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OXALATES
4282 OXALATES
OXALATES S C Morrison, New Zealand Institute for Crop and Food Research, Lincoln, Canterbury, New Zealand G P Savage, Lincoln University, Canterbury, New Zealand Copyright 2003, Elsevier Science Ltd. All Rights Reserved.
Introduction 0001
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Oxalic acid and its salts occur as end products of metabolism in a number of plant tissues. When these plants are eaten they may have an adverse effect on mineral bioavailability because oxalates bind calcium and other minerals. While oxalic acid is a normal end product of mammalian metabolism, the consumption of additional oxalic acid may cause stone formation in the urinary tract when it is excreted in the urine. The mean daily intake of oxalate in the diet in the UK has been calculated to be 70– 150 mg; tea, rhubarb, spinach, and beet are common high oxalate-containing foods. Soaking and cooking foodstuffs high in oxalate will reduce the oxalate content by leaching. The consumption of high-oxalate foods is more likely to pose health problems in those who have an unbalanced diet or those with intestinal malfunction. A diet high in oxalate and low in essential minerals, such as calcium and iron, is not recommended. Vegans and lactose-intolerant persons may have a high-oxalate and low-calcium diet unless their diet is supplemented. Vegetarians who consume greater amounts of vegetables will have a higher intake of oxalates, which may reduce calcium availability. This may be an increased risk factor for women, who require greater amounts of calcium in the diet. Persons with an increased absorption rate of oxalate are advised to avoid or eat fewer high-oxalate foods to prevent kidney stone formation. In healthy individuals, the occasional consumption of high-oxalate foods as part of a balanced diet does not pose any particular problem.
Oxalates in Plants 0003
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Oxalate can be found in small amounts in many plants. Oxalate-rich foods are usually minor components in human diets but are present in higher quantities in seasonal diets in certain areas of the world (particularly in the tropics) as a component of grains, tubers, nuts, vegetables, and fruits. The highest levels of oxalates are found in the foods listed in Table 1. In general, oxalate content is highest in the leaves, then in the seeds, and lowest in the stems. Reports
show that the stems or stalks of plants, such as amaranth, rhubarb, spinach, and beet, contain significantly lower levels of oxalates than the leaves. In the buckwheat family (e.g., rhubarb, sorrel), there is almost twice as much oxalic acid in the leaves as in the stalk. However, in the goosefoot family (e.g., beet, spinach), oxalic acid is more abundant in the stalk than in the petiole of the leaf. It must be noted that the leaves of rhubarb are rarely eaten and therefore the oxalate content of its leaves is of no concern in human nutrition. Oxalic acid concentration tends to be higher in plants than in meats, which may be considered oxalate-free when planning low-oxalate diets. Meats, fats, and dairy products contain very low levels of oxalates. The levels of oxalates in fungi are low when compared to the levels found in spinach and rhubarb. The giant mushroom (Tricholoma giganteum), a large, edible fungi, is reported to contain 89 mg 100 g1 dry weight (DW) oxalic acid while tropical species of mushrooms, including termite and ear mushrooms, contain between 80 and 220 mg oxalate 100 g1 DW. High oxalate levels in tropical plants are of some concern. Taro (Colocasia esculenta) and sweet potato (Ipomoea batatas) were reported to contain 278– 574 mg 100 g1 fresh weight (FW) and 470 mg 100 g1, respectively. Total oxalate levels in yam (Dioscorea alata) tubers were reported in the range 486–781 mg 100 g1 DW, but may not be of nutritional concern since 50–75% of the oxalates were present in the water-soluble form and therefore may leach out during cooking. Oca or New Zealand yam (Oxalis tuberosa Mol.) contains 80–221 mg 100 g1 FW soluble oxalate. Higher levels of oxalates are usually found in the leaves and highest concentrations of oxalate have been found in the skin of these tropical root crops. Peanut greens, commonly consumed in tropical climates, are reported to contain 407 mg 100 g1. Coriander leaf (Coriandrum sativum) contains 1268 mg 100 g1; horsegram (Macrotyloma uniflorum) and santhi (Boernavia diffusa) contain 508 mg 100 g1 and 3800 mg 100 g1 respectively. Nuts such as peanuts, pecans, and cashews are relatively high in oxalates. Sesame seeds have been reported to contain high quantities of oxalate, ranging from 350 to 1750 mg 100 g1 FW. Beverages with a high-oxalate concentration include Indian black tea, cocoa drinks, Ovaltine, cola, and certain types of beer. The oxalic acid content is variable within some species; some cultivars of spinach (Universal, Winter
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Table 1 Common foods exhibiting high levels of oxalates Spinach Swiss chard Kale Purslane Collards Mustard and turnip greens
Beet Yam, oca, sweet potato Peanuts, pecans Soybean Wheat germ, wheat bran Sorrel, parsley, amaranth
Giant) contain 400–600 mg 100 g1, while others range from 700 to 900 mg 100 g1. Oxalic acid accumulates in plants, especially during dry conditions. A study comparing two cultivars of spinach, Magic (cv. summer) and Lead (cv. autumn), revealed that the summer cultivar contained greater amounts of oxalate (740 mg 100 g1 FW) than the autumn cultivar (560 mg 100 g1 FW). Oxalate content has been reported to increase as the plant ages and becomes overripe. The proportion of oxalic acid in the leaves of the goosefoot family can double during ripening. However, in tomatoes, oxalic acid content has been reported to decrease during ripening.
Absorption and Metabolism in Mammals 0010
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Calcium can combine with oxalate to form calcium oxalate in the intestinal lumen, making the calcium unavailable for absorption; calcium oxalate is then excreted in the feces. Free or soluble oxalate is absorbed by passive diffusion in the colon in humans; comparative studies between healthy individuals and those with ileostomies indicate that the colon is the principal site for oxalate absorption. However, it is suggested that the small intestine may be the major absorptive site rather than the colon. The absorption of oxalates from individual foods varies depending on their dietary conditions and source; in general, the absorption is quite limited. It has been estimated that 2–5% of administered oxalate is absorbed in humans. Experiments have shown that more oxalate is absorbed when consumed while fasting (12%) compared to only 7% oxalate absorption when consumed with a normal diet. The percentage of oxalate absorption varied markedly from 1% for rhubarb and spinach to 22% from tea, but generally absorption was higher at low doses. Oxalate is an end product of ascorbate, glyoxylate, and glycine metabolism in mammals. Thirty-three to fifty percent of urinary oxalate is derived from ascorbate, 40% from glycine and 6–33% from minor metabolic pathways and dietary oxalate; dietary oxalate appears to account for only 10–15% of excreted oxalates.
