The Dietary Glycemic Index during Pregnancy: Influence on Infant Birth Weight, Fetal Growth, and Biomarkers of Carbohydrate Metabolism

Theresa O. Scholl1 , Xinhua Chen1, Chor San Khoo2 and Carine Lenders3

1 Department of Obstetrics and Gynecology, School of Medicine, The University of Medicine and Dentistry of New Jersey, Stratford, NJ.
2 Campbell Institute of Research, Camden, NJ.
3 Department of Medicine, Children’s Hospital, Harvard Medical School, Boston, MA.

Received for publication February 26, 2003; accepted for publication September 18, 2003.


    ABSTRACT
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
During pregnancy, lower levels of maternal glucose before and during a glucose load have been associated with reduced infant birth weight and an increased risk of small-for-gestational-age births. A lower incremental area under the glucose response curve defines a low glycemic diet. Thus, during pregnancy the maternal diet, as measured by the glycemic index, may influence fetal growth and infant birth weight. A total of 1,082 gravidas who enrolled in the Camden Study between August 1996 and October 2002 were followed prospectively during pregnancy. The dietary glycemic index was computed from three 24-hour recalls in the course of pregnancy. Samples for plasma glucose and for glycosylated hemoglobin were obtained at 24–28 weeks’ gestation. The glycemic index was positively and significantly related to maternal glycosylated hemoglobin and plasma glucose. There were as well significant linear trends for dietary fat intake to decrease and for intakes of carbohydrate, sucrose, fiber, and folate to increase as the glycemic index declined. Gravidas with a low dietary glycemic index had reduced infant birth weight and approximately a twofold increased risk of a small-for-gestational-age birth. Consistent with data on maternal plasma glucose, data in this study show that the type of carbohydrate in the diet of urban, low-income women influences fetal growth and infant birth weight.

birth weight; diet; glycemic index; hemoglobin A, glycosylated; infant, small for gestational age

Abbreviations: Abbreviation: OR, odds ratio.


    INTRODUCTION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Glucose is a major fuel for fetal growth (13). Maternal glucose concentrations originate from both endogenous and dietary sources, that is, from the liver as well as from the diet. The primary source of glucose in the diet is carbohydrate, a macronutrient. In gravidas who are diabetic and in those who are not, there is a significant relation among increasing maternal glucose levels, greater fetal growth, and higher infant weight at birth (49). African-American women give birth to infants that weigh less for gestation than the infants of White women, and a portion of this ethnic difference is related to their lower circulating levels of glucose (10). During pregnancy, increased maternal plasma glucose also is a marker for an increased risk of serious complications that include chorioamnionitis, cesarean section, and preeclampsia (5, 6, 8, 9).

The glycemic index is a relative measure of the blood glucose response to a given amount of carbohydrate that represents the quality of the carbohydrate that is eaten. The glycemic index is defined as the incremental area under the glucose response curve following the intake of 50 g of carbohydrate from food compared with the glucose area generated from a similar amount of white bread or glucose (11, 12). Although there is variation within and between individuals, on average foods with a lower glycemic index give rise to a smaller blood glucose response than do foods with a higher glycemic index (13, 14). Several of the prospective studies that examined the glycemic index or glycemic load have found that high values generally are associated with increased risk of chronic disease, including type 2 diabetes (15, 16) and coronary heart disease (17). There is, however, only limited information on the effects of a low dietary glycemic index.

Some carbohydrates are absorbed more slowly than others and thus may have a weak effect on raising blood glucose levels. Therefore, it is possible that during pregnancy gravidas who eat foods with a lower glycemic index have lower circulating levels of blood glucose and thus less fuel for fetal growth. Infants who are small for gestational age have an increased risk of infant morbidity and mortality and may evidence persistent delay in their growth and development (1820). In addition, Barker (21) has linked reduced fetal growth in utero to an increased risk of diabetes and cardiovascular diseases in later life.

