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Korean J Physiol Pharmacol. 2018 Jan; 22(1): 35–42.
Published online 2017 Dec 22. doi:Β 10.4196/kjpp.2018.22.1.35
PMCID: PMC5746510
PMID: 29302210

Joon-Kyung Lee

1Department of Physical Pharmacy, College of Pharmacy, Chungnam National University, Daejeon 34134, Korea.

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Sang-Hyuk Jung

2Department of Pharmacology, College of Pharmacy, Chungnam National University, Daejeon 34134, Korea.

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Sang-Eun Lee

1Department of Physical Pharmacy, College of Pharmacy, Chungnam National University, Daejeon 34134, Korea.

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Joo-Hui Han

2Department of Pharmacology, College of Pharmacy, Chungnam National University, Daejeon 34134, Korea.

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Eunji Jo

Heartburn Remedies Warnings (πŸ‘ 9 Ways To Relieve) | Heartburn Remedies 12 Tipshow to Heartburn Remedies for 2Department of Pharmacology, College of Pharmacy, Chungnam National University, Daejeon 34134, Korea.

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Hyun-Soo Park

2Department of Pharmacology, College of Pharmacy, Chungnam National University, Daejeon 34134, Korea.

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Kyung-Sun Heo

2Department of Pharmacology, College of Pharmacy, Chungnam National University, Daejeon 34134, Korea.

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Deasun Kim

3PHARMCROSS Co., Ltd., Chuncheon 24398, Korea.

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Jeong-Sook Park

1Department of Physical Pharmacy, College of Pharmacy, Chungnam National University, Daejeon 34134, Korea.

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2Department of Pharmacology, College for 1 last update 29 May 2020 of Pharmacy, Chungnam National University, Daejeon 34134, Korea.2Department of Pharmacology, College of Pharmacy, Chungnam National University, Daejeon 34134, Korea.

Find articles by Chang-Seon Myung
1Department of Physical Pharmacy, College of Pharmacy, Chungnam National University, Daejeon 34134, Korea.
2Department of Pharmacology, College of Pharmacy, Chungnam National University, Daejeon 34134, Korea.
3PHARMCROSS Co., Ltd., Chuncheon 24398, Korea.
Corresponding author.
Correspondence: Jeong-Sook Park. [email protected]
Correspondence: Chang-Seon Myung. [email protected]
#These authors equally contributed to this work.
Received 2017 Apr 26; Revised 2017 Jul 25; Accepted 2017 Sep 20.
Copyright © 2018 The Korean Physiological Society and The Korean Society of Pharmacology
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

Ascorbic acid is one of the most well-known nutritional supplement and antioxidant found in fruits and vegetables. Calcium ascorbate has been developed to mitigate the gastric irritation caused by the acidity of ascorbic acid. The aim of this study was to compare calcium ascorbate and ascorbic acid, focusing on their antioxidant activity and effects on gastric juice pH, total acid output, and pepsin secretion in an in vivo rat model, as well as pharmacokinetic parameters. Calcium ascorbate and ascorbic acid had similar antioxidant activity. However, the gastric fluid pH was increased by calcium ascorbate, whereas total acid output was increased by ascorbic acid. In the rat pylorus ligation-induced ulcer model, calcium ascorbate increased the gastric fluid pH without changing the total acid output. Administration of calcium ascorbate to rats given a single oral dose of 100 mg/kg as ascorbic acid resulted in higher plasma concentrations than that from ascorbic acid alone. The area under the curve (AUC) values of calcium ascorbate were 1.5-fold higher than those of ascorbic acid, and the Cmax value of calcium ascorbate (91.0 ng/ml) was higher than that of ascorbic acid (74.8 ng/ml). However, their Tmax values were similar. Thus, although calcium ascorbate showed equivalent antioxidant activity to ascorbic acid, it could attenuate the gastric high acidity caused by ascorbic acid, making it suitable for consideration of use to improve the side effects of ascorbic acid. Furthermore, calcium ascorbate could be an appropriate antioxidant substrate, with increased oral bioavailability, for patients with gastrointestinal disorders.