Rhubarb Gooseberries, strawberries Black tea Cocoa, chocolate, Ovaltine Cola Beer
Chemical Properties and Toxic Effects Oxalic acid forms water-soluble salts with Naþ, Kþ, and NH4þ ions; it also binds with Ca2þ, Fe2þ, and Mg2þ, rendering these minerals unavailable to animals. However, Zn2þ appears to be relatively unaffected. Calcium oxalate (Ca(COO)2) is insoluble at a neutral or alkaline pH, but freely dissolves in acid. Ingestion of 4–5 g of oxalate is the minimum dose capable of causing death in an adult, but reports have shown that 10–15 g is the usual amount required to cause fatalities. Oxalic acid ingestion results in corrosion of the mouth and gastrointestinal tract, gastric hemorrhage, renal failure, and hematuria. Other associated problems include low plasma calcium, which may cause convulsions and high plasma oxalates. Most fatalities from oxalate poisoning are apparently due to the removal of calcium ions from the serum by precipitation. High levels of oxalate may interfere with carbohydrate metabolism, particularly by succinic dehydrogenase inhibition; this may be a significant factor in death from oxalate toxicity induced in animals grazing pastures containing high levels of Halogeton glomeratus. Halogeton (H. glomeratus) and wood sorrel (Oxalis cernua) are high in oxalates and are known to cause injury to grazing cattle and sheep. Although garden sorrel is a herb and not normally consumed in large quantities, there has been one report of fatal oxalate poisoning after a man consumed an estimated 6–8 g oxalate in vegetable soup containing 500 g sorrel. Both fatal and nonfatal poisoning by rhubarb leaves is thought to be caused by toxic anthraquinone glycosides rather than oxalates. Experiments involving the consumption of more than 30–35 g day1 of cocoa, a high-oxalate foodstuff, by eight women provoked symptoms of intoxication including loss of appetite, nausea, and headaches. However, cocoa contains theobromine (1500–2500 mg 100 g1) and tannic acid (4000– 6000 mg 100 g1), both of which are more toxic than the oxalic acid present (500–700 mg 100 g1). There appears to be a great deal of confusion as to what was responsible for these poisonings and it would be unwise to assume that only one factor was responsible.
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Effect on Bioavailability of Minerals 0015
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High-oxalate foods have been known to inhibit calcium and iron absorption. Even though vegetables such as spinach, rhubarb, and Swiss chard are high in calcium, the calcium cannot be absorbed due to the presence of oxalates in these vegetables. When calcium absorption from spinach, a high-oxalate and high-calcium food, was compared with calcium absorption from milk, a high-calcium food, the results showed that the calcium from spinach is not readily available (only 5.1% absorbed), probably due to the high content of oxalates. The adverse effect of oxalates is greater if the oxalate-to-calcium ratio exceeds 9:4 (or approximately 2). The oxalate-tocalcium ratio in a food varies widely and can be classified into three groups, as summarized in Table 2. Oxalate and calcium levels and the oxalate-tocalcium ratio of specific foods are detailed in Table 3. Foods that have a ratio greater than two, as well as containing no utilizable calcium, have excess oxalate, which can bind calcium in other foods eaten at the same time. Foodstuffs with a ratio of about one do not encroach on the utilization of calcium provided by other products and therefore do not exert any demineralizing effects. However, these foods are not good sources of calcium. Although parsley (Petroselinum sativum) contains average levels of oxalate (140–200 mg 100 g1), its high calcium levels (180– 290 mg 100 g1) reduce the oxalate-to-calcium ratio to a low level. Oxalate appears to interfere only slightly with zinc absorption. A counteracting or protective mechanism may prevent the precipitation of zinc by oxalates. Increasing the proportion of magnesium ions in solution was reported to inhibit the binding of calcium and zinc oxalates. This observation explains the minor effect oxalates have on zinc absorption from some leafy vegetables, such as spinach, which has high levels of calcium and zinc, and relatively high levels of magnesium. Oxalic acid may cause greater decreases in mineral availability if consumed with a high-fiber diet but the decrease may be only temporary. Negative calcium, magnesium, zinc, and copper balances were detected in males consuming a diet containing fiber and oxalates. When spinach was replaced by cauliflower, a
low-oxalate vegetable, fiber had no effect on the minerals studied, indicating that the apparent negative balances obtained were due to the presence of oxalic acid.
Adverse Effects of Oxalates Acute
A number of plants contain calcium oxalate crystals (measured as insoluble oxalate). When ingested, they are not absorbed into the blood stream and remain largely undissolved within the digestive tract, so they have no systemic toxicity, but the sharp raphide crystals can penetrate the tissues of the mouth and the tongue, causing considerable discomfort. Most of the plants that contain calcium oxalate crystals are members of the arum family. It has been suggested that calcium oxalate crystals are responsible for the irritating sensation in kiwi fruit (Actinidia sp.) and soluble oxalates are thought to account for the bitter taste present in some oca (O. tuberosa Mol.). Conophor seeds (Tetracarpidium conophorum) are a popular Nigerian snack, which have a bitter taste when raw but are palatable when cooked. This observation was correlated with a 73% decrease in total oxalate concentration after cooking.
