Food science

Food fortification: A tool for fighting hidden hunger
A lesser-known grain, Chenopodium quinoa: Review of the chemical composition of its edible parts

Food fortification: A tool for fighting hidden hunger

Alberto Nilson and Jaime Piza

Alberto Nilson is based in São Paulo, Brazil, and is Director of the Regional Center for Latin America of the Vitamin Division of F. Hoffmann-La Roche Ltd., Basel, Switzerland. Jaime Piza is based in San Jose, Costa Rica, and is Manager for Central America and the Caribbean of the Vitamin Division of F. Hoffmann-La Roche.

This paper was presented at the Latin American Congress of Nutrition in Guatemala on November 12, 1997.

This paper reviews the fortification of staple food as a tool to prevent micronutrient deficiencies. The rationale for fortifying salt, wheat flour, milk, and margarine was developed in the 1920s and 1940s, mainly in industrialized countries. At that time, fortification of staple foods was considered by only a few developing countries. Recent research has shown that the prevalences of some deficiencies (clinical and marginal) in some developing countries are higher than expected. Even more important has been the realization that the impact of marginal deficiencies on health and socio-economic development is considerably more important than the impact of clinical deficiencies. Iron, vitamin A, and iodine have gained more attention, but deficiencies of other micronutrients are also relevant. This paper shows that fortification of staple foods to prevent micronutrient deficiencies is effective, easy, fast, safe, and relatively inexpensive.

Introduction

The scientific rationale, including technology, stability, interactions, and effectiveness, for fortifying staple foods was developed early this century. In the 1920s and 1940s fortification of salt with iodine, fortification of wheat flour with iron, vitamins B₁ and B₂, and niacin, fortification of milk with vitamins A and D, and fortification of margarine with vitamins A and D were fully evaluated and included as part of national intervention programmes in several countries. For whatever reason, these strategies were adopted only by some developed countries.

In the following decades, developing countries gave their attention mainly to clinical deficiencies, using the medical approach of supplementing the population at highest risk as soon as symptoms appeared. The most challenging problems have been xerophthalmia, anaemia, and goitre. Consequently, attention to other micronutrients has been practically nil.

Later research has shown that marginal deficiency is even more important than clinical deficiency, as it covers larger percentages of the population. Evidence has been accumulating showing the enormous impact of marginal deficiencies of vitamin A on infant and maternal mortality and morbidity, of iron on IQ in children and working capacity in the whole population, and of folic acid on neural tube defects.

Furthermore, there is growing evidence that micronutrients interact positively with each other. For example, vitamin C improves the absorption of non-haem iron from foods or supplements, and vitamin A together with supplementary iron is more effective than iron alone in reducing the prevalence of iron deficiency.

Although not the objective of this paper, it is worth mentioning that an adequate intake of some micronutrients, mainly vitamins E and C, sometimes at levels higher than the established recommended dietary allowances (RDAs), may play an important role in reducing the prevalence of cancer, cardiovascular diseases, and other health problems.

The above facts and the cost of potential intervention programmes show that the cost-benefit ratio of such programmes is highly favourable, motivating the scientific community, international agencies, and governments to seek alternatives for preventing micronutrient deficiencies through supplementation, fortification, and dietary diversification.

Staple foods such as wheat flour, milk, and margarine traditionally have been considered for fortification. Recent research has looked at alternative vehicles for one or more micronutrients, such as rice, oils, tea, maize, weaning foods, beverages, and foods for complementary feeding programmes [1].

Some more recent successful examples of efforts to prevent deficiencies include fortification of sugar with vitamin A in Central America, fortification of precooked corn flour with vitamins A, B₁ and B₂, and niacin and iron in Venezuela, and fortification of a milk substitute and biscuits with several micronutrients as part of the complementary feeding programmes in Peru.

It is also worth mentioning the fortification efforts of the food industry. Some examples are the fortification of milk with iron in Argentina and Brazil, fortification of noodles with iron and vitamin A in Thailand and the Philippines, and fortification of chocolate powder for milk with iron and several vitamins in Mexico.

Micronutrient deficiencies

Micronutrient malnutrition is a widespread problem throughout the world that has both health and economic consequences. The latest estimates show that 254 million children suffer from clinical and marginal vitamin A deficiency [2], 2.2 billion people, mainly children and pregnant women, suffer from iron deficiency [3], and 1 billion suffer from iodine deficiency [4].

Furthermore, there is some evidence that the prevalence of other micronutrient deficiencies could be much higher than expected. Table 1 shows a recent compilation, by Dr. José Mora, of the evidence available on micronutrient deficiencies in Latin America, confirming the high prevalence of vitamin A, iron, and iodine deficiencies. Despite the lack of information on other micronutrients, there is enough information to suggest that there could be a regional problem, at least for some groups or in some regions, for vitamin B₂, niacin, folic acid, calcium, zinc, and even vitamin C. If a micronutrient is not mentioned in table 1, it is not necessarily because there is no problem, but rather that there is a lack of information.

Global commitment

In 1990, at the World Summit for Children, WHO, UNICEF, and the US Agency for International Development set specific micronutrient goals for the year 2000. These goals were unanimously confirmed by 159 countries at the International Conference on Nutrition held in December 1992 in Rome [5], and a plan of action was adopted. These objectives are to:

» virtually eliminate vitamin A deficiency;

» virtually eliminate iodine deficiency;

» reduce iron-deficiency anaemia by one-third of the 1990 levels;

» pay attention to other micronutrient deficiencies, such as B-complex vitamins, vitamin C, zinc, and calcium.

Fortification

The results of fortification are fast, broad, and sustainable. The nutrient intakes of the targeted group improve immediately, and an impact on micronutrient status can be detected within one to three months. When a staple food that is consumed regularly by the majority of the population is used as a fortification vehicle, high population coverage can be easily achieved.

