect of breastfeeding on the progression of non-alcoholic fatty liver disease. Arch Dis Child 2009; 94(10): 801-5.
[http://dx.doi.org/10.1136/adc.2009.159566] [PMID: 19556219]
[34]
Ayonrinde OT, Oddy WH, Adams LA, et al. Infant nutrition and maternal obesity influence the risk of non-alcoholic fatty liver disease in adolescents. J Hepatol 2017; 67(3): 568-76.
[http://dx.doi.org/10.1016/j.jhep.2017.03.029] [PMID: 28619255]
[35]
Stuebe A. Associations among lactation, maternal carbohydrate metabolism, and cardiovascular health. Clin Obstet Gynecol 2015; 58(4): 827-39.
[http://dx.doi.org/10.1097/GRF.0000000000000155] [PMID: 26457850]
[36]
Stuebe AM, Rich-Edwards JW. The reset hypothesis: lactation and maternal metabolism. Am J Perinatol 2009; 26(1): 81-8.
[http://dx.doi.org/10.1055/s-0028-1103034] [PMID: 19031350]
[37]
McClure CK, Schwarz EB, Conroy MB, Tepper PG, Janssen I, Sutton-Tyrrell KC. Breastfeeding and subsequent maternal visceral adiposity. Obesity (Silver Spring) 2011; 19(11): 2205-13.
[http://dx.doi.org/10.1038/oby.2011.185] [PMID: 21720436]
[38]
Stuebe AM, Rich-Edwards JW, Willett WC, Manson JE, Michels KB. Duration of lactation and incidence of type 2 diabetes. JAMA 2005; 294(20): 2601-10.
[http://dx.doi.org/10.1001/jama.294.20.2601] [PMID: 16304074]
[39]
Aune D, Norat T, Romundstad P, Vatten LJ. Breastfeeding and the maternal risk of type 2 diabetes: a systematic review and dose-response meta-analysis of cohort studies. Nutr Metab Cardiovasc Dis 2014; 24(2): 107-15.
[http://dx.doi.org/10.1016/j.numecd.2013.10.028] [PMID: 24439841]
[40]
Gunderson EP, Jacobs DR Jr, Chiang V, et al. Duration of lactation and incidence of the metabolic syndrome in women of reproductive age according to gestational diabetes mellitus status: a 20-Year prospective study in CARDIA (Coronary Artery Risk Development in Young Adults). Diabetes 2010; 59(2): 495-504.
[http://dx.doi.org/10.2337/db09-1197] [PMID: 19959762]
[41]
Schwarz EB, McClure CK, Tepper PG, et al. Lactation and maternal measures of subclinical cardiovascular disease. Obstet Gynecol 2010; 115(1): 41-8.
[http://dx.doi.org/10.1097/AOG.0b013e3181c5512a] [PMID: 20027032]
[42]
Schwarz EB, Ray RM, Stuebe AM, et al. Duration of lactation and risk factors for maternal cardiovascular disease. Obstet Gynecol 2009; 113(5): 974-82.
[http://dx.doi.org/10.1097/01.AOG.0000346884.67796.ca] [PMID: 19384111]
[43]
Zachou G, Armeni E, Lambrinoudaki I. Lactation and maternal cardiovascular disease risk in later life. Maturitas 2019; 122: 73-9.
[http://dx.doi.org/10.1016/j.maturitas.2019.01.007] [PMID: 30797534]
[44]
Lankarani-Fard A, Kritz-Silverstein D, Barrett-Connor E, Goodman-Gruen D. Cumulative duration of breast-feeding influences cortisol levels in postmenopausal women. J Womens Health Gend Based Med 2001; 10(7): 681-7.
[http://dx.doi.org/10.1089/15246090152563560] [PMID: 11571098]
[45]
Ajmera VH, Terrault NA, VanWagner LB, et al. Longer lactation duration is associated with decreased prevalence of non-alcoholic fatty liver disease in women. J Hepatol 2019; 70(1): 126-32.
