Nutritional disturbance in acid–base balance and osteoporosis: a hypothesis that disregards the essential homeostatic role of the kidney
- https://doi.org/10.1017/S0007114513000962
- Published online: 04 April 2013
Роль вариаций питания в кислотном балансе и остеопорозе: гипотеза, которая игнорирует ключевую роль почек в гомеостазе
Гипотеза возникновения остеопороза в связи с пищевой кислотной нагрузкой с момента возникновения и до современных исследований испытывается внимательным рассмотрением ключевой, но часто игнорируемой роли почек в кислотном гомеостазе. Эта гипотеза постулирует, что пища, которую связывают с увеличением выделения мочевой кислоты, является разрушающей для скелета, и приводит к остеопорозу и увеличению рисков низкотравматичных переломов. И напротив, что пища, продуцирующая нейтральную или щелочную мочу, способствует росту костей и балансу кальция, предотвращает потерю костной массы и снижает риск остеопоротических переломов.
В настоящий момент эта теория существенно влияет на пищевые исследования, диетические рекомендации и продвижение продуктов, содержащих щелочные соли и медикаментов, которые должны улучшать здоровье костей и предотвращать остеопороз. Эта гипотеза произросла из типичных обследований пациентов, страдающих от хронических болезней почек (CKD – хроническая почечная недостаточность), проведенных в 60х годах.
Соответственно, при хронической почечной недостаточности, минеральная концентрация костей служила буферной системой для накопления кислот. Эта интерпретация позже подверглась сомнению и в теории, и в практике. Несмотря на сомнительную роль костных минералов в системном кислотном равновесии, не только при хронической недостаточности почек, но даже при отсутствии почечной недостаточности, постулируется, что у здоровых людей, пища, особенно содержащая животный белок, стимулирует «латентный» ацидоз и, в конечном счете, приводит к остеопорозу.
Таким образом, сомнительная интерпретация данных о пациентах с хронической почечной недостаточностью и их последующая экстраполяция на здоровых субъектов превратила данную гипотезу в диетические рекомендации по предотвращению остеопороза. Данное исследование отделяет домыслы и предположения от экспериментальных фактов и акцентирует ключевую роль почечных каналов в системном кислотном гомеостазе и поддержании уровня кальция.
References
1. Smith, HW (1961) From Fish to Philosopher. Garden City, NY: Anchor Books, Doubleday. Google Scholar
2. Barzel, US & Jowsey, J (1969) The effects of chronic acid and alkali administration on bone turnover in adult rats. Clin Sci 36, 517–524. Google Scholar
3. Heaney, RP (2001) Protein intake and bone health: the influence of belief systems on the conduct of nutritional science. Am J Clin Nutr 73, 5–6. Google Scholar | PubMed
4. Cordain, L, Eaton, SB, Sebastian, A, et al. (2005) Origins and evolution of the Western diet: health implications for the 21st century. Am J Clin Nutr 81, 341–354. Google Scholar | PubMed
5. Davenport, HW (1958) The ABC of Acid–Base Chemistry, 4th ed.Chicago, IL: University of Chicago Press. Google Scholar
6. Valtin, H (1979) Renal Dysfunction: Mechanisms Involved in Fluid and Solute Imbalance. Boston, MA: Little, Brown and Company. Google Scholar
7. Vormann, J & Goedecke, T (2006) Acid–base homeostasis: latent acidosis as a cause of chronic diseases. Swiss J Integr Med 18, 255–266. CrossRef | Google Scholar
8. Frassetto, LA, Morris, RC Jr & Sebastian, A (1996) Effect of age on blood acid–base composition in adult humans: role of age-related renal functional decline. Am J Physiol 271, F1114–F1122. Google Scholar | PubMed
