However, human studies are limited in their ability to determine the causal link between maternal obesity and the increased disease risk in the offspring due to several confounding factors including shared genetics, postnatal feeding habits and parental lifestyles. Circulation 125, 13811389, https://doi.org/10.1161/circulationaha.111.070060 (2012). In the pre-exposure phase, PE animals were placed in the shuttle chambers and received 50 presentation of 5s white noise CS presented at a random interval of 4015s. The NPE animals spent equivalent period in the chambers without any stimulus presentation. Differential effects of post-weaning juvenile stress on the behaviour of C57BL/6 mice in adolescence and adulthood. ISSN 2045-2322 (online). The origins of the developmental origins theory. Behaviorally nave animals were chosen from each sex and group for the metabolic and neurochemical analysis. Another key observation in the present study is that concomitant to schizophrenic traits Lact offspring develop the metabolic syndrome. Vitamins and minerals are essential for human health and development. N=(10m, 10f) per group. International journal of obesity (2005) 32, 550557 (2008). Meyer, U. In the amphetamine sensitivity test, no difference in baseline locomotor activity or following a saline injection was observed between the offspring groups (Fig. 6. 3LN). Lact offspring had less number of lipid droplets (F1,20=8.25; P<0.01) in the small adipocytes but the size of the lipid droplets was larger (F1,20=5.39; P<0.04) compared to CTR offspring. PubMedGoogle Scholar. In a study conducted by Frongillo et al., (2019) over 40% of pregnant women reported worry over the amount of food available; 5% of these mothers had no food in the household. The impact of food insecurity on the homeemotional environment among low-income mothers of young children. There was good evidence for MNT by an RDN during pregnancy on improving gestational weight gain among overweight/obese women. PubMed Central The effect of weight management interventions that include a diet component on weight-related outcomes in pregnant and postpartum women: a systematic review protocol. Besides other significant changes, the higher DA levels in the Nac and dSTR together with lower DOPAC and HVA levels indicate a baseline hyperdopaminergic state in the striatal regions which might play a crucial role in the emergence of positive symptoms of schizophrenia in this offspring group. The CT scanner measures the volumes of adipose tissue, bone, air and the rest based on the differences in X-ray density and distinguishes between intra-abdominal and subcutaneous adipose tissue. Endocrinology 151, 47564764 (2010). PubMed Central Reduction of dopamine release and synthesis by repeated amphetamine treatment: role in behavioral sensitization. Maternal overnutrition during critical developmental periods leads to different health adversities in the offspring: relevance of obesity, addiction and schizophrenia, https://doi.org/10.1038/s41598-019-53652-x. (D) Alcohol preference test: the bar graph shows the mean alcohol preference in three different concentrations (2%, 5% and 8%). It was approved by the Zurich Cantonal Veterinary Office, Switzerland. In the LI-active avoidance paradigm, a 22210 (maternal exposuresexpre-exposure10-trials block) repeated measures ANOVA was employed. An official website of the United States government. (Castro et al., 2017; Chilton et al., 2007; Fakhri & Tzouvala, 2020). In EG offspring, a dissociation between female and male offspring emerged exclusively in the Nac region where lower DA and HVA levels were detected in male offspring and higher DA levels in the female offspring compared to their controls. 4E). They can also lead to stillbirth, low birthweight, wasting and developmental delays for children. Hormones and behavior 76, 143152, https://doi.org/10.1016/j.yhbeh.2015.06.015 (2015). Mennella, J. Subsequent post hoc analysis depicted reduced avoidance responses in the PE group compared to the NPE group in CTR offspring (P<0.0001). The placenta is responsible for transport of nutrients from the maternal to fetal circulation, and the . Am J Physiol Regul Integr Comp Physiol 306, R527537 (2014). Similarly, in the sucrose preference test, both offspring groups preferred the sucrose solution over water (F1, 28=254.98; P<0.001). 