Common Pitfalls in the Management of Patients with Micronutrient Deficiency: Keep in Mind the Stomach
Abstract
:1. Introduction
2. Physiology of Gastric Oxyntic Mucosa: Secretion of Gastric Acid and Intrinsic Factor
3. The Role of the Stomach in Non-Bleeding-Related Iron Deficiency
4. The Role of the Stomach in Cobalamin Deficiency
5. The Role of the Stomach in Ascorbate Deficiency
6. Calcium, Reduced Bone Mineral Density, Fractures, and Impaired Gastric Acid Secretion
7. Other Micronutrient Deficiencies Related to Drug-Induced Hypochlorhydria
7.1. Magnesium Deficiency and Anti-Secretory Drugs
7.2. Other Micronutrients
8. Gastric Surgery and Micronutrient Deficiencies
9. Possible Role of Gastric Dysbiosis
10. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Biebinger, R.; Hurrell, R.F. 3—Vitamin and mineral fortification of foods. In Food Fortification and Supplementation; Ottaway, P.B., Ed.; Woodhead Publishing: Cambridge, UK, 2008; pp. 27–40. [Google Scholar]
- Maggini, S.; Pierre, A.; Calder, P.C. Immune Function and Micronutrient Requirements Change over the Life Course. Nutrients 2018, 10, 1531. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Halawi, R.; Moukhadder, H.; Taher, A. Anemia in the elderly: A consequence of aging? Expert Rev. Hematol. 2017, 10, 327–335. [Google Scholar] [CrossRef]
- Lahner, E.; Persechino, S.; Annibale, B. Micronutrients (Other than iron) and Helicobacter pylori Infection: A Systematic Review. Helicobacter 2012, 17, 1–15. [Google Scholar] [CrossRef] [PubMed]
- Annibale, B.; Capurso, G.; Fave, G.D. Consequences of Helicobacter pylori infection on the absorption of micronutrients. Dig. Liver Dis. 2002, 34, S72–S77. [Google Scholar] [CrossRef]
- Zilli, A.; Cavalcoli, F.; Ciafardini, C.; Massironi, S. Deficiency of micronutrients in patients affected by chronic atrophic autoimmune gastritis: A single-institution observational study. Dig. Liver Dis. 2019, 51, 505–509. [Google Scholar] [CrossRef] [PubMed]
- Carmel, R. 10 Malabsorption of food cobalamin. Baillieres Clin. Haematol. 1995, 8, 639–655. [Google Scholar] [CrossRef]
- Andrès, E.; Loukili, N.H.; Noel, E.; Kaltenbach, G.; Ben Abdelgheni, M.; Perrin, A.E.; Noblet-Dick, M.; Maloisel, F.; Schlienger, J.-L.; Blicklé, J.-F. Vitamin B12 (cobalamin) deficiency in elderly patients. Can. Med. Assoc. J. 2004, 171, 251–259. [Google Scholar] [CrossRef] [Green Version]
- Conrad, M.E.; Schade, S.G. Ascorbic Acid Chelates in Iron Absorption: A Role for Hydrochloric Acid and Bile. Gastroenterology 1968, 55, 35–45. [Google Scholar] [CrossRef]
- Salgueiro, J.; Zubillaga, M.; Goldman, C.; Barrado, A.; Sarrasague, M.M.; Leonardi, N.; Boccio, J. Review article: Is there a link between micronutrient malnutrition and Helicobacter pylori infection? Aliment. Pharmacol. Ther. 2004, 20, 1029–1034. [Google Scholar] [CrossRef]
- Annibale, B.; Capurso, G.; Fave, G.D. The stomach and iron deficiency anaemia: A forgotten link. Dig. Liver Dis. 2003, 35, 288–295. [Google Scholar] [CrossRef]
- Lahner, E.; Zagari, R.M.; Zullo, A.; Di Sabatino, A.; Meggio, A.; Cesaro, P.; Lenti, M.V.; Annibale, B.; Corazza, G.R. Chronic atrophic gastritis: Natural history, diagnosis and therapeutic management. A position paper by the Italian Society of Hospital Gastroenterologists and Digestive Endoscopists [AIGO], the Italian Society of Digestive Endoscopy [SIED], the Italian Society of Gastroenterology [SIGE], and the Italian Society of Internal Medicine [SIMI]. Dig. Liver Dis. 2019, 51, 1621–1632. [Google Scholar] [CrossRef] [PubMed]
- Ito, T.; Jensen, R.T. Association of Long-Term Proton Pump Inhibitor Therapy with Bone Fractures and Effects on Absorption of Calcium, Vitamin B12, Iron, and Magnesium. Curr. Gastroenterol. Rep. 2010, 12, 448–457. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lupoli, R.; Lembo, E.; Saldalamacchia, G.; Avola, C.K.; Angrisani, L.; Capaldo, B. Bariatric surgery and long-term nutritional issues. World J. Diabetes 2017, 8, 464–474. [Google Scholar] [CrossRef] [PubMed]
- Lange, J.; Königsrainer, A. Malnutrition as a Complication of Bariatric Surgery—A Clear and Present Danger? Visc. Med. 2019, 35, 305–311. [Google Scholar] [CrossRef] [PubMed]
- Shankar, P.; Boylan, M.; Sriram, K. Micronutrient deficiencies after bariatric surgery. Nutrition 2010, 26, 1031–1037. [Google Scholar] [CrossRef] [PubMed]
- Conti, L.; Annibale, B.; Lahner, E. Autoimmune Gastritis and Gastric Microbiota. Microorganisms 2020, 8, 1827. [Google Scholar] [CrossRef]
