FEATURES

The Role of Care in Nutrition - A Neglected Essential Ingredient
Update on the Nutrition Situation
Specific Deficiencies Versus Growth Failure: Type I and Type II Nutrients
Enrichment of Food Staples Through Plant Breeding. A New Strategy for Fighting Micronutrient Malnutrition

The Role of Care in Nutrition - A Neglected Essential Ingredient

The causes of poor child nutrition are undergoing a substantial reassessment with recent understanding of the importance of care. Richard Longhurst and Andrew Tomkins of the Institute of Child Health summarize current thinking.

by Richard Longhurst and Andrew Tomkins, Centre for International Child Health, Institute of Child Health, 30 Guilford St (University of London), London WC1N 1EH, UK

The causes of poor child nutrition, all reflected in child survival, growth and development are undergoing a substantial re-assessment. For a long time nutrition outcomes have been equated primarily as being dependent on availability of food, in which the term household food security is used, and the presence of infection which influences the intake, absorption and utilisation of food. There has been some recognition that 'other factors', never properly defined, were important. People with knowledge of nutrition at all levels: family members, village workers, government officials, international civil servants and academics, have often recognised other determinants in the process, usually referring to issues such as 'social factors', 'ignorance' and, in some cases, 'love and support'.

A problem in identifying these other 'social' factors, was that they were often seen as too closely inter-twined with 'food' and 'health' as to be separated. Now these non-food, non-health factors are being brought together in a coherent and practical manner within an understanding of the role of care in nutrition outcomes. Care consists of the actions necessary to promote survival, growth and development, involving actions at the household level parallel with household food security and health promoting behaviour. Resources for improving care exist at the household level: income, food, time, attitudes, relationships and knowledge.

Care for children is recognised within the Declaration on the Rights of the Child as follows: "the child... needs special safeguards and care, including appropriate legal protection, before as well as after birth" and in the UN Convention on the Rights of the Child in Article 3: "to ensure the child such protection and care as is necessary for his or her well-being" and elsewhere in Article 6 and in Articles related to protection from abuse and in especially difficult circumstances such as war and when deprived of the family environment.

The principal drive for promoting and clarifying the concept of care in child nutrition outcomes, within the context of food and health has come from UNICEF. Within its nutrition strategy, adopted in 1990, and in work leading to it, especially in the Iringa Nutrition Programme in Tanzania, care of women and children was recognised, with household food security and the nature of the health environment and health services as one of three conditions, each necessary but not sufficient, for the fulfillment of child survival, growth and development. The actions of food, health and care were the foundation of the work of the ACC/SCN group meeting of November 1990 which reviewed actions that had been undertaken to address the major problems of underconsumption and malnutrition especially among the poorest, to point the way for renewed efforts in the 1990s.

At the International Conference on Nutrition, held in Rome in December 1992, food, health and care were recognised as the three fundamental components for nutritional well being. The theme paper on care for the ICN drew on empirical work world-wide and on consultative meetings with nutritionists, medical doctors and child psychologists. The role of NGOs and religious groups has been invaluable.

Care within maternal and child health has been strongly promoted within WHO and more recently, economists have begun to delve within households as the basic decision-making unit in their efforts to understanding the allocation of resources (or 'household economies'), work that had been carried out among others by the International Food Policy Research Institute (IFPRI). Most recently, papers on topics relating to care and nutrition of the very young child (from birth to 3 years of age) were presented at a UNICEF-funded meeting at Cornell University, New York, in October 1994. At the Institute of Child Health in London, work has been performed on methods for assessing and analysing care situations, developing guidelines and designing workable interventions, particularly for children in especially difficult circumstances.

Research from three areas - 'positive deviance', 'failure to thrive' and fieldwork on care in Central America - has confirmed what many field workers have understood: that care in terms of affection, emotional support, and effective allocation of resources with an atmosphere of stability and security has a direct influence on child nutrition as defined in terms of survival, growth and development. This research has shown that even in situations of poverty involving household food insecurity and an unhealthy environment, enhanced care giving can promote good nutrition outcomes in young children.

Care means different things to different professions and people. "Care" in general refers to the provision in the household and the community, of time, attention and support to meet the physical, emotional, intellectual and social needs of the growing child and other family members. It leads to the optimal use of human, economic and organisational resources. At an extreme, lack of "care" is neglect. Care in terms of child nutrition refers to facilitating the optimal use of household food resources for child feeding, and the optimal use of parental (or other) resources to protect from infection and care for the sick child, or other vulnerable members (e.g. the disabled, elderly). Care in the form of stimulation, affection and support can have a direct effect on growth in the young child, by affecting the timing of release of growth hormones and matching of nutrient intake with requirements.

Among groups of people regarded as nutritionally vulnerable, attention is often devoted to the very young child. However, there are other vulnerable groups for whom care is important such as mothers, refugees, the elderly, the disabled, the school age child and those suffering the shock of an emergency. Children in especially difficult circumstances who have dropped through the safety net of family and community support require special care interventions. Positive care behaviours allocate the household food supply to household members according to need (it should be recognised that this may conflict with cultures where males feed first) and promote the dietary intake of family members who are unwell. Loss of appetite from infection or emotional stress is thus not accepted as an obligatory event. Care involves encouragement, coaxing, keeping food safe and even provision of alternative more expensive, appetizing food sources. Care behaviours also encourage health promoting behaviour such as the use of latrines and appropriate water supplies and support health seeking behaviour through regular visits to preventive and curative medical services. All of these behaviours can be promoted and supported by government ministries of health, agriculture, education and community development, together with NGOs. Programme planners who find it difficult to understand why children are not fed when adequate food appears to be available in the household, nor wash their hands when water and soap are already used may look to care behaviours for some of the reasons.

Development programmes aiming to improve nutrition outcomes need to recognise Care as a crucial ingredient along with 'food' and 'health'. Programme managers should start with a situation-specific appraisal. This involves finding out who are the caregivers involved and how existing child care practices can be protected and supported. This appraisal also involves a dynamic understanding of trends and how the pressure on child care practices are changing. Through a process of assessment, analysis and action, then re-assessment, re-analysis and so on - a recurring Triple-A cycle - resources available at household and community level can be activated by different forms of communication to improve care, and hence nutrition.

