Saudi Journal of Kidney Diseases and Transplantation

REVIEW ARTICLE
Year
: 2019  |  Volume : 30  |  Issue : 2  |  Page : 299--308

Birth weight, gestational age, and blood pressure: Early life management strategy and population health perspective


Issa Al Salmi1, Faisal A M. Shaheen2, Suad Hannawi3,  
1 Department of Renal Medicine, The Royal Hospital, Muscat, Oman
2 The Saudi Center for Organ Transplantation, Riyadh, Saudi Arabia
3 Department of Medicine, Ministry of Health and Prevention, Dubai, UAE

Correspondence Address:
Issa Al Salmi
Department of Renal Medicine, The Royal Hospital, Muscat
Oman

Abstract

The incidence of hypertension (HTN) is rising worldwide with an estimated prevalence of 22%, 7.5 million deaths (12.8%). It is a major risk factor for coronary heart diseases and hemorrhagic strokes. In Oman, the crude prevalence of HTN was 33.1%, whereas the age-adjusted prevalence was 38.3%. Among Gulf Cooperation Countries, 47.2% of the individuals were hypertensive, and women were more likely to have HTN than men. Similarly, the prevalence of low-birth-weight (LBW) is also rising globally with the more prevalent incidence in developing countries reaching almost a rate just lower than 20.0/100 births. In Oman, the prevalence of LBW was 4.2% in 1980, which doubled (8.1%) in 2000 and has shown a slow but steady increase reaching 10.2% in 2013. LBW term is the most commonly used surrogate measure of intrauterine growth retardation and has been related to increased cardiovascular mortality, due to increased risk of cardiovascular risk factors, including blood pressure (BP), diabetes, cholesterol level, and other risk factors. The epidemiologic evidence clearly points to an inverse association between birth weight and many hemodynamic cardiovascular risk markers. Possible mechanisms operating in fetal life that might determine BP include the structural development of resistance arteries, the setting of hormone levels, and nephron endowment. Retarded fetal growth leads to permanently reduced cell numbers in the kidney. Patients with high BP had almost 50% less number of glomeruli compared to that of the normotensive individuals, and subsequent accelerated growth may lead to excessive metabolic demand on this limited cell mass. It is not merely a reduced nephron number that is responsible for HTN, but compensatory maladaptive changes that occur internally when nephrogenesis is compromised. The likelihood of an adverse outcome is greatly amplified in those born with LBW who later develop obesity or an increased ponderal index.



How to cite this article:
Al Salmi I, M. Shaheen FA, Hannawi S. Birth weight, gestational age, and blood pressure: Early life management strategy and population health perspective.Saudi J Kidney Dis Transpl 2019;30:299-308


How to cite this URL:
Al Salmi I, M. Shaheen FA, Hannawi S. Birth weight, gestational age, and blood pressure: Early life management strategy and population health perspective. Saudi J Kidney Dis Transpl [serial online] 2019 [cited 2019 May 24 ];30:299-308
Available from: http://www.sjkdt.org/text.asp?2019/30/2/299/256836


Full Text



 Introduction



Hypertension (HTN) continues to be one of the main risk factors for cardiovascular disease (CVD) worldwide. It is a leading risk factor for morbidity and mortality in the world. The reported prevalence of HTN varies worldwide, with the lowest prevalence in rural India (3.4% in men and 6.8% in women) and the highest prevalence in Poland (68.9% in men and 72.5% in women).[1] Approximately 75 million adults have been diagnosed with HTN in the United States, and among Industrialized countries, it affects 25%–35% of individuals globally. HTN is estimated to cause 4.5% of the current global disease burden and is prevalent in many developing countries as in the developed world.[1]

In Oman, the age-adjusted prevalence of the metabolic syndrome was 21.0%, and over 87% of Omanis had at least one CVD risk factor (38% had hyperglycemia, 19% HTN and 34.5% had high total cholesterol).[2],[3] In Gulf Cooperation Countries (GCC) which consists of six countries, Bahrain, Kuwait, Oman, Qatar, Saudi Arabia, and United Arab Emirates (UAE), HTN ranged from 20.9 to 53%.[4],[5] The prevalence of HTN was also high among women in GCC countries. Data from the Second Gulf Registry of Acute Coronary Events (GulfRACE-2) showed that 47.2% of the registered individuals were hypertensive, and women were more likely to have HTN than men. It is forecasted that the number of people affected by HTN will endure a very high upsurge and, by 2025, approximately 1.5 billion individuals will be affected.[6]

