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Pasta meal intake in relation to risks of BMJNPH: first published as 10.1136/bmjnph-2020-000198 on 30 April 2021. Downloaded from
type 2 diabetes and atherosclerotic
cardiovascular disease in postmenopausal
women : findings from the Women’s
Health Initiative
1 2,3 1 4 5
Mengna Huang, Kenneth Lo , Jie Li , Matthew Allison, Wen- Chih Wu,
Simin Liu 3,6,7
To cite: Huang M, Lo K, Li J, ABSTRACT What this paper adds
et al. Pasta meal intake in Objective To evaluate the association between pasta
relation to risks of type 2 meal intake and long- term risk of developing diabetes
diabetes and atherosclerotic or atherosclerotic cardiovascular disease (ASCVD, ► The present study has found that higher pasta meal
cardiovascular disease in intake may be significantly associated with reduced
postmenopausal women : including coronary heart disease (CHD) and stroke) in long- term risk of stroke and atherosclerotic cardio-
findings from the Women’s postmenopausal women. vascular disease in postmenopausal women.
Health Initiative. BMJ Design Prospective cohort study. ► Substituting pasta for an equal amount of fried po-
Nutrition, Prevention & Setting Women’s Health Initiative (WHI) in the USA. tato or white bread could potentially be associated
Health 2021;0. doi:10.1136/ Participants 84 555 postmenopausal women aged with lower risk of stroke and atherosclerotic cardio-
bmjnph-2020-000198 50–79 in 1994, who were free of diabetes, ASCVD vascular disease.
► Additional supplemental and cancer at baseline who were not in the dietary
material is published online only. modification trial of the WHI, completed a validated food
To view, please visit the journal frequency questionnaire, and were evaluated for incident INTRODUCTION
online (http:// dx. doi. org/ 10. diabetes and ASCVD outcomes during the follow- up until Among major sources of dietary carbohy-
1136/ bmjnph- 2020- 000198). 2010. drates, pasta has long been a staple food in
For numbered affiliations see Main outcome measure Diabetes and ASCVD. diverse human cultures around the world. http://nutrition.bmj.com/
end of article. Results Cox proportional hazards models were used to Interest in the health effects of pasta on the
estimate the association (HR) between quartiles of pasta human body has steadily increased since the
Correspondence to meal consumption (residuals after adjusting for total 1980s during a series of clinical studies of
Professor Simin Liu, Center for energy) and the risk of incidence diabetes, CHD, stroke patients with diabetes showing that blood
Global Cardiometabolic Health, glucose response was remarkably reduced
Epidemiology, Brown University or ASCVD, accounting for potential confounding factors,
School of Public Health, with testing for linear trend. We then statistically evaluated after ingesting spaghetti compared with white
Providence, RI 02912, USA; the effect of substituting white bread or fried potato for bread,1–4 potato2–5 or rice.5 Many character-
simin_ liu@ brown. edu pasta meal on disease risk. When comparing the highest istics of pasta have been studied in relation on January 11, 2023 by guest. Protected by copyright.
to the lowest quartiles of residual pasta meal intake, we to its glycaemic response. Notably, the struc-
MH and KL contributed equally. observed significantly reduced risk of ASCVD (HR=0.89, ture (ie, viscosity, particle size and shape)
95% CI 0.83 to 0.96, p trend=0.002), stroke (HR=0.84, of pasta appears to be more important in
Received 31 October 2020 95% CI 0.75 to 0.93, p trend=0.001), CHD (HR=0.91, determining its glycaemic response than the
Revised 11 April 2021 95% CI 0.83 to 1.00, p trend=0.058) and no significant 6–8
Accepted 12 April 2021 types of cereal used in its production. It has
alteration in diabetes risk (HR=1.02, 95% CI 0.96 to 1.07, also been found that consumption of pasta
p trend=0.328). Replacing white bread or fried potato with meal produced a lower postprandial insulin
pasta meal was statistically associated with decreased response than consumption of white bread
risk of stroke and ASCVD. 6
Conclusions Pasta meal intake did not have adverse in healthy subjects. Given the same amount,
effects on long- term diabetes risk and may be associated pasta appears to have lower glycaemic index
with significant reduced risk of stroke and ASCVD. The (GI) as well as glycaemic load (GL) compared
4
potential benefit of substituting pasta meal for other with other major sources of carbohydrates.
