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University of Groningen

Skin autofluorescence, a non-invasive biomarker for advanced glycation end products, is not

related to the number of pregnancies

Van Waateringe, Robert P.; Truyens, Laura; Van Den Berg, Paul P.; Lutgers, Helen L.;

Wolffenbuttel, Bruce H. R.

Published in: Journal of diabetes DOI:

10.1111/1753-0407.12782

IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below.

Document Version

Publisher's PDF, also known as Version of record

Publication date: 2018

Link to publication in University of Groningen/UMCG research database

Citation for published version (APA):

Van Waateringe, R. P., Truyens, L., Van Den Berg, P. P., Lutgers, H. L., & Wolffenbuttel, B. H. R. (2018). Skin autofluorescence, a non-invasive biomarker for advanced glycation end products, is not related to the number of pregnancies. Journal of diabetes, 10(11), 899-901. https://doi.org/10.1111/1753-0407.12782

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RESEARCH LETTER

Skin auto

fluorescence, a non-invasive biomarker for

advanced glycation end products, is not related to the

number of pregnancies

Robert P. VAN WAATERINGE,1Laura TRUYENS,2Paul P. VAN DEN BERG,3Helen L. LUTGERS4and

Bruce H.R. WOLFFENBUTTEL 1

1

Department of Endocrinology, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands,2University of Louvain, Louvain, Belgium,3Department of Gynecology, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands, and4Department of Internal Medicine, Medisch Centrum Leeuwarden, Leeuwarden, The Netherlands

Keywords: aging, diabetes, epidemiology, pregnancy, skin autofluorescence.

To the Editor

The role of advanced glycation end products (AGEs) in the pathophysiology of diabetes-related complica-tions and aging has been studied extensively. The AGEs represent chronic exposure to hyperglycemia and oxida-tive stress. Tissue AGE accumulation can be assessed non-invasively by measuring skin autofluorescence (SAF) with a so-called AGE reader. Markers of oxida-tive stress are elevated during pregnancy, which can, in turn, increase the formation of AGEs.1 One study reported that SAF levels were higher in pregnant women with pre-existing diabetes than in women with gestational diabetes and women without diabetes.2

Preliminary data from our group suggested that SAF increases during pregnancy and does not return to pre-pregnancy levels (B. Groen et al., unpublished data, 2014). This phenomenon may be caused by increased

oxidative and glycemic stress during pregnancy. There-fore, the aim of the present study was to assess the rela-tionship between SAF and the number of pregnancies.

Methods

Subjects included in the study were participants from the Lifelines Cohort Study, a large population-based cohort study in the northern region of the Netherlands (www. lifelines.net, accessed 24 December 2017). The Lifelines study was approved by the Medical Ethics Committee of the University Medical Center Groningen. Written informed consent was obtained from all participants. The present study included women of Western European descent aged between 18 and 80 years for whom an SAF measurement was available. Subjects with type 1 and type 2 diabetes were excluded, as were as those with missing data for diabetes, leaving 47 834 individuals for analysis. Subjects completed a questionnaire on medical history, past and current diseases, use of medication, and health behavior. The questionnaire also included infor-mation on previous pregnancies and childbirth. Women were asked how many times they had been pregnant and how many children were born. In the present study, SAF was calculated as the mean of three consecutive measurements using an AGE Reader (DiagnOptics

Correspondence

Bruce H.R. Wolffenbuttel, Department of Endocrinology, University Medical Center Groningen, HPC AA31, P.O. Box 30001, 9700 RB Groningen, The Netherlands.

Tel: +31 50 3613962 Fax: +31 50 3619392 Email: bwo@umcg.nl

Received 25 December 2017; revised 20 April 2018; accepted 15 May 2018

doi: 10.1111/1753-0407.12782

Highlights

• Skin autofluorescence (SAF) assesses subcutaneous accumulation of advanced glycation end products and has been shown to predict future cardiovascular disease and diabetes.

• A higher number of pregnancies was significantly associated with higher SAF, even after correction for relevant confounders like waist circumference, creatinine clearance, and diabetes status, but not after correction for age. • Women with the highest SAF Z-score had a more unfavorable risk factor profile, with higher body mass index and waist circumference, higher blood pressure, lower high-density lipoprotein cholesterol, and higher triglycer-ide levels.