Birth weight varies globally. The highest proportion of low-birth-weight (LBW) babies in the world are born in Indian sub-continent where LBW babies are born at rate just lower than 20.0/100 births.[7] In Oman, LBW was 10.2% out of a total live birth of over 66,000 live birth during 2013. The worldwide prevalence of LBW is 15.5%, which amounts to about 20 million LBW infants born each year, 96.5% of them in the developing countries.[7] LBW has been increasing globally and regionally with various advancement in medical care; including that of obstetric and neonatal care and technological development with restricted growth, and pregnancy complications are taking place as live births. For example, in Oman, the prevalence of LBW was 4.2% in 1980, which doubled (8.1%) in 2000 and has shown a slow but steady increase reaching 10.2% in 2013.[8] This also causes an increase in the rate of LBW infants, and subsequently an increased rate of long-term medical sequelae.

Recently, over the last few decades, much attention has been steered toward the contribution of the intrauterine environment to the development of chronic and noncommunicable diseases (NCD). Epidemiological studies have demonstrated that a poor intrauterine environment is associated with an increased risk of HTN, chronic kidney disease, and diabetes.[7],[8],[9] Barker and Martyn hypothesized that nutrient deprivation during distinct periods of organ development prenatally programs the offspring for CVD later in life.[7],[8] It is now well proven that LBW, reflecting a poor intrauterine environment,[10] is associated with diminished nephron endowment and other pathophysiological mechanisms predisposing to the development of high blood pressure (BP).[11],[12]

 Epidemiological Evidence of the Relationship between Birth Weight and Blood Pressure



Essential HTN is multi-factorial in the cause, with both genetic and environmental components.[10] Several epidemiological studies have reported that LBW is associated with increased BP throughout various stages of life including infancy,[13] childhood,[11],[12],[13] childhood-adult,[14],[15],[16],[17] and adult life.[18],[19],[20] However, this relationship also has an important relation to catch up growth.[21],[22],[23]

A systematic review of 34 studies, based on >66,000 people, found that in both adults and prepubertal children, there was a consistent negative relationship between birth weight and current BP.[24] Another systemic review of more than 80 studies confirmed the inverse relationship between birth weight and BP.[25] However, others had criticized the claims of a strong inverse association between birth weight and subsequent BP may chiefly reflect the impact of random error, selective emphasis of particular results, and inappropriate adjustment for current weight and for confounding factors. Their systemic review findings suggest that birth weight is of little relevance to BP levels in later life.[10] The magnitude of the birth weight–BP association was found to increase with increasing age from childhood to adulthood.

Huxley et al review of 45 pediatric and adult studies reported a negative relationship between birth weight and systolic BP. They reported that for each one-kilogram increase in birth weight was associated with an almost 2 mm Hg/kg decrease in systolic BP.[10],[23] Other reviews of adult studies also were consistent with the earlier ones which showed a similar consistent negative association between birth weight and BP.[21],[22] Of the 28 cohort studies, 25 studies found an inverse association; however, not all were adjusted for body mass index (BMI). More recently, a meta-analysis of 27 studies conducted between 1995 and 2012 found that LBW (<2500 g) compared with birth weight greater than 2500 g was associated with an increased risk of HTN (odds ratio 1.21; 95% confidence interval 1.13, 1.30).[24],[25] Al Salmi et al took advantage of the longitudinal population-based resources of the AusDiab study (the Australian Diabetes, Obesity, and Lifestyle study), which is the national Australian longitudinal population-based study, to examine the prevalence and incidence of diabetes and its complications, to examine the associations of birth weight and BP in the general adult population of Australia.[26],[27],[28],[29],[30],[31],[32],[33],[34],[35],[36],[37],[38],[39],[40],[41],[42],[43] It is the first study of its kind to examine the effect of birth weight on the development of multiple of chronic diseases in a representative adult population. A significant association was identified between birth weight and systolic BP, diastolic BP, and HTN. This applied in analyses of unadjusted data in females and significance relationship persisted with adjustment for the age and current body size for both females and males. Furthermore, the relationship persisted with adjustment for physical activity, smoking, alcohol intake, family history, and current socioeconomic status.[31],[32],[33],[34]

Amplification of birth weight effect

The likelihood of an adverse outcome is greatly amplified in those born with LBW, who later develop obesity or an increased ponderal index (weight × 100]/(length3). Conversely, those born with LBW, who continue to be small or thin, are relatively protected in terms of metabolic demand in adult life.[28] Hence, researchers found that the rise of BP with age is closely related to growth and is accelerated by the adolescent growth spurt.[19],[44] An interaction between prenatal exposure and postnatal dietary intake may determine the level of HTN.[45] A study of children concluded that LBW, in combination with high current BMI, seems to be of particular importance in the development of high BP.[46]

