Skip Navigation


NDT Advance Access originally published online on August 25, 2006
Nephrology Dialysis Transplantation 2006 21(12):3422-3427; doi:10.1093/ndt/gfl466
This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow All Versions of this Article:
21/12/3422    most recent
gfl466v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrowRequest Permissions
Right arrow Disclaimer
Google Scholar
Right arrow Articles by Giapros, V.
Right arrow Articles by Andronikou, S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Giapros, V.
Right arrow Articles by Andronikou, S.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?

© The Author [2006]. Published by Oxford University Press on behalf of ERA-EDTA. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

Kidney growth in small-for-gestational-age infants: evidence of early accelerated renal growth

Vasileios Giapros1, Aikaterini Drougia1, Efthalia Hotoura1, Frederica Papadopoulou2, Maria Argyropoulou2 and Styliani Andronikou1

1Neonatal Intensive Care Unit and 2Radiology Department, University Hospital of Ioannina, Ioannina, Greece

Correspondence and offprint requests to: Vasileios Giapros, University Hospital of Ioannina PO Box 1186, Ioannina 451 10, Greece. Email: vgiapros{at}cc.uoi.gr



   Abstract
Top
 Abstract
Introduction
 Patients and methods
 Results
 Discussion
 Conclusion
 References
 
Background. Very few data are available on longitudinal renal growth in small for gestational age (SGA) infants born at term. The aim of this prospective study was to estimate comparatively the renal growth in SGA infants and in infants born appropriate for gestational age (AGA) during the first 2 years of life.

Methods. The study comprised groups of SGA and AGA infants with a gestational age (GA) of 36–41 weeks. The SGA group was classified into two subgroups of symmetrical and asymmetrical neonates according to the ponderal index. Serial renal ultrasonography (US) was performed at the ages of 41 weeks corrected age [GA (in weeks) plus age after birth (in weeks)] and at 3, 6, 12 and 24 months of chronological age and kidney length (KL) was related to other anthropometric indices.

Results. A total of 312 infants participated in the study out of which 197 were SGA, and a total number of 802 measurements were performed. The symmetrical SGA infants and, to a lesser degree, the asymmetrical SGA infants had smaller kidneys at birth compared with the AGA infants (P < 0.0001 and P < 0.001, respectively). The symmetrical SGA infants had a lower body weight (BW) (P < 0.001, P < 0.01) and crown-heel length (CHL) (P < 0.01, P < 0.05) than controls at the ages of 12 and 24 months of chronological age. The asymmetrical SGA infants had a lower BW (P < 0.01, P < 0.05) than controls at the ages of 12 and 24 months of chronological age. On the contrary, the KL in both SGA groups was not different from that of the AGA infants after the 41st week of corrected age and up to the 2nd year of life.

Conclusion. SGA term infants had shorter KL at birth compared with AGA infants but a similar length from the 3rd to the 24th month of life. Early catch-up kidney growth was observed in both SGA groups and is more prominent in the symmetrical SGA infants. This observation may represent either an accelerated renal maturation process or early compensatory kidney hypertrophy in this group of infants.

Keywords: kidney growth; neonate; renal hypertrophy; small for gestational age



   Introduction
Top
 Abstract
 Introduction
Patients and methods
 Results
 Discussion
 Conclusion
 References
 
Epidemiological studies have shown that children born small for gestational age (SGA) are at increased risk for development of renal disease and hypertension during adult life [1,2].

Studies in humans and animals have supported the concept that low birth weight may be associated with a lower number of nephrons at birth and later hypertension [3–8]. A recent histomorphometric study in adults demonstrated an association between reduced nephron number and primary hypertension [9].

Brenner and Chertow [10,11] have proposed that the crucial link between fetal growth restriction, adult hypertension and renal functional decline may be impaired nephrogenesis. They suggested that the reduced number of glomeruli leads to hyperfiltration, which in turn leads to systemic hypertension, glomerular sclerosis and progressive deterioration of renal function [10,11].

