Article Cite This: J. Agric. Food Chem. XXXX, XXX, XXX−XXX
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Potato Peels and Their Bioactive Glycoalkaloids and Phenolic Compounds Inhibit the Growth of Pathogenic Trichomonads Mendel Friedman,*,§ Vincent Huang,† Quincel Quiambao,† Sabrina Noritake,† Jenny Liu,† Ohkun Kwon,† Sirisha Chintalapati,† Joseph Young,† Carol E. Levin,§ Christina Tam,# Luisa W. Cheng,# and Kirkwood M. Land*,†
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Healthy Processed Foods Research Unit, Agricultural Research Service, United States Department of Agriculture, Albany, California 94556, United States † Department of Biological Sciences, University of the Pacific, Stockton, California 95211, United States # Foodborne Toxins Detection and Prevention Research Unit, Agricultural Research Service, United States Department of Agriculture, Albany, California 94556, United States ABSTRACT: Potato peel, a waste product of the potato processing industry, is high in bioactive compounds. We investigated the in vitro antitrichomonad activity of potato peel powders prepared from commercial Russet, red, purple, and fingerling varieties as well as several known potato components, alkaloids and phenolic compounds, against three pathogenic strains of trichomonads. Trichomonas vaginalis is a sexually transmitted protozoan parasite that causes the human disease trichomoniasis. Two distinct strains of the related Tritrichomonas fetus infect cattle and cats. The glycoalkaloids α-chaconine and α-solanine were highly active against all parasite lines, while their common aglycone solanidine was only mildly inhibitory. α-Solanine was several times more active than α-chaconine. The phenolic compounds caffeic and chlorogenic acids and quercetin were mildly active against the parasites. Most of the potato peel samples were at least somewhat active against all three trichomonad species, but their activities were wide-ranging and did not correspond to their glycoalkaloid and phenolic content determined by HPLC. The two Russet samples were the most active against all three parasites. The purple potato peel sample was highly active against bovine and mostly inactive against feline trichomonads. None of the test substances were inhibitory toward several normal microflora species, suggesting the potential use of the peels for targeted therapeutic treatments against trichomonads. KEYWORDS: Trichomonas vaginalis, Tritrichomonas fetus, infection, potato peel, α-chaconine, α-solanine, caffeic acid, chlorogenic acid, growth inhibition, trichomoniasis
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INTRODUCTION
to be increasing resistance to the 5-nitroimidazole drugs used against this disease, including ronidazole.4 We previously reported that the tomato glycoalkaloid tomatine strongly inhibited in vitro the growth of the following three pathogenic protozoa that, as mentioned above, are reported to infect humans, cattle, and domesticated cats: Trichomonas vaginalis strain G3, Tritrichomonas fetus strain D1, and Tritrichomonas fetus strain C1, respectively.5 In a second study, we reported that theaflavin-rich black tea and catechinrich green tea extracts were also effective under the in vitro conditions in inhibiting the growth of the same three parasitic trichomonads and that the most potent of the two preparations, the theaflavin-rich black tea extract, was also effective against metronidazole-resistant and cytoadherent strain of T. vaginalis.6 Interest in potato peels arises from the fact that the annual worldwide production of about 1.3 billion tons of food waste includes potato peels, a peeling byproduct of the industrial production of potato fries, chips, and flour. Because potato and other peels derived from fruits and vegetables contain
Related protozoa Trichomonas vaginalis and Tritrichomonas fetus infect and cause disease in humans and animals, respectively. Trichomonas vaginalis infection is worldwide the most common nonviral sexually transmitted disease (STD) in humans.1 Tritrichomonas fetus strains infect the reproductive tract of cattle and the gastrointestinal tract of cats. Treatment by drug therapy is complicated by the fact that reinfection is common (in part because sexual partners must both be treated), the disease is often misdiagnosed, and because antibiotic resistance is developing against the drugs of choice.1 For humans, infection with the organism can lead to infertility, poor outcomes of pregnancy, cancer, and increased susceptibility to human immunodeficiency virus (HIV) infection. The seriousness of these sequels and the increasing antibiotic-resistance suggests the need for finding new therapies. In cattle, the disease causes failed pregnancies. The disease is asymptomatic in bulls, leading to reinfection even after the cows are treated. The most cost-effective method to control the disease is often culling the infected animals.2 In domesticated cats, the disease infects the gastrointestinal tract and is transmitted by the oral-fecal route.3 The infection causes persistent diarrhea in the felines. Moreover, there seems © XXXX American Chemical Society