While the relationship has been detected at different ages, the strength of the inverse relationship increases with age such that among 64–71 years old, systolic BP was decreased by 5.2 mm Hg for each kilogram increase in weight at birth.[14],[19],[47] Law et al concluded that essential HTN is initiated in fetal life.[19],[48],[49] A raised BP is then augmented from early child period to old age, perhaps by a positive feedback mechanism[19],[48],[49] that progressively changes the structure or compliance of blood vessels. The vascular structure and compliance change with hemodynamic load with an increase in peripheral resistance and pulse pressure in early life could alter the structure and reduce compliance, which in turn would increase pulse pressure.[22] A meta-regression analysis presented evidence for the age-dependent association between birth weight and systolic BP.[24],[50] In addition, the inverse association between birth weight and systolic BP is amplified with age, with longitudinal BP measurements during adulthood, and the association was largely accounted for by current weight.[19],[22],[51],[52] The observation on the age amplification of the effect of birth weight indicates that fetal programming and the increasing burden of unhealthy lifestyle behaviors affect the development of adult HTN synergistically.[53] There are indications that ethnicity may modify the relationship between measures of body size and BP.[54] Ethnic differences in these associations might be due to differences in body composition, a parameter frequently compared between ethnic groups.

Numerous mechanisms interplay in the pathophysiology role in the association between body size and elevated BP. First, obesity and central body fat mass damage microvascular function that, in turn, may lead to the development of HTN. Second, obesity leads to enhanced secretion of inflammatory markers such as adipokines and cytokines, in addition to higher C-reactive protein (CRP) levels; a marker of inflammation which interfere with the normal physiological process, leading to HTN.[55],[56],[57],[58]

Earlier reports in adults and adolescents show that BP tended to be less influenced by BMI in Blacks compared to Whites. Others found a small regression coefficient in the non-Caucasian-Caribbean children, although these were not significantly different from the Dutch. Furthermore, Black-Africans in showed a highly similar association with the Dutch children.[59],[60]

Both cross-sectional and longitudinal studies have investigated the association between BMI and waist-hip ratio or waist circumstance with BP, but rarely considered the use of more directly assessed fat mass.[61] However, others found positive associations between BP and fat mass, which was determined by dual-energy X-ray absorptiometry. In addition, studies using bio-impedance to determine fat mass also found correlations with BP.[62],[63]

Blood pressure mechanisms in low-birth-weight individuals

[Table 1] demonstrates possible physiological attributes for the development of high BP in LBW individuals.[64],[65],[66],[67],[68],[69],[70],[71],[72],[73],[74],[75],[76],[77],[78],[79],[80],[81] Possible mechanisms operating in fetal life that might determine BP include the structural development of resistance arteries, setting of hormone levels, and nephron endowment.[82],[83],[84],[85]{Table 1}

Of these, nephron endowment seems to have received the most attention so far. A physiological basis for elevation in BP associated with LBW is not clear.

During maternal undernutrition, maternal glucocorticoids increase and this excess exposure of the fetus to maternal GC constitutes at least part of the “programming” stimulus.[59],[60],[61] The kidneys have higher levels of Angiotensin type 1 receptor following exposure to a low-protein diet in utero suggesting a role in the programming of HTN.[73],[74],[75] Receptor stimulation, via hormonal binding, mediates an increase in BP by promoting vasoconstriction.[86],[87],[88]

In addition, a decrease in arterial compliance is associated with elevated BP and HTN.[89],[90] A study of 337 men and women born in the Jessop Hospital, Sheffield, between 1939 and 1940 showed that the elasticity of the aorta was directly related to size at birth, birth weight (pounds); abdominal circumference (inches) and occipitofrontal circumference (inches), among 50-year-old men and women.[70] This decrease in arterial compliance, that is inversely related to pulse wave velocity as measured by transit times of blood flow pressure wave in aorto-iliac and femoro-popliteal-tibial arterial segments, in lower birth weight subjects is probably due to a decrease in the amount of elastin present in the vessel’s wall resulting from in utero effects on vascular elastogenesis.[71]

Nephron and blood pressure

HTN might originate through retarded growth in utero followed by accelerated post-natal growth as a result of good living conditions.[72] Retarded fetal growth leads to permanently reduced cell numbers in the kidney and other tissues, and subsequent accelerated growth may lead to excessive metabolic demand on this limited cell mass. The kidney plays a major role in the regulation of systemic BP. It is also known that BP gets disturbed, in both animals and humans, following kidney resection or experimental reduction of kidney mass.[76]