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Chronic
Oxalate is poorly absorbed under nonfasting conditions. Once absorbed free oxalate binds to calcium ions to form insoluble calcium oxalate, it remains in the insoluble form. Free oxalate and calcium can precipitate in the urine and may form kidney stones. These stones consist mainly of calcium oxalate (80%), which is relatively insoluble in urine, and calcium phosphate (5%). Oxalate crystallizes with calcium in the renal vasculature and infiltrates vessel walls causing renal tubular obstruction, vascular necrosis, and hemorrhage, which lead to anuria, uremia, electrolyte disturbances, or even rupture. Kidney stones are becoming more common in men between the ages 30 and 50 years in industrialized countries. The risk factors involved in stone formation are a low volume of urine, increased urinary excretion of oxalate, calcium, or uric acid, a persistently low or high urinary
Table 2 Examples of plants with varying oxalate to calcium ratios Oxalate-to-calciumratio
Examples
Group 1: Plants with a ratio greater than 2 Group 2: Plants with a ratio of approx. 1 Group 3: Plants with a ratio less than 1
Spinach, rhubarb, beet, sorrel, cocoa Potatoes, amaranth, gooseberries, currants Lettuce, cabbage, cauliflower, green beans, peas
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OXALATES tbl0003
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Table 3 Oxalate, calcium, and oxalate-to-calcium ratio (Ox:Ca) of some common foods Foodstuff
Group 1 Rhubarb (Rheum rhaponticum) cv. Victoria, forced, stewed raw Common sorrel (Rumex acetosa) Red beetroot (Beta vulgaris) Garden sorrel (Rumex patientia) Pig spinach (Chenopodium spp.) Purslane (Portulaca oleracea) Spinach (Spinacia oleracea) Garden orach (Atriplex hortensis) New Zealand spinach (Tetragonia expansa) Coffee (Coffea arabica) Cashew (Anacardium occidentale) Cocoa (Theobroma cacao) Beet leaves (Beta vulgaris var. cicla) Rhubarb (Rheum rhaponticum) cv. Crimson, end of season, stewed Group 2 Potato (Solanum tuberosum) Amaranth (Amaranthus polygonoicles) Tea (Thea chinensis) Amaranth (Amaranthus tricolor) Rhubarb (Rheum rhaponticum) cv. Victoria, end of season, stewed Group 3 Apple (Malus spp.) Blackcurrant (Ribes nigrum) Tomato (Lycopersicum esculentum) Parsley (Petroselinum sativum) Cabbage (Brassica oleracea) Lettuce (Lactuca sativa)
Oxalate (mg 100 g1FW)
Calcium (mg 100 g1FW)
Ox:Ca ratio
Range
Range
Mean
(mmoll1)
12.4 45 40 275 45 99 125 101 100 100 12 41 125 110
9.32 7.95 5.56 5.09 4.94 4.94 4.60 4.27 4.00 3.96 3.70 2.50 2.49 2.46
91.5
2.23
275–1336 270–730 121–450 300–700 910–1679 320–1260 300–1500 50–150 500–900 300–920
Mean
260 805 500 275 500 1100 1294 970 900 890 100 231 700 610
40–50 35–45 121–450 40–50 13–236 80–122
10–15 100–150 100–120
460 20–141 300–2000
80 1586 1150 1087
10–34 400–500
620 0–30 2–90 5–35 140–200 0–125 5–20
15 50 20 170 60 12
5–15 19–50 10–20 180–290 200–300 73–90
22 595 450 453
1.62 1.18 1.14 1.07
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1.04
10 35 15 235 250 81
0.67 0.63 0.58 0.32 0.11 0.07
FW, fresh weight. Adapted from Zarembski PM and Hodgkinson A (1962) The oxalic acid content of English diets. British Journal of Nutrition 16: 627–634; Gontzea I and Sutzescu P (1968) Natural Antinutritive Substances in Foodstuffs and Forages, pp. 84–108. Basel: S Karger; Meena BA, Umapathy KP, Pankaja N and Prakash J (1987) Soluble and insoluble oxalates in selected foods. Journal of Food Science and Technology 24: 43–44; Noonan SC and Savage GP (1999) Oxalates and its effects on humans. Asia Pacific Journal of Clinical Nutrition 8: 64–74 with permission.
pH, and a low concentration of urinary inhibitors, such as magnesium, citrate, and high-molecularweight polyanions. Normal urine is usually supersaturated with calcium oxalate. The normal urinary excretion of oxalate is less than 40–50 mg day1 with less than 10% coming from the diet. Intakes of oxalate exceeding 180 mg day1 lead to a marked increase in the amount excreted. Small increases in oxalate excretion have pronounced effects on the production of calcium oxalate in the urine, implying that foods high in oxalate can promote hyperoxaluria (high oxalate excretion) and increase the risk of stone formation. Rhubarb, spinach, beet, nuts, chocolate, tea, coffee, parsley, celery, and wheat bran cause significant increases in urinary oxalate excretion in healthy individuals and have been identified as the main dietary sources in the risk of kidney stone formation. It
has been reported that black tea increased oxalate excretion by only 7.9%, compared with increases of 300% and 400% for spinach and rhubarb, respectively. Therefore 2–3 cups a day of black tea would have little effect on the risk of urinary stone formation when compared to spinach and rhubarb. It appears that tea is a significant source of oxalate intake in UK diets. The main reason for the strong relationship between the risk of calcium stones and urinary oxalate excretion appears to be the effect that the latter has on the supersaturation of urine with calcium oxalate. The amount of oxalate excreted in the urine was higher in individuals with kidney stones than in healthy individuals, suggesting that those with kidney stones absorb more oxalate, consume more oxalate or oxalate-producing substances such as ascorbate, or metabolize more oxalate precursors. Excessive or
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increased absorption of oxalate from normal diets is the result of intestinal abnormalities or malfunction. This is termed ‘enteric hyperoxaluria’ and is the commonest cause of increased renal oxalate excretion. It has been indicated that people with abnormal gastrointestinal absorption are at greater risk for hyperoxaluria and, as a result, kidney stone formation, than healthy individuals and should reduce their intake of oxalate and its precursors, such as ascorbate. A lowoxalate diet has prevented stone formation in some cases involving gastrointestinal disorders associated with hyperoxaluria. An increase in calcium intake should be accompanied by a lower oxalate consumption, because a lowcalcium and high-oxalate diet enhances oxalate absorption and excretion, which carries an even greater risk of stone formation than high calcium excretion. An increase in calcium intake may reduce urinary oxalate excretion by binding to more oxalate in the gut, thus reducing the risk of stone formation. Varying the amounts of calcium does not significantly alter levels of urinary calcium. From experimental work, it has been concluded that hypercalciuria plays, at most, a secondary role in the formation of calcium stones compared with mild hyperoxaluria. Excessive ascorbic acid (vitamin C) intake may increase urinary oxalate output with an increased risk of forming kidney stones. An excess dose is considered to be 2000 mg of vitamin C per day. However, ascorbic acid doses greater than 500 mg day1 were reported to induce a significant increase in urinary oxalate, and doses of 1000 mg day1 would increase urinary oxalate excretion by 6–13 mg day1. The recommended daily intake in many countries is in the region of 80 mg.