Glomerular hypertrophy is regarded as an early marker for the development of glomerulosclerosis [6,10]. The precise time point during life at which hypertrophy and the ensuing renal damage occur is not known [6,10,11]. Renal size, as estimated by ultrasography (US), may be a potential surrogate measure for nephron numbers and also an indirect index of accelerated renal growth under a variety of clinical conditions [12–14].

Data on postnatal kidney growth in SGA infants born full-term are very limited [15]. The present longitudinal prospective study was designed to investigate comparatively the renal growth pattern in SGA and appropriate for gestational age (AGA) neonates with a gestational age GA > 36 weeks and to correlate the growth of the kidneys with other anthropometric indices during the first 2 years of life.



   Patients and methods
Top
 Abstract
 Introduction
 Patients and methods
Results
 Discussion
 Conclusion
 References
 
This study was performed prospectively and included infants born at term (>36 to 41 weeks GA) with low birth weight for GA. The infants enrolled in the study were born at the University Hospital of Ioannina where they were subsequently followed up at the out-patient clinic for monitoring of growth and development. All neonates born SGA at full-term during a period of 2 years were eligible for the study. The study protocol was approved by the Hospital Ethics Committee and informed parental consent was obtained. Exclusion criteria were infants with congenital anomalies, a history of prenatal hydronephrosis, urinary tract infection and other renal anomalies detected before or during the study period. At the time of the study, this regional hospital took care of the majority of deliveries (85%) in the area of Northwestern Greece. The control group comprised infants born in the hospital during the same period with the same GA but with appropriate weight for that GA (AGA).

The GA at birth was assessed according to the mothers’ menstrual history and US at 12–18 weeks of GA, and then confirmed by assessment of the babies’ maturity by neonatologists within 24 h of delivery [16]. Body weight (BW), crown-heel length (CHL) and head circumference (HC) were recorded immediately after delivery. Infants were categorized as SGA (BW at birth <10th percentile for GA) or AGA (BW at birth 10th–90th percentile for GA) using the corresponding age-gender-specific percentiles in growth curves among Greek children [17].

SGA neonates are a heterogeneous group in terms of the aetiology, severity of growth restriction and body proportionality. According to the timing of embryonic damage, intrauterine growth restriction can be divided into two types: early, usually leading to symmetric growth restriction (type I) affecting the BW, CHL and HC equally, and late (often in the third trimester) affecting mainly the BW and leading to asymmetric growth restriction (type II) [18]. Thus, the SGA infants were further classified into two groups, symmetrical and asymmetrical, according to their ponderal index (weight at birth in g x 100/length at birth in cm, cubed) [19].

US examinations were performed blindly and independently by two senior radiologists, who were specialists in paediatric radiology (Maria Argyropoulou and Frederica Papadopoulou). As the neonates of the study were not of the same GA (>36–41weeks), for more precision, the first US estimation was performed at the time they reached the corrected age [corrected age (in weeks) = GA (in weeks) plus age after birth (in weeks)] of 41 weeks. Subsequent measurements were made at the chronological ages of 3, 6, 12 and 24 months in all study infants. Measurements of kidney length (KL) were performed using 5–8 MHz linear or curved array transducers (7 MHz) (HDI Philips 5000). A single maximal longitudinal measurement of each kidney was obtained sonographically in the supine position [20–22]. Renal length measurement was performed because this method has been reported to have the lowest inter-observer variation and better reproducibility compared with sonographic volumetric estimations of the renal size, especially when comparing repeated measurements [23]. The inter-observer variability and the limits of agreement for this study were estimated in a sample of 30 KL measurements in infants based on the method of Bland and Altman [24]. The mean value of the difference (MV) and the standard deviation of the difference (SDD) were 0.99 and 0.63 mm, respectively. The SDD is a measurement of the inter-observer variability. The respective 95% limits of agreement: [MV ± (1.98 x SDD)] expressed as percentage (%) of KL varied from –0.52 to +4.5%.