In 1933, Hayman and Johnson reported a close inverse correlation between nephron number and BP.[91] Weder and Schork postulated that BP increases in parallel with growth to match kidney function to the increased demands of greater body mass.[75] They suggested that where kidney growth lags behind somatic growth, sodium retention is favoured and BP rises, thereby predisposing to HTN.[75] Subsequently, it was suggested that a reduced number of nephrons, either genetically determined or acquired in utero, provides an explanation for retardation of kidney growth.[58]

Keller et al studied the kidneys of 10 patients who had primary HTN and died in accidents.[76] They found that the number of nephrons was reduced in white patients with primary HTN. It is not merely a reduced nephron number that is responsible for HTN, but compensatory maladaptive changes that occur internally when nephrogenesis is compromised [Figure 1].{Figure 1}

Brenner et al hypotheses, during late 1980s, that a low nephron number is a risk factor for high BP in later life. The hypothesis stated that a reduction in the total filtration surface area of the kidneys is associated with a compensatory increase in the single nephron glomerular filtration rate.[9],[83],[85],[92],[93] This reduction of nephron number leads to an adaptive structural change that occur within the nephron including glomerular and tubular enlargement and an increase in the number of glomerular capillaries. Subsequently, the afferent arteriole dilates while the efferent arteriole constricts resulting in an increase in the glomerular capillary pressure. This reduction in the afferent arteriolar resistance further fuels an increased transmittance of systemic BP into the glomerulus.[92],[94],[95],[96] Hence, physiological changes occur that contribute to the development of HTN including increased salt reabsorption, higher volume strokes and cardiac output, and resetting of the pressure-natriuresis curve.[97] Pathological changes such as podocyte detachment and tuft adhesion to Bowman’s capsule have been noted in sclerosed kidneys compensating for hyper-filtration (e.g., secondary to vesicoureteral reflux).[83],[93],[98] Over time, this sclerosis of the glomeruli fuels a vicious cycle resulting in a decreased nephron number, the compensatory glomerular hypertrophy, and the progressive HTN and chronic kidney disease.[9],[83],[85],[92],[93] Nephrons that hypertrophied get atrophy sooner, causing further decrease in the number of nephrons.[9],[83],[85],[92],[93] Patients with high BP had almost 50% less number of glomerular number compared to that of the normotensive individuals.[94]

In conclusion, much epidemiological and laboratory evidence suggests that LBW is a risk factor for the development of HTN. However, most studies found significant results when adjustment made for BMI and without considering other factors such as smoking status, alcohol intake, physical activity and socioeconomic status. Oman, like many developing countries, has very high prevalence of NCD and similarly has very high LBW. Hence, determining the mechanisms of HTN that may result from fetal programming is critical in reducing the incidence of future HTN. Most importantly, health care provision to mother and fetus is of great importance to ameliorate the development of LBW. Utmost importance as well, is the provision of life long surveillance of risk factors and markers of development of NCD including HTN in this specific group of population to enable early health care strategy to be instituted to further reduce the burden of disease and provide cost-effective medical strategies.

Conflict of interest: None declared.