TABLE 1. Evidence of micronutrient deficiencies in Latin America

Country	National deficiency	Deficiency in certain areas	Deficiency in certain groups	Widespread low intake
Argentina	Fe	I	Fe	Vitamins A, C, E
Bolivia	Fe	I, vitamin C	Vitamin A	Ca, vitamins B1, B2, niacin
Brazil	Fe	I, vitamin A	Vitamin A	Vitamins B2, E
Chile			Fe	Ca, vitamins B1, B2, B6, C
Colombia	Fe	I		Vitamins A, B1, B2, niacin
Costa Rica		I
Dominican Republic	Fe, vitamin A, folate	I
Ecuador	Fe, vitamins A, B2, niacin	Zn	Zn
El Salvador	Fe, vitamin A, I
Guatemala	Fe, vitamin A	I
Honduras	Fe, vitamin A	I
Mexico	Fe, vitamin B2	I, Ca, niacin	Vitamin C, folate	Vitamins A, B1, B2, C, niacin, Zn
Nicaragua	Fe, vitamin A	I		Vitamin B1 niacin
Panama	Fe	I	Vitamin A
Peru	Fe, I	Vitamin A	Folate, vitamin B12, Zn	Ca, vitamins B1, B2

Fortification vehicles

To ensure that the most vulnerable members of the population benefit from food fortification, the food vehicle(s) must be staple food(s) consumed throughout the year by a large proportion of the population at risk. In order to reach different segments of the population who have different diets, it may be more effective to select more than one food vehicle.

When selecting a staple food as a suitable vehicle for compulsory fortification with micronutrients, the following generally accepted criteria must be met [6]:

» The food selected as a vehicle should be consumed by the population at risk.

» The intake of the food should be stable and uniform; the upper and lower levels of intake should be known.

» The essential nutrient(s) should be present in amounts that are neither excessive nor insignificant, taking into account intakes from other dietary sources.

» The amount of essential nutrient(s) should be sufficient to correct or prevent the deficiency when the food is consumed in normal amounts by the population at risk.

» The nutrient(s) added should not adversely affect the metabolism of any other nutrients.

» The nutrient(s) added should be sufficiently stable in the food under customary conditions of packing, storage, distribution, and use.

» The nutrient(s) added should be physiologically available from the food.

» The nutrient(s) added should not impart undesirable characteristics to the food (changes in colour, taste, smell, texture, or cooking properties) and should not unduly shorten the shelf life.

» The technology and processing facilities should be available to permit addition of the nutrient(s) in a satisfactory manner.

» The additional cost to the consumer resulting from the fortification should be reasonable.

» Methods of measuring, controlling, and enforcing the levels of the essential nutrient(s) added to food should be available.

In 1923 Switzerland was the first country to fortify salt with iodine to prevent goitre and cretinism, which were widespread throughout the Alpine region. The initiative was later followed by the United States in 1930 [6].

Rickets, caused by vitamin D deficiency, was once common in young children in the northern hemisphere because of the lack of sunshine in the winter months and the low consumption of this vitamin. In 1923 the United Kingdom and the United States started fortifying milk with vitamin D to prevent rickets [6].

Margarine was the first substitute or imitation food produced on a large industrial scale. Its introduction in Denmark in 1910 led to widespread clinical deficiency of vitamin A in children (xerophthalmia). It was soon recognized that to be nutritionally equivalent to butter, margarine had to be fortified with vitamin A, eliminating xerophthalmia in Denmark. Vitamin D was added later [7].

Before 1933 the population of Newfoundland suffered from multiple nutrient deficiencies. The government, aware of the micronutrient losses during wheat milling, banned the consumption of white wheat flour in order to preserve the nutritional value of wheat. However, the population did not like to consume whole-wheat flour, and the programme failed to achieve the expected results. In 1944 the government started fortifying white wheat flour with vitamins B₁ and B₂, niacin, and iron and fortifying margarine with vitamin A. The results were remarkable. Various clinical symptoms and indications of vitamins A and B deficiencies, such as skin follicular changes, eye hyperaemia, and magenta tongue, were substantially reduced or eliminated. Beriberi was eliminated completely (fig. 1), and infant mortality in the first year of life fell from 102/1,000 live births in 1944 to 61 in 1947. The biochemical indicators of deficiency of vitamins A, B₁ and B₂ improved dramatically as well (fig. 2).

FIG. 1. Effect of enrichment of flour on beriberi in Newfoundland, 1931-49. Source: ref. 8

FIG. 2. Biochemical deficiencies of vitamins in Newfoundland before (1944: grey bars) and after (1948: black bars) enrichment of flour. Source: ref. 8

FIG. 3. Effect of enrichment of flour on deaths from pellagra in the United States, 1938-54. Source: ref. 9

In the United States during the late 1930s, pellagra caused more than 3,000 deaths annually, mainly in the southern states among a population relying on maize as the main staple food. In 1938, three years before the mandatory introduction of flour enrichment, bakers voluntarily began enriching flour with B vitamins and iron. This measure was associated with a rapid and dramatic decline in pellagra mortality to zero by 1954 (fig. 3).

The introduction of polished rice in the Philippines at the turn of the century led to large outbreaks of beriberi. In 1947, in the Province of Bataan, more than 12% of the population was affected by the disease. The distribution of thiamine-fortified rice began on October 1,1948. This measure was followed by a spectacular reduction in deaths from beriberi from 254/100,000 to 80 (fig. 4).

Fortification of sugar with vitamin A was initiated in Guatemala in 1974. Sugar was selected because researchers from the Institute of Nutrition of Central America and Panama (INCAP) realized that there was no other staple food reaching all target groups in the country. The prevalence of deficient retinol plasma levels in children (less than 10 µg per 100 ml) was reduced from 3.3% to less than 0.2% within two years (fig. 5).

In 1993 Venezuela started fortifying pre-cooked yellow and white corn flour with vitamins A, B₁, and B₂, niacin, and iron. At the same time wheat flour was fortified with vitamins B₁ and B₂ niacin, and iron. These two cereals were selected as vehicles because they accounted for 45% of the total caloric intake of the population. A survey carried out in Caracas on 397 children showed that the prevalence of iron deficiency (as measured by serum ferritin concentration) and the prevalence of anaemia were reduced from 37% and 19%, respectively, in 1992 to 15% and 10% in 1994 [12].

In 1994 Guatemala revised the fortification of wheat flour, previously fortified with vitamins B₁ and B₂, niacin, and iron, to include folic acid, on the basis of available information on the high prevalence of deficiency of this vitamin and its function in preventing foetal neural tube defects and some anaemias. This measure was later followed by nearly all Central American countries.

In 1998 the United States will include folic acid in the fortification of wheat flour (1.54 mg/kg flour) in order to prevent the high prevalence of pregnancies affected by spina bifida and other neural tube defects. Most of the newborns affected by this problem die. The US Public Health Service has recommended that women of childbearing age consume at least 400 µg of folic acid daily to prevent neural tube defects [13].