BW was determined to the nearest 0.1 kg with the child dressed only in underwear and wearing no shoes, using a digital electronic scale (SECA, Hamburg, Germany). HC was measured, with a measuring tape, as the maximum circumference between the supraorbital ridge and the occiput. CHL was measured to the nearest 0.1 cm by a Harpenden stadiometer. Serum creatinine (Scr) levels were estimated, using a modified Jaffe reaction, in the three groups of children at the time of the 12 months US examination.

Sample size
The number of infants was selected to allow a minimum of 45–50 measurements for each comparison in any study period, after taking into account the drop-off trends from a previous study of similar design [25]. This number of infants was considered to be sufficient to document a 10% difference in kidney length between groups with a power of >0.90 at a significance level of 0.05. In sample size calculation, data of the mean values of renal length (±SD) of the earlier study in preterm infants was used [25,26].

Statistical analysis
Overall statistical analysis was performed by repeated measures analysis of variance using the StatView software of S.A.S. Institute Inc. Differences between symmetrical and asymmetrical groups and the control group for each parameter, and for every time period were evaluated by using the one-way ANOVA test followed by the Fisher's PLSD test. Differences were considered significant at P < 0.05. Regression analysis models were also used in order to investigate possible significant statistical relationships between the KL measurements and the anthropometric indices throughout the study period.



   Results
Top
 Abstract
 Introduction
 Patients and methods
 Results
Discussion
 Conclusion
 References
 
A total of 312 infants participated in the study. Of 246 SGA neonates eligible for the study, the parents of 197 (80%) agreed for them to participate in the study. The non-participants did not differ in respect to the anthropometric indices, GA, gender and socioeconomic status from the participant group. The total numbers of measurements in the subgroups of symmetrical and asymmetrical SGA infants were 262 and 264, respectively. The number of measurements in the AGA group (controls) was 276. The children had a mean of 2.5 US examinations during the period of the study; 253 (81%) had more than one US examination, and 114, 71, 38 and 30 had 2, 3, 4 and 5 US examinations, respectively. The smaller cohort sizes, later in the study, were due almost solely to parents’ lack of interest in continuing the study, with a small percentage of drop-off (<10%) due to a change in area of living or to loss of contact. There were no significant differences in GA and gender between the two SGA groups and the respective control group at any study period.

Risk factors for fetal growth retardation were identified in 61% of the SGA infants of the study (75% of asymmetrical and 48% of symmetrical SGA infants). In asymmetrical neonates, these were: pregnancy–induced hypertension in 39%, placental insufficiency in 17%, previous SGA-born child in 6.5%, chronic maternal disease in 6.5% and low weight gain during pregnancy in 6.5%. In symmetrical SGA infants, they were pregnancy–induced hypertension in 12.5%, maternal undernutrition or low weight gain during pregnancy in 12.5%, drug taking or cigarette smoking in 8%, placental factors in 7%, chronic maternal disease in 4% and small pre-pregnancy maternal size in 4%.

Table 1 depicts the mean (±SD) values of anthropometric indices and the KL in the two groups of SGA infants (symmetrical and asymmetrical) and the AGA infants (controls) during the first 2 years of life. No major difference was observed between the lengths of the right kidney and the left kidney, a finding observed previously [17,18,21], therefore the mean value of both kidneys (KL) was used in the analysis. No differences were observed in KL between male and female infants throughout the study period.