Keywords: Antioxidant, Ascorbic for 1 last update 29 May 2020 acid, Bioavailability, Calcium ascorbate, Gastric pHAntioxidant, Ascorbic acid, Bioavailability, Calcium ascorbate, Gastric pH

INTRODUCTION

Vitamin C (ascorbic acid) is one of the elements required for the maintenance of human health and function [1,2]. As the main function of ascorbic acid is as an antioxidant for the removal of active oxygen, and it therefore has anti-aging, immune enhancement, drinking and smoking detoxification, gastric cancer prevention, vascular health protection, and atherosclerosis prevention effects [3,4,5]. Ascorbic acid is found in many vegetables and fruits, in particular, oranges, tomatoes, spinach, strawberries, potatoes, etc. The recommended daily intake of this vitamin is 90 mg for adults [1,2]. The lack of ascorbic acid in the human body inhibits the synthesis of collagen, causing swelling and bleeding of the gums, scurvy, chronic fatigue, nosebleeds, digestive disorders, and depression. Although excessive intake of ascorbic acid is not toxic, it could induce diarrhea, abdominal pain, acid indigestion, frequent urination, and headaches [6,7]. As mentioned above, the main effect of ascorbic acid is as an antioxidant for eliminating free radicals in the body and inhibiting various inflammatory conditions [8,9]. With its antioxidant activity, ascorbic acid plays an important role in the production of some major proteins, such as collagen, serotonin, and norepinephrine [10,11].

As humans cannot synthesize ascorbic acid in vivo, the vitamin has to be ingested from an external source. Although ascorbic acid can be from synthetic and natural sources, but the human body can accept either type, indicating that the body''s origin. The oxidation product of ascorbic acid is dehydroascorbic acid, but high doses of ascorbic acid are metabolized to oxalate, where metabolism of accumulated oxalate can lead to urinary stone formation [12,13]. Excess intake of this supplement also causes diarrhea [14] and pyrolysis [15].

Gastritis or peptic ulcer is a disease that causes a change of the gastric mucosa, eliciting a variety of symptoms, such as indigestion, nausea, and heartburn. An excess intake of food or a sudden intake of high-acidity foods will lead to excessive secretion of gastric juices into the stomach and increased pepsin secretion in the mucous membrane chief cells. Pepsin represents active protein degradation at low pH (pH 1.8–2.0) [16,17], its activity and continuous exposure to gastric juice can induce damage of the stomach wall. The best known way to treat gastritis is to control the one''s instructions. In brief, the area under curve (AUC) of each Trolox concentration (0, 2.5, 5, 10, 20, 30, 40, and 50 µM) was calculated using the standard curve for ORAC activity. Ascorbic acid and calcium ascorbate were calculated as the mmol Trolox equivalents (TE) by comparison against the standard curve. The ORAC values were expressed as TE/L.

Pharmacokinetics of ascorbic acid after oral administration

Using an animal feeding needle (oral zonde needle, stainless, 7 cm), ascorbic acid (105.96 mg/kg) or calcium ascorbate (135.24 mg/kg) was administered to the rats. An orbital blood sample (1.0 ml) was collected at 0.5, 1, 2, 4, 6, and 24 h post ingestion [25]. The plasma was separated by centrifugation of the blood sample at 12,000 rpm, 4℃, for 10 min, and then 100 µl was stored in the deep freezer at −70℃ prior to HPLC analysis. The HPLC method used was a modification of previous HPLC quantification methods [26]. To determine the concentration of ascorbic acid in the plasma, standard solutions were prepared by mixing the stock solution with blank plasma. For plasma deproteination, the collected plasma (30 µl) was mixed with acetonitrile (90 µl) by vortex mixing, and the mixture was then separated by centrifugation at 12,000 rpm, 4℃, for 10 min (Micro 17TR, Hanil Science, Korea). To remove impurities, the solutions were filtered through a polytetrafluoroethylene syringe filter (pore size 0.45 µm, diameter 13 mm; Whatman, Maidstone, UK). The concentration of ascorbic acid was determined using an SP-LC model HPLC system (PeakmanSP, Seoul, Korea) equipped with two SP 3101 pumps, an SP 3002 UV/Vis detector, an SP 3004 column oven, an SP 3010 switching valve and a 3023 SI-2 autosampler (Shiseido, Tokyo, Japan). The separation was performed on a Shiseido Capcell Pak MGII column (4.6 mm i.d.×150 mm, 5 µm) maintained at 30℃. The mobile phase was prepared by mixing distilled water, methanol, and acetic acid (91.9:8:0.1, v/v/v) and eluted at a flow rate 0.5 ml/min. After 10 µl samples were injected onto the column, the signals were monitored at a UV wavelength of 240 nm.

Statistical analysis

All data were expressed as the mean±SEM of three or more independent experiments. Analysis of variance was used to compare parameters among multiple groups (GraphPad, San Diego, CA, USA). If a significant difference between treated groups was found, Dunnett's test was applied. Differences with p<0.05 were considered statistically significant.