Effects of Processing 0026
Oxalates may be removed from food by leaching in water but this is not the most effective method as it removes only the soluble oxalate. Although the amount of oxalate in raw soybean (Glycine max) is relatively low, soaking and germination of the seed reduced the oxalate concentration. Cooking germinated soybeans reduced oxalate concentration below that in uncooked germinated soybeans. Soaking followed by cooking also proved to be effective, although not as effective as germination. Oxalate content in horsegram seeds (M. uniflorum) decreased by 38% when seeds were dehulled (508 and 315 mg 100 g1, for seed and dehulled seed, respectively). Roasting was found to be the least effective method. Roasting chicory roots was reported to increase oxalate content. Roasting oca (New Zealand yam,
O. tuberosa Mol.) also increased oxalate levels by 10–26%. This may be caused by the decrease in moisture content, a hypothesis supported by reports of dry tropical leafy vegetables having higher oxalate concentrations than fresh vegetables. A 40–50% loss of total oxalates by leaching was reported when yam tubers (D. alata and D. esculenta) were boiled, compared to steaming (20–25%) and baking (12–15%). Cooking proved most effective in reducing total oxalates. However, it must be noted that water-soluble minerals also leach out at the same time. Mineral leaching appears to vary between plant species. Blanching has been reported to decrease the oxalic acid content in spinach. However blanching, by conventional and microwave methods, reduced the oxalic acid content of sweet potato, peanut, and collard leaves only slightly whereas other antinutritional factors such as tannic and phytic acid were reduced significantly. Spinach, orach, and silverbeet are generally eaten after being boiled. However, rhubarb, cocoa, and common and garden sorrel may be consumed in the raw state and therefore should be eaten in smaller quantities. Fermentation, frequently used in Asian countries, has been reported to decrease the oxalate content of foods. A marked decrease in oxalic acid content was reported in Icacinia manni (a starch tuber) after fermentation. Oxalic acid was observed to decrease by 37% (86 to 54 mg 100 g1 FW) during souring of poi (a cooked taro paste) at 20 C.
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Recommendations Foods high in oxalates should be consumed in moderation to insure optimum intake of minerals from the diet. Although some foods are reported to be high in calcium and other essential minerals, the amount available may be limited due to the presence of oxalates. For instance, spinach is a high-calcium food, yet because of its high oxalate content, the calcium availability is almost negligible. The availability of magnesium, iron, sodium, potassium, and phosphorus may also be restricted. High-oxalate foods should be cooked to reduce the oxalate content. Soaking raw foods will also reduce the oxalate content but other useful nutrients such as water-soluble vitamins and minerals may also be lost at the same time. Oxalates tend to occur in higher concentrations in the leafy parts of vegetables rather than in roots or stalks. For the general population, the occasional consumption of high-oxalate foods as part of a balanced diet does not pose any health problems. However, there are some groups of people who may be at risk from oxalate-induced side-effects.
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Vegans and vegetarians should be aware that some foods contain high levels of oxalates. The diets of vegans and those persons with lactose intolerance may be low in calcium as a result of the exclusion of dairy products, unless their diet is supplemented by some other high-calcium food products. It is recommended that high-oxalate foods should be accompanied by calcium-rich foods such as dairy products and shellfish. If high-oxalate foods are consumed in conjunction with a low-calcium diet, then the consumer may be at risk of hyperoxaluria, which may lead to kidney stone formation. Women tend to be more susceptible to calcium and iron deficiencies than men. Osteoporosis is a concern amongst females, especially after menopause. People suffering from fractures should also be aware of the potential effects of oxalates on mineral availability, as high calcium levels are required for bone repair. Once again, consumption of high-oxalate foods with an adequate-to-high calcium intake should pose no health problems. It must also be noted that calcium is only absorbed and used when there are adequate levels of vitamin D in the body, either obtained via the diet or synthesized by the body when exposed to sunlight. Women should eat red meats, which are low in oxalate, to satisfy their iron intake. Adequate levels of vitamin C are required for the absorption of iron, but excess amounts are not advised because ascorbic acid is converted into oxalate. The risk of stone formation is three times greater in males and they should avoid eating excess amounts of high-oxalate foods. Sufferers of hyperoxaluria and kidney stones are advised to restrict their diet to foods containing low or medium levels of oxalates, as although urinary oxalate arises predominantly from endogenous sources, it can be influenced by dietary intake. Excess vitamin C intake is not recommended in these patients. Inhabitants of tropical countries should be aware that leafy tropical plants and tropical root crops tend to contain higher levels of oxalates than plants from temperate climates. People living in these areas are at possible risk of stone formation due to hyperoxaluria, and mineral deficiencies if sufficient minerals are not consumed. See also: Ascorbic Acid: Properties and Determination Physiology; Calcium: Properties and Determination; Physiology; Iron: Properties and Determination; Physiology; Plant Antinutritional Factors:
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Characteristics; Renal Function and Disorders: Nutritional Management of Renal Disorders; Toxins in Food – Naturally Occurring
Further Reading Concon JM (1988) Food Toxicology – Principles and Concepts, pp. 416–419. New York: Marcel Dekker. Dobbins JW and Binder HJ (1977) Importance of the colon in enteric hyperoxaluria. New England Journal of Medicine 296: 298–301. Gontzea I and Sutzescu P (1968) Natural Antinutritive Substances in Foodstuffs and Forages, pp. 84–108. Basel: S Karger. Hagler L and Herman RH (1973) Oxalate metabolism I. American Journal of Clinical Nutrition 26: 758–765. Hanson CF, Frankos VH and Thompson WO (1989) Bioavailability of oxalic acid from spinach, sugar beet fibre and a solution of sodium oxalate consumed by female volunteers. Food and Chemical Toxicology 27: 181–184. Linder MC (1991) Nutritional Biochemistry and Metabolism with Clinical Applications, 2nd edn. New York: Elsevier. Massey LK, Roman-Smith H and Sutton RAL (1993) Effect of dietary oxalate and calcium on urinary oxalate and risk of formation of calcium oxalate kidney stones. Journal of the American Dietetic Association 93: 901–906. Meena BA, Umapathy KP, Pankaja N and Prakash J (1987) Soluble and insoluble oxalates in selected foods. Journal of Food Science and Technology 24: 43–44. Noonan SC and Savage GP (1999) Oxalates and its effects on humans. Asia Pacific Journal of Clinical Nutrition 8: 64–74. Ross AB, Savage GP, Martin RJ and Vanhanen L (1999) Oxalates in oca (New Zealand yam) (Oxalis tuberosa Mol.). Journal of Agricultural and Food Chemistry 47: 5019–5022. Sangketkit C, Savage GP, Martin RJ, Mason SL and Vanhanen L (1999) Oxalates in oca: a negative feature? In: Jenson J and Savage GP (eds) Second South West Pacific Nutrition and Dietetic Conference Proceedings, pp. 44–50. Auckland, New Zealand. Strenge A, Hesse A, Bach D and Vahlensieck W (1981) Excretion of oxalic acid following the ingestion of various amounts of oxalic acid-rich foods. In Smith LH, Robertson WG and Finlayson B (eds) Urolithiasis: clinical and basic research, pp. 789–794. New York: Plenum Press. Wanasundera JPD and Ravindran G (1994) Nutritional assessment of yam (Dioscorea alata) tubers. Plant Foods for Human Nutrition 46: 33–39. Zarembski PM and Hodgkinson A (1962) The oxalic acid content of English diets. British Journal of Nutrition 16: 627–634.
