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Alan C. Wong, MD, MPH Cynthia W. Ko, MD, MS

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1 Alan C. Wong, MD, MPH Cynthia W. Ko, MD, MS
Carbohydrate Intake:  A Risk Factor for Biliary Sludge and Stones During Pregnancy Alan C. Wong, MD, MPH Cynthia W. Ko, MD, MS Department of Medicine Division of Gastroenterology Seattle, Washington

2 Introduction Gallstone disease results in >700,000 cholecystectomies each year. Female gender is a risk factor, and pregnancy is a high risk period for gallstone formation. Gallbladder (GB) disease is the most common non-obstetrical cause of maternal rehospitalization in the first 60 days after delivery. Carbohydrate intake has been linked to increased risk of cholecystectomy in women. The effect of carbohydrate consumption on GB disease during pregnancy is unclear.

3 Study Aim To determine the effect of dietary carbohydrate intake on the formation of biliary sludge and stones during pregnancy.

4 Study Design – General Overview
Prospective study Cohort of pregnant women Exposure: Carbohydrate consumption during pregnancy, determined by food frequency questionnaire. Outcome: Formation of new GB sludge/stones, determined by serial GB ultrasound.

5 Consecutive women attending 1st obstetrics clinic (n = 8,929)
Age <18, poor language comprehension, >20 weeks pregnant, declined to participate (n = 4,032) Eligible and interested (n = 4,897) Gallstones on entry GB ultrasound (n = 208) Had cholecystectomy (n = 33) Fewer than two GB ultrasounds (n = 1,402) Did not complete dietary questionnaire (n = 184) Included in analysis (n = 3,070)

6 Serial fasting gallbladder ultrasounds
1st trimester (10-12 weeks) 2nd trimester (17-19 weeks) 3rd trimester (26-28 weeks) Post-partum (4-6 weeks) Minimum of 2 interpretable ultrasounds per subject Definition of incident GB sludge/stones: Progression of baseline sludge to stones or New sludge or New stones

7 Ultrasonographic Definitions:
1) Sludge: low-level echoes, shift with positional changes, no post-acoustic shadowing. 2) Stones: high-amplitude echoes, >2 mm in diameter, post-acoustic shadowing present. Interpretation: Technicians had specific training in GB ultrasound Images reviewed by 1 of 2 radiologists

8 Measurement of Carbohydrate Intake
1st trimester 2nd trimester 3rd trimester 3rd trimester Post-partum Dietary Questionnaire Validated food frequency questionnaire Daily consumption (g/day) of total carbohydrate, starch, sucrose, galactose, fructose, lactose, and maltose.

9 Statistical Methods Risk of incident GB sludge/stones determined for each quartile of intake of total carbohydrate and individual carbohydrates (starch, sucrose, galactose, fructose, lactose, and maltose) Multivariate logistic regression adjusting for: age pre-pregnancy body mass index weight gain during pregnancy parity Hispanic origin smoking history of diabetes intake of alcohol, caffeine, total calories, protein, fat, fiber, cholesterol, fatty acids

10 Results

11 Results Incidence of GB disease = 10.2% New sludge = 5.1%
New stones = 2.8% Baseline sludge to stones = 2.3%

12 Characteristics of Study Subjects
Results Characteristics of Study Subjects No new sludge/stones New sludge/stones P - value n = 2756 n = 314 Hispanic origin (%) 10.4 17.8 0.001 BMI pre-pregnancy (kg/m2) 24 27 <0.0001 Weight gain during pregnancy (kg) 14.6 12.6 Caffeine intake (mg/day) 40 50 0.018 Alcohol intake (g/day) 0.1 0.5 0.038 No significant difference between groups: history of diabetes gestational diabetes intake of calories, fat, fiber

13 Results Carbohydrate consumption and the risk of incident gallstone disease Nutrient Adjusted Odds Ratio 95% Confidence Interval Total carbohydrate 2.295 Starch* 1.812 Fructose* 2.054 Galactose* 0.664 - Highest quartile of intake compared to lowest quartile - Adjusted for: age, pre-pregnancy BMI, weight gain, parity, Hispanic origin, smoking, history of diabetes, intake of alcohol, caffeine, calories, protein, fat, fiber, cholesterol, fatty acids * With additional adjustment for total carbohydrate intake

14 Carbohydrate consumption and the risk of incident gallstone disease
* P < 0.05, compared to Quartile 1

15 Discussion

16 ↑ human placental lactogen
Pregnancy ↑ cortisol ↑ estrogen ↑ progesterone ↑ human placental lactogen

17 ↑ human placental lactogen
Pregnancy ↑ cortisol ↑ estrogen ↑ progesterone ↑ human placental lactogen Hyperinsulinemia + Insulin resistance

18 Hyperinsulinemia + Insulin resistance
Pregnancy ↑ cortisol ↑ estrogen ↑ progesterone ↑ human placental lactogen Postprandial insulin ↑ 3-fold Hyperinsulinemia + Insulin resistance Basal insulin ↑ 2-fold Insulin sensitivity ↓ 50-70%

