Reply to MF McCarty

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In a recent crossover trial that recruited subjects with chronic kidney disease, a week of a meat- rich diet was alternated with a week of a vegetarian diet (only 5%.
Letters to the Editor

Lower bioavailability of plant-derived phosphorus Dear Sir: The analysis by Chang et al (1) is an important contribution to the growing literature that pinpoints bioavailable phosphorus intake as a key determinant of disease risk and mortality, not only in patients suffering from renal failure but in the general population as well. The authors correctly state that inorganic phosphate additives have greater bioavailability than ‘‘organic’’ sources of phosphorus. However, it is important to note that the phosphorus bioavailability of natural foods is also variable. Phosphorus in flesh foods, dairy, and eggs tends to have relatively high bioavailability, whereas the bioavailability of phosphorus in phosphate-rich plant foods such as whole grains, legumes, peas, nuts, and seeds tends to be relatively low, because a high proportion of it is tied up in poorly absorbed phytates; humans do not make a gastrointestinal phytase (2). In a recent crossover trial that recruited subjects with chronic kidney disease, a week of a meatrich diet was alternated with a week of a vegetarian diet (only 5% of protein from animal sources); the 2 diets were designed to be nearly identical in macronutrient and phosphorus content (3). The fasting serum phosphorus concentration (mean 6 SD) was lower after the vegetarian diet than after the meat diet (3.2 6 0.5 compared with 3.7 6 0.6 mg/dL; P = 0.02), and, more notably, plasma fibroblast growth factor 23—the secretion of which is evoked by plasma phosphate—was ;40% lower (P = 0.008). Similarly, a cross-sectional study in chronic kidney disease patients concluded that the percentage of dietary protein provided by plant sources correlates inversely with fibroblast growth factor 23 concentrations (4). In conjunction with the findings of Chang et al and of other recent studies linking high phosphorus intakes to increased morbidity and mortality (5), these considerations suggest that the relatively low bioavailability of phosphorus from natural plant foods may be a mediating factor in the favorable health outcomes associated with whole-food plant-based diets. Chang et al may wish to consider conducting a supplemental analysis in which they use estimated correction factors to take account of the relative bioavailabilities of phosphorus from inorganic, animal, and plant sources; such an analysis might render their conclusions even stronger. The author had no conflicts of interest.

Mark F McCarty Catalytic Longevity 7831 Rush Rose Drive Apartment 316 Carlsbad, CA 92009 E-mail: [email protected]

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REFERENCES 1. Chang AR, Lazo M, Appel LJ, Gutie´rrez OM, Grams ME. High dietary phosphorus intake is associated with all-cause mortality: results from NHANES III. Am J Clin Nutr 2014;99:320–7. 2. Kalantar-Zadeh K, Gutekunst L, Mehrotra R, Kovesdy CP, Bross R, Shinaberger CS, Noori N, Hirschberg R, Benner D, Nissneson AR, et al. Understanding sources of dietary phosphorus in the treatment of patients with chronic kidney disease. Clin J Am Soc Nephrol 2010;5:519–30. 3. Moe SM, Zidehsarai MP, Chambers MA, Jackman LA, Radcliffe JS, Trevino LL, Donahue SE, Asplin JR. Vegetarian compared with meat dietary protein source and phosphorus homeostasis in chronic kidney disease. Clin J Am Soc Nephrol 2011;6:257–64. 4. Scialla JJ, Appel LJ, Wolf M, Yang W, Zhang X, Sozio SM, Miller ER III, Bazzano LA, Cuevas M, Glenn MJ, et al. Plant protein intake is associated with fibroblast growth factor 23 and serum bicarbonate levels in patients with chronic kidney disease: the Chronic Renal Insufficiency Cohort Study. J Ren Nutr 2012;22:379–88. 5. Ellam TJ, Chico TJ. Phosphate: the new cholesterol? The role of the phosphate axis in non-uremic vascular disease. Atherosclerosis 2012;220:310–8. doi: 10.3945/ajcn.113.081612.