9. Fenton, TR, Eliasziw, M, Tough, SC, et al. (2010) Low urine pH and acid excretion do not predict bone fractures or the loss of bone mineral density: a prospective cohort study. BMC Musculoskelet Disord 11, 88. CrossRef | Google Scholar | PubMed
10. Fenton, TR, Tough, SC, Lyon, AW, et al. (2011) Causal assessment of dietary acid load and bone disease: a systematic review & meta-analysis applying Hill’s epidemiologic criteria for causality. Nutr J 10, 41. CrossRef | Google Scholar | PubMed
11. Stewart, PA (1978) Independent and dependent variables of acid–base control. Respir Physiol 33, 9–26. CrossRef | Google Scholar | PubMed
12. Stewart, PA (1983) Modern quantitative acid–base chemistry. Can J Physiol Pharmacol 61, 1444–1461. CrossRef | Google Scholar | PubMed
13. Kurtz, I, Kraut, J, Ornekian, V, et al. (2008) Acid–base analysis: a critique of the Stewart and bicarbonate-centered approaches. Am J Physiol Renal Physiol 294, F1009–F1031. CrossRef | Google Scholar | PubMed
14. Relman, AS (1954) What are acids and bases? Am J Med 17, 435–437. CrossRef | Google Scholar | PubMed
15. Christiensen, HN (1959) Anion–cation balance. In Diagnostic Biochemistry: Quantitative Distribution of Body Constituents and their Physiological Interpretation, pp. 128–134. New York: Oxford University Press. Google Scholar
16. Weiner, ID & Hamm, LL (2007) Molecular mechanisms of renal ammonia transport. Annu Rev Physiol 69, 317–340. CrossRef | Google Scholar | PubMed
17. Hamm, LL, Alpern, RJ & Preisig, PA (2008) Cellular mechanisms of renal tubular acidification. In Seldin and Giebisch’s The Kidney, 4th ed. [Alpern, RJ and Hebert, SC, editors]. London: Academic Press. Google Scholar
18. Koeppen, BM (2009) The kidney and acid–base regulation. Adv Physiol Educ 33, 275–281. CrossRef | Google Scholar | PubMed
19. Weiner, ID & Verlander, JW (2011) Role of NH3 and NH4+ transporters in renal acid–base transport. Am J Physiol Renal Physiol 300, F11–F23. CrossRef | Google Scholar | PubMed
20. Bernard, C (1865) Introduction à l’étude de la médecine expérimentale (Introduction to the Study of Experimental Medicine). Paris: Garnier Flammarion. Google Scholar
21. Relman, AS, Lennon, EJ & Lemann, J Jr (1961) Endogenous production of fixed acid and the measurement of the net balance of acid in normal subjects. J Clin Invest 40, 1621–1630. CrossRef | Google Scholar | PubMed
22. Goodman, AD, Lemann, J Jr, Lennon, EJ, et al. (1965) Production, excretion, and net balance of fixed acid in patients with renal acidosis. J Clin Invest 44, 495–506. CrossRef | Google Scholar | PubMed
23. Lemann, J Jr, Litzow, JR & Lennon, EJ (1966) The effects of chronic acid loads in normal man: further evidence for the participation of bone mineral in the defense against chronic metabolic acidosis. J Clin Invest 45, 1608–1614. CrossRef | Google Scholar | PubMed
24. Litzow, JR, Lemann, J Jr & Lennon, EJ (1967) The effect of treatment of acidosis on calcium balance in patients with chronic azotemic renal disease. J Clin Invest 46, 280–286. CrossRef | Google Scholar | PubMed
25. Morgan, EF, Barnes, GL & Einhorn, TA (2008) The bone organ system: form and function. In Osteoporosis, 3rd ed., pp. 3–25 [Marcus, R, Feldman, D, Nelson, DA and Rosen, CJ, editors]. Amsterdam, Boston: Elsevier, Academic Press. CrossRef | Google Scholar | PubMed
26. Rizzoli, R & Bonjour, JP (2006) Physiology of calcium and phosphate homeostasis. In Dynamics of Bone and Cartilage Metabolism: Principles and Clinical Applications, 2nd ed., pp. 345–360 [Seibel, MJ, Robins, SP and Bilezikian, JP, editors]. San Diego, CA: Academic Press. CrossRef | Google Scholar
27. Lutz, J (1984) Calcium balance and acid–base status of women as affected by increased protein intake and by sodium bicarbonate ingestion. Am J Clin Nutr 39, 281–288. Google Scholar | PubMed