Journal of Diabetes 10 (2018), 899–901

© 2018 The Authors. Journal of Diabetes published by John Wiley & Sons Australia, Ltd and Ruijin Hospital, Shanghai Jiaotong University School of Medicine. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

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Technologies, Groningen, Netherlands).3 Age-adjusted

SAF (Z-scores) was calculated because SAF is strongly affected by aging.3

Data are given as the meanSD or as the median with interquartile range (IQR) in the case of non-normally distributed data. Linear regression analysis was per-formed to examine the association between the number of pregnancies and SAF. In the multivariate models, we adjusted for relevant factors, such as waist circumference, body mass index (BMI), renal function, and smoking. Two-tailed P < 0.001 was considered significant.

Results

The clinical characteristics of the study population are given in Table S1, available as Supplementary Material to this paper. Mean subject age was 4412 years, mean waist circumference was 8712 cm, and mean BMI was 25.84.6 kg/m2. The median number of pregnancies was 2.0 (IQR 1.0–3.0). In total, 20.5% of women had not been pregnant, 42% reported one to two pregnancies, 30% reported three to four pregnan-cies, and 7.5% reported five or more pregnancies. A higher number of pregnancies was associated with higher SAF, which persisted after correction for waist circumference and renal function (P < 0.0001). How-ever, after further correction for age, SAF was no lon-ger associated with the number of pregnancies (P = 0.713; Table 1). Fig. 1 shows that SAF Z-scores are comparable in the various groups of women divided according to the number of pregnancies. Women in the highest quartile of the SAF Z-score had a higher preva-lence of metabolic syndrome, as well as higher BMI, waist circumference, glucose, HbA1c, and lipids (all

P < 0.01) than women in the other three quartiles, and a similar number of pregnancies compared with those in the lowest quartile (Table S2).

Discussion

After correction for important confounders, SAF increased with the number of pregnancies in women from the general population. However, after correction for age, this association was no longer significant. The increased oxidative stress that occurs during pregnancy may significantly affect SAF measurements. Indeed, it has been reported that SAF is elevated in women with pre-eclampsia and associated with increased carotid artery intima–media thickness, a marker for atheroscle-rosis.4 Moreover, SAF was associated with higher blood pressure, triglycerides, and C-reactive protein levels, indicating the potential cardiovascular risk asso-ciated with these factors.5 Therefore, we postulate that the effect of pregnancy on SAF may only be restricted to pathological pregnancies, such as those complicated by pre-eclampsia.4,5Unfortunately, the Lifelines dataset did not record any complications of pregnancy.

Two important studies have reported on the associa-tion between reproductive history and cardiovascular health. One of these studies reported that a higher num-ber of pregnancies was associated with lower cardiovascu-lar mortality,6 whereas the other study showed that the

Table 1 Univariate and multivariate analyses for skin autofluorescence

Model Parameters β P-value R2(%) 1 No. pregnancies 0.061 <0.0001 5.3 2 No. pregnancies 0.0003 0.800 30.7 Age 0.020 <0.0001 3 No. pregnancies 0.0031 <0.0001 19.7 Waist 0.013 <0.0001 GFR −0.006 <0.0001 4 No. pregnancies 0.030 <0.0001 20.5 Waist 0.012 <0.0001 GFR −0.006 <0.0001 Diabetes or glucose 0.084 <0.0001 5 No. pregnancies −0.0001 0.941 31.3 Age 0.17 <0.0001 Waist 0.004 <0.0001 GFR −0.001 <0.0001 Diabetes 0.015 <0.0001 GFR, glomerularfiltration rate.

4.0 3.0 2.0 1.0 0.0 -1.0 SAF ( Z -score) -2.0 -3.0 -4.0 0 1–2 3–4 No. pregnancies 5–6 ≥7

Figure 1 Number of pregnancies and age-corrected skin auto fluor-escence (SAF) Z-score. The boxes show the interquartile range, with the median value indicated by the horizontal line; whiskers show the range. Dots indicate outliers.

