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A Prospective Study of Women with Pre-Existing Diabetes in Pregnancy

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A Prospective Study of Women with Pre-Existing Diabetes in Pregnancy Diabetes Care 1 Suja Padmanabhan,1,2 Vincent W. Lee,2,3 The Association of Falling Insulin Mark Mclean,1,4,5 Neil Athayde,6 CLIN CARE/EDUCATION/NUTRITION/PSYCHOSOCIAL Valeria Lanzarone,7 Qemer Khoshnow,7 Requirements With Maternal Michael J. Peek,8 and N. Wah Cheung1,2 Biomarkers and Placental Dysfunction: A Prospective Study of Women With Pre-existing Diabetes in Pregnancy https://doi.org/10.2337/dc17-0391 OBJECTIVE To investigate the association of falling insulin requirements (FIR) among women with pre-existing diabetes with adverse obstetric outcomes and maternal bio- markers longitudinally in pregnancy. RESEARCH DESIGN AND METHODS 1Diabetes and Endocrinology, Westmead Hospital, A multicenter prospective cohort study of 158 women (41 with type 1 diabetes and Sydney, New South Wales, Australia 117 with type 2 diabetes) was conducted. Women with FIR of ‡15% from the peak 2Sydney Medical School, University of Sydney, total daily dose after 20 weeks gestation were considered case subjects (n =32). Sydney, New South Wales, Australia 3 The primary outcome was a composite of clinical markers of placental dysfunction Renal Medicine, Westmead Hospital, Sydney, £ New South Wales, Australia (pre-eclampsia, small for gestational age [ 5th centile], stillbirth, premature delivery 4Diabetes and Endocrinology, Blacktown Hospital, [<30 weeks], and placental abruption). Maternal circulating angiogenic markers Sydney, New South Wales, Australia (placental growth factor [PlGF] and soluble fms-like tyrosine kinase 1 [sFlt-1]), 5Western Sydney University, Sydney, New South Wales, Australia placental hormones (human placental lactogen, progesterone, and tumor necrosis 6 a Obstetric Medicine, Westmead Hospital, Sydney, factor- ), HbA1c, and creatinine were studied serially during pregnancy. New South Wales, Australia 7Obstetric Medicine, Nepean Hospital, Sydney, RESULTS New South Wales, Australia FIR ‡15% was associated with an increased risk of the composite primary outcome 8College of Medicine, Biology and Environment, (odds ratio [OR] 4.38 [95% CI 1.9–10.3]; P < 0.001), pre-eclampsia (OR 6.76 [95% CI The Australian National University, Canberra, Australian Capital Territory, Australia 2.7–16.7]; P < 0.001), and was more common among women with type 1 diabetes P Corresponding author: Suja Padmanabhan, (36.6 vs. 14.5%; = 0.002). Creatinine was modestly elevated among women with [email protected]. ‡ FIR 15%; however, there was no difference in HbA1c. The ratio of sFlt-1 to PlGF was Received 22 February 2017 and accepted 9 July significantly higher among women with FIR at 25, 30, and 36 weeks, with differences 2017. maintained in the subgroup that developed pre-eclampsia. There was no difference This article contains Supplementary Data online in placental hormones between the groups. at http://care.diabetesjournals.org/lookup/ suppl/doi:10.2337/dc17-0391/-/DC1. CONCLUSIONS © 2017 by the American Diabetes Association. This is the first prospective study to associate FIR with altered expression of placental Readers may use this article as long as the work antiangiogenic factors and pre-eclampsia. FIR is an important clinical sign, among is properly cited, the use is educational and not for profit, and the work is not altered. More infor- women with pre-existing diabetes, that should alert the clinician to investigate un- mation is available at http://www.diabetesjournals derlying placental dysfunction. .org/content/license. Diabetes Care Publish Ahead of Print, published online August 10, 2017 2 Insulin Requirements and Placental Dysfunction Diabetes Care Although the majority of women with pre- markersaswellashormonesofinsulin Outcomes existing diabetes need increasing doses resistance. As there is currently no universally ac- of insulin with advancing gestation (1), a cepted definition of placental insufficiency, proportion need a reduction in insulin re- RESEARCH DESIGN AND METHODS the primary outcome was defined a priori quirements in late pregnancy, the signifi- FIRST in Pregnancy was conducted at as a composite of adverse clinical out- cance of which remains unclear. Because three tertiary referral hospitals with ded- comes associated with placental dysfunc- insulin resistance is driven by placental- icated diabetes in pregnancy services in tion in the literature (4,14,15). These mediated hormone production, falling in- Sydney, Australia, between June 2013 included pre-eclampsia (defined as per sulin requirements (FIR) are considered to and October 2015. The study was ap- the International Society for the Study be a marker of fetoplacental compromise, proved by the Western Sydney Local of Hypertension in Pregnancy 2014 crite- prompting