OXALATES S C Morrison, New Zealand Institute for Crop and Food Research, Lincoln, Canterbury, New Zealand G P Savage, Lincoln University, Canterbury, New Zealand Copyright 2003, Elsevier Science Ltd. All Rights Reserved.
Introduction 0001
0002
Oxalic acid and its salts occur as end products of metabolism in a number of plant tissues. When these plants are eaten they may have an adverse effect on mineral bioavailability because oxalates bind calcium and other minerals. While oxalic acid is a normal end product of mammalian metabolism, the consumption of additional oxalic acid may cause stone formation in the urinary tract when it is excreted in the urine. The mean daily intake of oxalate in the diet in the UK has been calculated to be 70– 150 mg; tea, rhubarb, spinach, and beet are common high oxalate-containing foods. Soaking and cooking foodstuffs high in oxalate will reduce the oxalate content by leaching. The consumption of high-oxalate foods is more likely to pose health problems in those who have an unbalanced diet or those with intestinal malfunction. A diet high in oxalate and low in essential minerals, such as calcium and iron, is not recommended. Vegans and lactose-intolerant persons may have a high-oxalate and low-calcium diet unless their diet is supplemented. Vegetarians who consume greater amounts of vegetables will have a higher intake of oxalates, which may reduce calcium availability. This may be an increased risk factor for women, who require greater amounts of calcium in the diet. Persons with an increased absorption rate of oxalate are advised to avoid or eat fewer high-oxalate foods to prevent kidney stone formation. In healthy individuals, the occasional consumption of high-oxalate foods as part of a balanced diet does not pose any particular problem.
Oxalates in Plants 0003
0004
Oxalate can be found in small amounts in many plants. Oxalate-rich foods are usually minor components in human diets but are present in higher quantities in seasonal diets in certain areas of the world (particularly in the tropics) as a component of grains, tubers, nuts, vegetables, and fruits. The highest levels of oxalates are found in the foods listed in Table 1. In general, oxalate content is highest in the leaves, then in the seeds, and lowest in the stems. Reports
show that the stems or stalks of plants, such as amaranth, rhubarb, spinach, and beet, contain significantly lower levels of oxalates than the leaves. In the buckwheat family (e.g., rhubarb, sorrel), there is almost twice as much oxalic acid in the leaves as in the stalk. However, in the goosefoot family (e.g., beet, spinach), oxalic acid is more abundant in the stalk than in the petiole of the leaf. It must be noted that the leaves of rhubarb are rarely eaten and therefore the oxalate content of its leaves is of no concern in human nutrition. Oxalic acid concentration tends to be higher in plants than in meats, which may be considered oxalate-free when planning low-oxalate diets. Meats, fats, and dairy products contain very low levels of oxalates. The levels of oxalates in fungi are low when compared to the levels found in spinach and rhubarb. The giant mushroom (Tricholoma giganteum), a large, edible fungi, is reported to contain 89 mg 100 g1 dry weight (DW) oxalic acid while tropical species of mushrooms, including termite and ear mushrooms, contain between 80 and 220 mg oxalate 100 g1 DW. High oxalate levels in tropical plants are of some concern. Taro (Colocasia esculenta) and sweet potato (Ipomoea batatas) were reported to contain 278– 574 mg 100 g1 fresh weight (FW) and 470 mg 100 g1, respectively. Total oxalate levels in yam (Dioscorea alata) tubers were reported in the range 486–781 mg 100 g1 DW, but may not be of nutritional concern since 50–75% of the oxalates were present in the water-soluble form and therefore may leach out during cooking. Oca or New Zealand yam (Oxalis tuberosa Mol.) contains 80–221 mg 100 g1 FW soluble oxalate. Higher levels of oxalates are usually found in the leaves and highest concentrations of oxalate have been found in the skin of these tropical root crops. Peanut greens, commonly consumed in tropical climates, are reported to contain 407 mg 100 g1. Coriander leaf (Coriandrum sativum) contains 1268 mg 100 g1; horsegram (Macrotyloma uniflorum) and santhi (Boernavia diffusa) contain 508 mg 100 g1 and 3800 mg 100 g1 respectively. Nuts such as peanuts, pecans, and cashews are relatively high in oxalates. Sesame seeds have been reported to contain high quantities of oxalate, ranging from 350 to 1750 mg 100 g1 FW. Beverages with a high-oxalate concentration include Indian black tea, cocoa drinks, Ovaltine, cola, and certain types of beer. The oxalic acid content is variable within some species; some cultivars of spinach (Universal, Winter
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OXALATES tbl0001
Table 1 Common foods exhibiting high levels of oxalates Spinach Swiss chard Kale Purslane Collards Mustard and turnip greens
Beet Yam, oca, sweet potato Peanuts, pecans Soybean Wheat germ, wheat bran Sorrel, parsley, amaranth
Giant) contain 400–600 mg 100 g1, while others range from 700 to 900 mg 100 g1. Oxalic acid accumulates in plants, especially during dry conditions. A study comparing two cultivars of spinach, Magic (cv. summer) and Lead (cv. autumn), revealed that the summer cultivar contained greater amounts of oxalate (740 mg 100 g1 FW) than the autumn cultivar (560 mg 100 g1 FW). Oxalate content has been reported to increase as the plant ages and becomes overripe. The proportion of oxalic acid in the leaves of the goosefoot family can double during ripening. However, in tomatoes, oxalic acid content has been reported to decrease during ripening.
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Calcium can combine with oxalate to form calcium oxalate in the intestinal lumen, making the calcium unavailable for absorption; calcium oxalate is then excreted in the feces. Free or soluble oxalate is absorbed by passive diffusion in the colon in humans; comparative studies between healthy individuals and those with ileostomies indicate that the colon is the principal site for oxalate absorption. However, it is suggested that the small intestine may be the major absorptive site rather than the colon. The absorption of oxalates from individual foods varies depending on their dietary conditions and source; in general, the absorption is quite limited. It has been estimated that 2–5% of administered oxalate is absorbed in humans. Experiments have shown that more oxalate is absorbed when consumed while fasting (12%) compared to only 7% oxalate absorption when consumed with a normal diet. The percentage of oxalate absorption varied markedly from 1% for rhubarb and spinach to 22% from tea, but generally absorption was higher at low doses. Oxalate is an end product of ascorbate, glyoxylate, and glycine metabolism in mammals. Thirty-three to fifty percent of urinary oxalate is derived from ascorbate, 40% from glycine and 6–33% from minor metabolic pathways and dietary oxalate; dietary oxalate appears to account for only 10–15% of excreted oxalates.
