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Association of famine exposure during early life with the risk of type 2 diabetes in adulthood: a meta-analysis

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Purpose: The association between famine exposure (defined as lengthy and continuous deprivation of food) during early life and type 2 diabetes (T2DM) in adulthood remains controversial. A meta-analysis was performed to better clarify the relation of famine exposure to later T2DM risk. Methods: A systematic literature search was performed in PubMed, Web of Science, Embase and China National Knowledge Infrastructure for relevant available articles. The articles were limited to those in English or Chinese from January 1990 to June 2016. Observational studies evaluating the association between famine exposure and T2DM were included. The pooled relative risk (RR) with 95% confidence interval (CI) was used to estimate the effect of famine exposure on T2DM. The I (2) was used to assess heterogeneity, and the random effects model (REM) was adopted as the pooling method. Results: We included 11 published articles with 12391 T2DM cases for this meta-analysis. A significant association of early life famine exposure with increased risk of T2DM was observed (RR = 1.38, 95% CI 1.17-1.63; I (2) = 63.4%; P heterogeneity = 0.002). Compared with the unexposed, the RRs of T2DM were 1.36 (95% CI 1.12-1.65) for fetal-infant exposed and 1.40 (95% CI 0.98-1.99) for childhood exposed. After excluding one article that had a strong effect on heterogeneity, the pooled RR was 1.46 (95% CI 1.27-1.69). Conclusion: The meta-analysis indicates that famine exposure during early life especially fetal-infant exposure may increase the risk of T2DM in adulthood. Measures should be taken to prevent malnutrition during important stages of growth and development to reduce the prevalence of T2DM.
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Eur J Nutr (2018) 57:741–749
https://doi.org/10.1007/s00394-016-1363-1
ORIGINAL CONTRIBUTION
Association of famine exposure during early life with the risk
of type 2 diabetes in adulthood: a meta‑analysis
Li Liu1,2 · Weijing Wang1 · Jianping Sun2 · Zengchang Pang1,2
Received: 20 July 2016 / Accepted: 11 December 2016 / Published online: 20 December 2016
© Springer-Verlag Berlin Heidelberg 2016
a strong effect on heterogeneity, the pooled RR was 1.46
(95% CI 1.27–1.69).
Conclusion The meta-analysis indicates that famine expo-
sure during early life especially fetal-infant exposure may
increase the risk of T2DM in adulthood. Measures should
be taken to prevent malnutrition during important stages
of growth and development to reduce the prevalence of
T2DM.
Keywords Famine exposure · Type 2 diabetes · Risk ·
Meta-analysis
Introduction
Diabetes mellitus (DM) is one of the most prevalent
chronic diseases, and it can lead to lots of complications
including heart disease, stroke, kidney failure, amputation
and blindness. The world prevalence of DM among adults
is expected to increase from 6.4% in 2010 to 7.7% in 2030
[1]. T2DM makes up about 90% of all DM cases. Several
factors have been thought to be associated with the risk of
T2DM, such as age, family history of diabetes and obesity
[2, 3]. In addition, famine, lengthy and continuous depriva-
tion of food, might also exert an influence on the risk of
T2DM [49]. The reason may be that malnutrition during
fetal life, infancy and early childhood could result in met-
abolic and structural changes of the body. These changes
might be beneficial to survive in the short term but could
increase the risk of T2DM in adulthood [10]. The relation
between malnutrition and increased T2DM risk has been
supported by animal experiments [11].
Different periods of famines around the world have been
used to explore the association of early life nutrition with
T2DM risk in adult. It has been reported that fetal/infant
Abstract
Purpose The association between famine exposure
(defined as lengthy and continuous deprivation of food)
during early life and type 2 diabetes (T2DM) in adulthood
remains controversial. A meta-analysis was performed to
better clarify the relation of famine exposure to later T2DM
risk.
Methods A systematic literature search was performed
in PubMed, Web of Science, Embase and China National
Knowledge Infrastructure for relevant available articles.
The articles were limited to those in English or Chinese
from January 1990 to June 2016. Observational studies
evaluating the association between famine exposure and
T2DM were included. The pooled relative risk (RR) with
95% confidence interval (CI) was used to estimate the
effect of famine exposure on T2DM. The I2 was used to
assess heterogeneity, and the random effects model (REM)
was adopted as the pooling method.