Several technologies are available for fortifying rice. Using the technology of simulated kernels, Dr. H. Flores demonstrated in Recife, Brazil, that consumption of fortified rice for one month had the same effect as a single dose of 200,000 IU of vitamin A in improving serum retinol levels in children (fig. 6) [14].

FIG. 4. Effect of enrichment of rice on deaths from beriberi in Bataan, Philippines, 1947-50. Grey bars: experimental area; black bars: control area. Source: ref. 10

FIG. 5. Effect of enrichment of sugar with vitamin A on plasma levels of retinol in children in Guatemala, 1975-77. Source: ref. 11

Foods supplied to the population as part of complementary feeding programmes can be excellent vehicles for micronutrients. In the Peruvian School Lunch Program, started in 1993, children receive 100 g of biscuits fortified with vitamins B₁, and B₂, niacin, and iron and a glass of a milk substitute fortified with vitamins A, B₁, B₂, B₁₂, and C niacin, folic acid, iron, zinc, and iodine. In Huancayo, one of the regions covered by the programme, the prevalence of anaemia (haemoglobin less than 13 g/dl, considering altitude) was reduced from 68% to 18% in six months [15].

In 1996 Colombia, Bolivia, and Ecuador started fortification of wheat flour with vitamins B₁, and B₂, niacin, folic acid, and iron. Fortification of wheat flour with iron and B-complex vitamins and fortification of sugar with vitamin A are being considered by many other countries.

FIG. 6. Effect of fortification of rice with vitamin A (grey bars) in comparison with effect of supplementation with vitamin A (black bars) on serum retinol levels in Brazil. Source: ref. 14

Fortification with several micronutrients

Because diets are seldom deficient in one micronutrient alone, as shown in table 1, combinations of micronutrients increase the cost-effectiveness of fortification even further by addressing more than one deficiency through the same food.

Furthermore, there are several positive interactions among micronutrients. This is especially true for anaemia, where the role of folate, as well as iron, is well known [16], and there is also enough evidence of the high prevalence of folate deficiency in Latin America, mainly in pregnant women.

Fortification of sugar with vitamin A brought an unexpected finding in Guatemala. As well as reducing the prevalence of vitamin A deficiency, the fortification programme reduced the prevalence of anaemia [17].

A recent study in Indonesia showed that supplementation of pregnant women with iron and vitamin A was significantly more effective in controlling anaemia than supplementation with iron alone (fig. 7).

There is ample evidence that vitamin C plays an important role in improving absorption of non-haem iron. Dr. A. Stekel reported that feeding children for 15 months with milk fortified with 15 mg/L of iron as ferrous sulphate reduced the incidence of anaemia from 36% in the control group to 13% in the fortified group [19]. A more significant reduction was found in children given milk fortified with the same amount of iron and 100 mg of vitamin C per liter, which reduced the prevalence of anaemia from 28% in the control group to 2% in the fortified group (fig. 8).

Fortification technologies

As shown in table 2, technologies exist for fortifying staple foods [20]. For most foods, the technology is quite simple. The water-soluble vitamins can be dissolved in water and then added to liquid foods such as dairy products, fruit juices, and beverages, or they can be mixed in powdered form directly with foods such as wheat flour, corn flour, corn starch, instant powdered beverages, and dry milk. The fat-soluble vitamins can be added directly to foods such as dressing oils, margarine, mayonnaise, and recombined milk. The industry has been able to microencapsulate the fat-soluble vitamins in order to get them into a water-soluble powdered form and to protect them from oxygen and other components of foods. These powdered forms can be mixed with the water-soluble vitamins and added to foods, as described before.

FIG. 7. Effect of supplementation with iron and vitamin A on anaemia in pregnant women in Indonesia. Source: ref. 18

FIG. 8. Effect of enrichment of milk with iron and vitamin C on anaemia in children during the first 15 months of life. Source: ref. 19

Fortification of rice and sugar requires more complex technologies. Vitamin A in powdered form is adhered to the sugar crystals with vegetable oil. Vitamins are sprayed on the rice kernels, which are then coated with appropriate food-grade resins to avoid leaching the vitamins when the rice is washed before cooking. Alternatively, simulated kernels can be produced by technologies similar to the those used for noodles. In this case, the vitamins and minerals in powdered form are mixed with the flour used to produce the simulated kernel.

Stability

Vitamins can be affected by oxygen, humidity, heat, acids, redox agents, and light. Furthermore, other components of foods, such as heavy metals, can interfere with the stability of some vitamins. The technology exists to prevent losses, but losses cannot be totally avoided. To ensure that the food contains the declared vitamin levels when it is ingested, the food industry adds extra nutrients to compensate for losses during processing and over the shelf life of the finished product.

TABLE 2. Staple foods that can be fortified

Food

Vitamins

Minerals

b-Carotene

A

D

E

B1

B2

B6

C

Niacin

Folic acid

B12

Fe

Ca

Milk

Liquid

+

+

+

+

+

+

+

+

+

+

+

0

+

Powder

+

+

+

+

+

+

+

+

+

+

+

+

+

With cereal

+

+

+

+

+

+

+

+

+

+

+

+

+

Flour

Wheat

0

+

+

+

+

+

+

x

+

+

+

+

+

Corn

0

+

+

+

+

+

+

0

+

+

+

+

+

Cassava

0

0

0

0

0

0

0

0

0

0

0

0

0

Rice

0

+

+

+

+

+

+

+

+

+

+

+

+

Rice

0

+

+

+

+

+

+

+

+

+

+

+

+

Snacks

0

+

+

+

+

+

+

+

+

+

+

+

+

Corn flakes

0

+

+

+

+

+

+

+

+

+

+

+

+

Oil

+

+

+

+

Margarine

+

+

+

+

0

0

0

0

0

0

0

x

0

Mayonnaise

+

+

+

+

0

0

0

0

0

0

0

0

0

Juices

+

0

0

+

+

+

+

+

+

+

+

+

+

Sugar

+

Powdered beverages

0

+

+

+

+

+

+

+

+

+

+

+

+

Source: ref. 20.
+, Possible; o, trials needed; x, not possible.

Figure 9 shows that vitamin A is very stable when microencapsulated in powdered form and added to different flours, even when the flours are fortified with iron at the same time. When wheat flour is fortified, the typical losses during the production of bread and biscuits are 30% to 40% for vitamin A, 20% to 30% for vitamin B₁, 15% to 20% for vitamin B₂, 5% to 10% for niacin, and 15% to 20% for folic acid.