Rhubarb Gooseberries, strawberries Black tea Cocoa, chocolate, Ovaltine Cola Beer
Chemical Properties and Toxic Effects Oxalic acid forms water-soluble salts with Naþ, Kþ, and NH4þ ions; it also binds with Ca2þ, Fe2þ, and Mg2þ, rendering these minerals unavailable to animals. However, Zn2þ appears to be relatively unaffected. Calcium oxalate (Ca(COO)2) is insoluble at a neutral or alkaline pH, but freely dissolves in acid. Ingestion of 4–5 g of oxalate is the minimum dose capable of causing death in an adult, but reports have shown that 10–15 g is the usual amount required to cause fatalities. Oxalic acid ingestion results in corrosion of the mouth and gastrointestinal tract, gastric hemorrhage, renal failure, and hematuria. Other associated problems include low plasma calcium, which may cause convulsions and high plasma oxalates. Most fatalities from oxalate poisoning are apparently due to the removal of calcium ions from the serum by precipitation. High levels of oxalate may interfere with carbohydrate metabolism, particularly by succinic dehydrogenase inhibition; this may be a significant factor in death from oxalate toxicity induced in animals grazing pastures containing high levels of Halogeton glomeratus. Halogeton (H. glomeratus) and wood sorrel (Oxalis cernua) are high in oxalates and are known to cause injury to grazing cattle and sheep. Although garden sorrel is a herb and not normally consumed in large quantities, there has been one report of fatal oxalate poisoning after a man consumed an estimated 6–8 g oxalate in vegetable soup containing 500 g sorrel. Both fatal and nonfatal poisoning by rhubarb leaves is thought to be caused by toxic anthraquinone glycosides rather than oxalates. Experiments involving the consumption of more than 30–35 g day1 of cocoa, a high-oxalate foodstuff, by eight women provoked symptoms of intoxication including loss of appetite, nausea, and headaches. However, cocoa contains theobromine (1500–2500 mg 100 g1) and tannic acid (4000– 6000 mg 100 g1), both of which are more toxic than the oxalic acid present (500–700 mg 100 g1). There appears to be a great deal of confusion as to what was responsible for these poisonings and it would be unwise to assume that only one factor was responsible.
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Effect on Bioavailability of Minerals 0015
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High-oxalate foods have been known to inhibit calcium and iron absorption. Even though vegetables such as spinach, rhubarb, and Swiss chard are high in calcium, the calcium cannot be absorbed due to the presence of oxalates in these vegetables. When calcium absorption from spinach, a high-oxalate and high-calcium food, was compared with calcium absorption from milk, a high-calcium food, the results showed that the calcium from spinach is not readily available (only 5.1% absorbed), probably due to the high content of oxalates. The adverse effect of oxalates is greater if the oxalate-to-calcium ratio exceeds 9:4 (or approximately 2). The oxalate-tocalcium ratio in a food varies widely and can be classified into three groups, as summarized in Table 2. Oxalate and calcium levels and the oxalate-tocalcium ratio of specific foods are detailed in Table 3. Foods that have a ratio greater than two, as well as containing no utilizable calcium, have excess oxalate, which can bind calcium in other foods eaten at the same time. Foodstuffs with a ratio of about one do not encroach on the utilization of calcium provided by other products and therefore do not exert any demineralizing effects. However, these foods are not good sources of calcium. Although parsley (Petroselinum sativum) contains average levels of oxalate (140–200 mg 100 g1), its high calcium levels (180– 290 mg 100 g1) reduce the oxalate-to-calcium ratio to a low level. Oxalate appears to interfere only slightly with zinc absorption. A counteracting or protective mechanism may prevent the precipitation of zinc by oxalates. Increasing the proportion of magnesium ions in solution was reported to inhibit the binding of calcium and zinc oxalates. This observation explains the minor effect oxalates have on zinc absorption from some leafy vegetables, such as spinach, which has high levels of calcium and zinc, and relatively high levels of magnesium. Oxalic acid may cause greater decreases in mineral availability if consumed with a high-fiber diet but the decrease may be only temporary. Negative calcium, magnesium, zinc, and copper balances were detected in males consuming a diet containing fiber and oxalates. When spinach was replaced by cauliflower, a
low-oxalate vegetable, fiber had no effect on the minerals studied, indicating that the apparent negative balances obtained were due to the presence of oxalic acid.
Adverse Effects of Oxalates Acute
A number of plants contain calcium oxalate crystals (measured as insoluble oxalate). When ingested, they are not absorbed into the blood stream and remain largely undissolved within the digestive tract, so they have no systemic toxicity, but the sharp raphide crystals can penetrate the tissues of the mouth and the tongue, causing considerable discomfort. Most of the plants that contain calcium oxalate crystals are members of the arum family. It has been suggested that calcium oxalate crystals are responsible for the irritating sensation in kiwi fruit (Actinidia sp.) and soluble oxalates are thought to account for the bitter taste present in some oca (O. tuberosa Mol.). Conophor seeds (Tetracarpidium conophorum) are a popular Nigerian snack, which have a bitter taste when raw but are palatable when cooked. This observation was correlated with a 73% decrease in total oxalate concentration after cooking.