28. Ball, D & Maughan, RJ (1997) Blood and urine acid–base status of premenopausal omnivorous and vegetarian women. Br J Nutr 78, 683–693. CrossRef | Google Scholar | PubMed
29. Fenton, TR & Lyon, AW (2011) Milk and acid–base balance: proposed hypothesis versus scientific evidence. J Am Coll Nutr 30, 471S–475S. CrossRef | Google Scholar | PubMed
30. Oh, MS (1991) Irrelevance of bone buffering to acid–base homeostasis in chronic metabolic acidosis. Nephron 59, 7–10. CrossRef | Google Scholar | PubMed
31. Uribarri, J, Douyon, H & Oh, MS (1995) A re-evaluation of the urinary parameters of acid production and excretion in patients with chronic renal acidosis. Kidney Int 47, 624–627. CrossRef | Google Scholar | PubMed
32. Oh, MS & Carroll, HJ (2008) External balance of electrolytes and acids and alkalis. In Seldin and Giebisch’s The Kidney, 4th ed. [Alpern, RJ and Hebert, SC, editors]. London: Academic Press. Google Scholar
33. Oh, MS (2000) New perspectives on acid–base balance. Semin Dial 13, 212–219. CrossRef | Google Scholar | PubMed
34. Uribarri, J (2000) Acidosis in chronic renal insufficiency. Semin Dial 13, 232–234. CrossRef | Google Scholar | PubMed
35. Hruska, KA & Mathew, S (2009) Chronic Kidney Disease Mineral Bone Disorder (CKD-MBD). In Primer on the Metabolic Bone Diseases and Disorders of Mineral Metabolism, 7th ed., pp. 343–353 [Rosen, CJ, Compston, JE and Lian, JB, editors]. Washington, DC: The American Society for Bone and Mineral Research. Google Scholar
36. Barzel, US (1969) The effect of excessive acid feeding on bone. Calcif Tissue Res 4, 94–100. CrossRef | Google Scholar | PubMed
37. Arnett, TR & Dempster, DW (1986) Effect of pH on bone resorption by rat osteoclasts in vitro. Endocrinology 119, 119–124. CrossRef | Google Scholar
38. Bushinsky, DA & Frick, KK (2000) The effects of acid on bone. Curr Opin Nephrol Hypertens 9, 369–379. CrossRef | Google Scholar | PubMed
39. Bushinsky, DA, Smith, SB, Gavrilov, KL, et al. (2003) Chronic acidosis-induced alteration in bone bicarbonate and phosphate. Am J Physiol Renal Physiol 285, F532–F539. CrossRef | Google Scholar | PubMed
40. Frick, KK, Krieger, NS, Nehrke, K, et al. (2009) Metabolic acidosis increases intracellular calcium in bone cells through activation of the proton receptor OGR1. J Bone Miner Res 24, 305–313. CrossRef | Google Scholar | PubMed
41. Barzel, US (1995) The skeleton as an ion exchange system: implications for the role of acid–base imbalance in the genesis of osteoporosis. J Bone Miner Res 10, 1431–1436. CrossRef | Google Scholar
42. Lanham-New, SA (2008) The balance of bone health: tipping the scales in favor of potassium-rich, bicarbonate-rich foods. J Nutr 138, 172S–177S. Google Scholar | PubMed
43. Wynn, E, Krieg, MA, Aeschlimann, JM, et al. (2009) Alkaline mineral water lowers bone resorption even in calcium sufficiency: alkaline mineral water and bone metabolism. Bone 44, 120–124. CrossRef | Google Scholar
44. Pizzorno, J, Frassetto, LA & Katzinger, J (2010) Diet-induced acidosis: is it real and clinically relevant? Br J Nutr 103, 1185–1194. Google Scholar | PubMed
45. Feskanich, D, Willett, WC, Stampfer, MJ, et al. (1996) Protein consumption and bone fractures in women. Am J Epidemiol 143, 472–479. CrossRef | Google Scholar | PubMed
46. Meyer, HE, Pedersen, JI, Loken, EB, et al. (1997) Dietary factors and the incidence of hip fracture in middle-aged Norwegians. A prospective study. Am J Epidemiol 145, 117–123. CrossRef | Google Scholar | PubMed
47. Mussolino, ME, Looker, AC, Madans, JH, et al. (1998) Risk factors for hip fracture in white men: the NHANES I Epidemiologic Follow-up Study. J Bone Miner Res 13, 918–924. CrossRef | Google Scholar | PubMed