Care, Nutrition and the Young Child

Care is vital in the nutrition of the young child. According to Professor Engle of CalPoly in California care giving behaviours include "breastfeeding, diagnosing illnesses, determining when a child is ready for supplementary feeding, stimulating language and other cognitive capacities, and providing emotional support". Thus, the use of bottle feeding breaks down the most effective way of caring for the very young child, which is via breast feeding. The role of the caregiver is obviously very important and although it is generally assumed that mothers are the primary caregivers, in many societies care is shared by older siblings, older relatives and possibly by other families in community-organised arrangements. The role of fathers is very important as they have specific care-giving behaviours to impart but often their care giving role is limited because of employment, personal leisure or attitudes.

Engle has also drawn attention to an important concept for analysing the need for, and impact of care, especially for the young child. This is the division of care behaviours into those which bring a child up to a minimally healthy level (compensatory behaviours) and those designed to increase the child's capabilities, growth or development (enhancement behaviours). She has pointed out that if parents do not value enhancement child care, extra time (an important resource) may be spent on other activities thought to be more important for the family such as income generation or leisure, rather than child care.

Research by psychologists has shown that the characteristics of a child strongly affect the nature of care that s/he receives. The two-way feedback between child and carer is very important: a non responsive child reduces the care s/he gets while a responsive and active child elicits more care from the care giver. Nutritionists have not given much attention to this, but it is acknowledged that characteristics such as appetite, temperament, responsiveness, health status and gender all influence caring behaviours. The need for care is often greatest with cases of severe protein-energy malnutrition. Inadequate levels of Care may well have been the reason for the cause of the nutrition problem in the first place. Therefore a re-inforcing cycle is set up.

Dr Urban Jonsson of UNICEF suggests that care behaviours for the young child can be grouped into four: i) feeding behaviours including breastfeeding, and complementary feeding especially those relating to frequency, amount and density; ii) hygiene behaviours related to food, personal and home, iii) psychosocial behaviours including responsiveness, warmth, involvement and opportunities for learning and iv) health behaviours such as service utilisation, oral rehydration therapy and home care. Feeding behaviours may be as important as food availability for child nutrition. Care factors provide specific lessons for supplementary feeding. The areas of appetite and complementary feeding are very important and only now are being properly understood.

Promoting care in the context of breast feeding involves several supporters. Employers need to provide adequate maternity support and facilitation of breast feeding in the workplace, governments must provide adequate control of the media and agreement by the food industry to ensure responsible activities regarding advertising of infant and child feeding commodities. Free or low cost supplies of breast-milk substitutes must not be provided to maternity services. Hospital personnel must be trained in the physical and psychological elements of breast feeding, with changes in hospital practices regarding births and stronger support for breast feeding. The lactating mother also needs support by other family members.

For severely malnourished children there is increasing consensus on the best regimes for treatment with regard to content of energy, protein, mineral, electrolytes and vitamins. There is also agreement, in general, on effective, affordable regimes of infection control. However, with few exceptions, there has been rather little attention to care issues that are necessary for the effective delivery of these interventions, including protecting and promoting traditional and effective child care practices. This obviously involves support for the carers; in some programmes this has been neglected such that the carers become demotivated, frustrated and ineffective. Such issues need attention within the family and organisations such as primary health care projects to prevent and manage organisational and personal stress.

A lot of the work on care has been directed at the child under three years of age and at pregnant and lactating women within the context of breast feeding. But care remains equally important for the nutrition of other groups and is equally neglected as a means of understanding how efforts to improve their welfare can be improved. Care has an important role in increasing nutrient intake and decreasing episodes of infection in high risk groups. Also, despite the considerable attention given to micronutrients over the last few years, for example, care as a factor in enabling their intake has been little examined.

Care, Nutrition and the School Age Child

The nutrition of the school age child has often been neglected, compared to the preschooler. But care and nutrition are vital for child development and health. Many school feeding programmes, for example, ignore care completely, their objective is often to make sure that a child consumes a specific amount of nutrients. The timing and nature of meals and the related social interaction are important opportunities to combine with knowledge of nutrition which might usefully be incorporated into the curriculum with practical experience of preparation and consumption of nutritious food prepared and eaten in hygienic environments. In such instances, care can be seen as the driving force which stimulates education ministries, schools and communities to ensure that resource provision accompanies theoretical learning. Care of individuals within schools who are 'not coping' because of malnutrition requires the incorporation of recognition and appropriate response within "teacher training". This is particularly important for children who do not receive breakfast or are micronutrient deficient. Similarly the special needs of children from particularly disadvantaged families require sensitive, informed and effective treatment.

In many countries the number of school age children attending school has remained constant; in some countries they are falling. The costs of primary school education, the need for the child as a worker in poor communities, decreasing opportunities for employment, civil disruption, and orphanhood from various causes including AIDs means that even in harmonious families and communities, school attendance may be limited. Add to this the burden of street children, those involved in exploited labour and the generally unattached, there is now increasing need to consider the care of school aged children who do not attend school. There is urgent need to promote appropriate interventions from the voluntary, religious and governmental sectors which involve unconditional care for individuals and the unattached. While these activities are normally considered the responsibility of social welfare services, the scale of the problem is so great that all avenues of response should be considered. Care may well involve avoidance of over-nutrition. With the one child policy in China for instance, there is likely to be increasing emphasis on essential micronutrient supplementation, by parents, in order to achieve scholastic and physical success. Similarly, foods that promote dental caries should be avoided.

Care, Nutrition and the Disabled Child

Many reports suggest that in both developed and developing countries about 7% of children have some form of disability. However, most studies show that, on average only 2-3% of children are considered disabled by the community and needy of special attention. Many causes of disability relate to poverty and care and nutrition can do much to prevent disabilities and ensure that the disabled child is not at a disadvantage.