- Burucoa, C.; Axon, A. Epidemiology of Helicobacter pylori infection. Helicobacter 2017, 22, e12403. [Google Scholar] [CrossRef]
- Black, R.E.; Victora, C.G.; Walker, S.; Bhutta, A.Z.; Christian, P.; De Onis, M.; Ezzati, M.; Grantham-McGregor, S.; Katz, J.; Martorell, R.; et al. Maternal and child undernutrition and overweight in low-income and middle-income countries. Lancet 2013, 382, 427–451. [Google Scholar] [CrossRef]
- Bailey, R.L.; West, K.P., Jr.; Black, R.E. The Epidemiology of Global Micronutrient Deficiencies. Ann. Nutr. Metab. 2015, 66, 22–33. [Google Scholar] [CrossRef]
- DeVault, K.R.; Talley, N.J. Insights into the future of gastric acid suppression. Nat. Rev. Gastroenterol. Hepatol. 2009, 6, 524–532. [Google Scholar] [CrossRef]
- Savarino, V.; Marabotto, E.; Zentilin, P.; Furnari, M.; Bodini, G.; De Maria, C.; Pellegatta, G.; Coppo, C.; Savarino, E. Proton pump inhibitors: Use and misuse in the clinical setting. Expert Rev. Clin. Pharmacol. 2018, 11, 1123–1134. [Google Scholar] [CrossRef] [PubMed]
- Angrisani, L.; Santonicola, A.; Iovino, P.; Formisano, G.; Buchwald, H.; Scopinaro, N. Bariatric Surgery Worldwide 2013. Obes. Surg. 2015, 25, 1822–1832. [Google Scholar] [CrossRef] [PubMed]
- Sáenz, J.B.; Mills, J.C. Acid and the basis for cellular plasticity and reprogramming in gastric repair and cancer. Nat. Rev. Gastroenterol. Hepatol. 2018, 15, 257–273. [Google Scholar] [CrossRef] [PubMed]
- Schubert, M.L.; Kaunitz, J.D. Gastric secretion. In Sleisenger and Fordtran’s Gastrointestinal and Liver Disease: Pathophysiology/Diagnosis/ Management, 9th ed.; Feldman, M., Friedman, L.S., Brandt, L.J., Eds.; Elsevier: Philadelphia, PA, USA, 2010; pp. 817–832. [Google Scholar]
- Kopic, S.; Geibel, J.P. Gastric Acid, Calcium Absorption, and Their Impact on Bone Health. Physiol. Rev. 2013, 93, 189–268. [Google Scholar] [CrossRef] [Green Version]
- Engevik, A.C.; Kaji, I.; Goldenring, J.R. The Physiology of the Gastric Parietal Cell. Physiol. Rev. 2020, 100, 573–602. [Google Scholar] [CrossRef]
- Schubert, M.L. Physiologic, pathophysiologic, and pharmacologic regulation of gastric acid secretion. Curr. Opin. Gastroenterol. 2017, 33, 430–438. [Google Scholar] [CrossRef]
- Festen, H.P.M. Intrinsic Factor Secretion and Cobalamin Absorption: Physiology and Pathophysiology in the Gastrointestinal Tract. Scand. J. Gastroenterol. 1991, 26, 1–7. [Google Scholar] [CrossRef]
- Conrad, M.E.; Umbreit, J.N.; Moore, E.G. Iron Absorption and Transport. Am. J. Med. Sci. 1999, 318, 213–229. [Google Scholar] [CrossRef]
- Anderson, G.J.; Frazer, D.M. Current understanding of iron homeostasis. Am. J. Clin. Nutr. 2017, 106, 1559S–1566S. [Google Scholar] [CrossRef] [Green Version]
- Sipponen, P.; Marshall, B.J. Gastritis and Gastric Cancer. Gastroenterol. Clin. N. Am. 2000, 29, 579–592. [Google Scholar] [CrossRef]
- Kuipers, E.J.; Klinkenberg-Knol, E.C.; Vandenbroucke-Grauls, C.M.; Appelmelk, B.J.; Schenk, B.E.; Meuwissen, S.G. Role of Helicobacter pylori in the pathogenesis of atrophic gastritis. Scand. J. Gastroenterol. 1997, 223, 28–34. [Google Scholar]
- Sugano, K.; Tack, J.; Kuipers, E.J.; Graham, D.Y.; El-Omar, E.M.; Miura, S.; Haruma, K.; Asaka, M.; Uemura, N.; Malfertheiner, P. Kyoto global consensus report onHelicobacter pylorigastritis. Gut 2015, 64, 1353–1367. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zagari, R.M.; Romano, M.; Ojetti, V.; Stockbrugger, R.; Gullini, S.; Annibale, B.; Farinati, F.; Ierardi, E.; Maconi, G.; Rugge, M.; et al. Guidelines for the management of Helicobacter pylori infection in Italy: The III Working Group Consensus Report 2015. Dig. Liver Dis. 2015, 47, 903–912. [Google Scholar] [CrossRef]
- Carabotti, M. Helicobacter pyloriinfection in obesity and its clinical outcome after bariatric surgery. World J. Gastroenterol. 2014, 20, 647–653. [Google Scholar] [CrossRef] [PubMed]
- Peach, H.G.; Bath, E.N.; Farish, S.J. Helicobacter pylori infection: An added stressor on iron status of women in the community. Med. J. Aust. 1998, 169, 188–190. [Google Scholar] [CrossRef]
- Milman, N.; Rosenstock, S.; Andersen, L.; Jørgensen, T.; Bonnevie, O. Serum ferritin, hemoglobin, and Helicobacter pylori infection: A seroepidemiologic survey comprising 2794 Danish adults. Gastroenterology 1998, 115, 268–274. [Google Scholar] [CrossRef]