admission to hospital for ma- Health District Ethics Committee. ria [16]), SGA (birth weight #5th percen- ternal and fetal monitoring and early de- Women with singleton pregnancy tile [17,18]), preterm delivery (,30 livery in some cases (2,3). and a diagnosis of pre-existing type 1, weeks) (19), placental abruption, and still- However, despite the potential impor- type 2, or a new diagnosis of overt diabe- birth (.20 weeks). Presence of one or tance of this clinical sign, only four stud- tes on a 75-g oral glucose tolerance test more of these outcomes in the pregnancy ies have investigated women with FIR in during pregnancy (defined as a fasting was the threshold for attribution of an the literature. We have previously shown, blood glucose level of $7.0 mmol/L [126 abnormal primary outcome. Additionally, through a retrospective cohort study, that mg/dL], a 2-h level of $11.1 mmol/L secondary outcomes were evaluated, in- FIR are associated with pre-eclampsia, [200 mg/dL], or an HbA1c of $6.5% cluding maternal and neonatal clinical small-for-gestational-age (SGA) babies, [48 mmol/mol] [12,13]) were prospec- outcomes, HbA1c, and serum creatinine, and increased admission to the neonatal tively recruited at their first visit to the as well as biomarkers associated with pla- intensivecareunit(NICU)(4).Incontrast, dedicated diabetes in pregnancy clinic. cental dysfunction, including the antian- other studies have not identified an asso- Only women presenting prior to 20 weeks giogenic factor sFlt-1 and proangiogenic ciation with adverse obstetric outcomes and progressing beyond 20 weeks gesta- factor PlGF (11), and hormones of insu- (5–7). Previous studies are limited by tion were included in the study. lin resistance including tumor necrosis retrospective design, differing defini- Information on baseline demograph- factor-a (TNF-a), human placental lacto- tions of FIR, limited representation of ics and medical and obstetric history gen (hPL), and progesterone (20,21). womenwithtype2diabetes,andin- were obtained via a structured question- Laboratory Procedures adequate statistical power for adverse naire at recruitment. Weight in kilograms, Blood and urine were collected from par- outcomes associated with placental blood pressure, insulin dose (total, basal, ticipants atfourtime points:146 1 weeks dysfunction. and prandial), and carbohydrate intake (or first visit if presenting later), 24 6 1 There is increasing evidence for the per meal (quantified in exchanges; 1 ex- weeks, 30 6 1 weeks, and 36 6 1weeks role of placental biomarkers in predicting change = 15 g) were recorded at each re- gestation. Samples from the end of each tri- and diagnosing obstetric conditions asso- view. For women treated with an insulin mester were tested immediately for HbA , ciated with placental dysfunction; how- pump, an upload containing data on av- 1c creatinine, urine albumin-to-creatinine ever, few studies have included women erage basal and prandial insulin dosing ratio (ACR), and protein-to-creatinine with pre-existing diabetes (8–10). An im- and daily carbohydrate intake for the pre- ratio (PCR), and results were made avail- balance between proangiogenic factors, ceding 1 to 2 weeks was recorded. At all able to the treating team. Remaining such as placental growth factor (PlGF), centers, insulin doses were titrated to samples were stored at 280°C and ana- and antiangiogenic factors, such as solu- the same blood glucose target of #5.5 lyzed within 18 months for sFlt-1, PlGF, ble fms-like tyrosine kinase 1 (sFlt-1), are mmol (100 mg/dL) fasting and #7 mmol TNF-a, hPL, and progesterone. Bio- thought to play a key role in diseases as- (126 mg/dL) 2 h postprandial by the treat- markers were analyzed by ELISAs using sociated with placental dysfunction (11). ing team, and intermittent checks of the commercially available kits: sFlt-1, PlGF, FIR among women with pre-existing glucose monitor were performed to ensure and TNF-a (R&D Systems), hPL (DRG Di- diabetes may be considered a clinical man- correlation between self-recorded glucose agnostics), and progesterone (Labor ifestation of the glycemic vascular inter- values and those in the machine. Partici- Diagnostika Nord). The interassay coefficients face between the fetoplacental unit and pants were reviewed at least every four of variation were 11.1, 15.5, 14, 22, and 5.2% the mother; however, no previous studies weeksupto28weeks,everytwoweeks for PlGF, sFlt-1, TNF-a, hPL, and progester- have examined the association between until 36 weeks, and weekly thereafter. one, respectively. FIR and placental biomarkers. FIR was calculated as a percentage from Considering this, we conducted the the peak total insulin dose (PTID), defined as Statistical Analysis Falling Insulin Requirements Study (FIRST), the highest total insulin dose in pregnancy, Statistical analysis was performed using a prospective
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