The nutritional status of the disabled child is often poor; in many cases the disability has been caused by previous nutritional insults such as vitamin A deficiency leading to blindness, cerebral palsy as a result of premature birth or low birth weight caused by poor maternal nutrition or iodine deficiency causing varying degrees of mental retardation. Malnutrition among the physically or mentally handicapped child is a common reason for marginalisation. In addition severe malnutrition due to insufficient energy intake is also a major disabling factor. Malnourished children get infections more seriously: diarrhoea for example can lead to serious dehydration, high fever and sometimes brain damage. Many disabilities can be prevented with improved care practices, protecting against infections and household and community accidents, making a strong case for care at community and national level to prevent energy and micronutrient deficiency induced disabilities. Communities need to have the resources to ensure iodised salt can be purchased and that, for example, vitamin A capsules can be distributed effectively and equitably.

As mentioned earlier, the obverse of care is neglect; many handicapped children may be neglected, but not because of any uncaring attitude on behalf of the family. In the scramble for scarce resources within a poor family there is a negative outcome for those who require more compensatory care, and may never even begin to receive the desperately needed enhancement care, especially in societies where the period of 'being cared for' is very short. For example, children who are disabled from birth with cerebral palsy may have feeding difficulties such that their families will continue to have to do everything for them long after other children have developed self-feeding skills. Extra attention paid at this stage will avoid future malnutrition and compounding of the disablement. Furthermore, the potential for improved function among disabled children and adults as a result of improved nutrition, is considerable. The problems of disabled children need more attention and advocacy with the introduction of programmes that recognise their special circumstances. They often 'fall between the cracks' of bureaucratically-defined programmes.

Care, Nutrition and the Urban Child

What are the principle differences between an 'urban' child compared to a 'rural' child and how does this affect care? There are increasing concentrations of people in urban areas depending on a higher level of economic diversification than an agriculturally based society. There is crowding, more of a cash economy, a lower level of physical activity in certain occupations, predominance of manufacturing, bureaucratic and service activities and some degree of organised public services. In addition it is believed that family ties may be weak especially for those who have entered an urban community recently. However, urban populations enjoy greater political clout. About twenty years ago the data showed that malnutrition was higher in rural areas but since then the differences have narrowed.

The urban economy and economic constraints resulting from recession and adjustment have caused an increase in the numbers of women working outside the home. The impact of women's work in terms of child nutrition appears to vary depending on the type of work undertaken, its intensity and location and level of income received. Women may not work longer than in rural areas but may have to travel further for that work. Employers may discourage accompanying children. Women may face confusion from health professionals and advertising with extra messages for child care and feeding. In many cases the time for child care is reduced. Fathers are often absent. Urban social systems are seen to differ from rural ones with important often destructive social consequences for child care. There is debate as to whether urbanisation results in a lack of community or different forms of community.

Social conditions are certainly different with additional stresses and dangers such as violence, drug addiction and prostitution. The urban environment is probably more unhealthy in terms of sanitary conditions: the disposal of both industrial and domestic waste are health hazards. Differing patterns of infection are seen both to cause and result from malnutrition. Breastfeeding is seen to have declined in many urban areas in terms of duration, if not of incidence, and thus emerges as a further cause of urban malnutrition.

It is in urban areas that especially disadvantaged children will exist. Children from the age of six upwards will be vulnerable to shocks from lack of supervision and discipline/nurture, prostitution, drugs and poisoning. Care programmes for urban children have to take account of the tact that they may not be located in a family, and that this care structure has to be provided in some form through other community institutions. Indigent children and orphans need to be considered as a special group for care and be included in nutrition programmes such as community kitchens.

Care, Nutrition and Refugees and People in Emergencies

The importance of care, within the context of food and health, is also leading to a different way in which we understand emergencies. Emergencies have grown in number and intensity over the last ten years, and many, especially in Africa, but also in the former Yugoslavia and Soviet Union, are also associated with conflict. As a result of these crises, the number of internally displaced people and refugees has grown; in Africa refugees and displaced now number 20 million, the size of a fair-sized nation. Many emergencies, including those of the sudden onset nature, have been seen as crises of food: people have nothing to eat and this has to be provided for them from outside as rapidly as possible. Famine relief has become common especially in the Horn of Africa and food aid operations have taken a lot of the resources of multilateral and bilateral agencies.

However, over the last ten years, the notion that food alone meets the short term needs of populations in an emergency has been re-assessed. For children there is now a clear understanding that food and infection control alone are not enough. The major reason for this reformulation is that not enough attention has been devoted to understanding how those affected by an emergency behave. In most cases, they are not 'helpless victims' but cope and adapt to a crisis whether unexpected or not. These coping mechanisms are now beginning to be understood within the operational context of many agencies: strategies involve a number of insurance mechanisms, disposal of productive assets, income diversification, leading to distress activities such as splitting of families and communities and migrating to relief camps. Several of these will have important implications for children.

Families often decide to protect livelihoods rather than lives, which suggests that food intake is reduced early in the crisis (rather than later as is often assumed) and that the wage earners and their assets (e.g. livestock) are also protected. This will have negative implications for child care. With income diversification and longer searches for water, food and work, the amount of time devoted to children is also likely to decrease. Distress and destitution activities include migration by entire family units, prostitution and in extremes, selling off and abandonment of children.

When families migrate and join other destitute families in camps then a food crisis becomes compounded by a health crisis'. Congregations of large numbers of weak people with poor sanitation often cause outbreaks of infectious diseases such as cholera and measles. It is for this reason that health care, including widespread immunisations of children and provision of clean water, is now a component of relief aid. (Recent analysis of data from some famines in India in the nineteenth century has shown that malaria (in the irrigated areas) was the greatest cause of mortality, not lack of food by itself.) Refugees suffer from the same types of nutritional deficiencies as other groups, but often more so due to their increased destitution. Mental and emotional illnesses are also common among the displaced. Recently the importance of micronutrient deficiencies among refugees and the displaced has been extensively documented. Apart from vitamin A and iron deficiencies, scurvy and pellagra deficiencies have been seen in refugee populations.