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Oxalate is poorly absorbed under nonfasting conditions. Once absorbed free oxalate binds to calcium ions to form insoluble calcium oxalate, it remains in the insoluble form. Free oxalate and calcium can precipitate in the urine and may form kidney stones. These stones consist mainly of calcium oxalate (80%), which is relatively insoluble in urine, and calcium phosphate (5%). Oxalate crystallizes with calcium in the renal vasculature and infiltrates vessel walls causing renal tubular obstruction, vascular necrosis, and hemorrhage, which lead to anuria, uremia, electrolyte disturbances, or even rupture. Kidney stones are becoming more common in men between the ages 30 and 50 years in industrialized countries. The risk factors involved in stone formation are a low volume of urine, increased urinary excretion of oxalate, calcium, or uric acid, a persistently low or high urinary
Table 2 Examples of plants with varying oxalate to calcium ratios Oxalate-to-calciumratio
Examples
Group 1: Plants with a ratio greater than 2 Group 2: Plants with a ratio of approx. 1 Group 3: Plants with a ratio less than 1
Spinach, rhubarb, beet, sorrel, cocoa Potatoes, amaranth, gooseberries, currants Lettuce, cabbage, cauliflower, green beans, peas
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Table 3 Oxalate, calcium, and oxalate-to-calcium ratio (Ox:Ca) of some common foods Foodstuff
Group 1 Rhubarb (Rheum rhaponticum) cv. Victoria, forced, stewed raw Common sorrel (Rumex acetosa) Red beetroot (Beta vulgaris) Garden sorrel (Rumex patientia) Pig spinach (Chenopodium spp.) Purslane (Portulaca oleracea) Spinach (Spinacia oleracea) Garden orach (Atriplex hortensis) New Zealand spinach (Tetragonia expansa) Coffee (Coffea arabica) Cashew (Anacardium occidentale) Cocoa (Theobroma cacao) Beet leaves (Beta vulgaris var. cicla) Rhubarb (Rheum rhaponticum) cv. Crimson, end of season, stewed Group 2 Potato (Solanum tuberosum) Amaranth (Amaranthus polygonoicles) Tea (Thea chinensis) Amaranth (Amaranthus tricolor) Rhubarb (Rheum rhaponticum) cv. Victoria, end of season, stewed Group 3 Apple (Malus spp.) Blackcurrant (Ribes nigrum) Tomato (Lycopersicum esculentum) Parsley (Petroselinum sativum) Cabbage (Brassica oleracea) Lettuce (Lactuca sativa)
Oxalate (mg 100 g1FW)
Calcium (mg 100 g1FW)
Ox:Ca ratio
Range
Range
Mean
(mmoll1)
12.4 45 40 275 45 99 125 101 100 100 12 41 125 110
9.32 7.95 5.56 5.09 4.94 4.94 4.60 4.27 4.00 3.96 3.70 2.50 2.49 2.46
91.5
2.23
275–1336 270–730 121–450 300–700 910–1679 320–1260 300–1500 50–150 500–900 300–920
Mean
260 805 500 275 500 1100 1294 970 900 890 100 231 700 610
40–50 35–45 121–450 40–50 13–236 80–122
10–15 100–150 100–120
460 20–141 300–2000
80 1586 1150 1087
10–34 400–500
620 0–30 2–90 5–35 140–200 0–125 5–20
15 50 20 170 60 12
5–15 19–50 10–20 180–290 200–300 73–90
22 595 450 453
1.62 1.18 1.14 1.07
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1.04
10 35 15 235 250 81
0.67 0.63 0.58 0.32 0.11 0.07
FW, fresh weight. Adapted from Zarembski PM and Hodgkinson A (1962) The oxalic acid content of English diets. British Journal of Nutrition 16: 627–634; Gontzea I and Sutzescu P (1968) Natural Antinutritive Substances in Foodstuffs and Forages, pp. 84–108. Basel: S Karger; Meena BA, Umapathy KP, Pankaja N and Prakash J (1987) Soluble and insoluble oxalates in selected foods. Journal of Food Science and Technology 24: 43–44; Noonan SC and Savage GP (1999) Oxalates and its effects on humans. Asia Pacific Journal of Clinical Nutrition 8: 64–74 with permission.
pH, and a low concentration of urinary inhibitors, such as magnesium, citrate, and high-molecularweight polyanions. Normal urine is usually supersaturated with calcium oxalate. The normal urinary excretion of oxalate is less than 40–50 mg day1 with less than 10% coming from the diet. Intakes of oxalate exceeding 180 mg day1 lead to a marked increase in the amount excreted. Small increases in oxalate excretion have pronounced effects on the production of calcium oxalate in the urine, implying that foods high in oxalate can promote hyperoxaluria (high oxalate excretion) and increase the risk of stone formation. Rhubarb, spinach, beet, nuts, chocolate, tea, coffee, parsley, celery, and wheat bran cause significant increases in urinary oxalate excretion in healthy individuals and have been identified as the main dietary sources in the risk of kidney stone formation. It
has been reported that black tea increased oxalate excretion by only 7.9%, compared with increases of 300% and 400% for spinach and rhubarb, respectively. Therefore 2–3 cups a day of black tea would have little effect on the risk of urinary stone formation when compared to spinach and rhubarb. It appears that tea is a significant source of oxalate intake in UK diets. The main reason for the strong relationship between the risk of calcium stones and urinary oxalate excretion appears to be the effect that the latter has on the supersaturation of urine with calcium oxalate. The amount of oxalate excreted in the urine was higher in individuals with kidney stones than in healthy individuals, suggesting that those with kidney stones absorb more oxalate, consume more oxalate or oxalate-producing substances such as ascorbate, or metabolize more oxalate precursors. Excessive or
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increased absorption of oxalate from normal diets is the result of intestinal abnormalities or malfunction. This is termed ‘enteric hyperoxaluria’ and is the commonest cause of increased renal oxalate excretion. It has been indicated that people with abnormal gastrointestinal absorption are at greater risk for hyperoxaluria and, as a result, kidney stone formation, than healthy individuals and should reduce their intake of oxalate and its precursors, such as ascorbate. A lowoxalate diet has prevented stone formation in some cases involving gastrointestinal disorders associated with hyperoxaluria. An increase in calcium intake should be accompanied by a lower oxalate consumption, because a lowcalcium and high-oxalate diet enhances oxalate absorption and excretion, which carries an even greater risk of stone formation than high calcium excretion. An increase in calcium intake may reduce urinary oxalate excretion by binding to more oxalate in the gut, thus reducing the risk of stone formation. Varying the amounts of calcium does not significantly alter levels of urinary calcium. From experimental work, it has been concluded that hypercalciuria plays, at most, a secondary role in the formation of calcium stones compared with mild hyperoxaluria. Excessive ascorbic acid (vitamin C) intake may increase urinary oxalate output with an increased risk of forming kidney stones. An excess dose is considered to be 2000 mg of vitamin C per day. However, ascorbic acid doses greater than 500 mg day1 were reported to induce a significant increase in urinary oxalate, and doses of 1000 mg day1 would increase urinary oxalate excretion by 6–13 mg day1. The recommended daily intake in many countries is in the region of 80 mg.