We therefore examined the relation among the glycemic index, biomarkers of maternal carbohydrate metabolism, and other nutrients in the diet of pregnant women. We hypothesized that, because of differences in the postprandial and postabsorptive maternal physiologic response, the glycemic index at one extreme would be associated with an increased risk of small-for-gestational-age births and at the other with increased fetal growth.


    MATERIALS AND METHODS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The Camden Study prospectively examines the effects of maternal nutrition and growth in generally healthy pregnant women from one of the poorest cities in the United States (9, 10, 22, 23), Camden, New Jersey. Participants include young (<=18 years) and more mature (19–32 years) women enrolling for prenatal care in Camden clinics. Gravidas with serious nonobstetric problems (e.g., lupus, chronic hypertension, diabetes mellitus type 1 or type 2, seizure disorders, malignancies, and drug or alcohol abuse) are not eligible. The Institutional Review Board of the University of Medicine and Dentistry of New Jersey School of Medicine approved the study. In this analysis, we focus on data from 1,082 delivered gravidas who enrolled in the study between August 1996 and October 2002.

Socioeconomic, demographic, lifestyle, and dietary data were obtained by interview at entry to prenatal care and were updated at weeks 20 and 28 of gestation. A 24-hour recall of the previous day’s diet was obtained on the same schedule. Food models as well as household and fast-food glasses, cups, and bowls were used to quantify portion size along with the use of specific dietary probes. Following a longstanding collaboration, dietary data were processed with databases from the Campbell Institute of Research and Technology (Campbell Soup Company) in Camden. The database contains descriptions of and codes for 1,875 foods consumed by women in Camden along with information on serving size and the foods’ weight in grams. It generates data for more than 70 nutrients and was updated from the US Department of Agriculture’s most current data set, the Nutrient Database for Standard Reference (release 13 from year 2000) and the Continuing Survey of Food Intakes by Individuals, as well as from the scientific literature, including information from food processors and food tables.

The value of the food glycemic index from published international tables (24, 25) was assigned to the food items in our database using the white bread standard. Pregnancy has been reported not to alter the glycemic index of the foods that have been tested (26). Following a method that has been described in the literature, glycemic index values were calculated for our data by multiplying the glycemic index for each food by the carbohydrate content and then dividing by the total carbohydrate intake for the day. The sum of the resulting values was termed the dietary glycemic index by Wolever et al. (27). The dietary glycemic index value based upon each of the three recalls was then averaged to give a mean value for each gravida over the course of her pregnancy. Three 24-hour recalls, each in excess of 15,000 kcal/day, were omitted from the calculations. As a corollary, another measure derived from the dietary glycemic index, the glycemic load, was also calculated (15). This involved multiplying the food glycemic index by the carbohydrate content, summing the values over all foods, and then averaging over all recalls as described above.

Pregravid weight was determined by recall at entry to prenatal care, and weight was measured at each visit using a beam balance scale. Recorded and recalled weights are generally well correlated (r = 0.75–0.98), with the caveat that women with higher body weight tend to underreport their weight (2830). Height was measured at entry to prenatal care using a stadiometer. Body mass index was computed as pregravid weight (kg)/height (m)2. The total gestational weight gain was calculated as the difference between the reported pregravid weight and the weight measured within 2 weeks before delivery; the rate of gestational weight gain was computed from the total weight gain and the duration of gestation. The adequacy of gestational weight gain was also defined to within 2 completed weeks of delivery using published criteria that adjust weight gain for the duration of gestation (31).

Information on current and past pregnancy outcomes, complications, and infant abnormalities was abstracted from the prenatal record, the delivery record, delivery logbooks, and the infant’s chart. A large-for-gestational-age fetus was defined by a birth weight for gestation above the 90th percentile of the standard described by Zhang and Bowes (32), which adjusts for maternal parity, ethnicity, and fetal sex. A small-for-gestational-age fetus was defined by birth weight for gestation below the 10th percentile of the same standard. Gestation duration was based upon the gravidas’ last normal menstrual period confirmed or modified by ultrasound.