Reply to MF McCarty Dear Sir: Although we agree with McCarty on many points, phosphorus bioavailability is a nuanced issue that requires further study before any ‘‘correction factor’’ for food source can be used with confidence. Bioavailability refers to the fraction of the ingested dose that is absorbed and can be measured in a variety of ways, the gold standard of which is the balance method [net absorption % = (intake 2 fecal excretion)/intake 3 100] (1). Whereas studies comparing animal- and vegetablebased sources of phosphorus on mineral metabolism in humans suggest lower bioavailability of phosphorus derived from plant-based proteins (2, 3), they have been of relatively short duration (1–7 d) and have lacked stool measurements. As mentioned by McCarty, the majority of phosphorus found in grains and legumes is in the form of phytate, which requires degradation by phytase, an enzyme not present in the small intestine of humans (4). Also important to mention is that food processing and household preparation can affect the bioavailability and amount of phosphorus content. For example, leavening of bread with phytase-producing yeasts (5) increases bioavailable phosphorus, whereas boiling foods reduces dietary phosphorus content (6). The other important issue when considering bioavailability is the contribution of food additives that contain highly bioavailable inorganic salts of phosphorus (7). One study found that 44% of top grocery items contained phosphorus-based additives in food products such as baked goods, packaged meats, soup, frozen vegetables, ready-to-eat meals, cheese, carbonated beverages, and shelf-stable juice drinks (8). Although a randomized controlled trial showed that education on the avoidance of phosphorus-based additives can result in lower serum phosphorus concentrations in hemodialysis patients (9), observational

Am J Clin Nutr 2014;99:966–7. Printed in USA. Ó 2014 American Society for Nutrition

LETTERS TO THE EDITOR studies have not shown any relation between processed meats, soda, and fast-food consumption with serum phosphorus (10). A possible explanation for this null relation is that these categories only represent a small fraction of an individual’s exposure to phosphorus-based additives. Until reliable methods that account for factors such as the use of phosphorus-based additives and food preparation are developed to estimate bioavailability of phosphorus, using a correction factor to estimate bioavailable phosphorus would likely introduce error into analyses. Measurements of 24-h urine phosphorus excretion would give a better approximation of bioavailable phosphorus intake, but these measurements were unavailable in the present study. Future research is needed to improve our understanding of the determinants of phosphorus bioavailability and the consequences of high phosphorus intake. ARC was supported by the National Institute of Diabetes and Digestive and Kidney Diseases (grant T32DK007732). OMG has served as a consultant to Vifor Pharma. The other authors had no conflicts of interest.

Alex R Chang Division of Nephrology Geisinger Health System 100 North Academy Avenue Danville, PA 17822 E-mail: [email protected] Mariana Lazo Lawrence J Appel Welch Center for Prevention, Epidemiology, and Clinical Research Johns Hopkins University Baltimore, MD Orlando M Gutie´rrez Division of Nephrology University of Alabama at Birmingham Birmingham, AL

967 Morgan E Grams

Division of Nephrology Johns Hopkins University Baltimore, MD

REFERENCES 1. Heaney RP. Factors influencing the measurement of bioavailability, taking calcium as a model. J Nutr 2001;131(suppl):1344S–8S. 2. Karp HJ, Vaihia KP, Karkkainen MU, Niemisto MJ, Lamberg-Allardt CJ. Acute effects of different phosphorus sources on calcium and bone metabolism in young women: a whole-foods approach. Calcif Tissue Int 2007;80:251–8. 3. Moe SM, Zidehsarai MP, Chambers MA, Jackman LA, Radcliffe JS, Trevino LL, Donahue SE, Asplin JR. Vegetarian compared with meat dietary protein source and phosphorus homeostasis in chronic kidney disease. Clin J Am Soc Nephrol 2011;6:257–64. 4. Schlemmer U, Frolich W, Prieto RM, Grases F. Phytate in foods and significance for humans: Food sources, intake, processing, bioavailability, protective role and analysis. Mol Nutr Food Res 2009;53(suppl 2):S330–75. 5. Haros M, Rosell CM, Benedito C. Use of fungal phytase to improve breadmaking performance of whole wheat bread. J Agric Food Chem 2001;49:5450–4. 6. Cupisti A, Comar F, Benini O, Lupetti S, D’Alessandro C, Barsotti G, Gianfaldoni D. Effect of boiling on dietary phosphate and nitrogen intake. J Ren Nutr 2006;16:36–40. 7. Uribarri J. Phosphorus homeostasis in normal health and in chronic kidney disease patients with special emphasis on dietary phosphorus intake. Semin Dial 2007;20:295–301. 8. Leon JB, Sullivan CM, Sehgal AR. The prevalence of phosphoruscontaining food additives in top-selling foods in grocery stores. J Ren Nutr. 2013;23(4):265–70.e2. 9. Sullivan C, Sayre SS, Leon JB, Machekano R, Love TE, Porter D, Marbury M, Sehgal AR. Effect of food additives on hyperphosphatemia among patients with end-stage renal disease: a randomized controlled trial. JAMA 2009;301:629–35. 10. Gutie´rrez OM, Katz R, Peralta CA, de Boer IH, Siscovick D, Wolf M, Diez Roux A, Kestenbaum B, Nettleton JA, Ix JH. Associations of socioeconomic status and processed food intake with serum phosphorus concentration in community-living adults: the Multi-Ethnic Study of Atherosclerosis (MESA). J Ren Nutr 2012;22: 480–9. doi: 10.3945/ajcn.113.082131.