Figure 10 shows the stability of vitamins in pre-cooked corn flour during the production of arepas (corn bread), according to results from our laboratories in Switzerland. It is worth mentioning that the flour was also fortified with iron.

Bioavailability

It is generally recognized that the bioavailability of vitamins added to foods is about the same as for those originally present in foods. Carotenoids and iron, however, require more attention. b-Carotene present in foods is less bioavailable than b-carotene added as a colour or fortificant. The bioavailability of iron depends on several factors. For reduced iron, the most important factor is the mesh size of the form used, the smallest size being the best. Figure 11 shows the relative bioavailability of some typical forms of iron used to fortify foods. As mentioned before, vitamin C significantly improves the bioavailability of non-haem forms of iron.

When selecting the form of iron to be used in the fortification of a food, in addition to its relative bioavailability, the food industry has to consider its cost and potential interactions with the food. Table 3 shows the relative cost of typical forms of iron.

FIG. 10. Stability of vitamins in pre-cooked corn flour (grey bars) and corn bread (arepas) (black bars) in Venezuela. White bars, percentage at addition.

Source: unpublished data of the authors

b-Carotene as colour and vitamin A

b-Carotene is extensively used as a food colour, at the same time contributing its nutritional value. As mentioned before, the bioavailability of b-carotene used as a colour is good. Figure 12 shows the nutritional contribution of b-carotene in the doses typically used as a colour for some selected foods.

Safety

J. N. Hathcok recently published a recompilation of the safety range for vitamins and minerals, defining the NOAEL (Non-Observed Adverse Effect Level) and LOAEL (Lowest Observed Adverse Effect Level) for every micronutrient [25]. Table 4 shows these levels expressed

TABLE 3. Iron content and relative cost of typical forms of iron used to fortify foods

Form of iron	Iron content (%)	Relative cost per unit of irona
Iron reduced with H,	98.0	1
Reduced iron, electrolytic	98.0	3
Ferrous sulphate, anhydrous	31.6	2.6
Ferrous fumarate	30.6	3.4
Ferric orthophosphate	26.0	5.9
Ferric lactate	20.5	22.8
Ferrous gluconate	12.5	26.2
FeNa EDTA + 3H2O	12.5	50.4

a. Iron reduced with H₂ is the reference substance. Relative cost considers cost and iron content, as multiples of the RDA [26].

Fortification cost

The direct cost of delivering nutrients as supplements or in food is remarkably low, compared with the social costs of deficiencies. The cost of fortification includes the costs of the fortificant, capital, and labour (for the blending operation), as well as the costs of transport and quality control. Depending on the type of food to be fortified and the fortification level and technology, fortification cost can vary over a wide range. In most cases, according to World Bank figures, it costs less than US$1 per year to protect an individual against deficiencies of vitamin A, iron, and iodine with food fortification [3]. The cost of fortification to protect an individual for one year against vitamin A deficiency is less than US$0.30 and against iron deficiency less than US$0.10. Table 5 shows typical costs of the quantity of micronutrients needed to cover the total requirement during a full year.

Eliminating micronutrient deficiencies can have major yet subtle social and economic benefits. When nutritional deficiencies are eliminated, adverse consequences, such as reduced IQ, impaired growth, reduced work capacity, and death associated with pregnancy and child-birth are reduced. Food fortification provides maximum benefit for minimum investment.

FIG. 12. Nutritional contribution of b-carotene used as food colour

Food fortification is generally recognized as being the most efficient as well as the most cost-effective means of eliminating micronutrient deficiencies when compared with supplementation and home gardening. In 1994 the USAID published an evaluation of the cost-effectiveness of three vitamin A interventions in Guatemala (fortification, supplementation, and home gardening) and compared the results with similar evaluations performed in Indonesia and the Philippines [27]. When the cost per high-risk person reached was considered, the conclusion was that fortification of staple foods was the cheapest intervention strategy (table 6). Furthermore, fortification was the most sustainable intervention and had the best coverage at the national level.

Voluntary versus mandatory fortification

The food industry has responded in some cases by voluntarily fortifying products. However, the development of voluntarily fortified foods has been impaired in some countries because of consumer and, in many cases, government lack of awareness of the prevalence of micronutrient deficiencies and their impact on health. Without consumer demand for fortified products, industry is often not motivated to fortify products voluntarily.

A number of staple foods around the world have been successfully fortified with micronutrients. Tables 7 and 8 show the countries with compulsory fortification of wheat flour and margarine, respectively [28]. As mentioned before, in 1998 the United States will start adding folic acid to wheat flour. In 1997 Ecuador, Bolivia, and Colombia started programmes to fortify wheat flour with vitamins B₁, and B₂, niacin, folate, and iron. The United States, Argentina, Venezuela, Mexico, the Philippines, and Malaysia fortify milk with vitamins A and D. Sugar is fortified with vitamin A in Guatemala, Honduras, and El Salvador. In addition to wheat flour, Venezuela has fortified pre-cooked corn flour with vitamins A, B₁ and B₂, niacin, and iron since 1993.

TABLE 4. Safety levels of micronutrients

Micronutrient	RDA	No. of times the RDA
		NOAEL	LOAEL
Vitamin A	3,333 IU	3	6.5
Vitamin D	200 IU	4	10
Vitamin E	15 IU	80	NE
Vitamin K	80 µg	375	NE
Vitamin C	60 mg	> 17	NE
Vitamin B1	1.5 mg	33	NE
Vitamin B2	1.7 mg	118	NE
Niacin	19 mg	79	158
Vitamin B6	2 mg	100	250
Folate	200 µg	5	NE
Vitamin B12	2 µg	1,500	NE
Biotin	100 µg	25	NE
Pantothenates	7 mg	143	NE
Ca	800 mg	1.9	>3.1
P	900 mg	1.9	>3.1
Mg	350 mg	2	NE
Cu	3 mg	3	NE
I	150 µg	6.7	NE
Fe	10 mg	6.5	10
Se	70 µg	2.9	13
Zn	15 mg	2	4

Source; refs. 25,26.

RDA, Recommended dietary allowance; NOAEL, non-observed adverse effect level; LOAEL, lowest observed adverse effect level; NE, not established.

