Published online May 14, 2007
PEDIATRICS Vol. 119 No. 6 June 2007, pp. e1314-e1318 (doi:10.1542/10.1542/peds.2006-2589)
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ARTICLE

Perinatal Circulating Visfatin Levels in Intrauterine Growth Restriction

Ariadne Malamitsi-Puchner, MDa, Despina D. Briana, MDa, Maria Boutsikou, MDa, Evangelia Kouskouni, MDa, Demetrios Hassiakos, MDa and Demetrios Gourgiotis, PhDb

a Neonatal Division, Second Department of Obstetrics and Gynecology
b Research Laboratories, Second Department of Pediatrics, Athens University, Athens, Greece


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
OBJECTIVE. The objective of this study was to investigate possible alterations in circulating levels of the adipocytokine visfatin in intrauterine growth-restricted and normal pregnancies, given that these groups differ considerably in fetal nutrition, body fat mass, and metabolic/endocrine mechanisms.

METHODS. Serum visfatin levels were prospectively measured by enzyme immunoassay in 40 mothers and their 40 singleton term fetuses and neonates on postnatal days 1 and 4. Twenty neonates had intrauterine growth restriction (birth weight ≤3rd customized centile, adjusted for parameters that influence growth potential), and 20 were appropriate for gestational age.

RESULTS. Circulating maternal visfatin levels were significantly elevated in pregnancies with intrauterine growth restriction compared with control pregnancies with appropriate-for-gestational-age infants and negatively correlated with customized centiles in the group with intrauterine growth restriction. Postnatal day-1 and -4 visfatin levels were significantly higher in neonates with intrauterine growth restriction compared with neonates who were appropriate for gestational age. Postnatal-day-1 prefeeding insulin levels were significantly lower in neonates with intrauterine growth restriction.

CONCLUSIONS. Pathologic conditions in pregnancy that lead to intrauterine growth restriction could be responsible for elevated maternal visfatin levels. Higher visfatin levels in neonates with intrauterine growth restriction may serve as an early marker with prognostic value for later development of insulin resistance or type 2 diabetes, whereas lower insulin levels may indicate reduced ß-cell mass and/or impaired ß-cell function.

Key Words: intrauterine growth restriction • visfatin • fetus • neonate • insulin resistance

Abbreviations: PBEF—pre–B-cell colony-enhancing factor • IUGR—intrauterine growth restriction • AGA—appropriate for gestational age • PI—pulsatility index • N1—postnatal day 1 • N4—postnatal day 4 • CI—confidence interval

Insulin resistance, obesity-related diabetes, and accompanying metabolic disorders are strongly associated with increased visceral adipose tissue mass.1–4 Visfatin, a 52-kd visceral fat–specific adipocytokine,5 probably links the expansion of adipose depot to insulin resistance.6 Visfatin, which is identical to pre–B-cell colony-enhancing factor (PBEF),7 is immunolocalized in both normal and infected human fetal membranes8 and upregulated during labor.9

Newborns with asymmetric intrauterine growth restriction (IUGR)10 are at increased risk for development of metabolic syndrome later in life,11–14 as a result of insulin resistance.11,15–17 We hypothesized that circulating visfatin levels should differ between infants with IUGR and control infants who are appropriate for gestational age (AGA), because the former present reduced fat mass18,19 and undergo adaptational changes of endocrine/metabolic mechanisms as a result of intrauterine malnutrition.11 Therefore, we aimed to evaluate circulating visfatin concentrations in IUGR and AGA mother-infant pairs at crucial perinatal time points.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
The ethics committee of our teaching hospital approved the study protocol. Participating mothers provided signed informed consent before enrollment. Forty parturients who gave birth consecutively either to 20 term singleton infants who were AGA or to 20 term singleton infants who had asymmetric IUGR (birth weight ≤3rd customized centile) were recruited. The Gestation Related Optimal Weight computer-generated program20,21 was used to calculate the customized centile for each pregnancy. Significant determinants of birth weight (maternal height and booking weight, ethnicity, parity, gestational age, and gender) were entered to adjust the normal birth weight centile limits.20

Possible causes of IUGR were in 9 cases preeclampsia and in 11 cases pregnancy-induced hypertension plus various pathologic conditions (iron-deficient anemia [n = 3], gestational diabetes [n = 2], hypothyroidism [n = 3], extreme obesity [n = 2], and cardiac arrhythmias [n = 1]) and smoking >10 cigarettes per day (n = 5).