View this table:
[in this window]
[in a new window]

  		Table 1. Anthropometric indices and KL in symmetrical and asymmetrical SGA and AGA children

 
Both groups of SGA infants had smaller anthropometric indices at birth compared with the AGA infants (Table 1). The SGA infants had also smaller BW, CHL, HC and KL at 41 weeks corrected age (Table 1). Symmetrical SGA infants had lower BW (P < 0.001), CHL (P < 0.01) and HC (P < 0 01) than controls at the age of 12 months and lower BW (P < 0.01) and CHL (P < 0.05) at 2 years of chronological age (Table 1). Asymmetrical SGA infants had lower BW (P < 0.01) and HC (P < 0.01) than controls at the age of 12 months and lower BW (P < 0.05) at 2 years of chronological age. Conversely, the KL in both groups of SGA infants was significantly shorter than that of the controls only at 41 weeks of chronological age (P < 0.0001, P < 0.001 for the symmetrical and asymmetrical groups, respectively) and did not differ significantly thereafter. The mean KL (mm) at 41 weeks was 44.3 ± 4.5, 45.5 ± 3.7 and 48 ± 3.8 for symmetrical, asymmetrical and control children, respectively. At 2 years, KL mean was 66 ± 5.1, 67.4 ± 3.9 and 66.7 ± 3.2 for the three groups, respectively.

Table 2 shows the correlations between KL and the anthropometric indices in all three groups of infants. At 41 weeks corrected age, a close correlation was observed between KL and each of the anthropometric indices in all three groups. In the control group, significant correlations were observed between KL and CHL and also between KL and BW throughout the study period. Similar correlations between KL and both CHL and BW were observed in the asymmetrical SGA infants. However, in the symmetrical SGA infants, although a positive correlation between KL and CHL or BW was observed at 41 weeks and at 12 and 24 months chronological age, no correlation was apparent at 3 and 6 months of chronological age (Table 2).


View this table:
[in this window]
[in a new window]

  		Table 2. The R values of KL vs BW, CHL and HC in the three study groups (symmetrical SGA, asymmetrical SGA, controls) during the first 2 years of life

 
Scr values were obtained in all symmetrical and asymmetrical SGA infants and in 37 of 42 controls at the time of the 12 months US examination. The mean values did not differ significantly among the three groups and were 0.39 ± 0.04, 0.40 ± 0.04 and 0.40 ± 0.05 (mg/dl mean ± SD), respectively.



   Discussion
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
Conclusion
 References
 
The symmetrical SGA infants in this study, and to a lesser degree the asymmetrical SGA infants, had smaller kidneys at birth compared with the AGA infants. The results of the present study show that in the early postnatal period, between the 41st week of corrected age and the 3rd month of life, rapid renal growth takes place in the groups of both symmetrical and asymmetrical SGA infants. As a consequence, the KL at 3 months is similar in the three groups despite the fact that the SGA infants remain considerably smaller and lighter at that time than the AGA controls. This catch-up growth is more prominent in the symmetrical SGA infants and kidney size was independent of the other anthropometric indices during the first months of life in this group. Only in the symmetrical group of SGA infants at 3 and 6 months of life was no correlation shown between the KL and the other auxological parameters, which may be attributable to the higher velocity of kidney growth at this period compared with the other anthropometric indices.

The early catch-up renal growth was followed by comparable kidney growth velocity up to the age of 24 months, by which time KL in both groups of SGA infants (symmetrical and asymmetrical) was no different from that of the controls (AGA). A small kidney size has been associated with hypertension in adults [27] although the converse has been shown in a group of hypertensive children [12]. A longer follow-up of children born SGA may reveal whether their kidney size declines with age or remains similar to the kidney size of children born AGA.

It has been shown that the last (third) period of nephronogenesis is completed at 34–36 weeks of embryonic age [28,29]. Preterm neonates born earlier than this age are able to continue to form nephrons postnatally while neonates born after 34–36 weeks have already completed this process [28,29]. In a previous study on kidney growth in preterm SGA infants with a GA of 31–36 weeks, similar rapid renal growth in this group of infants was shown during the first 6 months of life [25]. A continuing process of nephrogenesis, blocked in fetal life in an unfavourable intra-uterine environment, may have caused this catch-up growth in KL in children born preterm. In the present study, all the SGA infants were of GA >36 weeks. Thus nephron formation was considered complete before birth. It could be speculated that the catch-up in KL observed in the infants of the study can be in part attributable to compensatory hypertrophy.