Micronutrient	RDA	Annual cost per person (US$)
Vitamin A	1,000 µg RE	0.253
Vitamin D	400 IU	0.051
Vitamin E	10 mg TE	0.285
Vitamin B1	1.5 mg	0.032
Vitamin B2	1.7 mg	0.053
Vitamin B6	2 mg	0.064
Vitamin C	60 mg	0.558
Niacin	19 mg	0.067
Folate	200 µg	0.016
Vitamin B12	3 µg	0.053
Iron	15 mg	0.04
Total		1.47

Source: ref. 26.

Type of intervention		Annual cost per person (US$ in 1991)
		Guatemala 1979 Indonesia 1978 Philippines 1975	Philippines 1980	Guatemala 1991
Fortification
	Per person	0.16	0.14	0.29
	Per high-risk person	0.37	0.32	0.65
Capsule distribution
	Per high-risk person	0.48	0.32	1.52
Gardening
	Per person		2.32	1.60
	Per high-risk person			3.63

Source: ref. 27.

Country	Vitamin B1	Vitamin B2	Niacin	Folic acid	Iron
Canada	4.4-7.7	2.7-4.8	35-64	0.4-0.5	29-43
Chile	6.3	1.3	13		30
Costa Rica	4.4-5.5	2.6-3.3	35.2-44		28.7-36.4
Dominican Republic	4.45	2.65	35.62		29.29
El Salvador	4.41	2.65	35.3		28.7
Guatemala	4-6	2.5-3.5	35-40	0.35-0.45	55-65
Honduras	4.4	2.6	35.2		28.7
Nigeria	4.5-5.5	2.7-3.3	35.5-44.4		28.9-36.7
Panama	4.4	2.6	35.2		28.7
Saudi Arabia	> 6.38	> 3.96	> 52.91		> 36.3
United Kingdom	> 2.4		> 16		> 16.5
United States	6.4	4	52.9		44.1
Venezuela	1.5	2	20		20

Source: ref. 28.

Educated consumers can choose foods that enable them to maintain a balanced diet rich in vitamins and minerals. However, governments may need to intervene and require the food industry to provide consumers with the tools they need to make these educated choices.

In the United States, starting in 1975, the Food and Drug Administration (FDA) required most foods to be labeled with their nutritional content. Food labelling is a powerful tool to educate the consumer and to facilitate an informed choice of food. In 1993 the FDA revised the requirements of food labelling to include almost all the foods that consumers purchase. According to the FDA, “The purpose of food label reform is simple: to help consumers choose more healthful diets, and to offer an incentive to food companies to improve the nutritional qualities of their products” [29].

Along with information on saturated fat, cholesterol, and dietary fibre, the new labelling law mandated that nutrient levels of vitamins A and C, calcium, and iron must be reported on the label. These micronutrients were selected because of public health concerns and are listed on the label in order of priority (vitamin A, vitamin C, iron, and calcium) [29].

The mix of compulsory and voluntary fortification has produced an important increase in the availability of micronutrients in the United States, as shown in table 9.

Conclusions

More than 2 billion people, one-third of the world’s population, suffer from micronutrient deficiencies. Inexpensive and cost-efficient solutions to eradicate these deficiencies are readily available; of these, food fortification is recognized as the most efficient and sustainable solution. Successful fortification of a staple food reaches everyone, including the poor, pregnant women, young children, and populations that social services can never cover completely. In addition, fortification reaches secondary target risk groups, such as the elderly, the ill, and those who have an unbalanced diet, for whatever reason.

TABLE 8. Compulsory fortification of margarine in different countries (IU/kg)

Country	Vitamin A	Vitamin D
Belgium	22,500-27,000	2,500-3,000
Brazil	15,000-50,000	500-2,000
Canada	> 33,000	> 5,300
Chile	30,000	3,000
Colombia	3,180-7,950	480-1,200
Denmark	25,200
Ecuador	20,000-30,000	2,000-4,000
El Salvador	15,000
Guatemala	15,000-50,000
Honduras	35,000	1,500
India	> 30,000
Indonesia	25,000-35,000	2,500-3,500
Malaysia	25,000-35,000	2,500-3,500
Mexico	20,000	2,000
Netherlands	> 20,000	> 3,000
Panama	20,000	1,500
Peru	30,000	3,000
Portugal	18,000
Singapore	> 28,300	> 2,200
Sweden	> 30,000	> 3,000
Taiwan	> 45,000
Turkey	20,000	1,000
United Kingdom	24,000-30,000	2,800-3,520
United States	33,000	2,080

Source: ref. 28.

Micronutrient	Contribution (%)
	1970	1985
Vitamin A	10	13
Vitamin C	10	8
Vitamin B1	40	24
Vitamin B2	15	20
Niacin	20	18
Vitamin B6	4	6
Folic acid	0	6
Vitamin B12	2	4
Iron	25	24

Source: ref. 30.

References

1. Lotfi M, Mannar MGV, Merx RHJM, Naber-van den Heuvel P, Micronutrient fortification of foods: current practices, research and opportunities. Ottawa: The Micronutrient Initiative, and Wageningen, Netherlands, International Agriculture Centre, 1996.

2. World Health Organization. Prevalence of vitamin A deficiency. MDIS Working Paper No. 2. Geneva: WHO, 1995.

3. World Bank. Development in practice enriching lives: overcoming vitamin and mineral malnutrition in developing countries. Washington, DC: World Bank, 1994.

4. United Nations Administrative Committee on Coordination/Sub-Committee on Nutrition (ACC/SCN). Focus on micronutrients. SCN News No. 9, 1993.

5. World Health Organization/Food and Agriculture Organization (WHO/FAO). International conference on nutrition: final report of the conference. Rome: FAO, December 1992.

6. Blum M. Status paper: food fortification, a key strategy to end micronutrient malnutrition. NUTRIVIEW 97/Special Issue. Basel, Switzerland: Vitamin Division, F. Hoffmann-La Roche Ltd, 1997.

7. Bloch CE. Effects of deficiency in vitamins in infancy. Am J Dis Child 1931; 42: 271.

8. Aykroyd WR, Jolliffe M, Lowry OH, Moore PE, Sebrell WH, Shank RE, Tisdall FF, Wilder RM, Zamecnick PC. Medical survey of nutrition in Newfoundland 1948. Can Med Assoc J 1949; 60: 1-24.