RESULTS

Comparison of the antioxidant activities of ascorbic acid and calcium ascorbate

Heartburn Remedies 10 Foods To Eat (⭐️ Heartburn Relief) | Heartburn Remedies Heartburn Treatmentshow to Heartburn Remedies for It is well known that ascorbic acid aids cell growth and helps the body to stay healthy because of its antioxidant activity, which potentially offers protection from some diseases and degenerative aspects of aging [27]. To ascertain whether the antioxidant activity of calcium ascorbate was still functional, the antioxidant activities of calcium ascorbate and ascorbic acid were evaluated by measuring the fluorescence decrease rate from the production and decay of the peroxy radical by 2, 2′-azo-bis-2-methyl-propanimidamide, dihydrochloride (AAPH) using ORAC assay. Table 1 shows that with the antioxidant activity of ascorbic acid (25.24 mmol TE/L) was not significantly different from that of calcium ascorbate (25.65 mmol TE/L), and their relative percentages of antioxidant activity were also not significantly different (100% vs 101%, Table 1). These data show that calcium ascorbate and ascorbic acid have similar antioxidant activities.

Table 1

Antioxidant activity of calcium ascorbate measured by oxygen radical absorbance capacity (ORAC) assay (n=4)

TE, trolox equivalent.

Effect of calcium ascorbate on gastric juice pH and total acid output in human and rat simulated gastric fluids in vitro

Previously, several studies reported that ascorbic acid could induce gastrointestinal disorders such as indigestion, heartburn, nausea, diarrhea, abdominal cramps/pain, and esophagitis [15,28,29]. Because ascorbic acid is highly acidic and could stimulate the secretion of stomach acids such as pepsin, these excess acids may trigger these gastrointestinal symptoms. To determine the effect of calcium ascorbate on the pH and total acid output of gastric juice, the differences in pH and total acid of SGFs following treatment with calcium ascorbate and ascorbic acid were compared. When treated with ascorbic acid, the gastric fluid pH was not different to that of the DW control in both hSGF and rSGF (Figs. 1A and and2A).2A). In contrast, the pH of SGFs treated with calcium ascorbate was significantly higher than that of fluids treated with ascorbic acid (Heartburn Remedies Treatments (β˜‘ Foods To Avoid) | Heartburn Remedies Acid Refluxhow to Heartburn Remedies for Figs. 1A and for 1 last update 29 May 2020 and2A).and2A).2A). However, the total acid output was significantly higher in ascorbic acid-treated SGFs than in the DW control ( for 1 last update 29 May 2020 Figs. 1BFigs. 1B and for 1 last update 29 May 2020 and2B),and2B),2B), whereas calcium ascorbate treatment resulted in no significant changes relative to the control (Figs. 1B and and2B).and2B).2B). These results indicate that calcium ascorbate could act to increase gastric pH without increasing the total acid output, thereby attenuating gastric symptoms.

Effect of calcium ascorbate on the pH and total acid output of human simulated gastric fluid (hSGF).

After the addition of ascorbic acid or calcium ascorbate to the hSGF, the changes in hSGF pH and total acid were measured until 240 min. pH (A) and total acid (B) of hSGF; pH (C) and total acid (D) of hSGFw/P (hSGF with pepsin). Data are expressed as the mean±SEM (n=5). ***p<0.001 vs. distilled water (DW).

Effect of calcium ascorbate on the pH and total acid output of rat simulated gastric fluid (rSGF).

Heartburn Remedies How To Get Rid (β˜‘ Home Remedies) | Heartburn Remedies Treatment Ofhow to Heartburn Remedies for After the addition of ascorbic acid or calcium ascorbate to the rSGF, the changes in rSGF pH and total acid were measured until 240 min. pH (A) and total acid (B) of rSGF; pH (C) and total acid (D) of rSGFw/P (rSGF with pepsin). Data are expressed as the mean±SEM (n=5). ***p<0.001 vs. distilled water (DW).

Because pepsin is one of the major enzymes in gastric fluid and is stimulated by low pH and acid [30], its effect on gastric pH and total acid output was investigated in the SGFs treated with calcium ascorbate or ascorbic acid. The gastric pH and total acid output were not affected by pepsin in the hSGFw/P and rSGFw/P (Figs. 1C, 1D, 2C, and 2D).

Effect of calcium ascorbate on gastric juice pH and total acid output in the in vivo rat pylorus ligation-induced ulcer model

The reduction of gastric pH and the secretion of gastric juices both work to exacerbate damage to the gastric wall in gastric disorders [30]. Therefore, the effect of calcium ascorbate was further confirmed in the rat pylorus ligation-induced ulcer model. Although the secreted volume of gastric juice was not significantly different between ascorbic acid and calcium ascorbate treatments (Fig. 3A), the gastric juice pH was significantly increased by calcium ascorbate as compared with ascorbic acid until 30 min after administration (Fig. 3B). In contrast, the total acid output was not significantly increased by calcium ascorbate (Fig. 4A).