References

1Kearney PM, Whelton M, Reynolds K, Whelton PK, He J. Worldwide prevalence of hypertension: a systematic review. J Hypertens 2004;22:11-9.
2Al-Lawati JA, Jousilahti P. Body mass index, waist circumference and waist-to-hip ratio cutoff points for categorisation of obesity among Omani Arabs. Public Health Nutr 2008;11: 102-8.
3Al-Lawati JA, Mohammed AJ, Al-Hinai HQ, Jousilahti P. Prevalence of the metabolic syndrome among Omani adults. Diabetes Care 2003;26:1781-5.
4Al-Said J. The prevalence of hypertension in Persian Gulf countries and its correlation with demographic and socio-economic factors. J Hypertens 2005;23:1275-7.
5Shaheen FA, Al Wakeel J, Al-Ghamdi SM, et al. Cardiovascular and cerebrovascular comorbidities in hemodialysis patients from the Gulf Cooperation Council countries enrolled in the dialysis outcome and practice pattern study phase 5 (2012-2015). Saudi J Kidney Dis Transpl 2016;27(6 Suppl 1):S24-30.
6Kearney PM, Whelton M, Reynolds K, Muntner P, Whelton PK, He J. Global burden of hypertension: analysis of worldwide data. Lancet 2005;365:217-23.
7Barker DJ, Martyn CN. The fetal origins of hypertension. Adv Nephrol Necker Hosp 1997; 26:65-72.
8Barker DJ, Osmond C, Forsen TJ, Kajantie E, Eriksson JG. Trajectories of growth among children who have coronary events as adults. N Engl J Med 2005;353:1802-9.
9Brenner BM, Chertow GM. Congenital oligonephropathy and the etiology of adult hypertension and progressive renal injury. Am J Kidney Dis 1994;23:171-5.
10Huxley R, Neil A, Collins R. Unravelling the fetal origins hypothesis: is there really an inverse association between birthweight and subsequent blood pressure? Lancet 2002;360: 659-65.
11Brenner BM, Chertow GM. Congenital oligonephropathy: an inborn cause of adult hypertension and progressive renal injury? Current Opin Nephro Hypertens 1993;2:691-5.
12Whincup PH, Bredow M, Payne F, Sadler S, Golding J. Size at birth and blood pressure at 3 years of age. The Avon Longitudinal Study of Pregnancy and Childhood (ALSPAC). Am J Epidemiol 1999;149:730-9.
13Ley D, Stale H, Marsal K. Aortic vessel wall characteristics and blood pressure in children with intrauterine growth retardation and abnormal foetal aortic blood flow. Acta Paediatr 1997;86(3):299-305.
14Barker DJ, Osmond C, Golding J, Kuh D, Wadsworth ME. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ 1989;298: 564-7.
15Singh GR, Hoy WE. The association between birthweight and current blood pressure: a cross-sectional study in an Australian Aboriginal community. Med J Aust 2003;179:532-5.
16Falkner B. Birth weight as a predictor of future hypertension. Am J Hypertens 2002;15(2 Pt 2):43S-5S.
17Gennser G, Rymark P, Isberg PE. Low birth weight and risk of high blood pressure in adulthood. Br Med J (Clin Research Ed) 1988; 296:1498-500.
18Curhan GC, Willett WC, Rimm EB, Spiegelman D, Ascherio AL, Stampfer MJ. Birth weight and adult hypertension, diabetes mellitus, and obesity in US men. Circulation 1996;94:3246-50.
19Law CM, de Swiet M, Osmond C, et al. Initiation of hypertension in utero and its amplification throughout life. BMJ 1993;306: 24-7.
20Wadsworth ME, Cripps HA, Midwinter RE, Colley JR. Blood pressure in a national birth cohort at the age of 36 related to social and familial factors, smoking, and body mass. Br Med J (Clin Research Ed) 1985;291:1534-8.
21Adair LS. Developing world perspective: the importance of growth for short-term health. Nestle Nutr Workshop Ser Pediatr Program 2010;65:71-9; discussion 79-83.
22Adair LS, Martorell R, Stein AD, et al. Size at birth, weight gain in infancy and childhood, and adult blood pressure in 5 low- and middle-income-country cohorts: when does weight gain matter? Am J Clin Nutr 2009;89:1383-92.
23Huxley RR, Shiell AW, Law CM. The role of size at birth and postnatal catch-up growth in determining systolic blood pressure: a systematic review of the literature. J Hypertens 2000;18:815-31.
24Gamborg M, Byberg L, Rasmussen F, et al. Birth weight and systolic blood pressure in adolescence and adulthood: meta-regression analysis of sex- and age-specific results from 20 Nordic studies. Am J Epidemiol 2007;166: 634-45.
25Mu M, Wang SF, Sheng J, et al. Birth weight and subsequent blood pressure: a meta-analysis. Arch Cardiovasc Dis 2012;105:99-113.