However there had been little attention paid to components of care in relief interventions, until the effects of conflict on children became better understood. Care interventions involve maintaining intellectual and cognitive development, psycho-social care relating to the direct traumatic effects on child emotional development related to loss of personal security, and broader aspects relating to a child's wider social needs. In several emergencies involving conflict (popularly known as "complex" emergencies), children have suffered traumatic experiences including the sight of parents and others being killed. Therefore compensatory care related interventions have been needed for psychological rehabilitation. Emotional stress as a result of recent traumatic experiences may be very severe, affecting care of self and children. Withdrawal, depression, anxiety and despair have profound impact on appetite. Thus improved management of such problems should become an integral part of nutritional care. It is particularly important that teachers recognise that post traumatic disaster disorders may be an explanation for the "difficult" child, refusing to pay attention or eat.

More recently care has been broadened as an important emergency intervention to mitigate the disruption that occurs to a child's environment: loss of schooling, normal patterns of social life, separation from the family and protection during conflict from abduction, conscription, rape, imprisonment, abuse wounding and murder, all in contravention of the Geneva Convention. Care in the form of maintaining school education is increasingly being recognised as essential during a crisis, although it remains a low priority for donors after feeding and health care. A school binds a community together maintaining an air of normality, keeping children's minds off the shocks that the emergency may be causing.

In refugee camps, activities are designed to be very service delivery oriented to mechanistically deliver food, immunisations and water. Care interventions are not usually included. Breast feeding is not encouraged and organising social activities for children happens only in rare cases. Child play is not usually encouraged. More can be done to ensure that family and social units stay together and maintain some cohesiveness so that young children do not become cut off from their families. Informal schooling could be organised in the camps. All of these have positive effects on nutrition and child development.

Conclusions

Care for improving nutrition, it has been emphasised, revolves around the allocation of resources and appropriate behaviours. Resources for the poor are always scarce; when resources are constrained, allocation always has negative implications for someone. So the whole issue of care has to revolve around the rights of children. Actions for improved child care has to be driven by an ethical position that the child has first call on resources. The fact that improving care also improves nutrition and function is therefore a helpful, but not necessary, imperative for improving nutrition.

Many interventions can have an impact on care, directly or indirectly. Actions taken by governments and other bodies at international and national or regional level can affect care at household level. It is not a closed family matter for the mother and child. At all levels care has to be recognised as an important factor in nutrition. Much is already known about food intake and health as inputs for nutrition; emphasis on care does not weaken their importance. In fact it does the opposite: understanding care issues will enable a more effective understanding of first, food as a commodity to be consumed and be used as a resource for improving livelihoods and family welfare and second, the health environment and health services in the context of available family practices and resources. Most importantly basing nutritional improvement on care, as well as food and health means that communities can take power into their own hands to improve the welfare of their children and not be solely directed by service delivery options from outside their community.

At national level many economic activities can have an impact on care in terms of improving the resources available at community level, including income generation and credit programmes that improve women's control over income, literacy and nutrition education that reflects resource scarcity at the household level, technology devices for workload reduction and legislation for rights for women and children. Whether these can be translated into improved care depends on whether care is seen as a responsibility for all, not just the primary care giver. Protection against harmful trends including necessary legislation and enforcement is another measure that can be taken nationally. Breast feeding should be protected and encouraged. In the community, care can be legitimised as an activity for the responsibility of all. Informal young child care networks can be strengthened with resources to expand beyond custodial services to provide enhancement care in terms of nutrition supplementation and cognitive and psycho-social stimulation. There are good models for this in several countries, notably Nepal. Within formal and informal employment relations, child care facilities could be instituted and strengthened. The importance of care in the promotion of nutrition is too important to be neglected any longer.

Bibliography

Engle, P. (1992) Care and Child Nutrition Paper for the International Conference on Nutrition. UNICEF, New York.

Gillespie, S. & Mason, J. (1991) Nutrition Relevant Actions: Some Experiences from the Eighties and Lessons for the Nineties. ACC/SCN State-of-the Art Series Nutrition Policy Discussion Paper No 10. ACC/SCN, Geneva.

Hanbury, C. (1992) Child-to-Child and Children Living in Camps Child-to-Child Trust, Institute of Education, University of London.

ICN (1992) Caring for the Socio-Economically Deprived and Nutritionally Vulnerable. Theme Paper No 3. FAO/WHO, Rome.

Myers, R. (1992) The Twelve Who Survive: Strengthening Programmes of Early Childhood Development in the Third World. Routledge/UNESCO, London. (See especially Chapter 9).

Ressler, E., Tortorici J., & Marcelino, A. (1993) Children in War: A Guide to the Provision of Services. UNICEF, New York.

Richman, N. (1993) Children in Situations of Political Violence. J. Child Psychol. Psychiat., 34(8), 1286-1302.

Werner, D. (1987) Disabled Village Children: A Guide for Community Health Workers, Rehabilitation Workers, and Families. Hesperian Foundation, Palo Alto

Zeitlin. M., Gassemi, H. & Mansour, M. (1990) Positive Deviance in Child Nutrition. UNU, Tokyo.

Update on the Nutrition Situation

Summary of findings from the recently published ACC/SCN "Update on the Nutrition Situation, 1994".

The ACC/SCN's "Update on the Nutrition Situation, 1994" was published recently. Here is a brief summary of its main findings.

¹ Many national surveys have been assisted by the Demographic and Health Surveys (DHS) project.

Over half the underweight children in the World are in South Asia, thus estimates of trends in this region have enormous importance. New data are scarce. A surveillance system in Bangladesh indicates improvement from 1990 to 1993. Recent changes in the situation in India are harder to assess, as data gathered in 1991/92 are from a rather small sample - tentative results are that, of seven states assessed, three showed a deterioration, and four had no significant change. General improvement was previously estimated between 1975-79 and 1988-90. India suffered an economic slow-down in the early 1990s, and there is reason to hope that the reversal of the improving trend indicated may be temporary.

Rates of change in underweight prevalences can be compared with those necessary to reach the nutrition improvement goals - halving the prevalence from 1990 -2000 - endorsed by the World Summit for Children (UN, 1990) and the International Conference on Nutrition (FAO/WHO, 1992).

In South East Asia, China, Middle America/Caribbean, South America, and Near East/North Africa, the rates of improvement in many countries are good enough to reach the goal of halving the prevalence.