Renal growth occurs as a result of normal development or as compensation to a reduction in renal mass [30]. It has been postulated that tubular overgrowth primarily accounts for the observed renal enlargement in both developmental and compensatory renal growth, since the glomerular mass accounts for only a small percentage of the total renal mass [30].

In the single published study on early renal growth in full-term and preterm SGA infants, Schmidt et al. [15] examined a large cohort of neonates at birth, 3 and 18 months of life estimating kidney volume by US [15]. They observed, in accordance with the results of this study, that SGA infants had smaller kidneys at birth than AGA infants. They also found, in the group of 80 SGA full-term infants with birth weight below the 10th percentile, slight but statistically significant catch-up kidney growth from birth to 18 months of life (mean {Delta}z score = +0.22 SD), which they interpret as a limited catch-up, possibly explaining in part the link between prenatal growth retardation and later diseases. In the present study, rapid catch-up growth in KL was observed. The different findings between the two studies may be accounted for by study design, methodology and definitions. Although in both the studies, infants born with birth weight <10th percentile were classified as SGA, the birth weights (not reported in the study of Schmidt et al. [15]) may have different distribution in these two studies and differences in the severity of growth restriction cannot be ruled out. Differences in the aetiology of growth restriction between the two studied populations of SGA infants may also have played a role. In Schmidt's study [15], it was found that among the AGA infants, females had a smaller KL than males at birth but not at the 18th month and, a gender difference not observed in the present study, possibly because of the lower number of infants.

The timing of growth restriction is very important and a recent experimental study showed that reduced nephron number is dependent on the timing of the growth restriction and not on the LBW per se [31]. This parameter was taken into account in the design of this study by making the classification into symmetrical and asymmetrical neonates. Despite the fact that KL was less affected in asymmetrical SGA infants than in symmetrical SGA infants in the early postnatal period, no other differences in regard to KL were observed thereafter.

During the first 3–4 months of life, most infants double their birth weight and the kidney matures rapidly to cope with the increased metabolic demands [28]. Most SGA infants seem to have more rapid growth (catch-up) compared with AGA infants during the same period [32]. SGA infants, such as those studied, with their kidneys having possibly a smaller nephron number, can compensate by accelerating the functional and structural maturation of the existing nephrons. The recruitment of the cortical non-perfused glomeruli could be accelerated as has been shown experimentally [30]. Glomerular compensatory hypertrophy could also contribute to this adaptation process and, as a consequence, a prolonged hyperfiltration period may already begin soon after birth.

SeCr did not differ among the three study groups at 12 months. Although this may indicate similar renal function at this age, other more sensitive indexes of renal function (e.g. urine microalbumin) were not examined. So, subtle differences in renal function between the three groups cannot be excluded.

Based on the findings of the present study, it is not possible to speculate about later renal complications (e.g. hypertension) in the neonates of the study because although in autopsy studies kidney volume has been shown to correlate well, although indirectly, with the number of functioning nephrons [27], there has been no study reported showing a direct relation between KL estimated by US and nephron number.



   Conclusion
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Conclusion
References
 
It is concluded that SGA children born at term have small kidneys at birth and show accelerated renal growth, which occurs early and continues up to 3 months of life. Further studies are needed to delineate the long-term effects of this phenomenon.

Conflict of interest statement. None declared.