Results We included 11 published articles with 12391
T2DM cases for this meta-analysis. A significant asso-
ciation of early life famine exposure with increased risk
of T2DM was observed (RR = 1.38, 95% CI 1.17–1.63;
I2 = 63.4%; Pheterogeneity = 0.002). Compared with the
unexposed, the RRs of T2DM were 1.36 (95% CI 1.12–
1.65) for fetal-infant exposed and 1.40 (95% CI 0.98–1.99)
for childhood exposed. After excluding one article that had
* Zengchang Pang
15726227711@163.com
1 Department of Public Health, Qingdao University Medical
College, Qingdao 266021, Shandong Province, China
2 Qingdao Municipal Center for Disease Control
and Prevention, Qingdao 266033, Shandong Province, China
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Malnutrition in intrauterine and in early life were potential risk factors for metabolic disorders in later life. Meta-analysis indicated famine exposure or low birth weight in fetal increased risk of obesity, diabetes, hypertension and metabolic syndrome in adulthood [3][4][5][6]. ...
... The Chinese Famine 1959-1961 is a natural disaster, referring to sharp drop on grain production and 30 million excess death. Observational studies across China have indicated that individuals exposed famine was associated with higher prevalence of diabetes than unexposed counterparts [4], while the cause relationship was not well established. In the current study, we recruited two longitudinal studies from the Qingdao Diabetes Prevention Program to investigate the relationship between famine exposure in early life and type 2 diabetes incidence in adulthood in China. ...
... Several observational studies investigated that prenatal exposure in famine was associated with prevalence of type 2 diabetes, with an increased risk of odd ratios from 1.22 to 2.20 [10,11]. A metaanalysis found that individuals exposed in fetal stage was a 36% higher risk of type 2 diabetes, but not in child exposed, as compared with those unexposed counterparts [4], with the pooled RRs(95%CIs) of 1.36 (1.12-1.65) and 1.40 (0.98-1.99), respectively. ...
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Background: This study will investigate effect of famine exposure in early life associated with the risk of type 2 diabetes in adulthood during the Chinese Famine. Methods: A total of 3,418 individuals aged 35-74 years free of diabetes in 2006 and in 2009 study surveys, were prospectively followed up to 2009 and 2012, respectively. Individuals were grouped into non-exposed (1962-1978), fetal-exposed (1959-1961), childhood-exposed (1949-1958) and adolescence/adult-exposed cohorts (1931-1948). Logistic regression model was employed to assess effect of famine exposure on diabetes incidence, adjusting for potential covariates. Results: During a mean follow up of 3 years, the age-adjusted cumulative incidences of type 2 diabetes were 6.3%, 13.0% 11.0% and 13.8% in non-exposed, fetal, child and adolescence/adult-exposed cohorts, respectively (P=0.026). Compared with non-exposed individuals, relative risks (95% confidence intervals) for diabetes incidence were 2.15(1.29-3.60), 1.53(0.93-2.51), and 1.65(0.75-3.63) in those exposure in fetal, child and adolescence/adult, controlling for covariates. The interactions between famine exposure and obesity, education, family history of diabetes were not observed, except for famine exposure and residential areas. Individuals lived in rural areas increased risk for type 2 diabetes in fetal and child exposure, with an incidence relative risk (95% confidence interval) of 8.79(1.82-42.54) and 2.33(1.17-4.65), respectively. Conclusions: Our findings indicate that famine exposure in early life is an independent predictor on type 2 diabetes, particularly in women. The identification and intervention on critical time can prevent residents from diabetes in later life. The clinical trial was registered, more detail linked in https://clinicaltrials.gov/ct2/home, as registration no. NCT01053195.
... The Impact of Malnutrition in Early (4). Çok sayıda araştırma bulgusu, gen ekspresyonunun kontrolünde yer alan epigenetik mekanizmaların (DNA metilasyonu ve histon modifikasyonları) ve mikroR-NA etkileşimleri dâhil olmak üzere, erken yaşamdaki olumsuz durumlar ile daha sonraki yaşamda T2DM dâhil olmak üzere kronik hastalık riski arasındaki bağlantıya aracılık etmede merkezi bir rol oynadığını göstermektedir (5,6). ...