South Asia has the largest task, starting with both the highest prevalences and massive population. Thus although the rate of improvement here is estimated to be fairly similar to that in other improving regions - with the possible exception of India recently - these rates are not enough to meet the halving-the-prevalence goals. The rate required (because the starting prevalence is so much higher) is almost twice that of elsewhere, at nearly three percentage points per year, compared with one and a half for Sub-Saharan Africa or South East Asia. In contrast, in Sub-Saharan Africa a prevalence change of -1.5 percentage points per year would on average be required to meet the goal of halving the prevalence by the year 2000; but most of the observed trends in this region are actually positive, indicating deterioration in nutritional status.

An important determinant of nutrition trends is the economic growth rate. Comparing rates of change of GDP per caput with rates of change in prevalence shows an intriguingly close fit - see Figure 2. A first use of this relationship is to get some idea as to how generalizable prevalence data are, using the known GDP growth rates.

The question of how typical are the recent estimates is particularly important for Sub-Saharan Africa. Here there are eight recent national estimates available - most showing deterioration - but these only cover a minority of the population (in contrast, for example, to the data coverage in Asia). The average GDP change for the eight countries was recently slightly negative (-0.2% for 1985-92), compared with -0.8% for Sub-Saharan Africa overall. Thus these eight countries were slightly better off, if anything, than the average for Sub-Saharan Africa in 1985-92. The nutrition situation in Sub-Saharan Africa probably deteriorated somewhat more than indicated from the eight countries with available data.

Was the trend in the early 1990s worse than that in the 1980s? Nutritional trends in Sub-Saharan Africa are estimated as static in 1985-90 and increased in 1990-92. The nutritional trend probably worsened in the early 1990s in Sub-Saharan Africa. The situation in South Asia depends on average largely on India, for which direct estimates indicate increasing prevalences in some states.

In other areas of the world the underweight trends in the early 1990s were generally similar to those in the late 1980s. In fact, in most regions the GDP growth rate improved after 1990, and nutritional improvement outside Sub-Saharan Africa and possibly India probably continued into the early 1990s.

Figure 1. Recent Trends in Prevalence of Underweight Children

(New results are shown as solid lines and points; dotted lines are data previously given in Figure 1.3 of Second Report, Volume II, page 5)

Sub-Saharan Africa

Near East and North Africa

South Asia

South East Asia and China

Middle America and Caribbean

South America

Figure 2. Plot of Change in Underweight Prevalence by Economic Growth Rate

Key

Country	From.	To
1. Ethiopia	1983,	1992
2. Kenya	1982,	1987
3. Kenya	1987,	1993
4. Madagascar	1984,	1992
5. Malawi	1981,	1992
6. Rwanda	1976,	1985
7. Rwanda	1985,	1992
8. Senegal	1986,	1992
9. Tanzania	1987,	1992
10. Togo	1977,	1988
11. Zambia	1984,	1992
12. Zimbabwe	1984,	1988
13. Egypt	1978,	1988
14. Egypt	1990,	1992
15. Morocco	1987,	1992
16. Tunisia	1975,	1988
17. Bangladesh	1981,	1989
18. Bangladesh	1990,	1993
19. India	1977,	1989
20. India	1989,	1992
21. Pakistan	1977,	1990
22. Srilanka	1980,	1987
23. Indonesia	1986,	1989
24. Malaysia	1983,	1986
25. Myanmar	1982,	1990
26. Philippines	1982,	1990
27. Philippines	1990,	1992
28. Thailand	1982,	1990
29. VietNam	1987,	1990
30. China	1987,	1990
31. CostaRica	1982,	1992
32. El Salvador	1975,	1988
33. Jamaica	1978,	1985
34. Jamaica	1985,	1989
35. Panama	1980,	1992
36. Nicaragua	1982,	1993
37. Trin/Tobago	1976,	1987
38. Bolivia	1981,	1989
39. Brazil	1975,	1989
40. Colombia	1980,	1989
41. Peru	1984,	1992
42. Venezuela	1982,	1987

For the first time, economic growth and nutritional change can be compared, as illustrated in figure 2. Rapid economic growth is associated with improving nutrition - certainly for such countries as Thailand and Vietnam in the 1980s (points 28 and 29 in Figure 2), and also for those growing well but less fast such as Indonesia (23) and China (30). Other countries with positive economic growth rates generally show nutritional improvement - with considerable variation - but the relationship becomes more diffuse around and below zero growth. Interestingly, prevalence probably still decreases somewhat (about -0.3 pp/year) at zero growth.

An underlying long-term tendency to improvement seems to be the good news - associated with such factors as increasing education and falling fertility - but this is often disturbed by shorter-term crises, which may be economic, political, environmental, or a combination of these. Worse, pessimism is reinforced concerning what the real long-term nutritional trend is in Sub-Saharan Africa.

The deviations from the average line in figure 2 are important. Many of the points seen in figure 2 to be improving faster than the average (for growth) seem plausible - e.g. Jamaica (34), Sri Lanka (22), Zimbabwe (12); similarly a number of notably deteriorating cases are well-recognized - e.g. Ethiopia (1), Madagascar (4), Rwanda (6). (Note that the data for India, 1989-92, point 20, are particularly tentative). Nonetheless, factors explaining the better-than-expected deviations should be examined systematically - for example are they related to social expenditures (health, education, etc.)'? increased food security'? - and preliminary observations outside the scope of this overview, indicate that this may be so.

Interpretation is complicated by the fact that many countries with good economic performance are also able to support specific nutritional activities - Thailand and Indonesia are again examples of this. More detailed investigation is needed to disentangle the relative effects of such different nutrition-relevant actions. Economic growth (in part through increased food security), health and education, and community-based nutrition programmes all probably contribute to improving nutrition.

The availability of nutritional data has improved to such an extent that it is increasingly feasible to assess trends, and indeed in future it will be more possible to focus selectively on countries of special concern and interest. For this analysis in late 1994, 46 trend estimates (country-periods in 35 countries) were available in 1992, 29 national trends could be assessed and for the Update Report in 1989. in only around ten cases could trends be directly estimated. National data (observations at one point in time) are available now from over 100 surveys. The data, compiled by WHO, now usually include prevalences of stunting and wasting, as well as underweight and greater use of these indicators can be foreseen. A number of important publications now regularly include these indicators, such as UNICEF's State of the World's Children and Progress of Nations, UNDP's Human Development Reports, the World Bank's World Development Reports, and Bread for the World's annual Reports on the State of World Hunger. These estimates and publications all use the same basic data, and are generally consistent with each other.