Received: April 4, 2018 Revised: June 26, 2018 Accepted: July 16, 2018
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DOI: 10.1021/acs.jafc.8b01726 J. Agric. Food Chem. XXXX, XXX, XXX−XXX
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Journal of Agricultural and Food Chemistry
The extracted and purified sample was analyzed by UV HPLC under the following conditions: column, Resolve (Waters Corp., Milford, MA, USA) C18 90 Å 5 μm particles, 3.9 × 300 mm column; eluent, 0.8 mL/min 30% acetonitrile, 100 mM ammonium phosphate buffer, pH 3.5; detection, 200 nm UV. The well-separated chromatographic peaks of α-solanine and α-chaconine eluted between 9 and 11 min. Preparation of Stock Solutions and Stock Culture. Cultures of G3 strain of T. vaginalis and C1 and D1 strains of T. fetus were grown and maintained in 11 mL of completed TYM Diamond medium of pH 6.2. Every 24 h, the parasites from C1, D1, and G3 strains were passed by inoculating 1000 μL of parasites into a new 15 mL conical tube, containing 10 mL of completed TYM Diamond medium. Then, the parasites were incubated for 24 h at 37 °C. Dilutions of freeze-dried, powdered potato peels were made at a 10% dilution and dissolved in a 1:1 DMSO-Millipore water solution. Dilutions of caffeic acid and chlorogenic acid were weighed out by mass and diluted to 100 mM concentration. Dilutions of α-chaconine, α-solanine, and solanidine were weighed by mass and diluted to 20 mM. Growth Inhibition of the Parasites by Compounds Present in Potato Peels. During General Screening, 100 μM DMSO solutions of quercetin, caffeic acid, chlorogenic acid, α-chaconine, α-solanine, and solanidine were screened against the G3 strain of T. vaginalis and the C1 and D1 strains of T. fetus for growth inhibition in 5 mL of TYM Diamond medium. The microliters of cell culture added to 5 mL of TYM Diamond media were determined by dividing parasites (4000) by the average number of parasites observed by counting 10 μL of parasites using a hemocytometer and light microscope. This volume was then added to 5 mL of TYM Diamond medium. DMSO controls were set up to ensure it had no inhibitory effect on the parasites. The parasite count for each strain and compound was determined by using a hemocytometer and light microscope. Percent inhibition was determined relative to the DMSO control. Test substances above that showed greater than 50% inhibition of the trichomonads were retested to determine their IC50 values. The calculated IC50 values (concentration that inhibits 50% parasites) were determined from serial dilutions of a specific compound. The IC50s were performed a minimum of three times to a standard error of 0.10. The software Prism (GraphPad, San Diego, CA) was used to calculate a theoretical value of IC50 using the titration dyad. Effects of Compounds and Peels on Normal Flora Microbiota. A number of different nonpathogenic bacteria known to be a part of the human mucosal microbiome were cultured and analyzed for inhibition by potato compounds and peels. Lactobacillus reuteri (ATCC 23272), Lactobacillus acidophilus (ATCC 43560), and Lactobacillus rhamnosus (ATCC 53103) were grown in Lactobacilli MRS media at 37 °C under anaerobic conditions. Nonpathogenic Escherichia coli K12 MG1655 were cultured in Luria broth at 37 °C aerobically. One hundred mM stock solutions of the different compounds and the vehicle control DMSO were diluted to 100 μM in media to generate working dilutions. Empty BDL-sensi discs (6 mm) were incubated in the working dilutions for 20 min at room temperature. Streaked agar plates of these different bacteria were incubated with discs containing the vehicle control, compounds, or various antibiotic discs [levofloxacin (5 μg), gentamicin (10 μg), and gentamicin (120 μg)] and incubated overnight at 37 °C. Sensitivity to the vehicle control, compounds, and antibiotics was determined via measurement of zones of growth inhibition around each disc in millimeters. All of these bacteria were purchased from the American Type Culture Collection (ATCC).