9. Miller DF. Enrichment programs: helping mother nature along. Food Prod Dev 1978; 12(4): 30-8.

10. Quiogue ES. The rice enrichment project in Bataan, Philippines. Am J Public Health 1952; 42: 1086-94.

11. Arroyave G. Evaluation of sugar fortification with vitamin A at the national level. Scientific Publication No. 384. Washington, DC: Pan American Health Organization, 1979.

12. Layrisse M, Cháves JF, Méndez-Castellano H, Bosch V, Tropper E, Bastardo B, Gonzalez E. Early response to the effect of iron fortification in the Venezuelan population. Am J Clin Nutr 1996; 64: 903-7.

13. US Federal Register, 1996; Vol. 61, No. 173.

14. Flores H. Fortification of rice with vitamin A. NUTRIVIEW 3/96. Basel, Switzerland: Vitamin Division, F. Hoffmann-La Roche Ltd, 1996.

15. Pollitt E, Jacoby E, Cueto S. School breakfast and cognition among nutritionally at-risk children in the Peruvian Andes. Nutr Rev 1996; 54: 5522-6.

16. Machiln LJ, ed. Handbook of vitamins. 2nd ed. New York: Marcel Dekker, 1991.

17. Mejía L. Vitamin A deficiency as a factor in nutritional anemia. In: Hanck A, Hornig D, eds. Vitamins: nutrients and therapeutic agents. J Vit Nutr Res (suppl 27). Bern, Stuttgart, Toronto: Hans Huber, 1985: 75-84.

18. Suharno D, West CE, Karyadi D, Hautvast JGAJ. Supplementation with vitamin A and iron for nutritional anemia in pregnant women in West Java, Indonesia. Lancet 1993; 342: 1325-8.

19. Stekel A. The role of ascorbic acid in the bioavailability of iron from infant foods. In: Hanck A, Hornig D, eds. Vitamins: nutrients and therapeutic agents. J Vit Nutr Res (suppl 27). Bern, Stuttgart, Toronto: Hans Huber, 1985: 165-75.

20. Nilson A. Fortification of staple food. NUTRIVIEW 3/94. Basel, Switzerland: Vitamin Division, F. Hoffmann-La Roche Ltd, 1994.

21. Parrish DB, Eustace WD, Ponte JG, Herod LH. Distribution of vitamin A fortified flours and effect of processing, simulated shipping and storage. Cereal Chem 1980; 57: 284-7.

22. Iron EDTA for food fortification. A report of the International Anemia Consultative Group (INACG). Washington, DC: INACG, 1993.

23. Hurrell RE. Nonelemental sources. In: Clydesdale FM, Wiemer KL, eds. Iron fortification of foods. Orlando, Fla, USA: Academic Press, 1985: 39-53.

24. Shah BG, Giroux A, Belonje B. Specifications for reduced iron as a food additive. J Agric Food Chem 1977; 25: 592-4.

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28. Raunhardt O, Bowley A. Mandatory food enrichment. NUTRIVIEW, Supplement to 1/1996. Basel, Switzerland: Vitamin Division, F. Hoffmann-La Roche Ltd, 1996.

29. US Federal Register, 1993; Vol. 58, No. 3, January 6.

30. LaChance PA, Bauernfeind J. Concepts and practices of nutrifying foods. In: Bauernfeind J, LaChance PA, eds. Nutrient additions to food. Trumbull, Conn, USA: Food and Nutrition Press, 1991: 19-86.

A lesser-known grain, Chenopodium quinoa: Review of the chemical composition of its edible parts

N. Thoufeek Ahamed, Rekha S. Singhal, Pushpa R. Kulkarni, and Mohinder Pal

N. Thoufeek Ahamed, Rekha S. Singhal, and Pushpa R. Kulkarni are affiliated with the Food and Fermentation Technology Division in the University Department of Chemical Technology in Bombay, India. Mohinder Pal is affiliated with the National Botanical Research Institute in Lucknow, India.

In this era of ever-increasing world population, newer food and feed crops that have been hitherto neglected are gaining recognition. The rejection of such lesser-known food crops has been due not to any inferiority but to the lack of research resources in the place of origin and often to their being scorned as “poor people’s plants.” The genus Chenopodium supplies tasty and nutritious leaves as well as pink- to cream-coloured edible seeds. Tolerance to cold, drought, and salinity and the high lysine content of the seed protein are the attractive features of quinoa (Chenopodium quinoa), the most frequently consumed species in the Andean regions of South America, Africa, some parts of Asia, and Europe. This review compares and evaluates the nutritional and antinutritional constituents of the leaves and seeds of C. quinoa vis-a-vis their conventional counterparts and argues for the acceptance of this plant in human diets.

Introduction

Most of the world’s food today comes from a mere 20 or so plant species. Throughout history mankind has used some 3,000 plant species for food, but over the centuries the tendency has been to concentrate on fewer and fewer. The rejection of lesser-known food crops has not been due to any inherent inferiority. Many have been overlooked merely because they are native to the tropics, a region generally neglected because the world’s research resources are concentrated in the temperate zones. Others are neglected because they are scorned as “poor people’s plants.”

Quinoa (Chenopodium quinoa) is one of the lesser-known food crops, a poor people’s crop that is native to the Andean regions of South America [1]. In contrast to maize, potatoes, and Phaseolus beans, all of which are staple crops originating from the Andes, quinoa has not attained global importance, possibly because the bitter, antinutritional saponins [2] need to be removed from the seed before cooking or processing [3].

Quinoa has an exceptionally attractive amino acid balance for human nutrition because of its high level of lysine. The tasty and nutritious leaves and seeds are consumed frequently in the Andean regions of South America, Africa, some parts of Asia, and Europe. The plant is native to Peru, and the seeds are used whole in soups or ground into flour to make bread and cakes [4]. The seeds are also used as poultry feed, in medicine, and for making beer.

Agronomic aspects of Chenopodium

C. quinoa is a dicotyledonous plant and is botanically classified as follows [5]:

Subclass: Dicotyledoneae
Group: Thalamiflorae
Order: Caryophyllales
Family: Chenopodiaceae
Genus: Chenopodium
Species: quinoa

The family is found worldwide but it is centred in alkaline areas. Some species are restricted to wet, salty, or alkaline soil, such as that of coastal marshes or alkaline plains and desert areas. On the whole, the family is made up of weedy plants. Some of the more important genera are Chenopodium (goosefoot, pigweed, or lamb’s quarters), Kochia (red sage), and Salsola [5].