- Parkinson, A.; Gold, B.D.; Bulkow, L.; Wainwright, R.B.; Swaminathan, B.; Khanna, B.; Petersen, K.M.; Fitzgerald, M.A. High Prevalence of Helicobacter pylori in the Alaska Native Population and Association with Low Serum Ferritin Levels in Young Adults. Clin. Diagn. Lab. Immunol. 2000, 7, 885–888. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- BergBeckhoff, G.; Bode, G.; Blettner, M.; Boeing, H.; Brenner, H. Helicobacter Pylori Infection and Serum Ferritin: A Population-Based Study Among 1806 Adults in Germany. Am. J. Gastroenterol. 2001, 96, 1014–1018. [Google Scholar] [CrossRef]
- Qu, X.-H.; Huang, X.-L.; Xiong, P.; Zhu, C.-Y.; Huang, Y.-L.; Lu, L.-G.; Sun, X.; Rong, L.; Zhong, L.; Sun, D.-Y.; et al. Does Helicobacter pylori infection play a role in iron deficiency anemia? A meta-analysis. World J. Gastroenterol. 2010, 16, 886–896. [Google Scholar] [CrossRef] [PubMed]
- Muhsen, K.; Cohen, D. Helicobacter pyloriInfection and Iron Stores: A Systematic Review and Meta-analysis. Helicobacter 2008, 13, 323–340. [Google Scholar] [CrossRef]
- López-García, Y.K.; Colunga-Pedraza, P.R.; Tarín-Arzaga, L.; Garza, M.I.L.; Jaime-Pérez, J.C.; Gómez-Almaguer, D. Iron deficiency anemia referral to the hematologist. Real-world data from Mexico: The need for targeted teaching in primary care. Hematology 2018, 23, 658–663. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- El Demerdash, D.M.; Ibrahim, H.; Hassan, D.M.; Moustafa, H.; Tawfik, N.M. Helicobacter pylori associated to unexplained or refractory iron deficiency anemia: An Egyptian single-center experience. Hematol. Transfus. Cell Ther. 2018, 40, 219–225. [Google Scholar] [CrossRef] [PubMed]
- Hudak, L.; Jaraisy, A.; Haj, S.; Muhsen, K. An updated systematic review and meta-analysis on the association between Helicobacter pylori infection and iron deficiency anemia. Helicobacter 2016, 22, e12330. [Google Scholar] [CrossRef] [PubMed]
- Capurso, G.; Lahner, E.; Marcheggiano, A.; Caruana, P.; Carnuccio, A.; Bordi, C.; Fave, G.D.; Annibale, B. Involvement of the corporal mucosa and related changes in gastric acid secretion characterize patients with iron deficiency anaemia associated with Helicobacter pylori infection. Aliment. Pharmacol. Ther. 2001, 15, 1753–1761. [Google Scholar] [CrossRef]
- Cook, J.D.; Brown, G.M.; Valberg, L.S. The Effect of Achylia Gastrica on Iron Absorption*. J. Clin. Investig. 1964, 43, 1185–1191. [Google Scholar] [CrossRef]
- Dickey, W. Iron deficiency, gastric atrophy and Helicobacter pylori. Dig. Liver Dis. 2002, 34, 313–315. [Google Scholar] [CrossRef]
- Dickey, W.; Kenny, B.D.; McMillan, S.A.; Porter, K.G.; McConnell, J.B. Gastric as well as Duodenal Biopsies May Be Useful in the Investigation of Iron Deficiency Anaemia. Scand. J. Gastroenterol. 1997, 32, 469–472. [Google Scholar] [CrossRef]
- Marignani, M.; Fave, D.G.; Mecarocci, S.; Bordi, C.; Angeletti, S.; D’Ambra, G.; Aprile, M.; Corleto, V.; Monarca, B.; Annibale, B.; et al. High Prevalence of Atrophic Body Gastritis in Patients With Unexplained Microcytic and Macrocytic Anemia. Am. J. Gastroenterol. 1999, 94, 766–772. [Google Scholar] [CrossRef]
- Annibale, B.; Capurso, G.; Chistolini, A.; D’Ambra, G.; DiGiulio, E.; Monarca, B.; Dellefave, G. Gastrointestinal causes of refractory iron deficiency anemia in patients without gastrointestinal symptoms. Am. J. Med. 2001, 111, 439–445. [Google Scholar] [CrossRef]
- Hershko, C.; Ronson, A.; Souroujon, M.; Maschler, I.; Heyd, J.; Patz, J. Variable hematologic presentation of autoimmune gastritis: Age-related progression from iron deficiency to cobalamin depletion. Blood 2006, 107, 1673–1679. [Google Scholar] [CrossRef]
- Malfertheiner, P.; Megraud, F.; O’Morain, C.; Gisbert, J.P.; Kuipers, E.; Axon, A.; Bazzoli, F.; Gasbarrini, A.; Atherton, J.; Graham, D.; et al. Management of Helicobacter pylori infection—the Maastricht V/Florence Consensus Report. Gut 2016, 66, 6–30. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Green, R.; Allen, L.H.; Bjørke-Monsen, A.-L.; Brito, A.; Guéant, J.-L.; Miller, J.W.; Molloy, A.M.; Nexo, E.; Stabler, S.; Toh, B.-H.; et al. Vitamin B12 deficiency. Nat. Rev. Dis. Prim. 2017, 3, 17040. [Google Scholar] [CrossRef] [PubMed]
- Nielsen, M.J.; Rasmussen, M.R.; Andersen, C.B.F.; Nexø, E.; Moestrup, S.K. Vitamin B12 transport from food to the body’s cells—A sophisticated, multistep pathway. Nat. Rev. Gastroenterol. Hepatol. 2012, 9, 345–354. [Google Scholar] [CrossRef] [PubMed]
