AN AUTHOR REPLIES

AN AUTHOR REPLIES We appreciate the thoughtful comments made by Macdonald and Yang (1) regarding our recent study (2) and are happy to provide additional information in response to each point raised. Regarding questions about individual food sources of vegetable protein, our results evaluating risk of early menopause associated with each 1-serving/day increase in protein-rich foods were strongest for pasta, dark bread, and cold breakfast cereal (2). These foods are indeed rich in carbohydrates, minerals, and B vitamins, as well as protein. While these nutrients could potentially confound an association between vegetable protein and early menopause, we did not find this to be the case. As we noted in our paper, adjustment for additional nutrients and dietary factors, including carbohydrates, vitamin B6, calcium, vitamin D, saturated fat, ω-3 fatty acids, and Alternative Healthy Eating Index score, did not materially change the hazard ratios for vegetable protein (2). Although soy food intake was relatively uncommon in our population and our power to evaluate associations for soy was low, the magnitude of the hazard ratio for soy/tofu was similar to that for pasta and stronger than that for dark bread and cold cereal (per 1-serving/day increase in soy/tofu intake, hazard ratio = 0.61, 95% confidence interval: 0.31, 1.20). These findings, in conjunction with results from animal studies (3), suggest that both soy-based and non-soy-based vegetable proteins may be associated with menopause timing and warrant further study. Macdonald and Yang pointed out that we included nuts along with pasta, breakfast cereal, and tofu as examples of foods rich in vegetable protein in our Discussion. While results from evaluation of the risk associated with daily servings of nuts were null, nuts and peanut butter contributed to calculations on overall vegetable protein intake and were important sources of between-person variation in vegetable protein intake in our population. Nonetheless, we agree that our findings do not suggest that nuts are specifically associated with lower risk of early menopause. We recently observed lower risk of early menopause among Nurses’ Health Study II participants with higher intakes of vitamin D and calcium from food sources, especially dairy foods (4); that paper was under review concurrently with our paper on protein intake and thus was not available for referencing. Both analyses addressed the possibility of mutual confounding of protein, vitamin D, and calcium intakes in multivariable models. As is shown in Table 1, results for vegetable protein and vitamin D demonstrate independent associations of each nutrient with incidence of early menopause, and results are consistent with hazard ratios presented in each of the 2 separate manuscripts (2, 4). Table 1. Hazard Ratios for Early Menopause According to Cumulatively Averaged Intakes of Vegetable Protein and Vitamin D From Food Sources in a Multivariable Model, Nurses’ Health Study II, 1996–2011 Intake Variable and Quintile Quintile Median Hazard Ratioa 95% Confidence Interval Vegetable protein, % of calories/day  1 3.9 1.00 Referent  2 4.6 0.85 0.74, 0.97  3 5.1 0.88 0.77, 1.01  4 5.6 0.79 0.68, 0.90  5 6.5 0.81 0.71, 0.94 Vitamin D from food sources, IU/day  1 148 1.00 Referent  2 232 0.95 0.83, 1.09  3 301 0.83 0.72, 0.95  4 383 0.98 0.85, 1.12  5 528 0.79 0.68, 0.92 Intake Variable and Quintile Quintile Median Hazard Ratioa 95% Confidence Interval Vegetable protein, % of calories/day  1 3.9 1.00 Referent  2 4.6 0.85 0.74, 0.97  3 5.1 0.88 0.77, 1.01  4 5.6 0.79 0.68, 0.90  5 6.5 0.81 0.71, 0.94 Vitamin D from food sources, IU/day  1 148 1.00 Referent  2 232 0.95 0.83, 1.09  3 301 0.83 0.72, 0.95  4 383 0.98 0.85, 1.12  5 528 0.79 0.68, 0.92 Abbreviation: MET, metabolic equivalent of task. a Adjusted for age (months; continuous), animal protein intake (% of calories/day; quintiles), calories (kcal/day; quintiles), pack-years of smoking (0, <20, or ≥20), body mass index (weight (kg)/height (m)2; <18.5,18.5–24.9, 25–29.9, or ≥30.0), age at menarche (≤11, 12, 13–15, or ≥16 years), number of pregnancies of ≥6 months’ duration (0, 1–2, or ≥3), total duration of breastfeeding (0, ≤2, or >2 years), oral contraceptive use (never, former, or current use), dairy protein intake (% of calories/day; quintiles), and physical activity level (<3.0, 3.0–8.9, 9.0–17.9, 18.0–26.9, 27.0–41.9, or ≥42.0 MET-hours/week). Table 1. Hazard Ratios for Early Menopause According to Cumulatively Averaged Intakes of Vegetable Protein and Vitamin D From Food Sources in a Multivariable Model, Nurses’ Health Study II, 1996–2011 Intake Variable and Quintile Quintile Median Hazard Ratioa 95% Confidence Interval Vegetable protein, % of calories/day  1 3.9 1.00 Referent  2 4.6 0.85 0.74, 0.97  3 5.1 0.88 0.77, 1.01  4 5.6 0.79 0.68, 0.90  5 6.5 0.81 0.71, 0.94 Vitamin D from food sources, IU/day  1 148 1.00 Referent  2 232 0.95 0.83, 1.09  3 301 0.83 0.72, 0.95  4 383 0.98 0.85, 1.12  5 528 0.79 0.68, 0.92 Intake Variable and Quintile Quintile Median Hazard Ratioa 95% Confidence Interval Vegetable protein, % of calories/day  1 3.9 1.00 Referent  2 4.6 0.85 0.74, 0.97  3 5.1 0.88 0.77, 1.01  4 5.6 0.79 0.68, 0.90  5 6.5 0.81 0.71, 0.94 Vitamin D from food sources, IU/day  1 148 1.00 Referent  2 232 0.95 0.83, 1.09  3 301 0.83 0.72, 0.95  4 383 0.98 0.85, 1.12  5 528 0.79 0.68, 0.92 Abbreviation: MET, metabolic equivalent of task. a Adjusted for age (months; continuous), animal protein intake (% of calories/day; quintiles), calories (kcal/day; quintiles), pack-years of smoking (0, <20, or ≥20), body mass index (weight (kg)/height (m)2; <18.5,18.5–24.9, 25–29.9, or ≥30.0), age at menarche (≤11, 12, 13–15, or ≥16 years), number of pregnancies of ≥6 months’ duration (0, 1–2, or ≥3), total duration of breastfeeding (0, ≤2, or >2 years), oral contraceptive use (never, former, or current use), dairy protein intake (% of calories/day; quintiles), and physical activity level (<3.0, 3.0–8.9, 9.0–17.9, 18.0–26.9, 27.0–41.9, or ≥42.0 MET-hours/week). Finally, we appreciate the suggestion to consider associations of dietary patterns with incidence of early menopause. Results from such analyses would likely provide an important complement to results from evaluations of individual nutrients. Abbreviations MET metabolic equivalent of task Acknowledgments This project was supported by grants UM1CA176726 and R01HD078517 from the National Institutes of Health, US Department of Health and Human Services. Conflict of interest: none declared. References 1 Macdonald HM , Yang T . Re: “Dietary protein intake and early menopause in the Nurses’ Health Study II” [letter]. Am J Epidemiol . 2018 ; 187 ( 6 ): 1341 – 1342 . 2 Boutot ME , Purdue-Smithe A , Whitcomb BW , et al. . Dietary protein intake and early menopause in the Nurses’ Health Study II . Am J Epidemiol . 2018 ; 187 ( 2 ): 270 – 277 . Google Scholar CrossRef Search ADS PubMed 3 Appt SE , Chen H , Goode AK , et al. . The effect of diet and cardiovascular risk on ovarian aging in cynomolgus monkeys (Macaca fascicularis) . Menopause . 2010 ; 17 ( 4 ): 741 – 748 . Google Scholar PubMed 4 Purdue-Smithe AC , Whitcomb BW , Szegda KL , et al. . Vitamin D and calcium intake and risk of early menopause . Am J Clin Nutr . 2017 ; 105 ( 6 ): 1493 – 1501 . Google Scholar PubMed © The Author(s) 2018. Published by Oxford University Press on behalf of the Johns Hopkins Bloomberg School of Public Health. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png American Journal of Epidemiology Oxford University Press