[http://dx.doi.org/10.1016/j.jhep.2018.09.013] [PMID: 30392752]
[46]
Nobili V, Schwimmer JB, Vajro P. Breastfeeding and NAFLD from the maternal side of the mother-infant dyad. J Hepatol 2019; 70(1): 13-4.
[http://dx.doi.org/10.1016/j.jhep.2018.10.030] [PMID: 30414736]
[47]
Paolella G, Vajro P. Maternal microbiota, prepregnancy weight, and mode of delivery: intergenerational transmission of risk for childhood overweight andobesity. JAMA Pediatr 2018; 172(4): 320-2.
[http://dx.doi.org/10.1001/jamapediatrics.2017.5686] [PMID: 29459936]
[48]
Gareau MG, Sherman PM, Walker WA. Probiotics and the gut microbiota in intestinal health and disease. Nat Rev Gastroenterol Hepatol 2010; 7(9): 503-14.
[http://dx.doi.org/10.1038/nrgastro.2010.117] [PMID: 20664519]
[49]
Johnson CL, Versalovic J. The human microbiome and its potential importance to pediatrics. Pediatrics 2012; 129(5): 950-60.
[http://dx.doi.org/10.1542/peds.2011-2736] [PMID: 22473366]
[50]
Mulligan CM, Friedman JE. Maternal modifiers of the infant gut microbiota: metabolic consequences. J Endocrinol 2017; 235(1): R1-R12.
[http://dx.doi.org/10.1530/JOE-17-0303] [PMID: 28751453]
[51]
Pierri L, Saggese P, Guercio Nuzio S, et al. Relations of gut liver axis components and gut microbiota in obese children with fatty liver: A pilot study. Clin Res Hepatol Gastroenterol 2018; 42(4): 387-90.
[http://dx.doi.org/10.1016/j.clinre.2018.03.015] [PMID: 29773420]
[52]
Paolella G, Mandato C, Pierri L, Poeta M, Di Stasi M, Vajro P. Gut-liver axis and probiotics: their role in non-alcoholic fatty liver disease. World J Gastroenterol 2014; 20(42): 15518-31.
[http://dx.doi.org/10.3748/wjg.v20.i42.15518] [PMID: 25400436]
[53]
Vajro P, Paolella G, Fasano A. Microbiota and gut-liver axis: their influences on obesity and obesity-related liver disease. J Pediatr Gastroenterol Nutr 2013; 56(5): 461-8.
[http://dx.doi.org/10.1097/MPG.0b013e318284abb5] [PMID: 23287807]
[54]
Soderborg TK, Clark SE, Mulligan CE, et al. The gut microbiota in infants of obese mothers increases inflammation and susceptibility to NAFLD. Nat Commun 2018; 9(1): 4462.
[http://dx.doi.org/10.1038/s41467-018-06929-0] [PMID: 30367045]
[55]
Jantscher-Krenn E, Bode L. Human milk oligosaccharides and their potential benefits for the breast-fed neonate. Minerva Pediatr 2012; 64(1): 83-99.
[PMID: 22350049]
[56]
Houghteling PD, Walker WA. Why is initial bacterial colonization of the intestine important to infants’ and children’s health? J Pediatr Gastroenterol Nutr 2015; 60(3): 294-307.
[http://dx.doi.org/10.1097/MPG.0000000000000597] [PMID: 25313849]
[57]
Ho NT, Li F, Lee-Sarwar KA, et al. Meta-analysis of effects of exclusive breastfeeding on infant gut microbiota across populations. Nat Commun 2018; 9(1): 4169.
[http://dx.doi.org/10.1038/s41467-018-06473-x] [PMID: 30301893]
[58]
Isolauri E, Rautava S, Salminen S, Collado MC. Early-life nutrition and microbiome development. Nestle Nutr Inst Workshop Ser 2019; 90: 151-62.