2A). Biol Psychiatry 59, 546554, https://doi.org/10.1016/j.biopsych.2005.07.031 (2006). Kominiarek, M. A. A. et al. Accumulating evidence report the occurrence of metabolic dysfunction in psychosis-prone subjects as well as in drug nave schizophrenic patients, which might be linked to environmental insults during development58,59. Similar alterations in striatal DA levels are reported in chronic methamphetamine users64 as well as rodent models of addiction following withdrawal from cocaine65, amphetamine66 and ethanol67. The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Sections were de-paraffinized and stained with haematoxylin and eosin on a Varistain 244 (Thermo Scientific) before mounting and drying. In the LG group, both male and female offspring show reduced DA levels in the Nac whereas only male offspring show lower DA levels in the dSTR compared to the other groups. are not significant B.) Neurotransmitters were separated on a reversed-phase column (125mm3mm YMC column, Nucleosil 1203C 18, YMC Europe GmbH, Germany). volume9, Articlenumber:17322 (2019) Abstract. Bolton, J. L. & Bilbo, S. D. Developmental programming of brain and behavior by perinatal diet: focus on inflammatory mechanisms. CTR=control; Lact=lactation; HFD=high fat diet; PE=pre-exposure; NPE=non pre-exposure. For example, differential effects on offsprings metabolic programming following a pre-pregnancy short-term HFD exposure26 or specific periods of gestation27 have been explored. Conversely, we observe that 3 weeks preconception HFD exposure does not affect the metabolic health of the offspring. Am J Perinatol 33, 433441, https://doi.org/10.1055/s-0035-1567856 (2016). The bar plot depicts the comparison of the mean %PPI between the groups. J Nutr Biochem 24, 13401348, https://doi.org/10.1016/j.jnutbio.2012.10.009 (2013). N=(91m, 76f) EG; N=(43m, 37f) LG and N=(32m, 36f) CTR. Google Scholar. Effect of high-fat diet prior to pregnancy on hepatic gene expression and histology in mouse offspring. Acta Psychiatr Scand 119, 414, https://doi.org/10.1111/j.1600-0447.2008.01317.x (2009). In the early (EG) and late (LG) gestation groups, dams are exposed to HFD during GD011 or during GD 12-21, respectively. Medical hypotheses 43, 420435 (1994). As the fragile body continues to function on depreciating enzyme counts, metabolic rate slows and hormone production decelerates. The latter, is manifested by impaired sensory motor gating, and latent inhibition as well as enhanced sensitivity to amphetamine. The motion inside the tube was recorded by a piezoelectric accelerometer below the frame. Dahlhoff, M. et al. Hochner, H. et al. Association of food insecurity with childrensbehavioral, emotional, and academic outcomes: a systematic review. For data analysis, an average of the last 3 days was taken, and HFD preference was calculated as percentage of HFD intake in relation to total food intake23. Maternal dietary pattern during breastfeeding and its influence on weight gain and the poor feeding habits in children has also been reported in several human studies40. The American journal of clinical nutrition 80, 15791588, https://doi.org/10.1093/ajcn/80.6.1579 (2004). Sullivan, E. L., Riper, K. M., Lockard, R. & Valleau, J. C. Maternal high-fat diet programming of the neuroendocrine system and behavior. One possible explanation could be that the duration of exposure is too short (only 11 days) to induce metabolic abnormalities. N=(10m, 10f) per group and condition. a. Nutritional neuroscience, 112, https://doi.org/10.1080/1028415x.2018.1432096 (2018). Among 94 identified studies, five controlled trials met the inclusion criteria. CAS Indeed, Pacheco-Lopez, et al.60 show in a mouse model of prenatal infection that adult male offspring develop a schizophrenia-like phenotype that is accompanied by metabolic syndrome related phenotypes. The adaptation to self-sustainment in a nutrient deprived environment translates to malabsorption. A reduction in avoidance responses in the pre-exposed (PE) compared to the non pre-exposed (NPE) groups constituted the LI phenomenon. Such a difference was not evident in the lactation group. Opposed to our findings, an earlier study report that 34 weeks preconception MHFD exposure increases weight gain, adiposity and hepatic lipid droplet size in the adult offspring26. Such an altered mesolimbic system is also observed in our previous model of 9 weeks MHFD22. It is incredibly not safe for the infant or smart to consume alcohol during pregnancy. The US food system iskilling Americans. & Stickland, N. C. A maternal junk food diet in pregnancy and lactation promotes an exacerbated taste for junk food and a greater propensity for obesity in rat offspring. An ANOVA revealed no difference in the number of large lipid droplets in the visceral fat depot (F1,20=1.73; P=0.203). Images were obtained using an Axioscope A.1 (Zeiss). Maternal adiposity prior to pregnancy is associated with ADHD symptoms in offspring: evidence from three prospective pregnancy cohorts. America is suffering its worst hungercrisis in decades. The first two months are critical periods and a woman may not know she is pregnant which is most common when fetal alcohol syndrome occurs. With such affirmations, it is pertinent to invest in broader studies which investigate the provisional cost and overall effectiveness of the interventions; nonetheless, the widespread adaptation of this holistic and potentially low cost strategy is an astute method to combat and ultimately eliminate the severity of food insecurity while administering to vulnerable mothers and their developing children. In the PPI test, the %PPI increased as a function of higher levels of prepulse intensities in both groups (main effect of prepulse intensity, F2,100=49.64; P<0.0001) as shown in Fig. Scientific Reports (D) Alcohol preference test: the bar graph shows the mean alcohol preference in three different concentrations (2%, 5% and 8%). 