The genus Chenopodium has a worldwide distribution and contains about 250 species [3]. About eight species are found in India [7]. Some species of Chenopodium and the countries in which they are found are listed in table 1 [8]. Chenopodium species have been considered weeds [9], and many efforts have been directed towards their eradication [10].

Interest in quinoa as a valuable food source has been renewed in Asia in recent years because of its versatility and its ability to grow under conditions normally inhospitable to other grains. These include low rainfall, high altitude, thin cold air, hot sun, and sub-freezing temperatures.

The average yield of the fruit, as reported by Simmonds [11], is 840 to 3,000 kg/ha, whereas Weber [12] reported yields for quinoa as low as 450 kg/ha to a record of 5,000 kg/ha, with an average yield of 800 to 1,000 kg/ha. Quinoa is extensively grown in Peru and Bolivia. Because of its resistance to frost and drought, it is very suitable for cultivation in highlands and temperate regions. Production of quinoa in Ecuador has gone from backyard cultivation to extensive cultivation. In 1987 around 431 ha were harvested, producing 720 tonnes.

Quinoa as a vegetable

Quinoa leaves are widely used as food for humans and livestock [12] and constitute an inexpensive source of vitamins and minerals. Generally, the younger leaves are used for human food. The correlation between the nutrient content of a leaf and its age (as shown by its position on the plant) is an important factor in choosing leaves for harvesting. Chenopodium leaves have more protein and minerals than commonly consumed spinach and cabbage but less than amaranth leaves. The leaves of Chenopodium species contain from 3% to 5% dry weight nitrate [8]. The nitrate content in amaranth leaves ranges from 0.8% to 2% [13]. However, most of the nitrate is concentrated in the stem portion, which is generally discarded [8]. The oxalate content of Chenopodium leaves ranges from 0.9 to 3.9 g/100 g fresh weight, concentrated mainly in the stems [8]. Flavonoids have been identified in five species of Chenopodium. Quercitin (a flavonol) was found in all five species, kaempferol in four, and isorhamnelins in one [14]. The biological function of these flavonoids could be to provide resistance against viruses [15].

TABLE 1. Distribution of some Chenopodium species^a

Species	Countries
C. quinoa, C. pallidicaule	Argentina, Bolivia, Chile, Guatemala, Peru
C. berlandieri	Mexico
C. album	India (valleys of Himalayas)
C. ambrosoides	India
C. amaranticolor	India
C. murale	India
C. striatum	Czechoslovakia
C. opulifolium	Czechoslovakia
C. foliosum-polyspermum	Finland

Source: ref. 8.

a. Hybrids available: C. album-quinoa, C. foliosum-polyspermum.

Quinoa leaves can also be eaten in salads and are important in regions where vegetables are scarce. The leaves and stems are also fed to ruminants, and the chaff and the gleanings are generally fed to pigs.

Quinoa seed

C. quinoa is a starchy, dicotyledonous seed, not a cereal [17]. The small, round, flat seeds measure about 1.5 mm in diameter, and 350 seeds weigh about 1 g [18,19]. Quinoa has been an important grain crop in the Andes for many centuries and now is gaining popularity elsewhere in the world. In comparison with the common cereals, quinoa generally has a higher content of lysine-rich protein (12%-19%; average, 15%), fat (5%-10%), and crude fibre (2%-3%). This makes it nutritionally superior to most cereal grains. Table 3 gives the proximate composition of quinoa in comparison with some other food grains. After mechanical abrasion, the a-amylase and protease activities of quinoa seeds increase [25]. High a-amylase activity is probably the cause of the low amylograph values of quinoa. The iron, calcium, and phosphorus levels are higher than those of maize and barley [13, 26].

The main food uses for quinoa are for soups, sweets, and a coarse bread called kispina. Various hot or fermented drinks can be prepared from it. High-protein cakes, cookies, and biscuits can be made by mixing up to 60% quinoa flour with wheat flour [12, 21]. The fermented beverage made from quinoa seeds is called chicha. Noodles can be made using 40% quinoa flour without affecting the appearance or other characteristics of the product. A number of recipes for cookies, chowders, croquettes, and casseroles using quinoa are available [27]. Quinoa can be germinated at 22°C in fresh water; the germination rate is 74% to 86%. However, germination at 0°C caused a decrease in the germination rate of 12% to 30% [28].

The protein, fat, and fatty acid composition of Chenopodium seeds is similar to that of amaranth [29].

TABLE 2. Amino acid composition of quinoa leaves compared with that of other leafy vegetables

Vegetable	Total N (g/100 g)	Amino acid (%)
		Arg	His	Lys	Trp	Phe	Tyr	Met	Cys	Thr	Leu	Ile	Val
Quinoa	0.6	0.92	0.32	0.75	0.02	0.11	0.37	0.05	-a	0.17	0.41	0.41	0.29
Amaranth	0.6	0.24	0.13	0.25	0.07	0.18	0.19	0.07	0.04	0.14	0.37	0.29	0.28
Cabbage	0.3	0.45	0.13	0.24	0.07	0.20	0.12	0.06	0.07	0.22	0.34	0.23	0.26
Drumstick leaves	1.1	0.38	0.14	0.32	0.10	0.29	-a	0.11	0.13	0.25	0.46	0.28	0.35
Spinach	0.3	0.35	0.14	0.40	0.10	0.33	0.31	0.11	0.08	0.29	0.53	0.3	0.35

Source: ref. 16.
a. - trace or absent.

Seed	Moisture	Ash	Protein	Fat	Carbohydrate	Crude fibre
Quinoa	10-13	3	12-19	5-10	61-74	2-3
Amaranthus paniculatas	6-9	3-4	13-18	6-8	63	4-14
Wheat	13	2	14	2	69	1
Oats	8	2	14	8	68	1
Rice	15	1	8	1	78	2
Maize	15	2	13	4	66	3
Sorghum	12	2	12	2	73	2
Soya bean	8	5	47	21	14	4
Barley	13	2-3	12	1	70	4

Source: refs. 13,16,17,19-24.

Quinoa seeds contain high-quality protein [30] and large amounts of carbohydrates, fat, vitamins, and minerals. The seeds have a higher nutritive value than most cereal grains. The protein content of about 15% in quinoa is much higher than that found in cereals such as wheat, barley, oats, rice, and sorghum. The soluble protein contents in quinoa are similar to those in barley and higher than those in wheat and maize [26].