[http://dx.doi.org/10.1159/000490302] [PMID: 30865983]
[59]
D’Aniello R, Troisi J, D’Amico O, et al. Emerging pathomechanisms involved in obesity. J Pediatr Gastroenterol Nutr 2015; 60(1): 113-9.
[http://dx.doi.org/10.1097/MPG.0000000000000559] [PMID: 25199037]
[60]
Clemente MG, Mandato C, Poeta M, Vajro P. Pediatric non-alcoholic fatty liver disease: Recent solutions, unresolved issues, and future research directions. World J Gastroenterol 2016; 22(36): 8078-93.
[http://dx.doi.org/10.3748/wjg.v22.i36.8078] [PMID: 27688650]
[61]
Alisi A, Vajro P. Pre-natal and post-natal environment monitoring to prevent non-alcoholic fatty liver disease development. J Hepatol 2017; 67(3): 451-3.
[http://dx.doi.org/10.1016/j.jhep.2017.04.016] [PMID: 28619256]
[62]
Bonci E, Chiesa C, Versacci P, Anania C, Silvestri L, Pacifico L. Association of Nonalcoholic Fatty Liver Disease with Subclinical Cardiovascular Changes: A Systematic Review and Meta-Analysis. BioMed Res Int 2015; 2015: 213737
[http://dx.doi.org/10.1155/2015/213737] [PMID: 26273598]
[63]
Estrada LD, Ahumada P, Cabrera D, Arab JP. Liver dysfunction as a novel player in alzheimer’s progression: looking outside the brain. Front Aging Neurosci 2019; 11: 174.
[http://dx.doi.org/10.3389/fnagi.2019.00174] [PMID: 31379558]
[64]
Pinçon A, De Montgolfier O, Akkoyunlu N, et al. Non-alcoholic fatty liver disease, and the underlying altered fatty acid metabolism, reveals brain hypoperfusion and contributes to the cognitive decline in APP/PS1 mice. Metabolites 2019; 9(5): E104
[http://dx.doi.org/10.3390/metabo9050104] [PMID: 31130652]
[65]
Kurumbail RG, Calabrese MF. Structure and Regulation of AMPK. Exp Suppl 2016; 107: 3-22.
[PMID: 27812974]
[66]
Cai Z, Yan LJ, Li K, Quazi SH, Zhao B. Roles of AMP-activated protein kinase in Alzheimer’s disease. Neuromolecular Med 2012; 14(1): 1-14.
[http://dx.doi.org/10.1007/s12017-012-8173-2] [PMID: 22367557]
[67]
Ruderman NB, Xu XJ, Nelson L, et al. AMPK and SIRT1: a long-standing partnership? Am J Physiol Endocrinol Metab 2010; 298(4): E751-60.
[http://dx.doi.org/10.1152/ajpendo.00745.2009] [PMID: 20103737]
[68]
Desjardins EM, Steinberg GR. Emerging role of AMPK in brown and beige adipose tissue (BAT): implications for obesity, insulin resistance, and type 2 Diabetes. Curr Diab Rep 2018; 18(10): 80.
[http://dx.doi.org/10.1007/s11892-018-1049-6] [PMID: 30120579]
[69]
Luciano R, Barraco GM, Muraca M, et al. Biomarkers of Alzheimer disease, insulin resistance, and obesity in childhood. Pediatrics 2015; 135(6): 1074-81.
[http://dx.doi.org/10.1542/peds.2014-2391] [PMID: 25963004]
[70]
Martins IJ. Heat shock gene inactivation and protein aggregation with links to chronic diseases. Diseases 2018; 6(2): 6.
[http://dx.doi.org/10.3390/diseases6020039] [PMID: 29783682]
[71]
Liu E, Zhou Q, Xie AJ, et al. Enriched gestation activates the IGF pathway to evoke embryo-adult benefits to prevent Alzheimer’s disease. Transl Neurodegener 2019; 8: 8.
[http://dx.doi.org/10.1186/s40035-019-0149-9] [PMID: 30867903]

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