numerous bioactive compounds, they are a useful and inexpensive source for medical and food uses.7−12 As part of a systematic screening of food processing byproducts containing bioactive compounds, and that have been shown to be active against cancer cells13 and pathogenic microorganisms12 and to reduce weight gain in mice on a highfat diet,14 we tested potato peels, a byproduct of the potatoprocessing industry, against the three pathogenic trichomonads mentioned above. Potato peels are a rich source of bioactive compounds, including the glycoalkaloids α-solanine and αchaconine, as well as a number of antioxidative phenolic compounds such as quercetin and chlorogenic and caffeic acids. The objective of the present study was to determine using cell based assays the potential of potato peels, and their bioactive glycoalkaloids and phenolic compounds, to inactivate multiple strains of disease-causing protozoa and to relate the content of the pure compounds to the observed inhibitory activities.
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MATERIALS AND METHODS
Materials. Caffeic acid was acquired from MP Biomedicals (Solon, Ohio). Chlorogenic acid (min. 95.0%) was acquired from Fisher Scientific (Pittsburgh, PA). α-Chaconine (100%) was acquired from Cerilliant Corp. (Round Rock, TX). Solanidine (≥99%) was acquired from Indofine Chemical Co. (Hillsborough, NJ). α-Solanine (≥95%) was acquired from Sigma-Aldrich, (St. Louis, MO). Quercetin was acquired from Santa Cruz Biotechnology (Dallas, TX). TYM Diamond medium was prepared in the Department of Biological Sciences, University of the Pacific. The feline Tritrichomonas fetus-like organism strain C1 was acquired from Stanley Marks, School of Veterinary Medicine, University of California, Davis, CA. Bovine Tritrichomonas fetus strain D1 was acquired from Lynette Corbeil, School of Medicine, University of California, San Diego. Trichomonas vaginalis strain G3 was acquired from Patricia Johnson, University of California, Los Angeles. Preparation of Freeze-Dried Potato Peels. About 1.2−1.5 kg of red, purple, nonorganic fingerling (unknown variety), organic fingerling (unknown variety), and nonorganic and organic Russet potatoes obtained at local stores were individually washed with water, dried with absorbent paper tissues, hand-peeled using a standard domestic potato peeler, freeze-dried, and then ground to powders using an electric coffee grinder (Krups, Millville, NJ), yielding 32−52 g of peel powders. Glycoalkaloid Analysis of Potato Peels. The method by Friedman and Levin15 was used with some modifications to determine the α-chaconine and α-solanine content of the peels. To extract the glycoalkaloids, potato powder (100 mg) was weighed into a microfuge tube, in duplicate. Ethanol (1 mL, 50%)/acetic acid (0.5%) was added, and the tube was vortexed every 10 min over the course of 1 h. The tube was then centrifuged for 10 min at 10,000g. The extract was cleaned before chromatography using solid phase extraction, taking advantage of the hydrophilic property of the glycoalkaloids in acid and hydrophobic properties in basic solutions, as follows. A Sep-Pak Plus C18 cartridge (Waters Corp., Milford, MA, USA) was conditioned with methanol (2 mL). Acetic acid (0.1%, 10 mL) was added to the cartridge reservoir. About 2 mL was allowed to pass through the cartridge, after which 0.5 mL of the centrifuged extract supernatant was added to the remaining 8 mL remaining in the reservoir, followed by pipet mixing. The total solution was allowed to pass through the cartridge, followed sequentially by washes with water (2 mL), ammonium carbonate (2 mL, 100 mM), basified methanol (2 mL, 50% in 50 mM ammonium carbonate), and finally, water (3 mL). The sample was eluted with acidified methanol (3 mL, 80% in 0.02% acetic acid). The sample was dried on a Rotovapor (Buchi, Flawil, Switzerland) and reconstituted in ethanol (1 mL 50%) for chromatography.