Doppler studies (pulsatility index [PI]) were performed in the IUGR group every 10 to 15 days, starting from the 32nd gestational week. Concerning uterine and umbilical arteries, PI values were in the upper physiologic limits for gestational age in 13 cases, whereas in 7, they showed increased impedance to flow. PI values of middle cerebral arteries were in the lower physiologic limits for gestational age, indicating initiation of blood flow redistribution process. Amniotic fluid was diminished in all IUGR cases. For its evaluation, the largest fluid column on the vertical plane was assessed and defined as diminished when <2 cm. Placental weight ranged from 255 to 400 g.

In the AGA group, mothers were healthy nonsmokers. Ultrasound studies were evaluated as nonpathologic, and placentas were normal in appearance and weight.

Tests for congenital infections were negative in all women of both groups, and neonates showed no symptoms of intrauterine infection or signs of genetic syndromes. One- and 5-minute Apgar scores were ≥8 in all neonates.

The demographic data of participating mothers and infants are listed in Table 1. Blood was collected in pyrogen-free tubes from mothers during the first stage of labor or before anesthesia in cases of elective cesarean section, from doubly-clamped umbilical cords, reflecting fetal state, and from neonates on postnatal days 1 (N1) and 4 (N4). Blood was immediately centrifuged after clotting, and supernatant serum was kept frozen at –80°C until assay. Determination of visfatin levels was performed by enzyme immunoassay (visfatin C-terminal [human] EIA; Phoenix Pharmaceuticals, Belmont, CA). Minimum detectable concentration and intraassay and interassay coefficients of variation were 0.1 ng/mL and 5% and 12%, respectively.


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  		TABLE 1 Demographic Data of Participating Mothers and Their Fetuses/Neonates Who Were AGA or Had IUGR

 
In addition, prefeeding maternal N1 and N4 serum insulin levels were measured in both groups. Determination of insulin levels was performed by Microparticle Enzyme Immunoassay (Abbot Diagnostics [AxSYM System], Wiesbaden, Germany). Minimum detectable concentration and intra- and interassay coefficients of variation were <1 µU/mL and 4.1% and 5.3%, respectively.

Visfatin data, in contrast to insulin data, were normally distributed (Kolmogorov-Smirnov test). The effect of various parameters (maternal age, customized centile, birth weight, mode of delivery, gender, and parity) on circulating visfatin levels was assessed using linear regression analysis. Nonparametric procedures (Mann-Whitney U test and Wilcoxon rank-sum test), {chi}2 test, and Pearson's or Spearman's rank correlation coefficient, where appropriate, were applied. The SPSS 10.0 (SPSS, Chicago, IL) statistical software package was used for all calculations. P < .05 was considered statistically significant.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Determined mean (95% confidence intervals [CIs]) values of circulating visfatin levels in both groups are shown in Fig 1. Maternal visfatin levels were significantly elevated (by 3.346 ng/mL on average) in the IUGR compared with the AGA group (regression coefficient ß: 3.346 [95% CI: 0.049–6.644; P = .047]). Although infant customized centile was not an independent predicting variable for maternal visfatin levels, a significant negative correlation was found between the 2 variables in the IUGR group (r = –0.411 [P = .008]).


Figure 1
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  		FIGURE 1 Mean (95% CI) visfatin levels in the serum of mothers (MS), fetuses (UC), and neonates on N1 and N4 in AGA and IUGR groups.