Effects of Processing 0026
Oxalates may be removed from food by leaching in water but this is not the most effective method as it removes only the soluble oxalate. Although the amount of oxalate in raw soybean (Glycine max) is relatively low, soaking and germination of the seed reduced the oxalate concentration. Cooking germinated soybeans reduced oxalate concentration below that in uncooked germinated soybeans. Soaking followed by cooking also proved to be effective, although not as effective as germination. Oxalate content in horsegram seeds (M. uniflorum) decreased by 38% when seeds were dehulled (508 and 315 mg 100 g1, for seed and dehulled seed, respectively). Roasting was found to be the least effective method. Roasting chicory roots was reported to increase oxalate content. Roasting oca (New Zealand yam,
O. tuberosa Mol.) also increased oxalate levels by 10–26%. This may be caused by the decrease in moisture content, a hypothesis supported by reports of dry tropical leafy vegetables having higher oxalate concentrations than fresh vegetables. A 40–50% loss of total oxalates by leaching was reported when yam tubers (D. alata and D. esculenta) were boiled, compared to steaming (20–25%) and baking (12–15%). Cooking proved most effective in reducing total oxalates. However, it must be noted that water-soluble minerals also leach out at the same time. Mineral leaching appears to vary between plant species. Blanching has been reported to decrease the oxalic acid content in spinach. However blanching, by conventional and microwave methods, reduced the oxalic acid content of sweet potato, peanut, and collard leaves only slightly whereas other antinutritional factors such as tannic and phytic acid were reduced significantly. Spinach, orach, and silverbeet are generally eaten after being boiled. However, rhubarb, cocoa, and common and garden sorrel may be consumed in the raw state and therefore should be eaten in smaller quantities. Fermentation, frequently used in Asian countries, has been reported to decrease the oxalate content of foods. A marked decrease in oxalic acid content was reported in Icacinia manni (a starch tuber) after fermentation. Oxalic acid was observed to decrease by 37% (86 to 54 mg 100 g1 FW) during souring of poi (a cooked taro paste) at 20 C.
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Recommendations Foods high in oxalates should be consumed in moderation to insure optimum intake of minerals from the diet. Although some foods are reported to be high in calcium and other essential minerals, the amount available may be limited due to the presence of oxalates. For instance, spinach is a high-calcium food, yet because of its high oxalate content, the calcium availability is almost negligible. The availability of magnesium, iron, sodium, potassium, and phosphorus may also be restricted. High-oxalate foods should be cooked to reduce the oxalate content. Soaking raw foods will also reduce the oxalate content but other useful nutrients such as water-soluble vitamins and minerals may also be lost at the same time. Oxalates tend to occur in higher concentrations in the leafy parts of vegetables rather than in roots or stalks. For the general population, the occasional consumption of high-oxalate foods as part of a balanced diet does not pose any health problems. However, there are some groups of people who may be at risk from oxalate-induced side-effects.
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Vegans and vegetarians should be aware that some foods contain high levels of oxalates. The diets of vegans and those persons with lactose intolerance may be low in calcium as a result of the exclusion of dairy products, unless their diet is supplemented by some other high-calcium food products. It is recommended that high-oxalate foods should be accompanied by calcium-rich foods such as dairy products and shellfish. If high-oxalate foods are consumed in conjunction with a low-calcium diet, then the consumer may be at risk of hyperoxaluria, which may lead to kidney stone formation. Women tend to be more susceptible to calcium and iron deficiencies than men. Osteoporosis is a concern amongst females, especially after menopause. People suffering from fractures should also be aware of the potential effects of oxalates on mineral availability, as high calcium levels are required for bone repair. Once again, consumption of high-oxalate foods with an adequate-to-high calcium intake should pose no health problems. It must also be noted that calcium is only absorbed and used when there are adequate levels of vitamin D in the body, either obtained via the diet or synthesized by the body when exposed to sunlight. Women should eat red meats, which are low in oxalate, to satisfy their iron intake. Adequate levels of vitamin C are required for the absorption of iron, but excess amounts are not advised because ascorbic acid is converted into oxalate. The risk of stone formation is three times greater in males and they should avoid eating excess amounts of high-oxalate foods. Sufferers of hyperoxaluria and kidney stones are advised to restrict their diet to foods containing low or medium levels of oxalates, as although urinary oxalate arises predominantly from endogenous sources, it can be influenced by dietary intake. Excess vitamin C intake is not recommended in these patients. Inhabitants of tropical countries should be aware that leafy tropical plants and tropical root crops tend to contain higher levels of oxalates than plants from temperate climates. People living in these areas are at possible risk of stone formation due to hyperoxaluria, and mineral deficiencies if sufficient minerals are not consumed. See also: Ascorbic Acid: Properties and Determination Physiology; Calcium: Properties and Determination; Physiology; Iron: Properties and Determination; Physiology; Plant Antinutritional Factors:
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Characteristics; Renal Function and Disorders: Nutritional Management of Renal Disorders; Toxins in Food – Naturally Occurring
Further Reading Concon JM (1988) Food Toxicology – Principles and Concepts, pp. 416–419. New York: Marcel Dekker. Dobbins JW and Binder HJ (1977) Importance of the colon in enteric hyperoxaluria. New England Journal of Medicine 296: 298–301. Gontzea I and Sutzescu P (1968) Natural Antinutritive Substances in Foodstuffs and Forages, pp. 84–108. Basel: S Karger. Hagler L and Herman RH (1973) Oxalate metabolism I. American Journal of Clinical Nutrition 26: 758–765. Hanson CF, Frankos VH and Thompson WO (1989) Bioavailability of oxalic acid from spinach, sugar beet fibre and a solution of sodium oxalate consumed by female volunteers. Food and Chemical Toxicology 27: 181–184. Linder MC (1991) Nutritional Biochemistry and Metabolism with Clinical Applications, 2nd edn. New York: Elsevier. Massey LK, Roman-Smith H and Sutton RAL (1993) Effect of dietary oxalate and calcium on urinary oxalate and risk of formation of calcium oxalate kidney stones. Journal of the American Dietetic Association 93: 901–906. Meena BA, Umapathy KP, Pankaja N and Prakash J (1987) Soluble and insoluble oxalates in selected foods. Journal of Food Science and Technology 24: 43–44. Noonan SC and Savage GP (1999) Oxalates and its effects on humans. Asia Pacific Journal of Clinical Nutrition 8: 64–74. Ross AB, Savage GP, Martin RJ and Vanhanen L (1999) Oxalates in oca (New Zealand yam) (Oxalis tuberosa Mol.). Journal of Agricultural and Food Chemistry 47: 5019–5022. Sangketkit C, Savage GP, Martin RJ, Mason SL and Vanhanen L (1999) Oxalates in oca: a negative feature? In: Jenson J and Savage GP (eds) Second South West Pacific Nutrition and Dietetic Conference Proceedings, pp. 44–50. Auckland, New Zealand. Strenge A, Hesse A, Bach D and Vahlensieck W (1981) Excretion of oxalic acid following the ingestion of various amounts of oxalic acid-rich foods. In Smith LH, Robertson WG and Finlayson B (eds) Urolithiasis: clinical and basic research, pp. 789–794. New York: Plenum Press. Wanasundera JPD and Ravindran G (1994) Nutritional assessment of yam (Dioscorea alata) tubers. Plant Foods for Human Nutrition 46: 33–39. Zarembski PM and Hodgkinson A (1962) The oxalic acid content of English diets. British Journal of Nutrition 16: 627–634.