Effect of calcium ascorbate on gastric juice volume and pH in the rat pylorus ligation-induced ulcer model.

Heartburn Remedies Solutions (⭐️ Doesn't Help) | Heartburn Remedies Warningshow to Heartburn Remedies for After oral administration of distilled water (DW; as a control), ascorbic acid (105.96 mg/kg), or calcium ascorbate (135.24 mg/kg) to rats processed by pylorus ligation, the stomach was removed immediately following animal sacrifice and the gastric contents were collected at designated times. After the centrifugation of the gastric contents (1,800×g for 5 min), the volume (A) and pH (B) were measured. Data are expressed as the mean±SEM (n=5). **p<0.01, ***p<0.001 vs. distilled water (DW); ##p<0.01, ###p<0.001 vs. ascorbic acid.

Effect of calcium ascorbate on total acid output and pepsin secretion in the rat pylorus ligation-induced ulcer model.

After oral administration of distilled water (DW; as a control), ascorbic acid (105.96 the 1 last update 29 May 2020 mg/kg), or calcium ascorbate (135.24 mg/kg) to rats processed by pylorus ligation, the stomach was removed immediately following animal sacrifice and the gastric contents were collected at designated times. After centrifugation of the gastric contents (1,800×g for 5 min), the total acid output (A) and amount of secreted pepsin (B) were measured. Data are expressed as the mean±SEM (n=5). **p<0.01, ***p<0.001 vs. distilled water (DW); ##p<0.01, ###p<0.001 vs. ascorbic acid.After oral administration of distilled water (DW; as a control), ascorbic acid (105.96 mg/kg), or calcium ascorbate (135.24 mg/kg) to rats processed by pylorus ligation, the stomach was removed immediately following animal sacrifice and the gastric contents were collected at designated times. After centrifugation of the gastric contents (1,800×g for 5 min), the total acid output (A) and amount of secreted pepsin (B) were measured. Data are expressed as the mean±SEM (n=5). **p<0.01, ***p<0.001 vs. distilled water (DW); ##p<0.01, ###p<0.001 vs. ascorbic acid.

Pepsin, secreted by the mucous membrane chief cells, is also present in the gastric juice and shows proteolytic activity at low pH (1.8–2.0) [31]. It is also known that the high activity of pepsin induces gastric damage [32]. Therefore, we evaluated whether the secretion of pepsin was affected by calcium ascorbate treatment. Fig. 4B shows that pepsin secretion was not induced by dosing with calcium ascorbate in the rat pylorus ligation-induced ulcer model, whereas it was immediately induced after ascorbic acid administration. Taken together, these results demonstrate that calcium ascorbate is effective in attenuating ascorbic acid-induced gastric symptoms by increasing the gastric pH and preventing pepsin secretion in the rat pylorus ligation-induced ulcer model.

Pharmacokinetics of calcium ascorbate after oral administration to rats

To investigate whether calcium ascorbate could improve the oral bioavailability of ascorbic acid, a pharmacokinetic study was carried out. Calcium ascorbate administration resulted in significantly higher plasma concentrations of ascorbic acid than dosing of ascorbic acid, at 0.5, 1, 2, 4, 6, and 24 h post oral administration ( for 1 last update 29 May 2020 Fig. 5Fig. 5). The AUC0-24h value from calcium ascorbate (1277.0 ng/ml) was 1.5-fold higher than that from ascorbic acid (705.7 ng/ml), and the AUCinf value from calcium ascorbate (5769.6 ng/ml) was 2.8-fold higher than that from ascorbic acid (2024.7 ng/ml). The Cmax value of calcium ascorbate (91.0 ng/ml) was also higher than that of ascorbic acid (74.8 ng/ml). However, the Tmax values were similar (Heartburn Remedies Best (πŸ”΄ Home Remedies) | Heartburn Remedies 10 Easyhow to Heartburn Remedies for Table 2). After 24 h post dose, the plasma concentration of calcium ascorbate (45.3 ng/ml) was two times higher than that of ascorbic acid (22.6 ng/ml) (Fig. 5). Therefore, calcium ascorbate was obviously better absorbed and hence present in higher plasma levels than ascorbic acid.

Blood concentration of ascorbic acid after oral administration.

Plasma concentration versus time profiles obtained after the administration of ascorbic acid (105.96 mg/kg) and calcium ascorbate (135.24 mg/kg). Values for each time point are expressed as the mean±SEM (n=6).