 
No significant differences in visfatin levels were demonstrated between fetuses with IUGR and fetuses that were AGA. N1 and N4 circulating visfatin levels were significantly higher in neonates who had IUGR than in neonates who were AGA (regression coefficient ß: 3.755 [95% CI: 1.205–6.305; P = .005] and ß: 2.769 [95% CI: 0.519–5.019; P = .017], respectively). Maternal and fetal visfatin levels were significantly correlated (AGA group r = 0.742 [P < .001] and IUGR group r = 0.478 [P = .033]).

N1 prefeeding insulin levels (mean ± SD) were significantly lower in neonates who had IUGR than in neonates who were AGA (2.46 ± 3.57 vs 3.63 ± 2.80 µU/mL, respectively; P = .048). In contrast, maternal and N4 prefeeding insulin values did not vary significantly between IUGR and AGA groups (11.1 ± 12.18 vs 7.6 ± 5.21 and 4.04 ± 5.59 vs 4.58 ± 4.22 µU/mL, respectively). Circulating visfatin levels did not depend on gestational age, mode of delivery, or gender. Finally, no significant correlations were observed between serum visfatin and insulin levels in either group.


   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
To our knowledge, this preliminary study is the first to determine circulating visfatin concentrations in neonates with IUGR. Although included pregnancies were limited, circulating visfatin levels were investigated in the same mother-infant pairs at 4 crucial perinatal time points, and statistically significant results were found between the IUGR and AGA groups.

Circulating maternal visfatin levels were higher in the IUGR than in the AGA group and negatively correlated with the customized centiles in the former. Although preeclampsia and pregnancy-induced hypertension, main causes of IUGR22 in our study, are associated with obesity23 and subsequently with increased visfatin levels,5 the latter could be related to other yet-unidentified mechanisms. Indeed, maternal pathologic conditions that are associated with IUGR22 (eg, protein and energy restriction,24–26 iron-deficient anemia27) have been reported in animal models to cause changes in maternal circulating levels of several hormones and adipocytokines, such as leptin.25 Therefore, altered maternal endocrine environment in pregnancies that are complicated with IUGR25 could be responsible for higher visfatin levels.

In addition, higher circulating visfatin levels were found in neonates who had IUGR. There are 2 potential explanations for this finding. The first relies on the fact that visceral adipose tissue is the predominant source of visfatin,5 and data suggest that newborns with low birth weight may have increased visceral fat stores.28,29 In contrast, Harrington et al,19 by applying MRI, found no differences in intra-abdominal adipose tissue between newborns who had IUGR and newborns who were AGA. In this study, fat mass was not directly measured and centrality of fat distribution was not assessed. Therefore, we could not document whether a relationship between circulating visfatin levels and visceral fat exists at birth.

A second explanation might involve the increasing evidence that circulating visfatin levels are higher in states of insulin resistance.6,30–34 Epidemiologic studies point to a strong relationship between IUGR and the development of insulin resistance and type 2 diabetes,35–37 the exact onset of which is not fully elucidated. Nevertheless, several studies,17,38–40 including this one, have determined lower insulin levels in neonates with IUGR (possibly as a result of reduced ß-cell mass and poor intrauterine ß-cell function40,41) and higher insulin sensitivity.17,38–40 Lévy-Marchal et al13 speculated that altered fetal development of adiposity in IUGR might permanently change the regulation of its metabolic and hormonal functions, predisposing to the later development of insulin resistance. Respectively, animal and human studies42–44 indicated that infants who are small for gestational age compared with control infants who are AGA gain more abdominal fat and body adiposity during postnatal life. Therefore, although higher visfatin levels in neonates with IUGR cannot be attributed to insulin resistance at birth, they could probably serve as an early marker with prognostic value for the later development of metabolic syndrome in this population. A similar hypothesis was previously made for circulating adiponectin levels in newborns who were small for gestational age.45

Maternal and fetal blood visfatin concentrations were strongly correlated in both groups, indicating the likelihood of transplacental transfer of visfatin. Finally, no significant differences in fetal visfatin levels were demonstrated between IUGR and AGA groups. Because visfatin/PBEF originates from human fetal membranes during pregnancy8,9 and is upregulated during labor,9 the lack of difference could be attributed to varying visfatin membrane production in the 2 groups. In addition, the lack of insulin/visfatin correlation may be attributable to the possibility that perinatal visfatin could mostly reflect PBEF. However, relevant information does not exist, and additional studies are needed to clarify these results.