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RESULTS AND DISCUSSION A major objective of the present study was to investigate if potato peels, which contain a number of bioactive compounds known to vary by potato variety and environment,16 might be active against several strains of parasitic trichomonads that are reported to infect humans and farm and companion animals. We tested potato peels obtained by hand peeling six distinct B
DOI: 10.1021/acs.jafc.8b01726 J. Agric. Food Chem. XXXX, XXX, XXX−XXX
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Journal of Agricultural and Food Chemistry
Table 1. General Screening of Pure Compounds (100 μM) Reported as % Inhibition and Calculated IC50 Values for the Inhibition of Three Protozoan Parasites by Potato Phenolic Compounds and Potato Alkaloids T. fetus feline C1 compound
% inhibition
caffeic acid chlorogenic acid quercetin solanidine α-solanine α-chaconine
21.1 ± 5.1 21.9 ± 5.9 8.5 ± 2.2 22.6 ± 5.0 100 100
T. fetus bovine D1 IC50
% inhibition
12.55 μM 51.46 μM
43.7 ± 9.0 12.1 ± 6.2 18.9 ± 1.9 22.96 ± 6.1 100 100
T. vaginalis human G3 IC50
10.86 μM 35−60 μM
% inhibition 42.8 11.4 45.6 48.4 100 100
± ± ± ±
IC50
3.5 6.8 1.6 2.2 15.81 μM 3560 μM
Figure 1. Structures of the potato trisaccharide glycoalkaloids α-chaconine and α-solanine, their common aglycone alkaloid solanidine lacking the carbohydrate side chain, and the phenolic compounds caffeic and chlorogenic acids and the flavonoid quercetin evaluated in the present study for antitrichomonad activity.
lots of potatoes from five varieties of potatoes purchased from local stores: Russet, red, purple, and two fingerling varieties. The Russet variety was bought in two lots, one organic and one conventional. The two fingerling lots were, by visual inspection, obviously different varieties; however, the variety was unstated on the packages. The term “fingerling” potato is apparently used to describe the style, shape, and size, rather than the variety. One fingerling lot was organic, and the second lot was conventional (nonorganic) potatoes. We also tested the pure glycoalkaloids α-chaconine and αsolanine, their common aglycone solanidine, and three phenolic compounds, caffeic and chlorogenic acids and quercetin, known to be present in potato peels,17,18 by general screening of inhibitory activity at 100 μM. The test substances showing better than 50% inhibitory activity were further tested for dose−response against the organisms. The results show that the three strains of trichomonads substantially differed in their susceptibility to inactivation by the different potato compounds. Glycoalkaloid Content of Potato Peels. The potato peels showed considerable variation in the levels of glycoalkaloids. Large variations in bioactive potato compounds
are normal, and not surprising, in view of the fact that it is generally recognized that the content of glycoalkaloids and phenolic compounds in potatoes is affected by genetics and by both preharvest and postharvest events.19 Potatoes produce glycoalkaloids in response to stress; both before and after harvest. Preharvest conditions that can affect glycoalkaloids include soil fertility, climate, and exposure to phytopathogens. Postharvest events include the formation of glycoalkaloid-rich sprouts, storage conditions, exposure to light, and mechanical damage. On a dry basis, potato peels represent 5 to 9% of the whole potato; however, peels often contain 50% or more of the total glycoalkaloids in the tuber.20 An earlier survey of eight potato varieties showed total glycoalkaloids varied from 84 to 3500 ppm in the dry peel and from 2 to 130 mg per whole potato tuber, with the ratio of α-chaconine to α-solanine varying from 1.4 to 2.4.20 There were some unusual potato varieties in that set, but the numbers do illustrate the high variability of the glycoalkaloid content in potatoes. Typically, the peel waste product produced in potato processing is high in glycoalkaloids. Our potato peel samples ranged on a dry weight basis C
DOI: 10.1021/acs.jafc.8b01726 J. Agric. Food Chem. XXXX, XXX, XXX−XXX