26Al Salmi I, Hoy W, Gray P, Lamont T, Hannawi S. Reduced kidney volume in premature compared to full term children: preliminary results. Early Hum Dev 2007;83(Suppl 1):S109-10.
27Al Salmi I, Hoy W, Kondalsamy-Chennakesavan S, et al. Lower glomerular filtration rate in adults with low birthweight: results from the AusDiab study. Early Hum Dev 2007;83(Suppl 1):S109.
28Al Salmi I, Hoy W, Kondalsamy-Chennakesavan S, Wang Z, Barr E, Shaw J. Birthweight is inversely correlated with blood pressure independent of socioeconomic status: results from the AusDiab study. Early Hum Dev 2007;83 (Suppl 1):S109.
29Al Salmi I, Hoy W, Kondalsamy-Chennakesavan S, et al. Metabolic syndrome associated with birthweight in females more than males: Results from the AusDiab study. Early Hum Dev 2007;83(Suppl 1):S138.
30Al Salmi I, Hoy W, Kondalsamy-Chennakesavan S, et al. Chronic kidney disease patients have lower birth weight than the general Australian population. Nephrology (Carlton). 2006;11 (Suppl 2): A9: 1522.
31Al Salmi I, Hoy W, Wang Z, Gobe G, Barr E, Shaw J. Birthweight is inversely correlated with type 2 diabetes mellitus in the general population: results from the Ausdiab study. Diabetic Medicine 2006;23:iv-788. A692.
32Al Salmi I, Hoy W, Wang Z, Gobe G, Barr E, Shaw J. Birthweight is inversely correlated with indices of glycemia in the general population: results from the Ausdiab study. Diabet Med 2006;23(s4):iv-788. P1633.
33Al Salmi I, Hoy W, Wang Z, Gobe G, Barr E, Shaw J. Lower birthweights pre-dispose to the metabolic syndrome: results from the Ausdiab study. Diabet Med 2006;23(s4):iv-788. p2095.
34Al Salmi I, Hoy W, Wang Z, et al. Body composition and birthweight-results from the AusDiab study. Obes Rev 2006;7(Suppl 2): 153-4, A0135.
35Al Salmi I, Hoy W, Wang Z, Gobe G, Barr E, Shaw J. Metabolic syndrome and birthweight-results from the AusDiab study. Obes Rev 2006;7(Suppl 2):258, A0502.
36Al Salmi I, Hoy W, Wang Z, Gobe G, Barr E, Shaw J. Glucose disorders and birthweight-results from the AusDiab study. Obes Rev 2006;7(Suppl 2):258, A0503.
37Al Salmi I, Hoy W, Wang Z, Gobe G, Shaw J. Birth weight and Blood pressure-Results from AusDiab survey. Nephrology (Carlton). 2005; 10(3):A411.
38Al Salmi I, Hoy W, Wang Z, Gobe G, Shaw J. Urinary albumin creatinine Ratio levels are higher in low birthweight than normal birth-weight Australian: results from the AusDiab study. Nephrology (Carlton) 2006;11(Suppl 2): A51: 2560.
39Al Salmi I, Hoy W, Wang Z, Gobe G, Shaw J. Lower glomerular filtration rate among low birthweight people in the general Australian population: results from the AusDiab study. Nephrology (Carlton) 2006;11(Suppl 2):A49: 2555.
40Al Salmi I, Hoy W, Wang Z, Shaw J. Metabolic Syndrome and Birtheight-Results from the AusDiasb Survey. Diab Vascular Dis Res 2005;2:161.
41Al Salmi I, Hoy WE, Kondalsamy-Chennakes S, Wang Z, Healy H, Shaw JE. Birth weight and stages of CKD: a case-control study in an Australian population. Am J Kidney Dis 2008; 52(6):1070-8.
42Al Salmi I, Hoy W, Kondalsamy-Chennakesavan S, et al. Disorders of glucose regulation in adults and birth weight: results from the Australian Diabetes, Obesity and Lifestyle (AUSDIAB) Study. Diabetes Care 2008;31 (1):159-64.
43Al Salmi I, Kamble P, Jha A, Hannawi S. LBW people were predisposed to higher rates of kidney disease in adult life. World Congress of Nephrology, confirmation number is 1328; 2011; Vancouver, Canada.
44Barker DJ, Osmond C. Low birth weight and hypertension. BMJ 1988;297:134-5.
45Vickers MH, Breier BH, Cutfield WS, Hofman PL, Gluckman PD. Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. American J Physiol Endocrinol Metab 2000;279:E83-7.
46Uiterwaal CS, Anthony S, Launer LJ, et al. Birth weight, growth, and blood pressure: an annual follow-up study of children aged 5 through 21 years. Hypertension 1997;30(2 Pt 1):267-71.
47Whincup P, Cook D, Papacosta O, Walker M. Birth weight and blood pressure: cross sectional and longitudinal relations in childhood. BMJ 1995;311:773-6.
48Law C. Fetal influences on adult hypertension. J Hum Hypertens 1995;9:649-51.
49Li L, Law C, Power C. Body mass index throughout the life-course and blood pressure in mid-adult life: a birth cohort study. J Hypertens 2007;25(6):1215-23.