   CONCLUSIONS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Pathologic conditions in pregnancies that lead to IUGR may account for the elevated maternal visfatin levels. Higher visfatin levels in neonates with IUGR may serve as an early marker of insulin resistance or type 2 diabetes later in life. However, lacking adequate information on the physiologic role of visfatin in adults, it is difficult to speculate on its importance in the perinatal period. The source and the regulation of visfatin in the fetus and the neonate remain to be elucidated.


   FOOTNOTES
 
Accepted Nov 29, 2006.

Address correspondence to Ariadne Malamitsi-Puchner, MD, 19 Soultani St, 10682 Athens, Greece. E-mail: amalpu{at}aretaieio.uoa.gr, malamitsi{at}aias.gr

The authors have indicated they have no financial relationships relevant to this article to disclose.


   REFERENCES
TOP
 ABSTRACT
 METHODS
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 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

  1. Matsuzawa Y. Therapy insight: adipocytokines in metabolic syndrome and related cardiovascular disease. Nat Clin Pract Cardiovasc Med. 2006;3 :35 –42[CrossRef][Web of Science][Medline]
  2. Björntorp P. Metabolic implications of body fat distribution. Diabetes Care. 1991;14 :1132 –1143[Abstract]
  3. Frayn KN. Visceral fat and insulin resistance: causative or correlative? Br J Nutr. 2000;83(suppl 1) :S71 –S77
  4. Wajchenberg BL. Subcutaneous and visceral adipose tissue: their relation to the metabolic syndrome. Endocr Rev. 2000;21 :697 –738[Abstract/Free Full Text]
  5. Fukuhara A, Matsuda M, Nishizawa M, et al. Visfatin: a protein secreted by visceral fat that mimics the effects of insulin. Science. 2005;307 :426 –430[Abstract/Free Full Text]
  6. Sethi JK, Vidal-Puig A. Visfatin: the missing link between intra-abdominal obesity and diabetes? Trends Mol Med. 2005;11 :344 –347[CrossRef][Web of Science][Medline]
  7. Samal B, Sun Y, Stearns G, Xie C, Suggs S, McNiece I. Cloning and characterization of the cDNA encoding a novel human pre-B-cell colony-enhancing factor. Mol Cell Biol. 1994;14 :1431 –1437[Abstract/Free Full Text]
  8. Ognjanovic S, Bao S, Yamamoto SY, Garibay-Tupas J, Samal B, Bryant-Greenwood GD. Genomic organization of the gene coding for human pre-B-cell colony enhancing factor and expression in human fetal membranes. J Mol Endocrinol. 2001;26 :107 –117[Abstract]
  9. Ognjanovic S, Bryant-Greenwood GD. Pre-B-cell colony-enhancing factor, a novel cytokine of human fetal membranes. Am J Obstet Gynecol. 2002;187 :1051 –1058[CrossRef][Web of Science][Medline]
  10. Kanaka-Gantenbein C, Mastorakos G, Chrousos GP. Endocrine-related causes and consequences of intrauterine growth retardation. Ann N Y Acad Sci. 2003;997 :150 –157[CrossRef][Web of Science][Medline]
  11. Hales CN, Barker DJ. The thrifty phenotype hypothesis. Br Med Bull. 2001;60 :5 –20[Abstract/Free Full Text]
  12. Holt RI, Byrne CD. Intrauterine growth, the vascular system, and the metabolic syndrome. Semin Vasc Med. 2002;2 :33 –43[CrossRef][Medline]
  13. Jaquet D, Deghmoun S, Chevenne D, Collin D, Czernichow P, Lévy-Marchal C. Dynamic change in adiposity from fetal to postnatal life is involved in the metabolic syndrome associated with reduced fetal growth. Diabetologia. 2005;48 :849 –855[CrossRef][Web of Science][Medline]
  14. Van Assche FA, Holemans K, Aerts L. Fetal growth and consequences for later life. J Perinat Med. 1998;26 :337 –346[Web of Science][Medline]