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Journal of Agricultural and Food Chemistry from 1.2 to 5.3 mg/g total glycoalkaloids, with α-chaconine present at about twice the concentration of α-solanine. Trichomonad Growth Inhibition by α-Chaconine, αSolanine, and Solanidine. We found by general screening at 100 μM that the glycoalkaloids commonly found in potatoes, α-chaconine and α-solanine, completely inhibited T. vaginalis strain G3 and T. fetus strains D1 and C1. The inhibition by solanidine, the aglycone shared by both glycoalkaloids, was lower, ranging from about 23 to 48% (Table 1). Because of their high activity, the glycoalkaloids were further tested to determine their inhibitory dose response, which is reported in terms of IC50 values (Table 1). The inhibitory activity of αsolanine was several-fold higher than of α-chaconine. This result was surprising in view of the fact that studies of other bioactivities of these compounds discussed in detail elsewhere19 found that α-chaconine was generally more bioactive than α-solanine. The two glycoalkaloids have the same aglycone moiety, solanidine, but differ in the nature of the trisaccharide side chain (Figure 1). It would seem that the trisaccharide configuration or the particular sugars in the trisaccharide affect inhibitory potency. The IC50 values of these potato glycoalkaloids are higher (the inhibitory activity is lower) than the corresponding values we previously reported for the tomato glycoalkaloid tomatine (2.0 to 7.9 μM), which has a tetrasaccharide side chain.5 In that study we also reported that the aglycone tomatidine lacking the tetrasaccharide side chain was less active than tomatine. It appears from the above observations that the configuration and/or content of the sugar moieties of the molecules seem to be influencing activity. To further test this hypothesis, it might also be worthwhile to evaluate antiprotozoal activities of the two structurally related glycoalkaloids solasonine and solamargine present in some eggplant varieties.13,21,22 The solasodine aglycone of these two glycoalkaloids differs from the potato aglycone solanidine, but the trisaccharide side chains in solasonine and solamargine correspond to the side chains in αsolanine and α-chaconine, respectively.23 Evaluation of the bioactivities of these two compounds might provide additional information about the relative contribution of the trisaccharide side chain and the aglycone part of the glycoalkaloids to the inhibitory activity. Growth Inhibition of Trichomonad Parasites by Phenolic Compounds. Table 1 shows that the three tested potato phenolic compounds also inhibited the growth of the three tested strains. The inhibition was, however, much lower than by the two glycoalkaloids described above. The percentage inhibition of the C1 strain by the phenolic acids, caffeic and chlorogenic acids, was identical and about one-fifth that of the glycoalkaloids, whereas the flavonoid quercetin was less than half as active as the acids. The responses of the D1 and G3 strains to the phenolic acids were similar to each other but different than the C1 strain response; caffeic acid was much more active, and chlorogenic acid was less active than in C1. It is interesting that D1/G3 and C1 strains respond oppositely to these compounds. Chlorogenic acid is an ester of caffeic acid and about twice its size, so that the differences in activity might simply be due to accessibility of the molecules to the active sites on the parasites. With such striking differences in antimicrobial activity by molecules of similar structure, that vary by the trichomonad strain, it would be of interest to test additional phenolic acids of slightly different structure and size. The response to quercetin was unique among all strains. The
activity of quercetin may be associated with its ability to chelate iron,24 as trichomonads have a high iron requirement.25 The observed results with phenolic compounds might be significant in view of the fact that the phenolic compounds are present not only in potato peels but also in numerous other fruits and vegetables. Moreover, the antiprotozoan effect of the phenolic compounds observed in the present study complements other beneficial bioactive effects, including antifungal, antimicrobial, antivirulence, and antiviral properties.26−31 Inhibitory Activity of Potato Peels. A screen of the inhibitory activities of the peel powders against the three trichomonad strains summarized in Table 2 and Figure 2 Table 2. Percent Inhibition Potato Peel Powders (10% w/v) Tested Against Three Pathogenic Trichomonad Speciesa potato peels from commercial potatoes
feline C1
bovine D1
human G3
red purple organic fingerling nonorganic fingerling organic Russet nonorganic Russet
3.8 ± 1.5 0±0 30.30 ± 0.12 20.31 ± 0.48 48.62 ± 0.65 43.89 ± 0.41
9.0 ± 2.1a 41.0 ± 6.3b 12.86 ± 0.52a 25.3 ± 2.6c 41.4 ± 5.6b 26.7 ± 4.3c
1.1 ± 0.0 24.6 ± 7.5a,b 21.9 ± 5.3a 17.5 ± 3.0a 36.6 ± 7.0b 18.0 ± 5.9a
a Data within columns sharing a letter were not significantly different, p < 0.05.