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Tip 2 diyabetes mellitus (T2DM) genetik, epigenetik ve çevresel faktörlerin karmaşık bir etkileşimi olan çok faktörlü bir hastalıktır. Tip 2 diyabetes mellitusun küresel sağlık ve ekonomik yük üzerinde önemli etkileri vardır. Biriken kanıtlar doğrultusunda bu hastalığın dünya genelinde insidansındaki artışı sadece genetik veya yetişkin çevresel koşullardan değil aynı zamanda yaşamın erken dönemlerindeki olumsuz durumlardan etkilenebileceğini düşündürmektedir. Son yıllarda, hem hayvan deneyleri hem de kıtlık gibi doğal durumlardan elde edilen kanıtlar, erken yaşamda yetersiz besin alımını, yetişkin yaşamındaki T2DM riski ile ilişkilendirmiştir. İntrauterin yetersiz besin alımı ile ortaya çıkan büyüme kısıtlamasının, fetal gelişimi bozabileceği ve böylece fetal yağ dokusu ve pankreatik beta hücre disfonksiyonuna neden olabileceğine dair kanıtlar vardır. Bunun sonucunda insülin sekresyon kapasitesinde azalma ve insülin direnci de dâhil olmak üzere, glukoz-insülin metabolizmasında kalıcı adaptif değişiklikler meydana gelebilir. Bu değişiklikler artan bir yağ depolama kabiliyetine yol açabilir, böylece birey daha sonraki yaşamda T2DM gelişimine yatkın hâle gelebilir. Bu ilişkide DNA metilasyonu, histon modifikasyonu ve mikroRNA etkileşimleri gibi epigenetik mekanizmalar temel rol oynamaktadır. Bu derlemede, T2DM patogenezinde gelişimsel epigenetik varyasyonun rolünü gösteren temel mekanizmalar ve araştırma bulguları özetlenmiştir.
... 22 23 A recent meta-analysis also showed that early-life famine exposure, especially fetal-infant exposure, may increase the risk of developing type 2 diabetes in adulthood. 24 With regard to postnatal famine exposure, we and others believe that there is a link between famine exposure and type 2 diabetes and the development of other metabolic diseases in China. 9 11 12 24 25 In this study, we found that the rates at 5 years of incident diabetes were highest in the fetal famine-exposed group (12.5%) and gradually decreased with increasing age in famine-exposed individuals (childhood-exposed: 10.6%; adolescence/ adult-exposed: 7.9%), and the ORs for incident diabetes also followed this trend (fetal-exposed: 2.97; childhoodexposed: 2.87; adolescence/adult-exposed: 2.01). ...
Article
Full-text available
Introduction: Exposure to malnutrition in early life has been found to significantly elevate type 2 diabetes risk in adulthood. However, the changes in metabolites resulting from malnutrition in early life have not been studied. The aim of this study was to identify metabolites with levels associated with type 2 diabetes resulting from exposure to China's Great Famine (1959-1962). Research design and methods: Participants were from SPECT-China 2014 and SPECT-China2 2019, two cross-sectional studies performed at the same site. In total, 2171 subjects participated in SPECT-China and SPECT-China2 simultaneously. The sample size of fetal-exposed (1959-1962) versus non-exposed (1963-1974) individuals was 82 vs 79 in 2014 and 97 vs 94 in 2019. Metabolomic profiling was performed between famine-exposed and non-exposed groups. Results: Among the different famine exposure groups, the fetal-exposed group (1959-1962) had the greatest incidence rate (12.5%), with an OR of 2.11 (95% CI 1.01 to 4.44), compared with the non-exposed group (1963-1974). Moreover, compared with those in the non-exposed group (1963-1974), four metabolites (indole-3-carbinol (I3C), phosphatidylcholine (PC) (22:6(4Z,7Z,10Z,13Z,16Z,19Z)/16:1(9Z)), pyrimidine, and PC(16:1(9Z)/22:5(4Z,7Z,10Z,13Z,16Z))) showed significantly lower relative intensities in the famine and diabetes groups both in 2014 and 2019. Pyrimidine significantly mediated the association of famine exposure with diabetes, and I3C marginally mediated this association. Conclusions: Famine exposure in the fetal period could increase type 2 diabetes risk in adults, even those in their 60s. I3C and pyrimidine are potential mediators of the effects of famine exposure on diabetes development.
... As a frequent comorbidity of stroke, MetS was not related to an increased risk of recurrence of minor or lacunar stroke, but concurrent MetS and T2D add the recurrence risk (45,46). Consistent and relatively robust correlation between early age exposure to the Chinese GLF and increased female-specific risk of MetS or T2D were discovered (11,19,20,(47)(48)(49). Our study detects the influence of the interaction between T2D and early-age famine exposure on long-term (12-month) stroke recurrence but no interaction between MetS and famine exposure. ...