48. Munger, RG, Cerhan, JR & Chiu, BC (1999) Prospective study of dietary protein intake and risk of hip fracture in postmenopausal women. Am J Clin Nutr 69, 147–152. Google Scholar | PubMed
49. Hannan, MT, Tucker, KL, Dawson-Hughes, B, et al. (2000) Effect of dietary protein on bone loss in elderly men and women: The Framingham Osteoporosis Study. J Bone Miner Res 15, 2504–2512. CrossRef | Google Scholar
50. Sellmeyer, DE, Stone, KL, Sebastian, A, et al. (2001) A high ratio of dietary animal to vegetable protein increases the rate of bone loss and the risk of fracture in postmenopausal women. Study of Osteoporotic Fractures Research Group. Am J Clin Nutr 73, 118–122. Google Scholar | PubMed
51. Promislow, JH, Goodman-Gruen, D, Slymen, DJ, et al. (2002) Protein consumption and bone mineral density in the elderly: The Rancho Bernardo Study. Am J Epidemiol 155, 636–644. CrossRef | Google Scholar | PubMed
52. Wengreen, HJ, Munger, RG, West, NA, et al. (2004) Dietary protein intake and risk of osteoporotic hip fracture in elderly residents of Utah. J Bone Miner Res 19, 537–545. CrossRef | Google Scholar | PubMed
53. Dargent-Molina, P, Sabia, S, Touvier, M, et al. (2008) Proteins, dietary acid load, and calcium and risk of postmenopausal fractures in the E3N French women prospective study. J Bone Miner Res 23, 1915–1922. CrossRef | Google Scholar | PubMed
54. Wynn, E, Lanham-New, SA, Krieg, MA, et al. (2008) Low estimates of dietary acid load are positively associated with bone ultrasound in women older than 75 years of age with a lifetime fracture. J Nutr 138, 1349–1354. Google Scholar | PubMed
55. Darling, AL, Millward, DJ, Torgerson, DJ, et al. (2009) Dietary protein and bone health: a systematic review and meta-analysis. Am J Clin Nutr 90, 1674–1692. CrossRef | Google Scholar | PubMed
56. Misra, D, Berry, SD, Broe, KE, et al. (2011) Does dietary protein reduce hip fracture risk in elders? The Framingham Osteoporosis Study. Osteoporos Int 22, 345–349. CrossRef | Google Scholar | PubMed
57. Shi, L, Libuda, L, Schonau, E, et al. (2012) Long term higher urinary calcium excretion within the normal physiologic range predicts impaired bone status of the proximal radius in healthy children with higher potential renal acid load. Bone 50, 1026–1031. CrossRef | Google Scholar | PubMed
58. Oh, MS (1989) A new method for estimating G-I absorption of alkali. Kidney Int 36, 915–917. CrossRef | Google Scholar
59. Remer, T & Manz, F (1994) Estimation of the renal net acid excretion by adults consuming diets containing variable amounts of protein. Am J Clin Nutr 59, 1356–1361. Google Scholar | PubMed
60. Berkemeyer, S & Remer, T (2006) Anthropometrics provide a better estimate of urinary organic acid anion excretion than a dietary mineral intake-based estimate in children, adolescents, and young adults. J Nutr 136, 1203–1208. Google Scholar
61. Remer, T, Dimitriou, T & Manz, F (2003) Dietary potential renal acid load and renal net acid excretion in healthy, free-living children and adolescents. Am J Clin Nutr 77, 1255–1260. Google Scholar | PubMed
62. Remer, T & Manz, F (1995) Potential renal acid load of foods and its influence on urine pH. J Am Diet Assoc 95, 791–797. CrossRef | Google Scholar | PubMed
63. Frassetto, LA, Todd, KM, Morris, RC Jr, et al. (1998) Estimation of net endogenous noncarbonic acid production in humans from diet potassium and protein contents. Am J Clin Nutr 68, 576–583. Google Scholar | PubMed
64. Grases, F, Costa-Bauza, A & Prieto, RM (2006) Renal lithiasis and nutrition. Nutr J 5, 23. CrossRef | Google Scholar | PubMed