8600 Rockville Pike The test was conducted in four ventilated startle chambers (SR-LAB, San Diego Instruments, San Diego, CA, USA). Although, we do not exclude that other neurotransmitter systems are involved. Following sedation with 45% isoflurane, mice were laid in supine position in the mouse holder where the gas anesthesia (1.52.5% isoflurane) was maintained during scanning. European journal of pharmacology 218, 171173 (1992). To obtain Laruelle, M. Imaging synaptic neurotransmission with in vivo binding competition techniques: a critical review. At the end of day 4, the animals were subdivided into two groups: pre-exposed (PE) and non-pre-exposed (NPE), with their baseline drinking counterbalanced. The mice were then injected with (intraperitoneal; i.p) 0.9% NaCl solution and after 30min of locomotor assessment, mice were i.p injected with d-amphetamine sulfate (2.5mg/kg). The major nutrients of the chow diet are 18.5% crude protein, dry matter 88%, crude fat 4.5%, 54.2% nitrogen free extract (NFE). Oben, J. Sarker, G., Litwan, K., Kastli, R. et al. Outcomes included maternal gestational weight gain, maternal markers of glycemic control, maternal complications such as hypertension, incidence of caesarean section, infant birth weight both in grams and in clinical categories, infant gestational age, and infant complications. An increasing body of evidence suggests that poor nutrition at the very beginning of life - even before birth - leads to large and long term negative consequences for both mental and physical health. The HFD, sucrose, and alcohol preference tests were conducted chronologically with the same set of animals with a wash time period of at least 7 days in between tests. Psychopharmacology 214, 339351 (2011). Meyer, J. M. & Stahl, S. M. The metabolic syndrome and schizophrenia. Bayol, S. A., Farrington, S. J. To the best of our knowledge, the present study is the first to show in a mouse model that MHFD exposure exclusively during lactation is sufficient to induce schizophrenia-related abnormalities in the offspring later in life. A maternal proper diet has a fundamental role in decreasing pregnancy complications and to prevent possible diseases in postnatal life. The samples were homogenized using a sonicator and centrifuged at 10,000g for 20min at 4C. Mol Psychiatry 13, 918929, https://doi.org/10.1038/mp.2008.40 (2008). N=(10m, 10f) per group. A systematic review of studies published between 2000 and 2014 that incorporated MNT by an RDN during pregnancy were retrieved from a PubMed search, using criteria established by the Academy of Nutrition and Dietetics Evidence Analysis Process. To analyze the % PPI, a 2233 (maternal exposuresexpulse levelprepulse level) for the preconception and the lactation groups and a 3233 (maternal exposuresexpulse levelprepulse level) repeated measures ANOVA for the gestation group were used. Disruption of PPI, which refers to sensory motor gating deficits, and LI disruption, which reflects attention deficits, have been commonly reported in schizophrenic patients with marked positive symptoms48,49. Pathway-Specific Dopamine Abnormalities in Schizophrenia. Obes Rev 13, 518527, https://doi.org/10.1111/j.1467-789X.2011.00971.x (2012). https://doi.org/10.1007/s00737-017-0736-7, Chilton, M., Chyatte, M., & Breaux, J. Furthermore, significant alterations in the circulating insulin and lipids levels were detected (Fig. Avoidance failure immediately induced an electric foot shock presented in coincidence to the CS. https://www.usatoday.com/story/opinion/2020/10/01/how-confront-americas-worst-hunger-crisis-generations-column/3570835001/, Martin-Gronert, M.S. slow behavioral and intellectual development, possibly resulting in learning difficulties. By submitting a comment you agree to abide by our Terms and Community Guidelines. Journal of hepatology 52, 913920, https://doi.org/10.1016/j.jhep.2009.12.042 (2010). On the other hand, both male and female Lact offspring show higher basal DA levels in the Nac and dSTR compared to CTR offspring. Kaidanovich-Beilin, O., Cha, D. S. & McIntyre, R. S. Crosstalk between metabolic