© Author(s) (or their commonly consumed starchy foods on cardiometabolic The International Carbohydrate Quality
employer(s)) 2021. Re- use Consortium reached consensus in 2015 that
permitted under CC BY- NC. No outcomes warrants further investigation in additional there was convincing evidence that low GI/
commercial re- use. See rights high- quality and large prospective studies of diverse GL diets reduce the risk of type 2 diabetes
and permissions. Published by populations.
BMJ. and coronary heart disease (CHD), and GI
Huang M, et al. bmjnph 2021;0. doi:10.1136/bmjnph-2020-000198 1
BMJ Nutrition, Prevention & Health
represents another characteristic of carbohydrate foods hormone therapy (HT) trial, the calcium and vitamin BMJNPH: first published as 10.1136/bmjnph-2020-000198 on 30 April 2021. Downloaded from
9
apart from fibre and whole grain content. Dietary GL D (CaD) trial and the dietary modification (DM) trial.
and GI have been linked to numerous cardiometabolic We analysed baseline data from participants of the OS,
10–14 15–18
conditions and risk factors. Low- GI foods have and the HT and CaD trials of the WHI, for whom valid
been consistently associated with better glucose control information was obtained from a validated 122- item food
19 20
in patients with diabetes. Since pasta has been shown frequency questionnaire (FFQ). Participants of the DM
to produce lower glycaemic response, it is then natural trial were excluded due to potential major alterations in
to hypothesise that consumption of pasta meal may dietary behaviour after baseline. Additional exclusion
have beneficial effects on the long-term risk of diabetes criteria included: implausible total energy intake (<600
and atherosclerotic cardiovascular diseases (ASCVD, or >5000 kcal/day); prevalent diseases including diabetes,
including CHD and stroke), given the same total carbohy- cardiovascular disease (CVD) and cancer that may alter
drate consumption. However, few long- term studies have dietary behaviours; measurements not available for
prospectively and directly investigated long-term average outcomes of interest (incident diabetes, CHD or stroke);
intake of pasta and the risk of developing diabetes, CHD, measurements not available for important covariates such
stroke and ASCVD. In the current study, we also aim to as race and body mass index (BMI); and being under-
2
evaluate whether substituting other types of carbohydrate- weight (BMI <18.5 kg/m ) which may reflect underlying
dense food with pasta was associated with altered risk. To medical conditions (figure 1).
our knowledge, no other large- scale, long- term prospec-
tive cohort studies have specifically evaluated these Measurement of outcomes
relationships. Incident diabetes was assessed via questionnaires at enrol-
ment and each annual visit. Participants were asked if ‘a
doctor prescribed for the first time any of the following
METHODS pills or treatments: pills for diabetes or insulin shots for
Study population diabetes’ since their last medical update. Those who
The Women’s Health Initiative (WHI) recruited a total responded ‘yes’ were considered having been diagnosed
of 161 808 postmenopausal women aged 50–79 years with diabetes. Since these were all postmenopausal
at 40 clinical centres across the USA between 1993 and women, newly diagnosed diabetes cases were most likely
1998, including a cohort of 93 676 women in a prospec- type 2 diabetes cases, which have been shown to have a
tive observational study (OS) and 68 132 women in one high validity.21 22 Women who self- reported diabetes at
or more of the following three clinical trials (CTs): the baseline were excluded from the current analysis.
http://nutrition.bmj.com/
on January 11, 2023 by guest. Protected by copyright.