Maternal plasma glucose and red cells for glycosylated hemoglobin were obtained by venipuncture between 24–28 weeks of gestation. Plasma glucose levels were measured 1 hour after a 50-g glucose-screening test to detect gestational diabetes, routinely conducted in Camden gravidas. A total of 92 percent of the women provided a fasting sample, but fasting is not a requirement for either the glucose-screening test or the glycosylated hemoglobin. Samples were stored at –70°C until assayed. Glucose was measured with the glucose oxidase method (Sigma Diagnostics, St. Louis, Missouri) and with glycosylated hemoglobin by turbidimetric immune inhibition (Boehringer Mannheim, Indianapolis, Indiana). The coefficient of variation within and between assays was less than 5 percent for each method.

Linear regression was used to generate a dietary glycemic index adjusted for energy intake (33). Dietary residuals from these regressions were further categorized into quintiles. The significance of the linear trend was assessed across categories (quintiles) of the glycemic index using analysis of variance with 1 df. The chi-square statistic or overall F statistic from the analysis of variance was used to assess the relation between glycemic index quintiles and maternal background characteristics. Potential confounding variables traditionally associated with infant birth weight or risk of small-for-gestational-age births (e.g., age, smoking, ethnicity), known to be related to pregnancy outcomes in Camden and also associated with the dietary glycemic index (p < 0.20), were included in multivariable models. Separate models were fit for infant birth weight and each pregnancy outcome or bio-marker of carbohydrate metabolism using multiple logistic regression or multiple linear regression. In models of birth weight and pregnancy outcome, the highest quintile of the dietary glycemic index was compared with quintiles 1–4, and the lowest quintile of the dietary glycemic index was compared with quintiles 2–5. Confounding was assessed by comparing crude and adjusted odds ratios or regression coefficients. Adjusted odds ratios and their 95 percent confidence intervals were computed from the logistic regression coefficients and their corresponding covariance matrices (34). For the biomarkers of carbohydrate metabolism, we used the regression coefficients and the mean dietary glycemic index values from the highest quintile (mean, 89.42) and lowest quintile (mean, 62.17) of the dietary glycemic index to compare the difference between these extreme quintiles. We also expressed this difference as the percentage of change by dividing it by the mean concentration of the biomarker.


    RESULTS
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Little association was found between quintiles of the dietary glycemic index and variables such as maternal pregravid body mass index and the adequacy or rate of gestational weight gain. Women in the lower quintiles of the dietary glycemic index tended to be somewhat older and were slightly more likely to be nulliparous and less likely to smoke heavily (table 1). There was an overall ethnic difference in the dietary glycemic index for the group. Comparing data from African Americans with combined data from Hispanics and Whites showed that a high dietary glycemic index diet was more prevalent and a low dietary glycemic index less frequent among African Americans compared with other gravidas (p = 0.01).


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TABLE 1. Maternal background characteristics and the dietary glycemic index of gravidas who enrolled in the Camden Study between August 1996 and October 2002
 
Energy intake was somewhat lower for women in both the highest and lowest dietary glycemic index quintiles (table 2). With adjustment for energy, the dietary glycemic index was associated with other aspects of the maternal diet. There were significant trends for gravidas in the lower quintiles of the glycemic index to eat diets richer in carbohydrate, fiber, sucrose, and folate but lower in fat (table 2).


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TABLE 2. Mean intake of energy and energy-adjusted macronutrients, fiber, and selected micronutrients by quintile of the dietary glycemic index in gravidas who enrolled in the Camden Study between August 1996 and October 2002
 
Controlling for maternal ethnicity and other potential confounding variables, we found that the dietary glycemic index was positively related to biomarkers of maternal carbohydrate metabolism during the third trimester (table 3). These measures included levels of glycosylated hemoglobin (mean, 5.48 (standard deviation, 0.52) percent) and maternal plasma glucose 1 hour after a 50-g glucose load (mean, 106 (standard deviation, 26.8) mg/dl). Both of these biomarkers increased with every unit increase in the dietary glycemic index. Using coefficients from the regression equations, we calculated expected levels of plasma glucose and glycosylated hemoglobin for gravidas in the lowest and highest quintiles of the dietary glycemic index. The computations suggested a lower level of plasma glucose (–4.5 mg/dl, a 4.2 percent difference) and glycosylated hemoglobin (–0.12 percent, a 2.2 percent difference) for the lowest quintile.