- Stabler, S.P. Vitamin B12Deficiency. N. Engl. J. Med. 2013, 368, 149–160. [Google Scholar] [CrossRef]
- Carmel, R.; Aurangzeb, I.; Qian, D. Associations of food-cobalamin malabsorption with ethnic origin, age, Helicobacter pylori infection, and serum markers of gastritis. Am. J. Gastroenterol. 2001, 96, 63–70. [Google Scholar] [CrossRef]
- Andres, E.; Noel, E.; Kaltenbach, G.; Perrin, A.-E.; Vinzio, S.; Goichot, B.; Schlienger, J.-L.; Blickle, J.-F. Carences en vitamine B12 avec test de Schilling normal ou syndrome de non-dissociation de la vitamine B12 de ses protéines porteuses chez le sujet âgé. Étude de 60 patients. Rev. Méd. Interne 2003, 24, 218–223. [Google Scholar] [CrossRef]
- Kaptan, K.; Beyan, C.; Ural, A.U.; Çetin, T.; Avcu, F.; Gülşen, M.; Finci, R.; Yalçín, A. Helicobacter pylori—Is It a Novel Causative Agent in Vitamin B12 Deficiency? Arch. Intern. Med. 2000, 160, 1349–1353. [Google Scholar] [CrossRef]
- McCollMDa, K.E.L.; El-Omar, E.; Gillen, D. Helicobacter Pylori Gastritis and Gastric Physiology. Gastroenterol. Clin. North Am. 2000, 29, 687–703. [Google Scholar] [CrossRef]
- McColl, K.E.L. Effect of proton pump inhibitors on vitamins and iron. Am. J. Gastroenterol. 2009, 104, S5–S9. [Google Scholar]
- Qorraj-Bytyqi, H.; Hoxha, R.; Sadiku, S.; Bajraktari, I.H.; Sopjani, M.; Thaçi, K.; Thaçi, S.; Bahtiri, E. Proton Pump Inhibitors Intake and Iron and Vitamin B12 Status: A Prospective Comparative Study with a Follow up of 12 Months. Open Access Maced. J. Med Sci. 2018, 6, 442–446. [Google Scholar] [CrossRef] [Green Version]
- Lam, J.R.; Schneider, J.L.; Zhao, W.; Corley, D.A. Proton Pump Inhibitor and Histamine 2 Receptor Antagonist Use and Vitamin B12Deficiency. JAMA 2013, 310, 2435–2442. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lenti, M.V.; Rugge, M.; Lahner, E.; Miceli, E.; Toh, B.-H.; Genta, R.M.; De Block, C.; Hershko, C.; Di Sabatino, A. Autoimmune gastritis. Nat. Rev. Dis. Prim. 2020, 6, 1–19. [Google Scholar] [CrossRef] [PubMed]
- Hammond, N.; Wang, Y.; Dimachkie, M.M.; Barohn, R.J. Nutritional Neuropathies. Neurol. Clin. 2013, 31, 477–489. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vannella, L.; Lahner, E.; Bordi, C.; Pilozzi, E.; Di Giulio, E.; Corleto, V.D.; Osborn, J.; Fave, G.D.; Annibale, B. Reversal of atrophic body gastritis after H. pylori eradication at long-term follow-up. Dig. Liver Dis. 2011, 43, 295–299. [Google Scholar] [CrossRef] [PubMed]
- Hwang, Y.-J.; Kim, N.; Lee, H.S.; Lee, J.B.; Choi, Y.J.; Yoon, H.; Shin, C.M.; Park, Y.S.; Lee, S.H. Reversibility of atrophic gastritis and intestinal metaplasia after Helicobacter pylori eradication—A prospective study for up to 10 years. Aliment. Pharmacol. Ther. 2017, 47, 380–390. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kyrtopoulos, S.A. Ascorbic acid and the formation of N-nitroso compounds: A possible role of ascorbic acid in cancer prevention. Am. J. Clin. Nutr. 1987, 45, 1344–1350. [Google Scholar] [CrossRef] [PubMed]
- De Tullio, M.C. The Mystery of Vitamin C. Nat. Educ. 2010, 3, 48. [Google Scholar]
- Sobala, G.; Schorah, C.; Sanderson, M.; Dixon, M.; Tompkins, D.; Godwin, P.; Axon, A. Ascorbic acid in the human stomach. Gastroenterololgy 1989, 97, 357–363. [Google Scholar] [CrossRef]
- Rathbone, B.J.; Johnson, A.W.; Wyatt, J.I.; Kelleher, J.; Heatley, R.V.; Losowsky, M.S. Ascorbic acid: A factor concentrated in human gastric juice. Clin. Sci. 1989, 76, 237–241. [Google Scholar] [CrossRef] [Green Version]
- Lombard, M.; Chua, E.; O’Toole, P. Regulation of intestinal non-haem iron absorption. Gut 1997, 40, 435–439. [Google Scholar] [CrossRef] [Green Version]
- Bothwell, T.H.; Baynes, R.D.; Macfarlane, B.J.; MacPhail, A.P. Nutritional iron requirements and food iron absorption. J. Intern. Med. 1989, 226, 357–365. [Google Scholar] [CrossRef]
- Woodward, M.; Tunstall-Pedoe, H.; McColl, K. Helicobacter pylori infection reduces systemic availability of dietary vitamin C. Eur. J. Gastroenterol. Hepatol. 2001, 13, 233–237. [Google Scholar] [CrossRef]