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Pharmacokinetic parameters of ascorbic acid and calcium ascorbate after oral administration to rats (mean±SEM, n=6)

*Means p<0.05 compared with the results of ascorbic acid.

DISCUSSION

This study had two major findings: (1) calcium ascorbate could act as an antioxidant substrate without acid-induced gastric high acidity, and (2) the rate of absorption and the maintenance of calcium ascorbate in the body were higher than those of ascorbic acid in vivo. Our observations suggest that calcium ascorbate could be used as an antioxidant substrate for individual health maintenance without gastric high acidity particularly for people with sensitive stomachs and illnesses such as indigestion, diarrhea, abdominal cramps/pain, and other gastric diseases.

Gastric acid is one of the most important factors causing gastritis and reflux esophagitis [33]. Control of the stomach pH is an essential method to protect the gastric mucosa against damage [30]. Ascorbic acid is known to have an adverse effect by decreasing the gastric pH in patients with gastrointestinal disorders [34]. In the present study, we found that ascorbic acid increased the total acid outputs in vitro and in vivo (Figs. 1B, 1D, 2B, 2D, and and4A).4A). However, calcium ascorbate increased the gastric pH without changing the total acid output (Figs. 1A, 1C, 2A, 2C, and and4A). the 1 last update 29 May 2020 4A4A). Because pepsin activity could induce gastric wall damage, the lower activity of pepsin at a higher pH in the stomach could suppress the deterioration of the stomach [35]. Therefore, the inhibition of pepsin secretion and activity would be a most important target in the treatment of gastric disorders from gastric acid [19]. We found that pepsin did not affect the gastric pH and total acid output in vitro ( for 1 last update 29 May 2020 Figs. 1C, 1DFigs. 1C, 1D, 2C, and 2D); however, its secretion was increased by ascorbic acid in vivo, but not by calcium ascorbate (Fig. 4A). Moreover, we found that the antioxidant activity of calcium ascorbate was similar to that of ascorbic acid (Table 1). Thus, the findings from the present study provide compelling evidence of the protective role of calcium ascorbate against gastric high acidity in vitro and in vivo.

In rats with pylorus ligation-induced ulcer, the volume of gastric juice was increased gradually because of the pylorus ligation, but the changes in pH within 30 min were not significant since gastric juice was not secreted until 30 min (Fig. 3A). Moreover, pH reduction was observed after 60 min because of the increase of gastric juice secretion over time. The values of total acid output within 30 min were measured as the acidity of ascorbic acid, because the volumes of gastric juices were not significantly increased until 30 min (Fig. 4A). However, the total acid output seemed to be reduced at 240 min by dilution of the secreted gastric juices. Similar results were observed for pepsin output (Fig. 4B), which was increased with ascorbic acid dosing but inhibited by calcium ascorbate.

Moreover, it was found that the oral bioavailability of calcium ascorbate was higher than that of ascorbic acid [25]. The AUC0-24h values of calcium ascorbate were greater than ascorbic acid with significant difference (p<0.05). The reason for the increased absorption of calcium ascorbate was likely due to the neutralizing effect of the calcium salt. However, the AUCinf values were not significantly different in those two groups. Since the general dosage regimen of ascobate preparation is once daily and water-soluble vitamins are easy to be excreted in urine, it is meaningful to show the higher AUC0-24h values instead of AUCinf values.

In conclusion, our results demonstrate that calcium ascorbate has the same antioxidant activity as ascorbic acid, but the 1 last update 29 May 2020 can alleviate the side effects of the vitamin C, such as gastric high acidity. Furthermore, calcium ascorbate could be an appropriate antioxidant substrate, with increased oral bioavailability, for patients with gastrointestinal disorders.In conclusion, our results demonstrate that calcium ascorbate has the same antioxidant activity as ascorbic acid, but can alleviate the side effects of the vitamin C, such as gastric high acidity. Furthermore, calcium ascorbate could be an appropriate antioxidant substrate, with increased oral bioavailability, for patients with gastrointestinal disorders.

ACKNOWLEDGEMENTS

This research was supported by a grant of PHARMCROSS (Chuncheon, Korea) and Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Korean government, MOE (No 2009-0093815).

Footnotes

Contributed by

Author contributions: J.S.P. and C.S.M. designed the study, analyzed the data, and wrote the manuscript. J.K.L., S.H.J., S.E.L., J.H.H., E.J., and H.S.P. performed the experiments, and K.S.H. analyzed the data. D.K. helped with the calcium ascorbate preparation and data analysis.

the 1 last update 29 May 2020

CONFLICTS OF INTEREST: The authors declare no conflicts of interest.

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