65. Moe, OW, Pearle, MS & Sakhaee, K (2011) Pharmacotherapy of urolithiasis: evidence from clinical trials. Kidney Int 79, 385–392. CrossRef | Google Scholar | PubMed
66. Sebastian, A, Harris, ST, Ottaway, JH, et al. (1994) Improved mineral balance and skeletal metabolism in postmenopausal women treated with potassium bicarbonate. N Engl J Med 330, 1776–1781. CrossRef | Google Scholar | PubMed
67. Sellmeyer, DE, Schloetter, M & Sebastian, A (2002) Potassium citrate prevents increased urine calcium excretion and bone resorption induced by a high sodium chloride diet. J Clin Endocrinol Metab 87, 2008–2012. CrossRef | Google Scholar | PubMed
68. Maurer, M, Riesen, W, Muser, J, et al. (2003) Neutralization of Western diet inhibits bone resorption independently of K intake and reduces cortisol secretion in humans. Am J Physiol Renal Physiol 284, F32–F40. CrossRef | Google Scholar | PubMed
69. Frassetto, L, Morris, RC Jr & Sebastian, A (2005) Long-term persistence of the urine calcium-lowering effect of potassium bicarbonate in postmenopausal women. J Clin Endocrinol Metab 90, 831–834. CrossRef | Google Scholar | PubMed
70. Rafferty, K, Davies, KM & Heaney, RP (2005) Potassium intake and the calcium economy. J Am Coll Nutr 24, 99–106. CrossRef | Google Scholar | PubMed
71. Jehle, S, Zanetti, A, Muser, J, et al. (2006) Partial neutralization of the acidogenic Western diet with potassium citrate increases bone mass in postmenopausal women with osteopenia. J Am Soc Nephrol 17, 3213–3222. CrossRef | Google Scholar | PubMed
72. Macdonald, HM, Black, AJ, Aucott, L, et al. (2008) Effect of potassium citrate supplementation or increased fruit and vegetable intake on bone metabolism in healthy postmenopausal women: a randomized controlled trial. Am J Clin Nutr 88, 465–474. Google Scholar | PubMed
73. Rafferty, K & Heaney, RP (2008) Nutrient effects on the calcium economy: emphasizing the potassium controversy. J Nutr 138, 166S–171S. Google Scholar | PubMed
74. Ceglia, L, Harris, SS, Abrams, SA, et al. (2009) Potassium bicarbonate attenuates the urinary nitrogen excretion that accompanies an increase in dietary protein and may promote calcium absorption. J Clin Endocrinol Metab 94, 645–653. CrossRef | Google Scholar | PubMed
75. Dawson-Hughes, B, Harris, SS, Palermo, NJ, et al. (2009) Treatment with potassium bicarbonate lowers calcium excretion and bone resorption in older men and women. J Clin Endocrinol Metab 94, 96–102. CrossRef | Google Scholar | PubMed
76. Mardon, J, Habauzit, V, Trzeciakiewicz, A, et al. (2008) Long-term intake of a high-protein diet with or without potassium citrate modulates acid–base metabolism, but not bone status, in male rats. J Nutr 138, 718–724. Google Scholar
77. Jehle, S, Hulter, HN & Krapf, R (2013) Effect of potassium citrate on bone density, microarchitecture, and fracture risk in healthy older adults without osteoporosis: a randomized controlled trial. J Clin Endocrinol Metab 98, 207–217. CrossRef | Google Scholar
78. Cannata-Andia, JB, Roman-Garcia, P & Hruska, K (2011) The connections between vascular calcification and bone health. Nephrol Dial Transplant 26, 3429–3436. CrossRef | Google Scholar | PubMed
79. Wang, L, Manson, JE & Sesso, HD (2012) Calcium intake and risk of cardiovascular disease: a review of prospective studies and randomized clinical trials. Am J Cardiovasc Drugs 12, 105–116. CrossRef | Google Scholar | PubMed
80. Frassetto, LA, Hardcastle, AC, Sebastian, A, et al. (2012) No evidence that the skeletal non-response to potassium alkali supplements in healthy postmenopausal women depends on blood pressure or sodium chloride intake. Eur J Clin Nutr 66, 1315–1322. CrossRef | Google Scholar | PubMed