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TABLE 3. Relation between the dietary glycemic index and markers of maternal carbohydrate metabolism in gravidas who enrolled in the Camden Study between August 1996 and October 2002
 
Like plasma glucose, the dietary glycemic index influenced fetal growth (table 4). After adjustment for the duration of gestation, a dietary glycemic index in the lowest quintile was associated with lower infant birth weight, a reduction of more than 100 g. After including other potential confounding variables along with gestational duration, we found that the birth weight difference increased to –116 g. Unlike with the low dietary glycemic index, there was no association between a diet that placed the mother in the highest quintile of the dietary glycemic index and the birth weight of her infant.


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TABLE 4. Influence of the dietary glycemic index on infant birth weight in gravidas who enrolled in the Camden Study between August 1996 and October 2002
 
Like the relation between plasma glucose and fetal growth, women with a dietary glycemic index in the lowest quintile had approximately a twofold increased risk of bearing a growth-restricted infant (table 5). This risk was not greatly altered by inclusion of other potential confounding variables (maternal age, cigarettes smoked per day, prior history of low birth weight) in the model. Consistent with the data on infant birth weight, a diet with a high glycemic index did not alter a woman’s risk of bearing a large- or small-for-gestational-age infant.


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TABLE 5. Influence of the dietary glycemic index on small-for-gestational-age and large-for-gestational-age births* of gravidas who enrolled in the Camden Study between August 1996 and October 2002
 
We repeated the analyses utilizing the energy-adjusted glycemic load in lieu of the dietary glycemic index. Using the same models depicted in tables 35, we found a weak, positive, but statistically significant relation between the glycemic load and the mother’s glycosylated hemoglobin concentration (ß = 0.0008 (standard error, 0.0003); p = 0.009). From these data, we estimated a small difference in glycosylated hemoglobin between the highest and lowest quintiles of the glycemic load (–0.022 percent, a 0.4 percent difference). However, the glycemic load was not related to infant birth weight, to risk of a small-for-gestational-age or a large-for-gestational-age birth, or to the mother’s plasma glucose level at week 28.


    DISCUSSION
 TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Glucose, the major substrate for fetal growth, is transported across the placenta in proportion to its concentration in the maternal circulation and according to the rate of placental red blood flow. Gluconeogenesis is virtually absent in the fetus so that the fetus obtains its glucose almost entirely from circulating levels in the mother (35). Maternal glucose and other metabolic fuels thus provide the energy for fetal growth and facilitate the passage of nutrients from mother to fetus (14). Circulating levels of glucose are produced by maternal metabolism from endogenous sources and also from the diet, principally from carbohydrate. Not all carbohydrates raise blood glucose levels to the same extent. The glycemic response to carbohydrate depends upon the type that is consumed. The glycemic index is a qualitative measure that classifies the type of carbohydrate according to the metabolic response that it elicits. The reference food used by researchers to determine tabled values for the food glycemic index is white bread or glucose (11, 12). White bread represents a more physiologic meal than glucose, although neither is the primary source of carbohydrate in populations that have been studied (36). In addition, the glycemic index for a food may also be influenced by the method of processing and preparation, its fat, protein, and fiber content, as well as other factors.