50Gamborg M, Andersen PK, Baker JL, et al. Life course path analysis of birth weight, childhood growth, and adult systolic blood pressure. Am J Epidemiol 2009;169(10):1167-78.
51Barker DJ, Forsen T, Eriksson JG, Osmond C. Growth and living conditions in childhood and hypertension in adult life: a longitudinal study. J Hypertens 2002;20:1951-6.
52Barker DJ, Gelow J, Thornburg K, Osmond C, Kajantie E, Eriksson JG. The early origins of chronic heart failure: impaired placental growth and initiation of insulin resistance in childhood. Eur J Heart Fail 2010;12:819-25.
53Chen W, Srinivasan SR, Berenson GS. Amplification of the association between birthweight and blood pressure with age: the Bogalusa Heart Study. J Hypertens 2010;28 (10):2046-52.
54Xu J, Barinas-Mitchell E, Kuller LH, Youk AO, Catov JM. Maternal hypertension after a low-birth-weight delivery differs by race/ ethnicity: evidence from the National Health and Nutrition Examination Survey (NHANES) 1999-2006. PLoS One 2014;9:e104149.
55Bennett NR, Ferguson TS, Bennett FI, et al. High-Sensitivity C-Reactive Protein is Related to Central Obesity and the Number of Metabolic Syndrome Components in Jamaican Young Adults. Front Cardiovasc Med 2014;1: 12.
56Joo Turoni C, Chaila Z, Chahla R, Bazan de Casella MC, Peral de Bruno M. Vascular Function in Children with Low Birthweight and Its Relationship with Early Markers of Cardiovascular Risk. Horm Res Paediatr 2016;85:396-405.
57Seven E. Overweight, hypertension and cardiovascular disease: focus on adipocytokines, insulin, weight changes and natriuretic peptides. Dan Med J 2015;62:B5163.
58Vargas R, Ryder E, Diez-Ewald M, et al. Increased C-reactive protein and decreased Interleukin-2 content in serum from obese individuals with or without insulin resistance: Associations with leukocyte count and insulin and adiponectin content. Diabetes Metab Syndr 2016;10(1 Suppl 1):S34-41.
59LA de Hoog, M, van Eijsden M, Stronks K, Gemke RJ, Vrijkotte TG. Association between body size and blood pressure in children from different ethnic origins. Cardiovasc Diabetol 2012;11:136.
60Painter RC, de Rooij SR, Bossuyt PM, et al. Maternal nutrition during gestation and carotid arterial compliance in the adult offspring: the Dutch famine birth cohort. J Hypertens 2007; 25(3):533-40.
61Minooee S, Ramezani Tehrani F, Mirmiran P, Azizi F. Low birth weight may increase body fat mass in adult women with polycystic ovarian syndrome. Int J Reprod Biomed (Yazd). 2016;14:335-40.
62Hokken-Koelega AC, van Pareren Y, Sas T, Arends N. Final height data, body composition and glucose metabolism in growth hormone-treated short children born small for gestational age. Horm Res 2003;60 Suppl 3:113-4.
63Khandelwal P, Jain V, Gupta AK, Kalaivani M, Paul VK. Association of early postnatal growth trajectory with body composition in term low birth weight infants. J Dev Orig Health Dis 2014;5:189-96.
64Barker DJ. The malnourished baby and infant. Br Med Bull 2001;60:69-88.
65Maruyama K, Koizumi T. Superior mesenteric artery blood flow velocity in small for gestational age infants of very low birth weight during the early neonatal period. J Perinat Med 2001;29:64-70.
66Goodfellow J, Bellamy MF, Gorman ST, et al. Endothelial function is impaired in fit young adults of low birth weight. Cardiovasc Res 1998;40:600-6.
67Szathmari M, Vasarhelyi B, Tulassay T. Effect of low birth weight on adrenal steroids and carbohydrate metabolism in early adulthood. Horm Res 2001;55:172-8.
68Cambien F, Leger J, Mallet C, Levy-Marchal C, Collin D, Czernichow P. Angiotensin I-converting enzyme gene polymorphism modulates the consequences of in utero growth retardation on plasma insulin in young adults. Diabetes 1998;47:470-5.
69Vasarhelyi B, Kocsis I, Schuler A, Nobilis A, Tulassay T. G protein in very low birth-weight infants. Lancet 2000;356:254.
70Byrne CD, Phillips DI. Fetal origins of adult disease: epidemiology and mechanisms. J Clin Pathol 2000;53:822-8.
71Langley-Evans SC. Fetal programming of cardiovascular function through exposure to maternal undernutrition. Proc Nutr Soc 2001; 60:505-13.
72Hawkins P, Steyn C, McGarrigle HH, Calder NA, Saito T, Stratford LL, et al. Cardiovascular and hypothalamic-pituitary-adrenal axis development in late gestation fetal sheep and young lambs following modest maternal nutrient restriction in early gestation. Reprod Fertility Dev 2000;12:443-56.