So, in the places where nutrition problems are coming under control - such as Latin America - the '90s have seen continued improvement. But in the two worst affected regions, in numbers and prevalence, the picture is worrisome. Sub-Saharan Africa is deteriorating. South Asia is improving only slowly, if at all. The mid-90s will be crucial.

John Mason
Marito Garcia

Update on the Nutrition Situation, 1994 Contents Chapter 1. Overview (from which this article is taken) Chapter 2. Recent Trends in 14 Countries: Bangladesh. Brazil. China, Costa Rica, Egypt, Ethiopia, India. Kenya. Madagascar, Malawi, Morocco, Philippines, Senegal, and Zambia. Chapter 3. The Nutrition Situation of Refugee and Displaced Populations. Sections on Asia (Afghanistan. Iraq, Butanese Refugees in Nepal, Myanmar (Rohingya) Refugees in Bangladesh) and Sub-Saharan Africa (Sudan, Rwanda/Burundi, Angola, Liberia Region, Mozambique Region. Somalia. Shaba Region in Zaire, Ethiopia, Refugees in Kenya.)

Specific Deficiencies Versus Growth Failure: Type I and Type II Nutrients

Two types of responses have been identified when a child's intake of an essential nutrient is insufficient - either there is continued growth whilst the body uses up the nutrient resulting in specific deficiency signs, or there is reduced growth while the tissue concentration of the nutrient is maintained. Michael Golden of the University of Aberdeen explains.

by Michael H.N. Golden, FRCP, Dept of Medicine and Therapeutics, University of Aberdeen, Scotland.

ⁱ Unfortunately the English language has no pronoun for he/she hence he is used to refer to both males and females.

Why is it important to distinguish these two classes of nutrient? We usually think about specific nutrient deficiencies as if they give a type I response. Type II deficiency is usually ascribed to protein-energy deficiency. Yet the possibility of this latter response - usually growth failure - resulting from other deficiencies has been generally ignored by nutritionists. The deficiencies may therefore remain largely unmeasured and uncorrected.

I have argued^1,2 that type II nutrient deficiency is responsible for considerable amounts of the widespread stunting in height. If this is correct then up to half the children in the world may have unrecognized type II nutrient deficiency. Let us compare and contrast the type I and type II nutrients and explore the implications of the different ways in which we respond to a dietary lack of these nutrients.

Type I Nutrient Deficiency

These are the nutrients (see table 1) which are required principally for specific metabolic functions in the body, rather than for metabolism in general. During deficiency the person continues to grow normally, the body store is consumed and then the concentration of the nutrient in the tissues falls so that the specific metabolic function that depends upon the nutrient declines until the person becomes ill. The illness is recognized by particular and characteristic signs and symptoms; growth may be affected secondary to the illness. Well-known examples are anaemia (iron deficiency); beri-beri (thiamin deficiency); pellagra (niacin or nicotinic acid deficiency); scurvy (vitamin C or ascorbic acid deficiency); xerophthalmia (vitamin A or retinol deficiency); and iodine deficiency disorders (IDD).

The diagnosis of a deficiency of a type I nutrient is relatively straightforward - we can usually recognize the clinical picture; then we either measure the concentration of the nutrient itself or measure the protein or enzyme that depends upon the presence of the nutrient or test the relevant metabolic pathway or physiological function. For example, with iron deficiency we recognize anaemia, examine the red cells and then measure ferritin, iron, transferrin or protoporphyrin. Similarly, with iodine we recognize the goitre and the signs of hypothyroidism and then measure iodine, thyroxine or other thyroid related hormones. Doctors, nurses and nutritionists learn to recognize, diagnose and treat all the type I nutrient deficiencies listed in the table. Because these deficiencies are well recognized, we give priority to ensuring that there are adequate amounts in the diet, we try to supplement or fortify foods where deficiency is common, and we develop specific programmes to alleviate the problems.

Type II Nutrient Deficiency

In contrast, there are no characteristic signs or symptoms that differentiate which type II nutrient deficiency an individual has. They all give the same picture of poor growth, stunting and wasting. This is very important because it means that a person can easily have a specific deficiency that is unrecognized. Usually this is ascribed to overall food inadequacy, or protein-energy malnutrition - but we have generally not distinguished this from other possible causes such as deficiency of other type II nutrients. Most of what follows refers not to energy itself, as discussed in the last section.

When there is a deficiency of one of the type II or 'growth' nutrients the person stops growing, the body starts to conserve the nutrient so that its excretion falls to very low levels and there is minimum reduction in the tissue concentration. With continued or severe deficiency the body may start to break down its own tissues to release the nutrient for use by the rest of the body; this process is associated with a reduction of appetite. There are no body stores of these nutrients, other than normal tissue, that can be called upon in an emergency and into which excess nutrients can be deposited. Thus, as the tissue is broken down to release the deficient nutrient, the excess of all the others that are released during tissue breakdown is excreted from the body and lost. During reversal they will all have to be given to the person to make good these losses as well as replacing the deficient nutrient. These deficiencies do not affect any organ or tissue in particular, except perhaps in relation to those with very a high mitotic and synthetic rate such as the immune system and the intestinal mucosa; rather all tissues and organs are affected.

These have always been the 'problem' nutrients without clearly defined diagnostic tests or determination of human requirements. With animals the requirements have been assessed with "growth" assays. In other words the experimental animal has been given a diet with graded amounts of the nutrient and the point at which there is no increase in growth rate is taken as the requirement. As such experiments have not been performed in humans for ethical reasons, we are not clear about the precise requirements for man. Nevertheless, it is clear that the desired rate of growth is the major determinant of the dietary requirement for all the type II nutrients. They all need to be supplied in greatly increased amounts when rapid weight gain is required, for example during convalescence from illness, and when catch-up in height or weight is needed.