   References
Top
 Abstract
 Introduction
 Patients and methods
 Results
 Discussion
 Conclusion
 References
 

  1. Barker DJP, Osmond C, Golding J, Kuh D, Wadsworth MEJ. (1989) Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. Br Med J 298:564–567.[Abstract/Free Full Text]
  2. Yiu V, Burka S, Zurakowski D, McCormick M, Brenner B, Jabs K. (1999) Relationship between birth weight and blood pressure in childhood. Am J Kidney Dis 33:253–260.[Web of Science][Medline]
  3. Manalich R, Reyes L, Herrera M, Melendi C, Fundora I. (2000) Relationship between weight at birth and the number and size of renal glomeruli in humans: a histomorphometric study. Kidney Int 58:770–773.[CrossRef][Web of Science][Medline]
  4. Hinchcliffe SA, Lynch MR, Sargent PH, Howard CV, Van VD. (1992) The effect of intrauterine growth retardation on the development of renal nephrons. Br J Obstet Gynecol 99:296–301.[Web of Science][Medline]
  5. Bassan H, Trejo LL, Bassan NKM, Berger E, Gozes AFI, Harel S. (2000) Experimental intrauterine growth retardation alters renal development. Pediatr Nephrol 15:192–195.[CrossRef][Web of Science][Medline]
  6. Rostand SG. (2003) Oligonephronia, primary hypertension and renal disease: ‘is the child father to the man?’. Nephrol Dial Transplant 18:1434–1438.[Free Full Text]
  7. Rostand SG, Cliver SP, Goldenberg RL. (2005) Racial disparities in association of foetal growth retardation to childhood blood pressure. Nephrol Dial Transplant 20:1592–1597.[Abstract/Free Full Text]
  8. Woods LL, Ingelfinger JR, Nyengaard JR, Rasch R. (2001) Maternal protein restriction suppresses the newborn renin-angiotensin system and programs adult hypertension in rats. Pediatr Res 49:460–467.[Web of Science][Medline]
  9. Keller G, Zimmer Mall G, Ritz E, Amann K. (2003) Nephron number in patients with primary hypertension. N Engl J Med 348:101–108.[Abstract/Free Full Text]
  10. Brenner BM and Chertow GM. (1994) Congenital oligonephronia and the etiology of adult hypertension and progressive renal disease. Am J Kidney Dis 23:171–175.[Web of Science][Medline]
  11. Luyckx V and Brenner B. (2005) Low birth weight, nephron number, and kidney disease. Kidney Int 68:S68–S77.[CrossRef][Web of Science]
  12. Lane P, Belsha C, Plummer J, Steinhardt G, Lynch R, Wood E. (1998) Relationship of renal size, body size, and blood pressure in children. Pediatr Nephrol 12:35–39.[CrossRef][Web of Science][Medline]
  13. Mesrobian H-GO, Land PW, Todd E, Gregg DC. (1998) The normal kidney growth rate year 1 of life is variable and age dependent. J Urol 160:989–993.[CrossRef][Web of Science][Medline]
  14. Koff SA and Peller PA. (1995) Diagnostic criteria for assessing obstruction in the newborn with unilateral hydronephrosis using the renal growth – renal function chart. J Urol 154:662–666.[CrossRef][Web of Science][Medline]
  15. Schmidt IM, Chellakooty M, Boisen KA, et al. (2005) Impaired kidney growth in low-birth-weight children: distinct effects of maturity and weight for gestational age. Kidney Int 68:731–740.[CrossRef][Web of Science][Medline]
  16. Dubowitz LM, Dubowitz V, Goldberg C. (1970) Clinical assessment of gestational age in the newborn infant. J Pediatr 77:1–10.[CrossRef][Web of Science][Medline]
  17. Chiotis D, Tsiftis G, Hatzisymeon M, Maniati-Christidi M, Dacou-Voutetakis A. (2003) Height and weight of children of Hellenic origin aged 0–18 years (2000–2001): comparison with data collected during the period 1978–1979. Ann Clin Pediatr Univ Atheniensis 50:136–155 (in Greek).
  18. Hoffman H and Bakketeig L. (1984) Heterogeneity in intrauterine growth retardation and reccurence risks. Semin Perinatol 8:15–24.[Web of Science][Medline]
  19. Lubchenco LD, Hausman C, Boyed E. (1966) Intrauterine growth in length and head circumference as estimated from live births at gestational ages from 26 to 42 weeks. Pediatrics 37:403–408.[Abstract/Free Full Text]