81. Fenton, TR, Eliasziw, M, Lyon, AW, et al. (2008) Meta-analysis of the quantity of calcium excretion associated with the net acid excretion of the modern diet under the acid–ash diet hypothesis. Am J Clin Nutr 88, 1159–1166. Google Scholar | PubMed
82. Fenton, TR, Lyon, AW, Eliasziw, M, et al. (2009) Meta-analysis of the effect of the acid–ash hypothesis of osteoporosis on calcium balance. J Bone Miner Res 24, 1835–1840. CrossRef | Google Scholar | PubMed
83. McLean, RR, Qiao, N, Broe, KE, et al. (2011) Dietary acid load is not associated with lower bone mineral density except in older men. J Nutr 141, 588–594. CrossRef | Google Scholar
84. Hill, AB (1965) The environment and disease: association or causation? Proc R Soc Med 58, 295–300. Google Scholar | PubMed
85. Muhlbauer, RC, Lozano, A & Reinli, A (2002) Onion and a mixture of vegetables, salads, and herbs affect bone resorption in the rat by a mechanism independent of their base excess. J Bone Miner Res 17, 1230–1236. CrossRef | Google Scholar
86. New, SA, MacDonald, HM, Campbell, MK, et al. (2004) Lower estimates of net endogenous non-carbonic acid production are positively associated with indexes of bone health in premenopausal and perimenopausal women. Am J Clin Nutr 79, 131–138. Google Scholar | PubMed
87. Macdonald, HM, New, SA, Fraser, WD, et al. (2005) Low dietary potassium intakes and high dietary estimates of net endogenous acid production are associated with low bone mineral density in premenopausal women and increased markers of bone resorption in postmenopausal women. Am J Clin Nutr 81, 923–933. Google Scholar | PubMed
88. New, SA (2002) Nutrition Society Medal lecture. The role of the skeleton in acid–base homeostasis. Proc Nutr Soc 61, 151–164. CrossRef | Google Scholar | PubMed
89. Sebastian, A, Frassetto, LA, Sellmeyer, DE, et al. (2002) Estimation of the net acid load of the diet of ancestral preagricultural Homo sapiens and their hominid ancestors. Am J Clin Nutr 76, 1308–1316. Google Scholar | PubMed
90. Bonjour, JP (2011) Calcium and phosphate: a duet of ions playing for bone health. J Am Coll Nutr 30, 438S–448S. CrossRef | Google Scholar | PubMed
91. Fenton, TR, Lyon, AW, Eliasziw, M, et al. (2009) Phosphate decreases urine calcium and increases calcium balance: a meta-analysis of the osteoporosis acid–ash diet hypothesis. Nutr J 8, 41. CrossRef | Google Scholar | PubMed
92. Miller, PD, Schwartz, EN, Chen, P, et al. (2007) Teriparatide in postmenopausal women with osteoporosis and mild or moderate renal impairment. Osteoporos Int 18, 59–68. CrossRef | Google Scholar | PubMed
93. Coresh, J, Astor, BC, Greene, T, et al. (2003) Prevalence of chronic kidney disease and decreased kidney function in the adult US population: Third National Health and Nutrition Examination Survey. Am J Kidney Dis 41, 1–12. CrossRef | Google Scholar | PubMed
94. Eustace, JA, Astor, B, Muntner, PM, et al. (2004) Prevalence of acidosis and inflammation and their association with low serum albumin in chronic kidney disease. Kidney Int 65, 1031–1040. CrossRef | Google Scholar | PubMed
95. Looker, AC, Orwoll, ES, Johnston, CC Jr, et al. (1997) Prevalence of low femoral bone density in older U.S. adults from NHANES III. J Bone Miner Res 12, 1761–1768. CrossRef | Google Scholar | PubMed
96. Hsu, CY & Chertow, GM (2002) Elevations of serum phosphorus and potassium in mild to moderate chronic renal insufficiency. Nephrol Dial Transplant 17, 1419–1425. CrossRef | Google Scholar | PubMed
97. Hsu, CY, Cummings, SR, McCulloch, CE, et al. (2002) Bone mineral density is not diminished by mild to moderate chronic renal insufficiency. Kidney Int 61, 1814–1820. CrossRef | Google Scholar