There are major conceptual and practical difficulties when we try to understand these deficiencies. Thus, for example, it is difficult to comprehend how an animal can die from zinc deficiency when it has a normal concentration of zinc in its tissues³; yet such an animal will die without zinc and it will respond rapidly and dramatically to small amounts of dietary zinc. The same applies to the other type II nutrients. To appreciate how this comes about is to understand these nutrients. They form part of the structure and fundamental metabolic machinery of each and every cell; they form the structure of the body and are concerned in practically every metabolic pathway and all the fundamental process such as protein and nucleic acid synthesis, metabolite transport and ionic gradients. During deficiency there is a reduction in all these processes so that the person is less able to withstand environmental stress or infection and maintain his "milieu interieur" and homeostatic control; this is how those with a type II deficiency die.

Responses

The strategy that the body uses for dealing with day to day fluctuations in intake is different for the two classes of nutrient. With the type I nutrients the body maintains a store that is added to and drawn upon to buffer changes in supply. In contrast, with the type II nutrients, some of the dietary intake is incorporated into functional tissue during its "turnover" and the rest, which is in excess, is excreted. In the face of a low intake the body homeostatically reduces the excretion to minute amounts and recycles the nutrient, within the body. However, this conservation and re-use strategy means that growth (which increases the required total pool of the nutrient if the concentration is to be maintained) cannot occur during a period of limited intake; the body maintains the concentration of the nutrient in the tissues mainly by stopping growth as soon as there is a dietary limitation of any one of these nutrients. The child's body goes into a 'maintenance mode', with all the functions, apart from growth, continuing normally. If the low dietary intake continues for a sufficient time then, as the individual 'maintains' himself, he falls further and further behind his peers to eventually present as growth failure.

As the response to a deficiency - growth failure - is the same for each of the nutrients, when we observe growth failure it could be caused by a lack of any one of the type II nutrients and we cannot be sure which is responsible. This is not a major problem in practice because we should treat type II deficiency by giving a diet which contains sufficient amounts of all of these nutrients in a balanced way.

The mechanisms by which the body ceases growth in response to nutritional lack (by reducing the production of the hormonal mediators of growth, down-regulation of receptors, reducing protein synthesis, etc.) give a similar hormonal picture to that seen in endocrine disease. Apart from poor growth, no feature reproducibly corresponds with deficiency, indeed there does not need to be any 'defect' in the animal's metabolic pathways that can be related to the diet and held responsible for the growth delay; only the adaptive hormonal changes mediating the slow growth need be present. Growth failure, and growth failure alone, is the clinical sign characteristic of a diet deficient in protein, zinc, magnesium, phosphorus, potassium, etc. The reduced cellular turnover will also affect the immune system, and these deficiencies may present with an increased prevalence of infectious disease. This is in line with the observation that growth failure is correlated with lowered immune response.

The response to a long standing mild deficiency is a diminutive person, with the body in proportion. The extent of the stunting will be in relation to the integral of the degree of shortfall of the nutrient and time. With a mild deficiency there will be no clinical signs whatsoever, until growth failure becomes apparent: if the diet is restored before growth failure is diagnosed the deficiency will go completely undetected. With a severe deficiency, or pathological loss of the nutrient, there may be loss of tissue leading to wasting, without necessarily time for stunting to become apparent; again the nutritional nature of the wasting may remain undiagnosed and be ascribed to toxins, infection, worms, persistent diarrhoea or another pathological agent. The balance between the severity of the deficiency and its duration will also determine the relative amounts of stunting and wasting that are produced. Mild, chronic deficiencies are expected to be more common than severe, acute deficiencies so that stunting would be predicted to be more common than wasting: this is what is observed.

As a consequence of not having a store for type II nutrients, when there is a negative balance for one of these nutrients, implying tissue catabolism, there is a negative balance for all the components of lean tissue. Thus protein, zinc or potassium deficiency, for example, will each lead to a negative balance of the other type II nutrients, in proportion to their relative concentrations in the tissues that are being broken down. This was shown elegantly by Rudman et al in parenterally fed adults⁴. Nutrient balance studies are thus unreliable in predicting which nutrient is deficient in the diet. When we observe a negative balance for any one nutrient such as nitrogen, we should consider a type II nutrient deficiency as a possible cause. During treatment, as whole tissue has been lost, all the components for that tissue to be resynthesized need to be given irrespective of the cause of the negative balance and weight loss.

Table 1 A. Classification of nutrients according to whether the response to a deficiency is a reduced concentration in the tissues and specific clinical signs (type I), or a reduced growth rate with non-specific signs (type II).
TYPE I nutrients	TYPE II nutrients
iron	potassium
copper	sodium
manganese	magnesium
iodine	zinc
selenium	phosphorus
calcium	protein
fluorine		nitrogen
thiamine		carbon skeletons of essential amino acids
riboflavine		threonine
pyridoxine		lysine
nicotinic acid		sulphur
cobalamin	[oxygen]
folate	[water]
ascorbic acid	[energy]
vitamin A (retinol)
vitamin E (tocopherol)
vitamin D
vitamin K
B. The differences between typical type I and type II deficiency responses
TYPE I			TYPE II
growth continues in early stages			growth failure first response
specific clinical signs develop			no specific clinical signs
tissue concentration drops with deficiency			tissue concentration maintained with deficiency
body stores exist			no body store of these nutrients
concentrated in particular tissues			not in any particular tissue
specific enzymes affected			general effect on metabolism
not usually anorexic			anorexia common response
tissue concentration independent of the other type I nutrients			tissue concentration dependent upon all the other type II nutrients
tissue concentration maintained in different metabolic states			tissue concentration may change (drop) with metabolic state
food sources very variable			ratio in foods not very variable
diagnosed by biochemical tests			do not give biochemical abnormalities
anthropometric abnormality only appears late in the deficiency			diagnosed by anthropometric abnormality

Because of the avid metabolic conservation possible, it is extremely difficult to produce a deficiency of one of these nutrients in the non-growing child or adult by dietary means alone; there usually has to be a pathological loss of the nutrient from the body. Thus, it is almost impossible to produce sodium deficiency in the normal adult⁵ unless there is excess sodium loss in sweat or diarrhoea. Depletion of the type II nutrients sufficiently severe to cause loss of function are thus usually found in association with disease such as persistent diarrhoea and are probably the reason that persistent diarrhoea is associated with anorexia and weight loss (instead of an increased appetite as one would expect with energy deficiency).