  20. Loftus WK, Gent RJ, Le Quesne GW, Matreveli C. (1998) Renal length in Chinese children. Sonographic measurement and comparison with western data. J Clin Ultrasound 26:349–352.[CrossRef][Web of Science][Medline]
  21. Zerin JM and Blane CE. (1994) Sonographic assessment of renal length in children: a reappraisal. Pediatr Radiol 24:101.[CrossRef][Web of Science][Medline]
  22. Michel SC, Forster I, Seifert B, Willi UV, Huisman J. (2004) Renal dimensions measured by ultrasonography in children: variations as a function of the imaging plane and patient position. Eur Radiol 14:1508–1512.[Web of Science][Medline]
  23. Emamian SA, Nielsen MB, Pedersen JF. (1995) Intraobserver and interobserver variations in sonographic measurements of kidney size in adult volunteers. A comparison of linear measurements and volumetric estimates. Acta Radiol 36:399–401.[Web of Science][Medline]
  24. Bland M and Altman D. (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 8:307–310.
  25. Hotoura E, Argyropoulou M, Papadopoulou F, et al. (2005) Kidney development in the first year of life in small-for-gestational-age preterm infants. Pediatr Radiol 35:991–994.[CrossRef][Web of Science][Medline]
  26. Altman D. (1994) Sample size. Practical Statistics for Medical Research(Chapman and Hall, London) pp. 456–460.
  27. Nyengaard JR and Bendtsen TF. (1992) Glomerular number and size in relation to age, kidney weight, and body surface in normal man. Anat Rec 232:194–201.[CrossRef][Medline]
  28. Yared A and Ichikawa I. (1992) Postnatal development of Glomerular filtration. In Polin R and Fox W (Eds.). Fetal and Neonatal Physiology.(WB Saunders, Philadelphia, PA) pp. 1200–1204.
  29. Rodriguez M, Gomez A, Abitbol , Chandar J, Duara S, Zilleruel G. (2004) Histomorphometric analysis of postnatal glomerulogenesis in extremely preterm infants. Pediatr Devel Pathol 7:17–25.
  30. Chevalier R. (1992) The response to nephron loss in early development. In Polin R and Fox W (Eds.). Fetal and Neonatal Physiology.(WB Saunders, Philadelphia, PA) pp. 1264–1268.
  31. Mitchell E, Louey S, Cock M, Harding R, Black J. (2004) Nephron endowment and filtration surface area in the kidney after growth restriction of fetal sheep. Pediatr Res 55:769–773.[CrossRef][Web of Science][Medline]
  32. Harding JE and McCowan LME. (2003) Perinatal predictors of growth patterns to 18 months in children born small for gestational age. Early Hum Dev 74:13–26.[CrossRef][Web of Science][Medline]
Received for publication: 31. 3.06
Accepted in revised form: 10. 7.06


Add to CiteULike CiteULike   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us    What's this?


This article has been cited by other articles:


Home page
 Nephrol Dial TransplantHome page
A. Drougia, V. Giapros, E. Hotoura, F. Papadopoulou, M. Argyropoulou, and S. Andronikou
The effects of gestational age and growth restriction on compensatory kidney growth
Nephrol. Dial. Transplant., January 1, 2009; 24(1): 142 - 148.
[Abstract] [Full Text] [PDF]

This Article
Right arrow Abstract Freely available
Right arrow FREE Full Text (PDF) Freely available
Right arrow All Versions of this Article:
21/12/3422    most recent
gfl466v1
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in ISI Web of Science
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to My Personal Archive
Right arrow Download to citation manager
Right arrowRequest Permissions
Right arrow Disclaimer
Google Scholar
Right arrow Articles by Giapros, V.
Right arrow Articles by Andronikou, S.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Giapros, V.
Right arrow Articles by Andronikou, S.
Social Bookmarking
Add to CiteULike   Add to Connotea   Add to Del.icio.us  
What's this?