and neuropsychiatric disorders. Such findings in human studies are also documented in rodent models of schizophrenia52,53. Google Scholar. Consequently, the food insecure seek support from food banks which are becoming increasingly unreliable. A recent survey has reported that around 27% women of reproductive age are overweight and 37% are obese in the United States with a similar pattern in Europe3. Since then, there have been many studies on the effects of early malnutrition. Bethesda, MD 20894, Web Policies The protocol for sucrose preference test was validated in our laboratory before and described in detail22. The brain regions were dissected according to the Mouse Brain Atlas in Stereotaxic Coordinates (Paxinos and Franklin, 2008) which were as follows: dSTR (bregma +1.34 to +0.14mm), Nac (bregma +1.60 to +0.98mm), mPFC (bregma +2.68 to+1.94mm), Hypo (bregma 1.34 to 2.06mm), SN (bregma 2.80 to 3.64mm), VTA (bregma 2.92 to 3.64mm). (Chilton et al., 2007) Although this dynamic issue demands numerous, potentially hefty financial adjustments and societal restructure, the prospective advantages outweigh all the costs. Malnutrition in developed countries is unfortunately still more common in situations of poverty, social isolation and substance misuse. The supernatant was then collected and filtered through a 0.2 m nylon filter (Spritzenfilter, Semadeni AG) to separate the insoluble residue. Am J Physiol Regul Integr Comp Physiol 288, R11221128, https://doi.org/10.1152/ajpregu.00335.2004 (2005). It contains 26% protein, 38% fat and 1% carbohydrates with total energy 22kJ/g or 5.25kcal/g76,77. Spencer L, Rollo M, Hauck Y, MacDonald-Wicks L, Wood L, Hutchesson M, Giglia R, Smith R, Collins C. JBI Database System Rev Implement Rep. 2015 Jan;13(1):88-98. doi: 10.11124/jbisrir-2015-1812. The animals were gradually acclimatized to a water-deprivation schedule over a 6-day period until they were kept on 23hours water deprivation, which was maintained throughout the experiment. Daria Peleg-Raibstein. Maternal undernutrition has detrimental effects on fetal development and adult health. The sample (20l from each brain region) was injected via a refrigerated autoinjector (ASI-100, Dionex, CA, USA). For the sucrose and alcohol preference tests, a 2223 (maternal exposuresexpreference substancesubstance concentrations) for the preconception and the lactation groups and a 3223 (maternal exposuresexpreference substancesubstance concentrations) repeated-measures ANOVA for the gestation group were used. Effects of high fat diet on Morris maze performance, oxidative stress, and inflammation in rats: contributions of maternal diet. Journal ofDevelopmental & Behavioral Pediatrics, 38(2), 135-150. https://doi.org/10.1097/DBP.0000000000000383, Thomas, M., Miller, D., & Morrissey, T. (2019). Clancy, B., Finlay, B. L., Darlington, R. B. (2) Late gestation HFD exposure induces most features of addictive-like behaviors that is further substantiated by the presence of lower striatal DA levels. This theory, also known as the Developmental Origin of Health and Disease, postulates that the fetus makes permanent adaptations in the homeostatic system in response to suboptimal intrauterine conditions leading to increased risk to develop non-communicable diseases later in life7. Hormones and behavior 76, 153161, https://doi.org/10.1016/j.yhbeh.2015.04.008 (2015). However, no difference in body mass was detected among the offspring from EG, LG and CTR groups (Fig. 5B). and JavaScript. Further, central insulin resistance could potentiate the development of obesity and peripheral insulin resistance via the disruption of insulin signaling in the homeostatic and hedonic circuitry, alteration of hepatic lipogenesis and white adipose tissue metabolism31,72. Experimental design illustrating the breeding scheme and dietary pattern. 5D). (E) %Prepulse inhibition of the acoustic startle reflex: the line graph shows the percent PPI as a function of different pulses (100, 110 and 120dB) and the corresponding prepulse intensities (+6, +12 and +18 DB above the background 65dB). Pacheco-Lopez, G., Giovanoli, S., Langhans, W. & Meyer, U. Priming of metabolic dysfunctions by prenatal immune activation in mice: relevance to schizophrenia. 3HK). & Sullivan, E. L. The role of maternal obesity in the risk of neuropsychiatric disorders. Exercise for pregnant women with gestational diabetes for improving maternal and fetal outcomes. Butte, N. F. Impact of infant feeding practices on childhood obesity. A. Dialogues Clin Neurosci 16, 307320 (2014). Glycaemia was measured 30, 60, 90 and 120minutes after the injection. Handb Exp Pharmacol, 361406, https://doi.org/10.1007/978-3-642-25761-2_14 (2012). J Child Psychol Psychiatry 51, 134143 (2010).
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