- Annibale, B.; Capurso, G.; Lahner, E.; Passi, S.; Ricci, R.; Maggio, F.; Fave, G.D. Concomitant alterations in intragastric pH and ascorbic acid concentration in patients with Helicobacter pylori gastritis and associated iron deficiency anaemia. Gut 2003, 52, 496–501. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, Z.-W.; Abdullahi, M.; Farthing, M.J.G. Effect of physiological concentrations of vitamin C on gastric cancer cells and Helicobacter pylori. Gut 2002, 50, 165–169. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, Z.W.; Patchett, E.S.; Perrett, D.; Katelaris, P.H.; Domizio, P.; Farthing, M.J.G. The relation between gastric vitamin C concentrations, mucosal histology, and CagA seropositivity in the human stomach. Gut 1998, 43, 322–326. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ruiz, B.; Rood, J.C.; Fontham, E.T.; Malcom, G.T.; Hunter, F.M.; Sobhan, M.; Johnson, W.D.; Correa, P. Vitamin C concentration in gastric juice before and after anti-Helicobacter pylori treatment. Am. J. Gastroenterol. 1994, 89, 533–539. [Google Scholar] [PubMed]
- Mei, H.; Tu, H. Vitamin C and Helicobacter pylori Infection: Current Knowledge and Future Prospects. Front. Physiol. 2018, 9, 1103. [Google Scholar] [CrossRef] [PubMed]
- Henry, E.B.; Carswell, A.; Wirz, A.; Fyffe, V.; McColl, K.E.L. Proton pump inhibitors reduce the bioavailability of dietary vitamin C. Aliment. Pharmacol. Ther. 2005, 22, 539–545. [Google Scholar] [CrossRef]
- Ellulu, M.S.; Rahmat, A.; Ismail, P.; Khaza’Ai, H.; Abed, Y. Effect of vitamin C on inflammation and metabolic markers in hypertensive and/or diabetic obese adults: A randomized controlled trial. Drug Des. Dev. Ther. 2015, 9, 3405–3412. [Google Scholar] [CrossRef] [Green Version]
- Banerjee, S.; Hawksby, C.; Miller, S.; Dahill, S.; Beattie, A.D.; McColl, K.E. Effect of Helicobacter pylori and its eradication on gastric juice ascorbic acid. Gut 1994, 35, 317–322. [Google Scholar] [CrossRef]
- Kahn, S.B.; Brodsky, I.; Fein, S.A. Metabolic Interrelationship between Vitamin B12 and Ascorbic Acid in Pernicious Anemia. Blood 1968, 31, 55–65. [Google Scholar] [CrossRef]
- Boyce, B.F. Stomaching calcium for bone health. Nat. Med. 2009, 15, 610–612. [Google Scholar] [CrossRef] [PubMed]
- Sipponen, P.; Härkönen, M. Hypochlorhydric stomach: A risk condition for calcium malabsorption and osteoporosis? Scand. J. Gastroenterol. 2009, 45, 133–138. [Google Scholar] [CrossRef] [PubMed]
- Recker, R.R. Calcium Absorption and Achlorhydria. N. Engl. J. Med. 1985, 313, 70–73. [Google Scholar] [CrossRef]
- Eastell, R.; Vieira, N.E.; Yergey, A.L.; Wahner, H.W.; Silverstein, M.N.; Kumar, R.; Riggs, B.L. Pernicious anaemia as a risk factor for osteoporosis. Clin. Sci. 1992, 82, 681–685. [Google Scholar] [CrossRef] [PubMed]
- Kitay, A.M.; Geibel, J. Stomach and Bone. Adv. Exp. Med. Biol. 2017, 1033, 97–131. [Google Scholar] [CrossRef] [PubMed]
- Antico, A.; Tozzoli, R.; Giavarina, D.; Tonutti, E.; Bizzaro, N. Hypovitaminosis D as Predisposing Factor for Atrophic Type A Gastritis: A Case–Control Study and Review of the Literature on the Interaction of Vitamin D with the Immune System. Clin. Rev. Allergy Immunol. 2012, 42, 355–364. [Google Scholar] [CrossRef]
- Massironi, S.; Cavalcoli, F.; Zilli, A.; Del Gobbo, A.; Ciafardini, C.; Bernasconi, S.; Felicetta, I.; Conte, D.; Peracchi, M. Relevance of vitamin D deficiency in patients with chronic autoimmune atrophic gastritis: A prospective study. BMC Gastroenterol. 2018, 18, 172. [Google Scholar] [CrossRef]
- Mizunashi, K.; Furukawa, Y.; Katano, K.; Abe, K. Effect of omeprazole, an inhibitor of H+, K+-ATPase, on bone resorption in humans. Calcif. Tissue Int. 1993, 53, 21–25. [Google Scholar] [CrossRef]
- Khalili, H.; Huang, E.S.; Jacobson, B.C.; Camargo, A.C.; Feskanich, D.; Chan, A.T. Use of proton pump inhibitors and risk of hip fracture in relation to dietary and lifestyle factors: A prospective cohort study. BMJ 2012, 344, e372. [Google Scholar] [CrossRef] [Green Version]
- Adams, A.L.; Black, M.H.; Zhang, J.L.; Shi, J.M.; Jacobsen, S.J. Proton-pump inhibitor use and hip fractures in men: A population-based case-control study. Ann. Epidemiology 2014, 24, 286–290. [Google Scholar] [CrossRef] [PubMed]
- Ding, J.; Heller, D.A.; Ahern, F.M.; Brown, T.V. The Relationship Between Proton Pump Inhibitor Adherence and Fracture Risk in the Elderly. Calcif. Tissue Int. 2014, 94, 597–607. [Google Scholar] [CrossRef] [PubMed]
- Lewis, J.R.; Barre, D.; Zhu, K.; Ivey, K.L.; Lim, E.M.; Hughes, J.; Prince, R.L. Long-Term Proton Pump Inhibitor Therapy and Falls and Fractures in Elderly Women: A Prospective Cohort Study. J. Bone Miner. Res. 2014, 29, 2489–2497. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chou, Y.-S.; Jiang, H.-J.; Chen, C.-H.; Ho, P.-S.; Lee, T. Proton pump inhibitor use and risk of hip fracture in patients with type 2 diabetes. Sci. Rep. 2020, 10, 1–8. [Google Scholar] [CrossRef] [PubMed]