Figure 1 Analytical sample flow chart. BMI, body mass index; CaD, calcium and vitamin D; CHD, coronary heart disease;
CVD, cardiovascular disease; FFQ, food frequency questionnaire; HT, hormone therapy; OS, observational study; WHI, Women’s
Health Initiative.
2 Huang M, et al. bmjnph 2021;0. doi:10.1136/bmjnph-2020-000198
BMJ Nutrition, Prevention & Health
Incident CHD was defined as the first occurrence of quartiles were tested by analysis of variance for contin- BMJNPH: first published as 10.1136/bmjnph-2020-000198 on 30 April 2021. Downloaded from
2
clinical myocardial infarction (MI), definite silent MI, uous variables and by χ test for categorical variables.
or a death due to definite or possible CHD. Clinical MI Cox proportional hazards models were used to evaluate
and death were adjudicated for CT and OS participants the association between residual total pasta meal intake
during the core WHI study (until 2005) and Extension and the risk of diabetes, CHD, stroke and ASCVD in terms
Study I (Ext1, until 2010). of HRs and associated 95% CIs, with study baseline as the
Incident stroke was defined as the first occurrence of origin of analysis and time to event or time to censoring as
stroke or death due to cerebrovascular event. Stroke was defined hereafter. For each disease condition of interest
adjudicated for CT and OS participants through Ext1. (diabetes/CHD/stroke/ASCVD), follow- up durations
We further examined the concept of incident ASCVD as were calculated as the interval between baseline and
an outcome, which encompassed incident cases of CHD the earliest of any of the following: (1) date of annual
and stroke as defined above, according to the 2013 Amer- medical history update when new disease was reported,
ican College of Cardiology/American Heart Association (2) date of last data collection from the main study if the
23 participant did not enter the Extension Study, (3) date of
Guideline on the Assessment of Cardiovascular Risk.
last data collection from the Extension Study, or (4) date
Measurement of pasta meal of reported death.
20 24 Residual pasta meal intake was analysed both in quar-
Using a validated semiquantitative FFQ, participants tiles and as continuous variables. We also tested for linear
reported on the baseline FFQ how often they consumed trend after assigning the median of each quartile to the
each of the following forms of pasta during the past 3 participants. The proportional hazards assumption was
months: macaroni and cheese/lasagna/noodles with a 26
cream sauce, spaghetti or other noodles with meat sauce tested following standard procedures. We adjusted for
and spaghetti or other noodles with tomato sauce (and the following potential confounding factors in model 1:
no meat), in frequency of medium servings (one cup). study group indicator (OS/HT/CaD), age (continuous),
Nine frequency options were given, including: ‘never or race/ethnicity (Caucasian, African- American, Hispanic,
less than 1 per month’, ‘1 per month’, ‘2–3 per month’, Asian/Pacific Islander or other) and region (Northeast,
‘1 per week’, ‘2 per week’, ‘3–4 per week’, ‘5–6 per week’, South, Midwest or West of the US). In model 2, we addi-
‘1 per day’ and ‘2+ per day’. Participants also had the tionally adjusted for BMI (continuous, computed from
choices of ‘small’, ‘medium’ and ‘large’ for portion size weight and height measured by trained study staff), total
per serving. The midpoint of the nine categories was used energy intake and per cent energy intake from carbo-
to compute the semicontinuous variables for these three hydrates. In model 3 and the final model, we further
forms of pasta meals, in number of medium servings per adjusted for cigarette smoking (never, past or current),
alcohol consumption (continuous), physical activity (in
day. The sum of the three was used as a measure of total metabolic equivalent hours/week, continuous), and http://nutrition.bmj.com/
pasta meal intake. The residual method was then used 27
where total pasta meal intake was first regressed on total Healthy Eating Index (HEI 2005, continuous), and
energy intake, and the residuals added with mean total the respective family history of each outcome (diabetes,
pasta meal intake were taken as a measure of pasta meal CHD, stroke or ASCVD). These potential confounding
25 factors were chosen a priori based on current under-
intake uncorrelated with total energy intake. standing of scientific literature and whether they could
In addition to residual total pasta meal intake, we also influence our exposure and outcomes of interest. Pasta to
constructed two measures of pasta meal intake analogous GL ratio and pasta to total energy ratio were analysed in
to energy density standardisation: (1) the ratio of pasta similar procedures as the residual total pasta meal intake, on January 11, 2023 by guest. Protected by copyright.