  15. Soto IN, Mericq GV. Fetal growth restriction and insulin resistance. New findings and review of the literature [in Spanish]. Rev Med Chil. 2005;133 :97 –104[Web of Science][Medline]
  16. Ozanne SE, Olsen GS, Hansen LL, et al. Early growth restriction leads to down regulation of protein kinase C zeta and insulin resistance in skeletal muscle. J Endocrinol. 2003;177 :235 –241[Abstract]
  17. Soto N, Bazaes RA, Pena V, et al. Insulin sensitivity and secretion are related to catch-up growth in small-for-gestational-age infants at age 1 year: results from a prospective cohort. J Clin Endocrinol Metab. 2003;88 :3645 –3650[Abstract/Free Full Text]
  18. Padoan A, Rigano S, Ferrazzi E, Beaty BL, Battaglia FC, Galan HL. Differences in fat and lean mass proportions in normal and growth-restricted fetuses. Am J Obstet Gynecol. 2004;191 :1459 –1464[CrossRef][Web of Science][Medline]
  19. Harrington TA, Thomas EL, Frost G, Modi N, Bell JD. Distribution of adipose tissue in the newborn. Pediatr Res. 2004;55 :437 –441[CrossRef][Web of Science][Medline]
  20. Gardosi J, Chang A, Kaylan B, Sahota D, Symonds EM. Customised antenatal growth charts. Lancet. 1992;339 :283 –287[CrossRef][Web of Science][Medline]
  21. Gardosi J, Mongelli M, Wilcox M, Chang A. An adjustable fetal weight standard. Ultrasound Obstet Gynecol. 1995;6 :168 –174[CrossRef][Web of Science][Medline]
  22. Ergaz Z, Avgil M, Ornoy A. Intrauterine growth restriction: etiology and consequences—what do we know about the human situation and experimental animal models? Reprod Toxicol. 2005;20 :301 –322[CrossRef][Web of Science][Medline]
  23. O'Brien TE, Ray JC, Chan WS. Maternal body mass index and the risk of preeclampsia: a systematic overview. Epidemiology. 2003;14 :368 –374[CrossRef][Web of Science][Medline]
  24. Fernandez-Twinn DS, Wayman A, Ekizoglou S, Martin MS, Hales CN, Ozanne SE. Maternal protein restriction leads to hyperinsulinemia and reduced insulin-signaling protein expression in 21-mo-old female rat offspring. Am J Physiol Regul Integr Comp Physiol. 2005;288 :R368 –R373[Abstract/Free Full Text]
  25. Fernandez-Twinn DS, Ozanne SE, Ekizoglou S, et al. The maternal endocrine environment in the low-protein model of intrauterine growth restriction. Br J Nutr. 2003;90 :815 –822[CrossRef][Web of Science][Medline]
  26. Garofano A, Czernichow P, Breant B. Effect of ageing on beta-cell mass and function in rats malnourished during the perinatal period. Diabetologia. 1999;42 :711 –718[CrossRef][Web of Science][Medline]
  27. Lewis RM, Petry CJ, Ozanne SE, Hales CN. Effects of maternal iron restriction in the rat on blood pressure, glucose tolerance, and serum lipids in the 3-month old offspring. Metabolism. 2001;50 :562 –567[CrossRef][Web of Science][Medline]
  28. Yajnik CS. Early life origins of insulin resistance and type II diabetes in India and other Asian countries. J Nutr. 2004;134 :205 –210[Abstract/Free Full Text]
  29. Yajnik CS, Lubree HG, Rege SS, et al. Adiposity and hyperinsulinemia in Indians are present at birth. J Clin Endocrinol Metab. 2002;87 :5575 –5580[Abstract/Free Full Text]
  30. Haider DG, Schindler K, Schaller G, Prager G, Wolzt M, Ludvik B. Increased plasma visfatin concentrations in morbidly obese subjects are reduced after gastric banding. J Clin Endocrinol Metab. 2006;91 :1578 –1581[Abstract/Free Full Text]