- Labenz, C.; Wörns, M.A.; Adarkwah, C.C.; Galle, P.R.; Schattenberg, J.M.; Kostev, K. Proton pump inhibitors increase risk of bone fractures in men with cirrhosis: A population-based study. Aliment Pharmacol Ther. 2020, 52, 1042–1050. [Google Scholar] [CrossRef] [PubMed]
- Zhou, B.; Huang, Y.; Li, H.; Sun, W.; Liu, J. Proton-pump inhibitors and risk of fractures: An update meta-analysis. Osteoporos. Int. 2016, 27, 339–347. [Google Scholar] [CrossRef] [PubMed]
- Poly, T.; Islam, M.; Yang, H.-C.; Wu, C.; Li, Y.-C. (Jack) Proton pump inhibitors and risk of hip fracture: A meta-analysis of observational studies. Osteoporos. Int. 2018, 30, 103–114. [Google Scholar] [CrossRef] [PubMed]
- Schubert, M.L. Proton pump inhibitors. Curr. Opin. Gastroenterol. 2020, 36, 493–500. [Google Scholar] [CrossRef] [PubMed]
- Epstein, M.; McGrath, S.; Law, F. Proton-Pump Inhibitors and Hypomagnesemic Hypoparathyroidism. N. Engl. J. Med. 2006, 355, 1834–1836. [Google Scholar] [CrossRef]
- Cundy, T.; Dissanayake, A. Severe hypomagnesaemia in long-term users of proton-pump inhibitors. Clin. Endocrinol. 2008, 69, 338–341. [Google Scholar] [CrossRef]
- Kuipers, M.T.; Thang, H.D.; Arntzenius, A.B. Hypomagnesaemia due to use of proton pump inhibitors—A review. Neth. J. Med. 2009, 67, 169–172. [Google Scholar] [PubMed]
- Broeren, M.A.; Geerdink, E.A.; Vader, H.L.; Bake, A.W.L.V.D.W. Hypomagnesemia Induced by Several Proton-Pump Inhibitors. Ann. Intern. Med. 2009, 151, 755. [Google Scholar] [CrossRef] [PubMed]
- Hoorn, E.J.; Van Der Hoek, J.; De Man, R.A.; Kuipers, E.J.; Bolwerk, C.; Zietse, R. A Case Series of Proton Pump Inhibitor–Induced Hypomagnesemia. Am. J. Kidney Dis. 2010, 56, 112–116. [Google Scholar] [CrossRef] [PubMed]
- Isse, N.; Hashimoto, M. Omeprazole-induced hypomagnesaemia, causing renal tubular acidosis with hypokalaemia, hypocalcaemia, hyperlactacidaemia and hyperammonaemia. BMJ Case Rep. 2020, 13, e235385. [Google Scholar] [CrossRef] [PubMed]
- Recart, D.A.; Ferraris, A.; Petriglieri, C.I.; Serena, M.A.; Bonella, M.B.; Posadas-Martinez, M.L. Prevalence and risk factors of long-term proton pump inhibitors-associated hypomagnesemia: A cross-sectional study in hospitalized patients. Intern. Emerg. Med. 2020, 1–7. [Google Scholar] [CrossRef]
- Chowdhry, M.; Shah, K.; Kemper, S.; Zekan, D.; Carter, W.; McJunkin, B. Proton pump inhibitors not associated with hypomagnesemia, regardless of dose or concomitant diuretic use. J. Gastroenterol. Hepatol. 2018, 33, 1717–1721. [Google Scholar] [CrossRef]
- Park, C.H.; Kim, E.H.; Roh, Y.H.; Kim, H.Y.; Kil Lee, S. The Association between the Use of Proton Pump Inhibitors and the Risk of Hypomagnesemia: A Systematic Review and Meta-Analysis. PLoS ONE 2014, 9, e112558. [Google Scholar] [CrossRef]
- Liao, S.; Gan, L.; Mei, Z. Does the use of proton pump inhibitors increase the risk of hypomagnesemia. Medicine 2019, 98, e15011. [Google Scholar] [CrossRef]
- Michalek, W.; Semler, J.R.; Kuo, B. Impact of Acid Suppression on Upper Gastrointestinal pH and Motility. Dig. Dis. Sci. 2010, 56, 1735–1742. [Google Scholar] [CrossRef]
- Bai, J.P.F.; Hausman, E.; Lionberger, R.; Zhang, X. Modeling and Simulation of the Effect of Proton Pump Inhibitors on Magnesium Homeostasis. 1. Oral Absorption of Magnesium. Mol. Pharm. 2012, 9, 3495–3505. [Google Scholar] [CrossRef]
- Elzen, W.P.D.; Groeneveld, Y.; De Ruijter, W.; Souverijn, J.H.M.; Le Cessie, S.; Assendelft, W.J.J.; Gussekloo, J. Long-term use of proton pump inhibitors and vitamin B12 status in elderly individuals. Aliment. Pharmacol. Ther. 2008, 27, 491–497. [Google Scholar] [CrossRef] [PubMed]
- Rozgony, N.R.; Fang, C.; Kuczmarski, M.F.; Bob, H. Vitamin B12 Deficiency is Linked with Long-Term Use of Proton Pump Inhibitors in Institutionalized Older Adults: Could a Cyanocobalamin Nasal Spray be Beneficial? J. Nutr. Elder. 2010, 29, 87–99. [Google Scholar] [CrossRef]
- Dharmarajan, T.; Kanagala, M.R.; Murakonda, P.; Lebelt, A.S.; Norkus, E.P. Do Acid-Lowering Agents Affect Vitamin B12 Status in Older Adults? J. Am. Med Dir. Assoc. 2008, 9, 162–167. [Google Scholar] [CrossRef] [PubMed]
- Hirschowitz, B.I.; Worthington, J.; Mohnen, J. Vitamin B12 deficiency in hypersecretors during long-term acid suppression with proton pump inhibitors. Aliment. Pharmacol. Ther. 2008, 27, 1110–1121. [Google Scholar] [CrossRef] [PubMed]