to dietary GL was computed by dividing total pasta meal in both continuous form and quartiles, and then tested
intake with total dietary GL and then multiplied by 100; for linear trend. We also evaluated the results adjusting
(2) the ratio of pasta to total energy intake was computed for potential dietary confounders, including daily intake
by dividing total pasta meal intake with dietary total whole grain, whole
energy intake and then multiplied by 1000. The respec- of fibre, total sugar, added sugar, non-
grain,
tive scaling was done to obtain physiologically interpre- frequency of eating a serving of vegetables and
table measurements. These two ratio measures were other major components in typical pasta meals (intake
analysed in multivariable models in parallel with residual of total cheese and total tomato in medium servings per
total pasta meal intake. day).
As a sensitivity analysis, we included only pasta meals
with spaghetti as the main carbohydrates source, as maca-
Statistical analysis roni and cheese had been observed to have higher GI,7
Baseline characteristics of participants included in the analysed similarly to residual total pasta meal intake. In
current analysis were described according to quartiles a second sensitivity analysis, we used age as the timescale
of residual total pasta meal intake. Means and SDs were in the Cox proportional hazards model instead of time
generated as descriptive statistics for continuous variables, to event. We also statistically tested for the substitutional
while frequencies and percentages were generated for effects of replacing pasta meal for the same amount of
categorical variables. Differences across pasta meal intake white bread or fried potato, measured with the same FFQ.
Huang M, et al. bmjnph 2021;0. doi:10.1136/bmjnph-2020-000198 3
BMJ Nutrition, Prevention & Health
To model such effects, if we take white bread as example, to 1.07, respectively), and the linear trend was also not BMJNPH: first published as 10.1136/bmjnph-2020-000198 on 30 April 2021. Downloaded from
first the residual variable for white bread was created significant (p value for trend=0.328). Results were largely
using the residual method; then residual total pasta meal similar when examining quartiles of pasta to GL ratio or
intake and the sum of residual pasta and residual white pasta to energy ratio.
bread were both included in model 3, so that the effect For the CHD outcome, overall increased intake of pasta
estimates for the residual pasta variable represented the meal appeared to be associated with a decreased risk of
estimated log(HR) for replacing one medium serving of developing CHD, especially when comparing women in
white bread or fried potato by pasta, respectively, since the the highest against the lowest quartile of residual total
interpretation of the effect of the residual pasta variable pasta meal intake (table 3). Specifically from model 3
28
was conditional on holding other covariates constant. (figure 2), compared with women in the lowest quartile of
29
All statistical analyses were conducted using R V.3.6.3. residual pasta meal intake, those in the second and third
quartiles had no change in the risk of developing CHD
(HR=0.99, 95% CI 0.90 to 1.09 and HR=1.02, 95% CI 0.93
RESULTS to 1.12, respectively), while women in the highest intake
A total of 84 555 participants of the WHI- OS, HT and CaD quartile had an estimated 9% reduction in risk (HR=0.91,
were included in the final analytical sample. Among these 95% CI 0.83 to 1.00), while holding constant age, race,
women, the median intake of pasta meal was 0.15 servings region, study indicators, BMI, total energy intake, per
per day, or equivalently 1.04 servings per week, with the cent energy from carbohydrates, smoking status, alcohol
IQR from 0.08 to 0.26 servings per day (equivalently 0.54– consumption, physical activity, HEI 2005 and family
1.84 servings per week). This group of participants were history of CHD; with borderline significant linear trend
on average 63.3 years old (SD=7.3), had an average BMI (p value for trend=0.058). Results were largely similar
2
of 27.3 kg/m (SD=5.6), an average total energy intake across models 1–3 as well as when examining quartiles of
of 1576.2 kcal/day (SD=598.8) and an average total pasta to GL ratio or pasta to energy ratio.