Carbohydrates with a higher glycemic index are absorbed quickly and can raise blood glucose concentrations rapidly, whereas carbohydrates with a lower glycemic index break down more steadily and have a gradual glucose rise (12). Consistent with this expectation, our data showed a positive relation between the maternal dietary glycemic index and biomarkers of maternal carbohydrate metabolism during pregnancy, including glycosylated hemoglobin, a measure of average plasma glucose over the past 2–3 months, and an acute measure, third trimester postload plasma glucose. Calculations from these data suggested that plasma glucose was about 4 percent lower and that glycosylated hemoglobin (HbA1c) was about 2 percent lower comparing the lowest and highest dietary glycemic index quintiles. Among patients with impaired glucose tolerance, diets with a lower dietary glycemic index lowered postprandial glucose levels by about 4 percent (37). In a small clinical trial, pregnant (n = 12) and nonpregnant (n = 14) women who exercised habitually were randomly assigned to diets containing "aboriginal" (dietary glycemic index = 71) or "cafeteria" (dietary glycemic index = 84) carbohydrate. Pregnant women on the aboriginal diet had lower glucose areas 3 hours after a mixed meal and a lower insulin response with advancing gestation than gravidas on the cafeteria diet (38). Data from studies on the management of type 1 or type 2 diabetes that have been incorporated into a recent review of the glycemic index suggested that glycolysated hemoglobin or fructosamine fell by about 10 percent on average with a low glycemic index diet (39).

Salmeron et al. (15) derived the glycemic load from the glycemic index to quantify the overall glycemic effect from food. In the present study of pregnant women, the glycemic load had a weaker relation with glycosylated hemoglobin (computed as 0.38 percent between extreme quintiles) than the dietary glycemic index (computed as 2 percent) and was unrelated to maternal plasma glucose, to infant birth weight, or to risk of small-for-gestational-age births.

The relation between the glycemic load and the glucose response depends upon the amount of carbohydrate as well as on the type. The diets of Camden gravidas are rich in sugar, and approximately 50 percent of the carbohydrate that they eat comes from sugar (table 2). However, simple sugars, including sucrose, have a lower glycemic index and elicit a lower blood glucose response than white bread and other starchy foods (40). Thus, because sugar makes a large contribution to carbohydrate intake in Camden, the effect that the carbohydrate "load" has on blood glucose may not be strong. It is also possible that the slowed gastric emptying and colonic transit that characterize pregnancy (41) have altered the relation among the glycemic load, maternal glucose levels, and fetal growth. Although one small study in diabetic gravidas suggested that pregnancy did not change the glycemic index of the eight foods that were tested, it did not examine the effects of the glycemic load on blood glucose (26).

Our observations are the first from a larger-scale observational study to report an increased risk of fetal growth restriction in association with a low maternal dietary glycemic index. This finding supports the hypothesis that reduced fetal growth is associated with the maternal diet during pregnancy. Although some studies of macronutrients and micronutrients (vitamins C and E and folate) in the maternal diet have suggested that maternal nutrition has little effect on the outcome of pregnancy in developed countries (42), they also have not included an examination of the mother’s dietary glycemic index. As we observed during pregnancy and as others have observed in the nonpregnant state (12, 43), a low dietary glycemic index diet is associated with lower concentrations of glucose, and a high dietary glycemic index is associated with higher concentrations of plasma glucose. Consistent with our findings on maternal plasma glucose, those of Scholl et al. (9) showed that a dietary glycemic index in the lowest quintile was associated with reduced infant birth weight and an increased risk of fetal growth restriction (9).

However, we did not observe that gravidas eating a diet with a high dietary glycemic index had concomitant increases in birth weight and other measures of fetal growth, such as a large-for-gestational-age birth. The influence of maternal plasma glucose on excessive fetal growth has been described in women with diabetes (4, 7). High circulating concentrations of maternal glucose are associated with increased transport of glucose and other nutrients to the fetus. Fetal insulin secretion is stimulated in order to prevent fetal hyperglycemia. Fetal insulin increases the storage of glucose and other nutrients and also acts as a growth factor for the fetus. With increases in the supply of nutrients and the production of growth factors, the intrauterine growth rate is higher and the infant birth weight greater (4, 7).

Although high dietary glycemic index diets have been reported to raise postprandial glucose and insulin (12, 43), it seems plausible that young women who are not diabetic should secrete a sufficient amount of insulin to maintain blood glucose levels in the normal range. Thus, there would be little extra maternal glucose for increased fetal growth. Some studies have suggested that a high dietary glycemic index may increase the risk of type 2 diabetes and other chronic diseases in later life (1517). Type 2 diabetes (odds ratio (OR) = 1.25–1.47) and coronary heart disease (OR = 1.98) were increased for participants in the Nurses’ Health Study when women with a dietary glycemic index or load in the highest quintile were compared with those in the lowest quintile (15, 17). An increased risk of type 2 diabetes (OR = 1.37) was noted for men with a high dietary glycemic index who took part in the Health Professionals’ Follow-up Study (16).