- Termanini, B.; Gibril, F.; Sutliff, E.V.; Yu, F.; Venzon, D.J.; Jensen, R.T. Effect of Long-Term Gastric Acid Suppressive Therapy on Serum Vitamin B12 Levels in Patients with Zollinger-Ellison Syndrome. Am. J. Med. 1998, 104, 422–430. [Google Scholar] [CrossRef]
- Stewart, A.C.; Termanini, B.; Sutliff, E.V.; Serrano, J.; Yu, F.; Gibril, F.; Jensen, R.T. Iron absorption in patients with Zollinger-Ellison syndrome treated with long-term gastric acid antisecretory therapy. Aliment. Pharmacol. Ther. 1998, 12, 83–98. [Google Scholar] [CrossRef] [PubMed]
- Koop, H.; Bachem, M.G. Serum Iron, Ferritin, and Vitamin B12 During Prolonged Omeprazole Therapy. J. Clin. Gastroenterol. 1992, 14, 288–292. [Google Scholar] [CrossRef]
- Sharma, V.R.; Brannon, M.A.; Carloss, E.A. Effect of Omeprazole on Oral Iron Replacement in Patients with Iron Deficiency Anemia. South Med. J. 2004, 97, 887–889. [Google Scholar] [CrossRef] [PubMed]
- Komorniak, N.; Szczuko, M.; Kowalewski, B.; Stachowska, E. Nutritional Deficiencies, Bariatric Surgery, and Serum Homocysteine Level: Review of Current Literature. Obes. Surg. 2019, 29, 3735–3742. [Google Scholar] [CrossRef] [Green Version]
- Kim, J.-H.; Bae, Y.-J.; Jun, K.H.; Chin, H.-M. The prevalence and clinical significance of postgastrectomy anemia in patients with early-stage gastric cancer: A retrospective cohort study. Int. J. Surg. 2018, 52, 61–66. [Google Scholar] [CrossRef]
- O’Kane, M.; Parretti, H.; Pinkney, J.; Welbourn, R.; Hughes, C.A.; Mok, J.; Walker, N.; Thomas, D.; Devin, J.; Coulman, K.D.; et al. British Obesity and Metabolic Surgery Society Guidelines on perioperative and postoperative biochemical monitoring and micronutrient replacement for patients undergoing bariatric surgery—2020 update. Obes. Rev. 2020, 21. [Google Scholar] [CrossRef] [PubMed]
- Jun, J.-H.; Yoo, J.E.; Lee, J.A.; Kim, Y.S.; Sunwoo, S.; Kim, B.S.; Yook, J.-H. Anemia after gastrectomy in long-term survivors of gastric cancer: A retrospective cohort study. Int. J. Surg. 2016, 28, 162–168. [Google Scholar] [CrossRef] [PubMed]
- Abrams, J.A.; Wang, T.C. Adenocarcinoma and other tumors of the stomach. In Sleisenger and Fordtran’s Gastrointestinal and Liver Disease: Pathophysiology/Diagnosis/Management, 9th ed.; Feldman, M., Friedman, L.S., Brandt, L.J., Eds.; Elsevier: Philadelphia, PA, USA, 2010; pp. 887–906. [Google Scholar]
- Tang, G.H.; Hart, R.; Sholzberg, M.; Brezden-Masley, C. Iron deficiency anemia in gastric cancer. Eur. J. Gastroenterol. Hepatol. 2018, 30, 1497–1501. [Google Scholar] [CrossRef]
- Liu, X.; Qiu, H.; Huang, Y.; Xu, D.; Li, W.; Li, Y.; Chen, Y.; Zhou, Z.-W.; Sun, X. Impact of preoperative anemia on outcomes in patients undergoing curative resection for gastric cancer: A single-institution retrospective analysis of 2163 Chinese patients. Cancer Med. 2018, 7, 360–369. [Google Scholar] [CrossRef] [PubMed]
- Goyal, H.; Perisetti, A.; Rahman, M.R.; Levin, A.; Lippi, G. Vitamin D and Gastrointestinal Cancers: A Narrative Review. Dig. Dis. Sci. 2018, 64, 1098–1109. [Google Scholar] [CrossRef]
- Anderson, M.G.; Nakane, M.; Ruan, X.; Kroeger, P.E.; Wu-Wong, J.R. Expression of VDR and CYP24A1 mRNA in human tumors. Cancer Chemother. Pharmacol. 2006, 57, 234–240. [Google Scholar] [CrossRef]
- Baek, S.; Lee, Y.-S.; Shim, H.-E.; Yoon, S.; Baek, S.-Y.; Kim, B.-S.; Oh, S.-O. Vitamin D3 regulates cell viability in gastric cancer and cholangiocarcinoma. Anat. Cell Biol. 2011, 44, 204–209. [Google Scholar] [CrossRef] [Green Version]
- Ren, C.; Qiu, M.-Z.; Wang, D.-S.; Luo, H.-Y.; Zhang, D.; Wang, Z.-Q.; Wang, F.; Li, Y.; Zhou, Z.-W.; Xu, R.-H. Prognostic effects of 25-hydroxyvitamin D levels in gastric cancer. J. Transl. Med. 2012, 10, 16. [Google Scholar] [CrossRef] [Green Version]
- Esmaillzadeh, A.; Khayatzadeh, S.; Feizi, A.; Saneei, P. Vitamin D intake, serum Vitamin D levels, and risk of gastric cancer: A systematic review and meta-analysis. J. Res. Med Sci. 2015, 20, 790–796. [Google Scholar] [CrossRef]
- Kwak, J.H.; Paik, J.K. Vitamin D Status and Gastric Cancer: A Cross-Sectional Study in Koreans. Nutrients 2020, 12, 2004. [Google Scholar] [CrossRef]
- Steenackers, N.; Van Der Schueren, B.; Mertens, A.; Lannoo, M.; Grauwet, T.; Augustijns, P.; Matthys, C. Iron deficiency after bariatric surgery: What is the real problem? Proc. Nutr. Soc. 2018, 77, 445–455. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pellitero, S.; Martínez, E.; Puig, R.; Leis, A.; Zavala, R.; Granada, M.L.; Pastor, C.; Moreno, P.; Tarascó, J.; Puig-Domingo, M. Evaluation of Vitamin and Trace Element Requirements after Sleeve Gastrectomy at Long Term. Obes. Surg. 2017, 27, 1674–1682. [Google Scholar] [CrossRef] [PubMed]