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Background and Purpose: Early age exposure to the Chinese Great Leap Forward famine (1959–1961) is associated with the incidence of risk factors for ischemic stroke. This study aims to examine the relationship between early age famine exposure and 12-month stroke recurrence. We sought to explore the interaction between famine exposure status and metabolic phenotypes on stroke recurrence and how the adherence of crucial evidence-based key performance indicators (KPI) would modify this interaction. Methods: We analyzed data of patients who were born between 1953 and 1964 in the China National Stroke Registry II (CNSR-II). The study population was further divided into five subgroups for comparing 12-month stroke recurrence. A multivariate Cox proportional hazard regression model was used in analyzing the impact of the concurrence of metabolic phenotypes—type 2 diabetes (T2D) or metabolic syndrome (MetS)—and early-age famine exposure on recurrent risk. The influence of the adherence to predefined KPI and concurrency of metabolic phenotype was also evaluated. Results: Concurrent T2D and early age famine exposure was associated with an increased recurrence risk of ischemic stroke with 12 months [adjusted hazard ratio (HR): 1.63, 95% confidence interval (CI) 1.28–2.07]. Optimal adherence to KPI was not associated with significantly reduced risk of 12-month stroke recurrence (adjusted HR: 0.80, 95% CI: 0.51–1.26). Conclusions: Concurrency of early-age famine exposure and diabetes mellitus was associated with a higher risk of stroke recurrence within 12 months, and adherence to evidence-based KPI did not reduce the risk significantly.
... We have also noticed a growing interest in using meta-analysis to summarize effect estimates of famine effect on health outcomes [30][31][32][33]. Their findings can be misleading without a careful examination of above problems. ...
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Famines in human history have been widely used as natural experiments to study how early-life environments may influence adult health outcomes, including overweight/obesity, diabetes and schizophrenia.
... Some studies found that exposure to severe famine in the prenatal or postnatal period was associated with the development of type 2 diabetes in adulthood. Data from different periods of famine around the world have been utilized to explore the association of early life malnutrition and type 2 diabetes risk in adulthood, and the "famine effect" has been found in China and some foreign studies, including Asian, European, and African populations [4][5][6][7][8][9][10][11]. The individuals exposed to famine may involve adaptations to malnutrition, with fetal adaptations including reduced growth, small size at birth, or low birth weight [12]. ...
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Increasing studies have demonstrated that gene and famine may interact on type 2 diabetes risk. The data derived from the cross-sectional 2010–2012 China National Nutrition and Health Survey (CNNHS) was examined to explore whether gene and famine interacted to influence type 2 diabetes risk. In total, 2216 subjects were involved. The subjects born in 1960 and 1961 were selected as the famine-exposed group, whereas subjects born in 1963 were selected as the unexposed group. A Mass Array system was used to detect the genotypes of 50 related single-nucleotide polymorphisms (SNPs). Interactions were found between prenatal exposure to famine and ten SNPs (rs10401969, rs10886471, rs10946398, rs1470579, rs2796441, rs340874, rs3794991, rs5015480, rs7961581, and rs9470794) on type 2 diabetes risk after adjustments. The stratified results showed that famine exposure exacerbated the effect of CILP2-rs10401969 to fasting serum insulin (FINS), GRK5-rs10886471 to fasting plasma glucose (FPG) and FINS, IGF2BP2-rs1470579 to FINS, TLE1-rs2796441 to impaired fasting glucose (IFG), PROX1-rs340874 to impaired glucose tolerance (IGT), GATAD2A-rs3794991 to FINS, TSPAN8/LGR5-rs7961581 to FPG, and ZFAND3-rs9470794 to IGT and FINS. Famine exposure weakened the effect of CDKAL1-rs10946398 to type 2 diabetes. Famine exposure weakened the effect of HHEX-rs5015480 to IFG, but exacerbated the effect of HHEX-rs5015480 to FINS. The present study suggests that ten SNPs may affect type 2 diabetes risk in interaction with prenatal exposure to Chinese famine.
... A meta-analysis study also observed strong link between famine exposure and growing T2D risk in adulthood (95% CI = 1.17-1.63 and pooled RR (relative risk) = 1.38) (Liu et al., 2018). Adults which experienced famine in utero had poor tolerance of glucose in comparison to those who were not experienced famine (Ravelli et al., 1998). ...