We observed ethnic differences in the glycemic index and found that African Americans were more likely to eat a high dietary glycemic index diet than were other gravidas. We and others have reported higher insulin and lower glucose concentrations among African-American girls and young women, pregnant and nonpregnant alike (22, 44, 45). Ethnic differences in insulin and glucose could reflect the influence of a higher dietary glycemic index. Regular consumption of a high glycemic index diet is thought to initiate a cycle of hyperinsulinemia (acute insulin resistance) followed by increases in counter regulatory hormones, the release of free fatty acids and, as observed in many studies of African Americans, lower postprandial glucose concentrations. During pregnancy, the lower postload levels of glucose in African-American gravidas are associated with 5–7 percent of the difference in fetal growth and infant birth weight between African Americans and Whites (10). A cycle of high blood glucose and insulin followed by episodes of reactive hypoglycemia and increased insulin resistance may eventually boost the demand for the beta cells to secrete more insulin, augment insulin resistance, impair beta-cell function, and increase risk of type 2 diabetes and other chronic diseases (39, 43, 46).

The observations from the present study are also consistent with those from an earlier report from Camden on adolescent pregnancy (47). In that study, Lenders et al. (47) observed that adolescents eating a diet rich in sugar had a greater than twofold increase in small-for-gestational-age births and concomitant reductions in infant birth weight compared with gravidas with a lower sugar intake. As Wolever et al. (27) pointed out, sugars have a lower glycemic index than do starchy foods. Sucrose (table sugar) has a glycemic index below those of white bread, rice, potatoes, and most breakfast cereals, and simple sugars such as those in milk products and fruit juices have a glycemic index below that of sucrose (24, 25). Consumption of a sugar-rich diet would by definition result in a lower dietary glycemic index with lower levels of maternal blood glucose (40) available for transmission to the fetus. Our data are also consistent with those from Clapp’s trial where regular exercise in combination with eating aboriginal carbohydrates reduced infant birth weight (48). The effect of the dietary glycemic index on carbohydrate metabolism and fetal growth, however, is difficult to disentangle from the effect of regular exercise on the same outcomes (49). Unlike Clapp, we found no influence of the dietary glycemic index on the maternal pregravid body mass index, rate of weight gain, or adequacy of weight gain during pregnancy in either the present study (table 1) or our prior work on sugar-rich diets (47).

In summary, we found that the dietary glycemic index, a measure of the type of carbohydrate in the maternal diet, influences the outcome of pregnancy and has utility for predicting the maternal metabolic response during pregnancy. Our results suggest that we should examine the diets of pregnant women to see if increasing the dietary glycemic index reduces the risk of small-for-gestational-age birth. Conversely, a lower dietary glycemic index diet might also help to raise postprandial glucose levels among African Americans. In this ethnic group, lower concentrations of maternal plasma glucose (possibly a reactive hypoglycemia in response to a high dietary glycemic index) have been associated with lower infant birth weight.


    ACKNOWLEDGMENTS
 
This research was supported by grants HD18269 and HD 38321 from the National Institutes of Health.

The authors are indebted to the staffs at the Osborn Family Health Center, Our Lady of Lourdes Hospital, and St. John the Baptist Prenatal Care Center in Camden for access to patients. Special thanks to Joan Murray for expert assistance with the nutrient and glycemic index databases, SaTonya Jones for laboratory assays, and Deborah Cruz for manuscript preparation.


    NOTES
 
Correspondence to Dr. Theresa O. Scholl, Department of Obstetrics and Gynecology, The University of Medicine and Dentistry of New Jersey-SOM, Two Medical Center Drive, Science Center, Suite 390, Stratford, NJ 08084 (e-mail: scholl{at}umdnj.edu). Back


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 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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