900 © 2018 The Authors.

Journal of Diabetes published by John Wiley & Sons Australia, Ltd and Ruijin Hospital, Shanghai Jiaotong University School of Medicine.

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number of pregnancies or live births was associated with higher left ventricular mass and end-systolic volume.7A recent review suggested that pre-eclampsia is an under-recognized risk factor for ischemic heart disease, chronic hypertension, peripheral vascular disease, and stroke.8

In conclusion, in the present study SAF increased with a higher number of pregnancies, but not after correction for participants’ age. Those with the highest age-corrected SAF had a worse risk factor profile for future cardiovascular disease.

Acknowledgements

The authors acknowledge all the participants of the Life-lines Cohort Study and everybody involved in the set-up and implementation of the study. Lifelines has been funded by a number of public sources, notably the Dutch Government, The Netherlands Organization of Scientific Research NWO (Grant 175.010.2007.006), the Northern Netherlands Collaboration of Provinces (SNN), the European Fund for Regional Development, Dutch Minis-try of Economic Affairs, Pieken in de Delta, Provinces of Groningen and Drenthe, the Target project, BBMRI-NL (Biobanking and BioMolecular resources Research Infra-structure The Netherlands), the University of Groningen, and the University Medical Center Groningen. This work was supported by the National Consortium for Healthy Ageing, and funds from the European Union’s Seventh Framework Program (FP7/2007–2013) through the Bio-bank Standardisation and Harmonisation for Research Excellence in the European Union (BioSHaRE-EU) pro-ject (Grant agreement 261433). Lifelines (BRIF4568) is engaged in a Bioresource research impact factor (BRIF) policy pilot study, details of which can be found at: https://www.bioshare.eu/content/bioresource-impact-factor (accessed 24 December 2017).

Disclosure None declared.

References

1. Toescu V, Nuttall SL, Martin U, Kendall MJ, Dunne F. Oxidative stress and normal pregnancy. Clin Endocrinol (Oxf ). 2002; 57: 609–13.

2. De Ranitz-Greven WL, Kaasenbrood L, Poucki WK et al. Advanced glycation end products, measured as skin

autofluorescence, during normal pregnancy and

preg-nancy complicated by diabetes mellitus. Diabetes Technol Ther. 2012; 14: 1134–9.

3. Meerwaldt R, Graaff R, Oomen PHN et al. Simple non-invasive assessment of advanced glycation endproduct accumulation. Diabetologia. 2004; 47: 1324–30.

4. Blaauw J, Smit AJ, van Pampus MG et al. Skin auto-fluorescence, a marker of advanced glycation end prod-ucts and oxidative stress, is increased in recently preeclamptic women. Am J Obstet Gynecol. 2006; 195: 717–22.

5. Coffeng SM, Blaauw J, Souwer ET et al. Skin auto

fluor-escence as marker of tissue advanced glycation end-products accumulation in formerly preeclamptic women. Hypertens Pregnancy. 2011; 30: 231–42.

6. Jacobs MB, Kritz-Silverstein D, Wingard DL, Barrett-Connor E. The association of reproductive history with all-cause and cardiovascular mortality in older women: The Rancho Bernardo Study. Fertil Steril. 2012; 97:

118–24.

7. Parikh NI, Lloyd-Jones DM, Ning H et al. Association of number of live births with left ventricular structure and function. The Multi-Ethnic Study of Atherosclerosis (MESA). Am Heart J. 2012; 163: 470–6.

8. Ahmed R, Dunford J, Mehran R, Robson S,

Kunadian V. Pre-eclampsia and future cardiovascular risk among women a review. J Am Coll Cardiol. 2014; 63:

1815–22.

Supporting information

Additional supporting information may be found online in the Supporting Information section at the end of the article:

Table S1. Baseline characteristics of the participating women.

Table S2. Skin autofluorescence Z-scores and

cardiovascu-lar risk factors.

© 2018 The Authors.

Journal of Diabetes published by John Wiley & Sons Australia, Ltd and Ruijin Hospital, Shanghai Jiaotong University School of Medicine.

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