19 Hyperinsulinemia + Insulin resistance
Pregnancy ↑ cortisol ↑ estrogen ↑ progesterone ↑ human placental lactogen ↑ bile cholesterol secretion ↓ bile acid synthesis Bile cholesterol super-saturation Hyperinsulinemia + Insulin resistance ↑ bile cholesterol saturation

20 Hyperinsulinemia + Insulin resistance
Pregnancy ↑ cortisol ↑ estrogen ↑ progesterone ↑ human placental lactogen ↑ bile cholesterol secretion ↓ bile acid synthesis Bile cholesterol super-saturation Hyperinsulinemia + Insulin resistance ↑ bile cholesterol saturation ↓ GB emptying response to CCK GB stasis ↓ GB ejection fraction

21 Hyperinsulinemia + Insulin resistance Carbohydrates
Pregnancy ↑ cortisol ↑ estrogen ↑ progesterone ↑ human placental lactogen ↑ bile cholesterol secretion ↓ bile acid synthesis Bile cholesterol super-saturation Hyperinsulinemia + Insulin resistance ↑ bile cholesterol saturation ↓ GB emptying response to CCK GB stasis Carbohydrates ↓ GB ejection fraction

22 Hyperinsulinemia + Insulin resistance Carbohydrates
Pregnancy ↑ cortisol ↑ estrogen ↑ progesterone ↑ human placental lactogen ↑ bile cholesterol secretion ↓ bile acid synthesis Bile cholesterol super-saturation Hyperinsulinemia + Insulin resistance ↑ bile cholesterol saturation ↓ GB emptying response to CCK GB stasis Carbohydrates ↓ GB ejection fraction

23 Hyperinsulinemia + Insulin resistance Carbohydrates
Pregnancy ↑ cortisol ↑ estrogen ↑ progesterone ↑ human placental lactogen ↑ bile cholesterol secretion ↓ bile acid synthesis Bile cholesterol super-saturation Hyperinsulinemia + Insulin resistance ↑ bile cholesterol saturation ↓ GB emptying response to CCK GB stasis Carbohydrates ↓ GB ejection fraction

24 Fructose

25 Fructose does not require insulin for uptake into cells
stimulates less insulin release than glucose largely metabolized in the liver

26 hepatic insulin resistance
Fructose hepatic lipogenesis ↑ triglyceride hepatic insulin resistance leptin resistance ↑ leptin level

27 hepatic insulin resistance
Fructose hepatic lipogenesis ↑ triglyceride hepatic insulin resistance leptin resistance ↑ leptin level Gallstone disease

28 Limitations Only one dietary time point
GB ultrasounds were done at varying stages of pregnancy No serum insulin/leptin levels

29 Conclusion High intake of total carbohydrate, starch, and fructose is associated with increased risk of developing biliary sludge/stones during pregnancy. Dietary modification during pregnancy may reduce this risk.

30 References American Gastroenterological Association. The burden of gastrointestinal diseases. Bethesda, MD: The American Gastroenterological Association, 2001. Lydon-Rochelle M et al. Association between method of delivery and maternal rehospitalization. JAMA May 10;283(18): Tsai CJ et al. Glycemic load, glycemic index, and carbohydrate intake in relation to risk of cholecystectomy in women. Gastroenterology Jul;129(1): Nakeeb A et al. Insulin resistance causes human gallbladder dysmotility. J Gastrointest Surg Jul-Aug;10(7):940-8; discussion Gielkens HA et al. Effect of insulin on basal and cholecystokinin-stimulated gallbladder motility in humans. J Hepatol Apr;28(4): Dubrac S et al. Insulin injections enhance cholesterol gallstone incidence by changing the biliary cholesterol saturation index and apo A-I concentration in hamsters fed a lithogenic diet. J Hepatol Nov;35(5):550-7. Biddinger SB et al. Hepatic insulin resistance directly promotes formation of cholesterol gallstones. Nat Med Jul;14(7): Epub 2008 Jun 29. Butte NF. Carbohydrate and lipid metabolism in pregnancy: normal compared with gestational diabetes mellitus. Am J Clin Nutr May;71(5 Suppl):1256S-61S. Wang HH et al. New insights into the molecular mechanisms underlying effects of estrogen on cholesterol gallstone formation. Biochim Biophys Acta Nov;1791(11): Wu Z et al. Progesterone inhibits L-type calcium currents in gallbladder smooth muscle cells. J Gastroenterol Hepatol Dec;25(12): Miller A et al. Dietary fructose and the metabolic syndrome. Curr Opin Gastroenterol Mar;24(2):204-9. Ko CW et al. Incidence, natural history, and risk factors for biliary sludge and stones during pregnancy. Hepatology Feb;41(2): This study is supported by National Institutes of Health (NIH) grant DK 46890

31 Thank You

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