- Al-Mulhim, A.S. Laparoscopic Sleeve Gastrectomy and Nutrient Deficiencies. Surg. Laparosc. Endosc. Percutaneous Tech. 2016, 26, 208–211. [Google Scholar] [CrossRef] [PubMed]
- Kwon, Y.; Kim, H.J.; Menzo, E.L.; Park, S.-S.; Szomstein, S.; Rosenthal, R.J. Anemia, iron and vitamin B12 deficiencies after sleeve gastrectomy compared to Roux-en-Y gastric bypass: A meta-analysis. Surg. Obes. Relat. Dis. 2014, 10, 589–597. [Google Scholar] [CrossRef] [PubMed]
- Weng, T.-C.; Chang, C.-H.; Dong, Y.-H.; Chang, Y.-C.; Chuang, L.-M. Anaemia and related nutrient deficiencies after Roux-en-Y gastric bypass surgery: A systematic review and meta-analysis. BMJ Open 2015, 5, e006964. [Google Scholar] [CrossRef]
- Parsons, B.; Ijaz, U.Z.; D’Amore, R.; Burkitt, M.D.; Eccles, R.; Lenzi, L.; Duckworth, C.A.; Moore, A.R.; Tiszlavicz, L.; Varro, A.; et al. Comparison of the human gastric microbiota in hypochlorhydric states arising as a result of Helicobacter pylori-induced atrophic gastritis, autoimmune atrophic gastritis and proton pump inhibitor use. PLoS Pathog. 2017, 13, e1006653. [Google Scholar] [CrossRef] [Green Version]
- Rajilic-Stojanovic, M.; Figueiredo, C.; Smet, A.; Hansen, R.; Kupcinskas, J.; Rokkas, T.; Andersen, L.; Machado, J.C.; Ianiro, G.; Gasbarrini, A.; et al. Systematic review: Gastric microbiota in health and disease. Aliment. Pharmacol. Ther. 2020, 51, 582–602. [Google Scholar] [CrossRef]
- Engstrand, L.; Graham, D.Y. Microbiome and Gastric Cancer. Dig. Dis. Sci. 2020, 65, 865–873. [Google Scholar] [CrossRef] [Green Version]
- Pich, O.Q.; Merrell, D.S. The ferric uptake regulator of Helicobacter pylori: A critical player in the battle for iron and colonization of the stomach. Futur. Microbiol. 2013, 8, 725–738. [Google Scholar] [CrossRef] [Green Version]
Mechanisms of Action | |
---|---|
Stimulants of gastric acid secretion | |
Histamine | Histamine is released by ECL cells. It stimulates HCl secretion directly (binding H2 receptors, placed on parietal cell, coupled with activation of adenylate cyclase and generation of 3′5′-cyclic adenylate cyclase), and indirectly (inhibiting somatostatin release from D cells). |
Gastrin | Gastrin is released by antral G cells. It stimulates HCl secretion directly (acting on the CCK2 receptor and activating the release of intracellular calcium) and indirectly (stimulating histamine release) |
Acetylcholine (ACh) | ACh is released by postganglionic enteric neurons. It acts directly (binding M3 receptors, placed on parietal cell, coupled with increasing intracellular calcium) and indirectly (inhibiting somatostatin secretion). |
Inhibitor of gastric acid secretion | |
Somatostatin | Somatostatin is released by D cells. It acts directly on parietal cells and indirectly by inhibiting histamine release. |
To-Do List |
---|
To look for and to eventually treat Helicobacter pylori |
To consider the presence of corpus atrophic gastritis and eventually perform gastroscopy with antral and corpus biopsies To advise vitamin C intake from fresh fruits and vegetables in patients with corpus atrophic gastritis |
To check for previous gastric surgery |
To routinely monitor patients with any previous gastric surgery for micronutrient deficiency |
To reassess the indication of long-term of proton pump inhibitors |
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Carabotti, M.; Annibale, B.; Lahner, E. Common Pitfalls in the Management of Patients with Micronutrient Deficiency: Keep in Mind the Stomach. Nutrients 2021, 13, 208. https://doi.org/10.3390/nu13010208
Carabotti M, Annibale B, Lahner E. Common Pitfalls in the Management of Patients with Micronutrient Deficiency: Keep in Mind the Stomach. Nutrients. 2021; 13(1):208. https://doi.org/10.3390/nu13010208
Chicago/Turabian StyleCarabotti, Marilia, Bruno Annibale, and Edith Lahner. 2021. "Common Pitfalls in the Management of Patients with Micronutrient Deficiency: Keep in Mind the Stomach" Nutrients 13, no. 1: 208. https://doi.org/10.3390/nu13010208
APA StyleCarabotti, M., Annibale, B., & Lahner, E. (2021). Common Pitfalls in the Management of Patients with Micronutrient Deficiency: Keep in Mind the Stomach. Nutrients, 13(1), 208. https://doi.org/10.3390/nu13010208