AN AUTHOR REPLIES

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© The Author(s) 2018. Published by Oxford University Press on behalf of the Johns Hopkins Bloomberg School of Public Health. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.
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Abstract

We appreciate the thoughtful comments made by Macdonald and Yang (1) regarding our recent study (2) and are happy to provide additional information in response to each point raised. Regarding questions about individual food sources of vegetable protein, our results evaluating risk of early menopause associated with each 1-serving/day increase in protein-rich foods were strongest for pasta, dark bread, and cold breakfast cereal (2). These foods are indeed rich in carbohydrates, minerals, and B vitamins, as well as protein. While these nutrients could potentially confound an association between vegetable protein and early menopause, we did not find this to be the case. As we noted in our paper, adjustment for additional nutrients and dietary factors, including carbohydrates, vitamin B6, calcium, vitamin D, saturated fat, ω-3 fatty acids, and Alternative Healthy Eating Index score, did not materially change the hazard ratios for vegetable protein (2). Although soy food intake was relatively uncommon in our population and our power to evaluate associations for soy was low, the magnitude of the hazard ratio for soy/tofu was similar to that for pasta and stronger than that for dark bread and cold cereal (per 1-serving/day increase in soy/tofu intake, hazard ratio = 0.61, 95% confidence interval: 0.31, 1.20). These findings, in conjunction with results from animal studies (3), suggest that both soy-based and non-soy-based vegetable proteins may be associated with menopause timing and warrant further study. Macdonald and Yang pointed out that we included nuts along with pasta, breakfast cereal, and tofu as examples of foods rich in vegetable protein in our Discussion. While results from evaluation of the risk associated with daily servings of nuts were null, nuts and peanut butter contributed to calculations on overall vegetable protein intake and were important sources of between-person variation in vegetable protein intake in our population. Nonetheless, we agree that our findings do not suggest that nuts are specifically associated with lower risk of early menopause. We recently observed lower risk of early menopause among Nurses’ Health Study II participants with higher intakes of vitamin D and calcium from food sources, especially dairy foods (4); that paper was under review concurrently with our paper on protein intake and thus was not available for referencing. Both analyses addressed the possibility of mutual confounding of protein, vitamin D, and calcium intakes in multivariable models. As is shown in Table 1, results for vegetable protein and vitamin D demonstrate independent associations of each nutrient with incidence of early menopause, and results are consistent with hazard ratios presented in each of the 2 separate manuscripts (2, 4). Table 1. Hazard Ratios for Early Menopause According to Cumulatively Averaged Intakes of Vegetable Protein and Vitamin D From Food Sources in a Multivariable Model, Nurses’ Health Study II, 1996–2011 Intake Variable and Quintile Quintile Median Hazard Ratioa 95% Confidence Interval Vegetable protein, % of calories/day  1 3.9 1.00 Referent  2 4.6 0.85 0.74, 0.97  3 5.1 0.88 0.77, 1.01  4 5.6 0.79 0.68, 0.90  5 6.5 0.81 0.71, 0.94 Vitamin D from food sources, IU/day  1 148 1.00 Referent  2 232 0.95 0.83, 1.09  3 301 0.83 0.72, 0.95  4 383 0.98 0.85, 1.12  5 528 0.79 0.68, 0.92 Intake Variable and Quintile Quintile Median Hazard Ratioa 95% Confidence Interval Vegetable protein, % of calories/day  1 3.9 1.00 Referent  2 4.6 0.85 0.74, 0.97  3 5.1 0.88 0.77, 1.01  4 5.6 0.79 0.68, 0.90  5 6.5 0.81 0.71, 0.94 Vitamin D from food sources, IU/day  1 148 1.00 Referent  2 232 0.95 0.83, 1.09  3 301 0.83 