73McMullen S, Gardner DS, Langley-Evans SC. Prenatal programming of angiotensin II type 2 receptor expression in the rat. Br J Nutr 2004;91:133-40.
74Sahajpal V, Ashton N. Renal function and angiotensin AT1 receptor expression in young rats following intrauterine exposure to a maternal low-protein diet. Clin Sci (Lond) 2003;104:607-14.
75Vehaskari VM, Stewart T, Lafont D, Soyez C, Seth D, Manning J. Kidney angiotensin and angiotensin receptor expression in prenatally programmed hypertension. Am J Physiol Renal Physiol 2004;287:F262-7.
76Brenner BM, Garcia DL, Anderson S. Glomeruli and blood pressure. Less of one, more the other? Am J Hypertens 1988;1(4 Pt 1):335-47.
77Vasarhelyi B, Dobos M, Reusz GS, Szabo A, Tulassay T. Normal kidney function and elevated natriuresis in young men born with low birth weight. Pediatr Nephrol 2000;15:96-100.
78Martyn CN, Greenwald SE. Impaired synthesis of elastin in walls of aorta and large conduit arteries during early development as an initiating event in pathogenesis of systemic hypertension. Lancet 1997;350:953-5.
79Martin H, Hu J, Gennser G, Norman M. Impaired endothelial function and increased carotid stiffness in 9-year-old children with low birthweight. Circulation 2000;102(22): 2739-44.
80McAllister AS, Atkinson AB, Johnston GD, McCance DR. Relationship of endothelial function to birth weight in humans. Diabetes Care 1999;22:2061-6.
81Tooke JE, Hannemann MM. Adverse endothelial function and the insulin resistance syndrome. J Intern Med 2000;247:425-31.
82Abitbol CL, Rodriguez MM. The long-term renal and cardiovascular consequences of prematurity. Nat Rev Nephrol 2012;8:265-74.
83Brenner BM, Mackenzie HS. Nephron mass as a risk factor for progression of renal disease. Kidney Int Suppl 1997;63:S124-7.
84Mackenzie HS, Brenner BM. Fewer nephrons at birth: a missing link in the etiology of essential hypertension? Am J Kidney Dis 1995;26:91-8.
85Mackenzie HS, Lawler EV, Brenner BM. Congenital oligonephropathy: The fetal flaw in essential hypertension? Kidney Int Suppl 1996; 55:S30-4.
86Ichinomiya K, Maruyama K, Inoue T, et al. Perinatal factors affecting serum hepcidin levels in low-birth-weight infants. Neonatology 2017; 112(2):180-6.
87Lybbert J, Gullingsrud J, Chesnokov O, et al. Abundance of megalin and Dab2 is reduced in syncytiotrophoblast during placental malaria, which may contribute to low birth weight. Sci Rep 2016;6:24508.
88Schultz NS, Broholm C, Gillberg L, et al. Impaired leptin gene expression and release in cultured preadipocytes isolated from individuals born with low birth weight. Diabetes 2014;63:111-21.
89Relf IR, Lo CS, Myers KA, Wahlqvist ML. Risk factors for changes in aorto-iliac arterial compliance in healthy men. Arteriosclerosis 1986;6:105-8.
90Girerd X, Laurent S, Pannier B, Asmar R, Safar M. Arterial distensibility and left ventricular hypertrophy in patients with sustained essential hypertension. Am Heart J 1991;122(4 Pt 2):1210-4.
91Hayman JM, Johnston SM. Experiments on the relation of creatinine and urea clearance Tests of kidney function and the number of glomeruli in the human kidney obtained at autopsy. J Clinical Invest 1933;12:877-84.
92Brenner BM. The etiology of adult hypertension and progressive renal injury: an hypothesis. Bull Mem Acad R Med Belg 1994;149: 121-5; discussion 5-7.
93Luyckx VA, Shukha K, Brenner BM. Low nephron number and its clinical consequences. Rambam Maimonides Med J 2011;2:e0061.
94Keller G, Zimmer G, Mall G, Ritz E, Amann K. Nephron number in patients with primary hypertension. N Engl J Med 2003;348:101-8.
95Koike K, Ikezumi Y, Tsuboi N, et al. Glomerular density and volume in renal biopsy specimens of children with proteinuria relative to Preterm birth and gestational age. Clin J Am Soc Nephrol 2017;12:585-90.
96Zandi-Nejad K, Luyckx VA, Brenner BM. Adult hypertension and kidney disease: the role of fetal programming. Hypertension 2006; 47:502-8.
97Perala MM, Moltchanova E, Kaartinen NE, et al. The association between salt intake and adult systolic blood pressure is modified by birth weight. Am J Clin Nutr 2011;93:422-6.
98Kandasamy Y, Smith R, Wright IM, Lumbers ER. Relationships between glomerular filtration rate and kidney volume in low-birth-weight neonates. J Nephrol 2013;26:894-8.