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Objective: To investigate the effects of famine-experience during early life on diabetes mellitus and impaired fasting glucose in the adulthood. Methods: In a total of 101 510 employees who took part in the health examination at the Kailuan Group between 2006 to 2007 were recruited. All the study subjects were born in Hebei province between 1956-10-01 and 1964-09-30 but those who had incomplete data were excluded. 19 347 subjects were finally included for analysis. Members from the famine-exposed group were born between Oct. 1, 1959 and Sep. 30, 1961. There was a semi-exposed group with members born between Oct. 1, 1958 and Sept. 30, 1959 and from Oct. 1, 1961 to Sept. 30, 1962 but members from the control group were born from Oct. 1, 1956 to Sept. 30, 1958 and from Oct. 1, 1962 to Sept. 30, 1964. Prevalence rates on diabetes mellitus and the detection rate of impaired fasting glucose among the three groups were compared. Logistic regression model was used to analyze the effects of famine-experience during early life with the prevalence of diabetes mellitus and the detection rate of impaired fasting glucose during adulthood. Results: Prevalence of diabetes mellitus and the detection rate of impaired fasting glucose in the famine-exposed adult-cohort groups were 8.99%, 8.96% while 8.05% and 9.35% in the semi-exposure groups, 7.71% and 8.20% in the control group. Results from the multivariate logistic regression analysis showed that experiences of famine during early life increased the risk of diabetes mellitus and impaired fasting glucose in adulthood with the odds ratios as 1.218 (95% CI: 1.056-1.404, P = 0.007) and 1.142 (95% CI: 0.994-1.312, P = 0.061). After stratification by sex, odds ratios in males were 1.163 (95% CI: 1.001-1.350, P = 0.048)and 1.213(95% CI:1.039-1.417, P = 0.015). The odds ratios in females were 1.319 (95% CI: 0.920-1.891, P = 0.132) and 0.990 (95% CI: 0.679-1.444, P = 0.959). Conclusion: Experiences of famine during early life increased the risk of diabetes mellitus and impaired fasting glucose in the adulthood. However, this negative effect existed mainly in the males, according to the results from our study.
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Background: Previous studies suggest that exposure to starvation and stress between conception and early infancy may have deleterious effects on health later in life; this phenomenon is termed fetal origin of adult disease. Objectives: To determine whether exposure to the Holocaust from preconception to early infancy is a cause of chronic morbidity in adulthood. Methods: This pilot study involved 70 European Jews born in countries under Nazi rule (exposed group) during the period 1940-1945 who were interviewed to determine the presence of chronic diseases. A control group of 230 Israeli-born individuals of the same descent, age, and gender distribution were extracted from the Israel National Health Interview Survey-2 (unexposed group). The prevalence of selected risk factors and chronic diseases was compared between the groups. Results: The prevalence of cardiovascular risk factors and morbidity was significantly higher in the exposed group: body mass index (BMI) (29.06 +/- 3.2 vs. 26.97 +/- 4.42, P = 0.015), hypertension (62.9% vs. 43%, P = 0.003), dyslipidemia (72.9% vs. 46.1%, P < 0.001), diabetes (32.9% vs. 17.4%, P = 0.006), angina pectoris (18.6% vs. 4.8%, P = 0.001) and congestive heart failure (8.6% vs. 1.7%, P = 0.013). The prevalence of cancer (30.0% vs. 8.7% P < 0.001), peptic ulcer disease (21.4% vs. 7%, P = 0.001), headaches/migraines (24.3% vs. 12.6%, P < 0.001) and anxiety/depression (50.0% vs. 8.3%, P < 0.001) was also higher in the exposed group. Conclusions: These results suggest that exposure to Holocaust conditions in early life may be associated with a higher prevalence of obesity, dyslipidemia, diabetes, hypertension, cardiovascular morbidity, malignancy and peptic diseases in adulthood. These findings set the stage for further research, which might define those exposed as a high risk group for chronic morbidity.
Article
Nutritional conditions in early life may causally affect health at older ages. This paper examines the effects of early life exposure to the Dutch famine (Winter 1944-45) on the prevalence of heart diseases, peripheral arterial diseases (PAD) and diabetes mellitus (DM) at ages 60-76. Analyses are performed using data from the fifth cycle of the Longitudinal Aging Study Amsterdam. Exposure to the famine is determined by reported place of residence during the Dutch famine, with those living in the cities in the West of the Netherlands defined as exposed (n = 278) and those living in the rural areas in the West or living in the North or East defined as non-exposed (n = 521). We successively compare the prevalence of heart diseases, PAD and DM at ages 60-76 of 370 males and 429 females exposed and non-exposed to the famine in early life. We distinguish four age classes of exposure in early life: gestation and infancy (ages 0-1), childhood (age 1-5), pre-adolescence (ages 6-10) and adolescence (ages 11-14). The analysis shows that exposure to severe undernutrition at ages 11-14 is significantly associated with a higher probability of developing DM and/or PAD at ages 60-76. The associations are found only in women, but not in men. If suggests that adolescence may be a critical period with respect to exposure to adverse (nutritional) conditions and that research should take this into account. These findings are relevant for children in developing countries who are exposed to severe nutritional deprivation.