0.72, 0.95  4 383 0.98 0.85, 1.12  5 528 0.79 0.68, 0.92 Abbreviation: MET, metabolic equivalent of task. a Adjusted for age (months; continuous), animal protein intake (% of calories/day; quintiles), calories (kcal/day; quintiles), pack-years of smoking (0, <20, or ≥20), body mass index (weight (kg)/height (m)2; <18.5,18.5–24.9, 25–29.9, or ≥30.0), age at menarche (≤11, 12, 13–15, or ≥16 years), number of pregnancies of ≥6 months’ duration (0, 1–2, or ≥3), total duration of breastfeeding (0, ≤2, or >2 years), oral contraceptive use (never, former, or current use), dairy protein intake (% of calories/day; quintiles), and physical activity level (<3.0, 3.0–8.9, 9.0–17.9, 18.0–26.9, 27.0–41.9, or ≥42.0 MET-hours/week). Table 1. Hazard Ratios for Early Menopause According to Cumulatively Averaged Intakes of Vegetable Protein and Vitamin D From Food Sources in a Multivariable Model, Nurses’ Health Study II, 1996–2011 Intake Variable and Quintile Quintile Median Hazard Ratioa 95% Confidence Interval Vegetable protein, % of calories/day  1 3.9 1.00 Referent  2 4.6 0.85 0.74, 0.97  3 5.1 0.88 0.77, 1.01  4 5.6 0.79 0.68, 0.90  5 6.5 0.81 0.71, 0.94 Vitamin D from food sources, IU/day  1 148 1.00 Referent  2 232 0.95 0.83, 1.09  3 301 0.83 0.72, 0.95  4 383 0.98 0.85, 1.12  5 528 0.79 0.68, 0.92 Intake Variable and Quintile Quintile Median Hazard Ratioa 95% Confidence Interval Vegetable protein, % of calories/day  1 3.9 1.00 Referent  2 4.6 0.85 0.74, 0.97  3 5.1 0.88 0.77, 1.01  4 5.6 0.79 0.68, 0.90  5 6.5 0.81 0.71, 0.94 Vitamin D from food sources, IU/day  1 148 1.00 Referent  2 232 0.95 0.83, 1.09  3 301 0.83 0.72, 0.95  4 383 0.98 0.85, 1.12  5 528 0.79 0.68, 0.92 Abbreviation: MET, metabolic equivalent of task. a Adjusted for age (months; continuous), animal protein intake (% of calories/day; quintiles), calories (kcal/day; quintiles), pack-years of smoking (0, <20, or ≥20), body mass index (weight (kg)/height (m)2; <18.5,18.5–24.9, 25–29.9, or ≥30.0), age at menarche (≤11, 12, 13–15, or ≥16 years), number of pregnancies of ≥6 months’ duration (0, 1–2, or ≥3), total duration of breastfeeding (0, ≤2, or >2 years), oral contraceptive use (never, former, or current use), dairy protein intake (% of calories/day; quintiles), and physical activity level (<3.0, 3.0–8.9, 9.0–17.9, 18.0–26.9, 27.0–41.9, or ≥42.0 MET-hours/week). Finally, we appreciate the suggestion to consider associations of dietary patterns with incidence of early menopause. Results from such analyses would likely provide an important complement to results from evaluations of individual nutrients. Abbreviations MET metabolic equivalent of task Acknowledgments This project was supported by grants UM1CA176726 and R01HD078517 from the National Institutes of Health, US Department of Health and Human Services. Conflict of interest: none declared. References 1 Macdonald HM , Yang T . Re: “Dietary protein intake and early menopause in the Nurses’ Health Study II” [letter]. Am J Epidemiol . 2018 ; 187 ( 6 ): 1341 – 1342 . 2 Boutot ME , Purdue-Smithe A , Whitcomb BW , et al. . Dietary protein intake and early menopause in the Nurses’ Health Study II . Am J Epidemiol . 2018 ; 187 ( 2 ): 270 – 277 . Google Scholar CrossRef Search ADS PubMed 3 Appt SE , Chen H , Goode AK , et al. . The effect of diet and cardiovascular risk on ovarian aging in cynomolgus monkeys (Macaca fascicularis) . Menopause . 2010 ; 17 ( 4 ): 741 – 748 . Google Scholar PubMed 4 Purdue-Smithe AC , Whitcomb BW , Szegda KL , et al. . Vitamin D and calcium intake and risk of early menopause . Am J Clin Nutr . 2017 ; 105 ( 6 ): 1493 – 1501 . Google Scholar PubMed © The Author(s) 2018. Published by Oxford University Press on behalf of the Johns Hopkins Bloomberg School of Public Health. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

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American Journal of EpidemiologyOxford University Press

Published: Mar 23, 2018

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