  31. Ye SQ, Simon BA, Maloney JP, et al. Pre-B-cell colony-enhancing factor as a potential novel biomarker in acute lung injury. Am Respir Crit Care Med. 2005;171 :361 –370[Abstract/Free Full Text]
  32. Jia SH, Li Y, Parodo J, et al. Pre-B-cell colony-enhancing factor inhibits neutrophil apoptosis in experimental inflammation and clinical sepsis. J Clin Invest. 2004;113 :1318 –1327[CrossRef][Web of Science][Medline]
  33. Chen MP, Chung FM, Chang DM, et al. Elevated plasma level of visfatin/pre-B-cell colony-enhancing factor in patients with type 2 diabetes mellitus. J Clin Endocrinol Metab. 2006;91 :295 –299[Abstract/Free Full Text]
  34. Tan BK, Chen J, Digby JE, Keay SD, Kennedy CR, Randeva HS. Increased visfatin messenger ribonucleic acid and protein levels in adipose tissue and adipocytes in women with polycystic ovary syndrome: parallel increase in plasma visfatin. J Clin Endocrinol Metab. 2006;90 :5022 –5028
  35. Barker DJ, Hales CN, Fall CH, Osmond C, Phipps K, Clark PM. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia. 1993;36 :62 –67[CrossRef][Web of Science][Medline]
  36. Li C, Johnson MS, Goran MI. Effects of low birth weight on insulin resistance syndrome in Caucasian and African-American children. Diabetes Care. 2001;24 :2035 –2042[Abstract/Free Full Text]
  37. Simmons R. Developmental origins of adult metabolic disease: concepts and controversies. Trends Endocrinol Metab. 2005;16 :390 –394[CrossRef][Web of Science][Medline]
  38. Bazaes RA, Salazar TE, Pittaluga, et al. Glucose and lipid metabolism in small for gestational age infants at 48 hours of age. Pediatrics. 2003;111 :804 –809[Abstract/Free Full Text]
  39. Mericq V, Ong KK, Bazaes R, et al. Longitudinal changes in insulin sensitivity and secretion from birth to age three years in small- and appropriate-for-gestational age children. Diabetologia. 2005;48 :2609 –2614[CrossRef][Web of Science][Medline]
  40. Setia S, Sridhar MG, Bhat V, Chaturvedula L, Vinayagamoorti R, John M. Insulin sensitivity and insulin secretion at birth in intrauterine growth retarded infants. Pathology. 2006;38 :236 –238[CrossRef][Web of Science][Medline]
  41. Limesand SW, Jensen J, Hutton JC, Hay WW Jr. Diminished beta-cell replication contributes to reduced beta-cell mass in fetal sheep with intrauterine growth restriction. Am J Physiol Regul Integr Comp Physiol. 2005;288 :R1297 –R1305[Abstract/Free Full Text]
  42. Ibanez L, Ong K, Dunger DB, de Zegher F. Early development of adiposity and insulin resistance after catch-up weight gain in small-for-gestational-age children. J Clin Endocrinol Metab. 2006;91 :2153 –2158[Abstract/Free Full Text]
  43. Hediger ML, Overpeck MD, Kuczmarski RJ, McGlynn A, Maurer KR, Davis WW. Muscularity and fatness of infants and young children born small- or large-for-gestational-age. Pediatrics. 1998;102(5) . Available at: www.pediatrics.org/cgi/content/full/102/5/e60
  44. Crescenzo R, Samec S, Antic V, et al. A role for suppressed thermogenesis favoring catch-up fat in the pathophysiology of catch-up growth. Diabetes. 2003;52 :1090 –1097[Abstract/Free Full Text]
  45. Kamoda T, Saitoh H, Saito M, Sugiura M, Matsui A. Serum adiponectin concentrations in newborn infants in early postnatal life. Pediatr Res. 2004;56 :690 –693[CrossRef][Web of Science][Medline]
PEDIATRICS (ISSN 1098-4275). ©2007 by the American Academy of Pediatrics

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