Figure 2. Trichomonad-inhibitory trends induced by the potato glycoalkaloids α-chaconine and α-solanine.
shows that nearly all peels were active in the assay; however, the relative inhibitory activities varied widely. Most of the peels inhibited all three organisms; however, the peels from the purple potatoes were unusual in that, although they were significantly effective against the bovine and human organisms, they showed no activity against the feline Tritrichomonas. The red peel had the lowest activity overall, and Russet peels had the highest. Relationship of Inhibitory Activities of Peels to Composition. Glycoalkaloid analysis of the peels revealed that, consistent with other reports,20 they all contained more αchaconine than α-solanine. This is of interest because we saw in the screening of the pure compounds that α-solanine was more effective against the trichomonads. Figure 2 shows the relationship between glycoalkaloid content and inhibitory activity. The peel sample containing the highest level of D
DOI: 10.1021/acs.jafc.8b01726 J. Agric. Food Chem. XXXX, XXX, XXX−XXX
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glycoalkaloids was the organic fingerling sample, which had only average potency against the organisms. Conversely, the organic Russet potato peel had the lowest level of glycoalkaloids but was the most effective of all the peels. It seems that these observations did not confirm our hypothesis that the activity of the peels against the trichomonads would correlate with their content of what we determined to be the most active pure compounds. Although the potato peels were active against the trichomonads, our efforts to correlate the composition of the peels to antitrichomonad activities were not successful. It is possible that other peel components affect the availability of the bioactive compounds to the cell receptor sites, positively or negatively. The potato samples with higher activity were the thicker-skinned varieties, and peeling of the thin-skinned varieties may have inadvertently included proportionally more of the flesh. This observation could account for some of the differences in the bioactivity between samples if a higher proportion of flesh essentially diluted active components in the peels. Then again, the flesh might include pro-trichomonad growth components or have components that interfere with glycoalkaloid activity. Other explanations for the lack of correlation between levels of peel bioactive compounds and parasite inhibition might be associated with concurrent and/or competitive binding of two or more compounds to the receptor sites of the parasites and/or that the bioactive phenolic compounds and glycoalkaloids in the peels act synergistically against the parasites. These aspects merit further study. In summary, this study demonstrated that the potato glycoalkaloids α-chaconine and α-solanine, the potato phenolic compounds chlorogenic acid, caffeic acid, and quercetin, and multiple potato peels prepared from commercial potatoes have antiprotozoal activity against pathogenic trichomonad strains that infect humans, farm animals, and felines. The potato glycoalkaloids were highly active against the three strains of the pathogenic trichomonad organisms. The inhibitory activity of the potato peels varied by both potato variety and trichomonad organism. The purple potato variety had the most extreme activity range, showing no activity against feline T. fetus, while good activity against the other 2 strains. The Russet potato peel samples had the highest activity against all strains of the evaluated peels. This is a promising result because Russet potatoes are the most common variety used in commercial food processing, and their peels are a waste product for which we are challenged to discover alternate uses. The results suggest that future studies should evaluate the efficacy of potato peel powders and their bioactive phenolic compounds and glycoalkaloids against trichomoniasis in infected farm and companion animals. Such studies should take into account possible adverse effects that might be associated with some of these compounds. Moreover, because our screen of the test substances also showed no activity against several strains of native vaginal bacteria, it is likely that if the investigated antitrichomonads are therapeutically effective in humans, they might not adversely affect the normal microflora. Finally, it is also relevant to note that the observed antitrichomonad properties of potato peels and their bioactive glycoalkaloids and phenolic compounds complement other reported potential health benefits of these substances, including antifungal, antimicrobial, antiviral, as well as antiobesity properties in mice, suggesting that they have the potential to help alleviate multiples diseases.
Article
AUTHOR INFORMATION
Corresponding Authors
*Phone: 510-559-5615. E-mail:
[email protected]. gov (M.F.). *Phone 209-946-7608. E-mail: kland@pacific.edu (K.M.L.). ORCID
Mendel Friedman: 0000-0003-2582-7517 Funding
S.N. was a 2016 SURF Fellow at the University of the Pacific. K.L. was supported by the Department of Biological Sciences at the University of the Pacific. L.W.C. and C.T. were funded by the United States Department of Agriculture, Agricultural Research Service (National Program 108, Project #532542000-039-00D). Notes
The authors declare no competing financial interest.
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ACKNOWLEDGMENTS The authors thank Denyse Sturges for assistance with the preparation of the potato peels. We also thank Dr. Lydia K. Fox for her continuous support of undergraduate research at the University of the Pacific.
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REFERENCES
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DOI: 10.1021/acs.jafc.8b01726 J. Agric. Food Chem. XXXX, XXX, XXX−XXX
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DOI: 10.1021/acs.jafc.8b01726 J. Agric. Food Chem. XXXX, XXX, XXX−XXX