carbohydrates intake of 203.7 g/day (SD=78.0), which Women within the highest intake quartile of pasta meal
translated into an average of 52.4% energy from carbohy- had a significantly reduced risk of developing stroke
drates (SD=9.6). Eighty-five per cent of them were white compared with those in the lowest intake quartile of
and 6.8% were smokers at study baseline. Thirty per cent pasta (HR=0.84, 95% CI 0.75 to 0.93), while those in the
had a family history of diabetes, while 51.8% had a family second and third quartiles had virtually no change in risk
history of CHD, 36.1% had a family of history of stroke (HR=0.97, 95% CI 0.88 to 1.08 and HR=1.00, 95% CI 0.91
and 65.2% had a family history of ASCVD. to 1.11, respectively) (table 4, figure 2). Testing for linear
Those in the higher quartiles of residual total pasta trend showed a significant inverse association (p value for
meal intake were on average younger, more likely to be trend=0.001), and results were highly consistent across
white, less likely to be never smokers and more likely to models 1–3 as well as when examining quartiles of pasta http://nutrition.bmj.com/
have family history of diabetes and CHD, but not stroke to GL ratio or pasta to energy ratio.
or ASCVD. In terms of dietary intakes, women in the With ASCVD being a composite outcome of CHD
lowest and highest quartiles of residual pasta meal intake and stroke, participants within the highest intake quar-
had on average higher total energy intake and GL, and tile of residual total pasta meal had an estimated 11%
higher intake of total carbohydrates, total sugar, added decreased risk of developing ASCVD (HR=0.89, 95% CI
sugar intake, fibre and both whole and non- whole grains. 0.83 to 0.96) compared with those in the lowest intake
Those in the lowest quartiles of residual total pasta meal quartile in model 3, while those in the second and third on January 11, 2023 by guest. Protected by copyright.
intake had relatively higher alcohol intake, but lower per quartiles had no change in risk (HR=0.99, 95% CI 0.92
cent energy from carbohydrates and dietary quality as to 1.06 and HR=1.03, 95% CI 0.96 to 1.11, respectively),
measured by HEI 2005. Physical activity levels and GI were with age, race, region, study indicators, BMI, total energy
relatively similar in magnitude across quartiles (table 1). intake, per cent energy from carbohydrates, smoking
Results from the Cox proportional hazards models were status, alcohol consumption, physical activity, HEI 2005
summarised as follows by outcomes of interest. Residual and family history of ASCVD being constant (table 5,
total pasta meal intake across quartiles was not associated figure 2). Significant inverse trends were also observed,
with risk of diabetes for postmenopausal women, after with p value for trend=0.002. Results were again highly
adjusting for age, race, region, study indicators, BMI, consistent across models 1–3 as well as when examining
total energy intake, per cent energy from carbohydrates, quartiles of pasta to GL ratio or pasta to energy ratio.
smoking status, alcohol consumption, physical activity, We also estimated the effects of one medium serving/
HEI 2005 and family history of diabetes (model 3). Models day increase in pasta meal intake variables on each
1–3 had similar results (table 2). Specifically, from model disease of interest by entering the continuous variables of
3 (figure 2), compared with those in the lowest quartile pasta meal intake into the models as exposure instead of
of residual pasta meal intake, women in the second, third quartiles. These analyses had similar results to the coun-
and highest intake quartiles had essentially no change in terparts with quartiles as exposure, but the effect sizes
risk for incident diabetes (HR=0.97, 95% CI 0.92 to 1.03; seemed generally larger in magnitude (online supple-
HR=1.00, 95% CI 0.94 to 1.05; HR=1.02, 95% CI 0.96 mental table 1). Results were also robust to adjustment
4 Huang M, et al. bmjnph 2021;0. doi:10.1136/bmjnph-2020-000198
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