Table 4 gives the contents of essential amino acids in quinoa as compared with other grains. Quinoa protein contains large amounts of lysine, which is limiting in many plant proteins. The Sajma variety (developed in Bolivia) contains approximately twice as much lysine as whole wheat on a dry weight basis. The high levels of lysine in quinoa protein make it nutritionally superior to wheat. Dini et al. [31] reported lysine, with a chemical score of 83, as the limiting amino acid, although the level is higher than that for wheat and rice, with chemical scores of 31 and 40, respectively.

It is an interesting observation that methionine and cysteine (chemical score 127) and phenylalanine and tyrosine (chemical score 125) are limiting in other grains. The ratio of tyrosine and phenylalanine to methionine and lysine is higher than FAO/WHO standards. Ruales and Nair [19] reported the aromatic amino acids tyrosine and phenylalanine, with a chemical score of 86, as the first limiting amino acids. However, the absence of gluten-like properties makes quinoa unsuitable for direct use in making bread. Telleria et al. [32] reported no differences in the amino acid composition of raw quinoa and quinoa seeds treated with water at different temperatures to remove saponins. Biological studies showed a decrease in protein efficiency ratio (PER) values after extraction at 85°C but not at 70°C.

TABLE 4. Essential amino acid composition of quinoa seeds compared with that of other seeds

Seed	Amino acid (g/100 g protein)
	Trp	Met	Thr	Ile	Val	Lys	Phe/Tyr	Leu	Cys
Quinoa	0.8-1.1	0.3-2.6	3.6-4.4	3.8-4.2	4.7-4.8	5.4-6.3	6.2-8.9	-a	0.6-1.4
Amaranthus cruentus (raw)	-a	4.1	3.4	3.6	4.2	5.1	6.0	5.1	2.1
A. cruentus (popped)	-a	3.7	3.5	3.6	4.3	4.3	6.0	5.2	1.8
A. edulis	1.1	4.0	3.8	3.9	4.5	5.7	7.8	5.9	2.3
Wheat	0.9	4.3	3.1	3.5	4.7	3.1	8.0	7.0	2.2
Oats	1.3	4.7	3.5	4.0	5.5	4.0	8.9	7.8	1.4
Soya bean	0.7	3.0	4.5	4.0	4.4	6.4	8.4	7.8	1.6
Corn	0.6	3.2	4.0	4.6	5.1	1.9	10.6	13.0	1.6
Rice	1.0	3.0	3.7	4.5	6.7	3.8	9.1	8.2	1.6
FAO/WHO standard	1.0	3.5	4.0	4.0	5.0	5.5	6.0	7.0	3.5

Source: refs. 13, 16, 17, 19, 20.

a. - trace or absent.

The protein content of seeds from Mexican Amaranthus spp. as well as South American Chenopodium spp. is 13% to 15%. Digestibility (53%-65%) improved when the seeds were toasted or popped (68%-78%). Their biological value was 73% and their PER [36] was similar to that of casein [1,20]. Processes such as extrusion are known to improve the PER of quinoa flour [37].

In animal experiments, the net protein utilization (NPU) values of 76% and the biological value of 92 for protein in quinoa were comparable with those of other high-quality food proteins [38].

Lipid content

Quinoa seeds have approximately 9% fat on a dry weight basis. Quinoa fat has a high content of oleic acid (24%) and linoleic acid (52%) [38]. Quinoa oil is colourless to yellowish with a pungent, disagreeable, camphoraceous odour, characteristic of the seed. The flavour is bitter and burning.

Quinoa oil has been in use since the American Civil War. The original methods of production were quite primitive. The plants were boiled in iron pots equipped with soapstone lids. The oil condensed against the lids and was skimmed off. It was sold mainly in Baltimore, where the old name “Baltimore oil” is still used [39]. Maryland remains the chief producer of quinoa oil; the area of production is concentrated largely within a 25-mile radius in Carroll, Frederick, Howard, and Montgomery counties, with wood pine as the fuel for distillation. The total production in normal years varies between 60,000 and 80,000 lb. The yield depends on the weather conditions, the stage of maturity of the plant, and other factors. One acre of quinoa produces, on average, about 50 to 60 lb of oil per year.

On extraction with petroleum ether, quinoa yields yellow oil ranging from 6% to 8% of the weight of the whole seed, depending on the variety. The hulls, bran, and flour account for 10%, 40%, and 50%, respectively, of seed weight. The total fat contents in whole seed, hulls, bran, and flour extracted with diethyl ether were 7.6%, 5.7%, 11.6%, and 3.2%, respectively The crude lipid content of quinoa was similar to that found in Amaranthus caudatus, a closely related plant [40, 41].

The constants of quinoa oil are compared with those of some selected edible oils in table 5. Quinoa seed oil is more unsaturated and also has a higher content of unsaponifiable matter than cereal oils.

Table 6 compares the fatty acid composition of quinoa seed oil and some other edible oils. Linoleic acid (C_18:2) accounted for over 50% of the fatty acids in quinoa oil, followed by oleic acid (C_18:1) and palmitic acid (C₁₆). The relatively high content of linolenic acid (C_18:3) in quinoa oil indicates an excellent nutritional quality of the grain. According to Morrison [44], the fatty acid composition of quinoa lipids is similar to that of wheat.

The ratio of polyunsaturated to saturated fatty acids (PS ratio) of quinoa oil is 4.9. This is higher than the PS ratios of most edible oils, such as soya bean oil (3.92), corn oil (4.65), and olive oil (0.65). The percentage of energy delivered by linoleic acid in quinoa seed oil is 10%, which is higher than the recommendation of the American Academy of Pediatrics that infant foods should contain at least 2.7% of their energy in the form of linoleic acid [38].

The percentage of free fatty acids is higher in quinoa seeds (18.9%) than in wheat (11%) and germinated barley (8.4%) [45]. Neutral lipids are predominant in cereals and have been reported to constitute around 90% of the lipids in members of the Amaranthaceae family [46] (table 7).

TABLE 5. Oil constants of quinoa seed oil compared with those of other seed oils

Variable	Oil
	Quinoa	A. paniculatas	Wheat	Corn	Rice
% oil in whole seed	6-8	8	2	3-7
% oil in bran	11-12	18-20	5-6		8-16
Specific gravity at 25°C	0.8910	0.9155	0.9248