Dietary Fellow Travellers

Because the type II nutrients are fundamental to basic biological processes throughout the plant as well as the animal kingdom, they tend to have similar concentration ratios in many foods. It is not, therefore, unusual for diets to be deficient in several of these nutrients. These nutrients are dietary 'fellow travellers'. It is very difficult or impossible to determine if a particular type II nutrient is causing growth failure in the individual², however, it is relatively simple to find out if a child with low weight-for-height or short stature has a deficiency of one of these nutrients. The growth response to a trial of a complete and balanced diet should form part of the assessment of such children, in a setting where such assessments can reasonably be undertaken.

Effect on Appetite

Apart from growth failure, the other response which is common with a deficiency of each of these nutrients is anorexia; this is corrected if the nutrient is supplied. Thus, if a child with zinc deficiency is supplemented with zinc, he will regain his appetite and have an increased intake of protein, energy, potassium, and even non-supplemental zinc, in response to the specific supplement⁶. Clearly with these nutrients it is impossible to interpret dietary intake data for single nutrients or energy as the increase, or decrease, in the intake and utilization of the nutrient under consideration may be caused by a dietary variation of a different nutrient altogether. In the study by Krebs et al⁶, protein intake was low; if supplemental protein (without zinc) had been given there would have been no response and the conclusion possibly drawn that the short stature was not nutritionally based at all. As growth will be limited by the most deficient nutrient, it is only possible to have a 'deficiency', in the classical sense, with one type II nutrient at a time - the limiting one. Thus, even if a diet contains very reduced quantities of a particular nutrient, protein for example, no response to supplementation and no specific consequences are to be expected, if another type II nutrient is even more limiting. When a poor appetite is seen in a patient it is a signal that there may be a type II nutrient deficiency.

The concepts of a type II nutrient have been accepted with respect to the essential amino acids being properly balanced each in its appropriate amount to make a protein with a high 'score' - it might be easiest to understand if this concept is expanded to include all the other type II nutrients as if they were essential amino acids in dietetic terms although, of course, they are nothing like amino acids in metabolic terms.

Strategies for Supplementation

When a dietary supplement is given, which does not contain all the nutrients required for new tissue synthesis, the rate of growth and the efficiency of growth will be determined by the most limiting nutrient in the new diet (basic diet plus supplement), not in the original diet or in the supplement alone, indeed by diluting the original diet an incomplete supplement can make a deficiency worse. Clearly, if an unbalanced supplement is given the other nutrients in the supplement will be used inefficiently; just as a diet with protein which has an amino acid score of zero, because it lacks an essential amino acid, is totally useless and is wasted. The degree of inefficiency is related to the magnitude of the imbalance between the actual limiting nutrient in the diet as a whole and the nutrient under consideration. When we observe an inefficient use of nutrients or energy we can infer that the diet may be unbalanced with respect to one of the type II ingredients that is limiting growth and efficiency. This may be one useful measure of the adequacy of a diet as a whole - the efficiency of use of its energy for growth. Gross inefficiency is almost universal in reported supplementation trials⁷. This is not surprising as all these supplementation trials concentrated on supplying extra protein and energy whilst ignoring the other type II nutrients, particularly potassium, magnesium, zinc and available phosphorus.

As a further complication, the response to the supplement, and the required balance of nutrients in the supplement, will depend upon the precise mix of tissues that the person is trying to lay down. This will depend, in turn, upon the age of the subject, the degree of wasting and stunting that has to be made good, and the composition of the required new tissues. Clearly, the dietary requirements for skeletal growth, for muscle synthesis, for adipose tissue and for skin synthesis are likely to differ - but, by how much, in what way and whether this is ever a major factor has not been explored. It is likely that giving a diet with the same balance of nutrients as that which constitute the tissues themselves, with adjustments made for intestinal absorption, is likely to be the best starting point in prescribing an appropriate intake to prevent undernutrition, promote rapid recovery from illness and shorten convalescence.

Supplementation studies have shown that substantial numbers of children may have a type II deficiency in affluent as well as developing countries. Early investigations in Scotland⁸ and Alabama⁹ showed a growth response to adding milk to poor children's diets, the same response was shown by Malcolm in New Guinea¹⁰. In Africa there are consistent height differences between population groups that have different staple foods¹¹. And there are differences between the growth of western infants with different formulae^12-14. In a series of studies in Colorado, Hambidge has shown a rapid increase in height with zinc supplementation of short children¹⁵. Similarly, in Ontario, 25% of short children responded to zinc supplementation with a height spurt¹⁶. Perhaps the children that did not respond to zinc had their height limited by one of the other type II nutrients. It would seem that the human response to a deficiency is the same as in experimental animals and that unsuspected nutritional limitation is a common cause of short stature.

I would emphasize that the examples chosen to illustrate the nature of deficiency of these nutrients have been largely drawn from work with zinc. This is because there has been a lot of interest and data published on the effect of zinc whereas magnesium, potassium and phosphorus, for example, have been ignored by nutritionists. However, the same principles apply to all of them and not just to the nutrients studied in the experiments reported. The crucial thing is to have the right balance of type II nutrients in the diet: this rarely happens and most of the supplemental diets we currently give to malnourished children or adults are limiting in one or other of the type II nutrients.

Deficiency of the type I nutrients give rise to biochemical abnormalities without any necessary anthropometric changes whereas the type II nutrients give rise to anthropometric abnormalities without biochemical changes. Clearly both are needed to assess the nutritional status of an individual patient. Nevertheless, it is ironic that anthropometric criteria are used to diagnose undernourished and malnourished individuals, who are then all too often treated with a diet that has energy and all the type I nutrients (whose deficiencies are prevalent) whilst the deficiencies (type II nutrients) that gave the wasting and stunting in the first place remain uncorrected. There is a pressing need for a new way of addressing the nutritional problems of the malnourished in a balanced and rational way.

Energy Deficiency

Although ENERGY could be regarded as similar to a type II nutrient in some respects, it really falls into a separate nutritional category. If type I nutrients are used for specific pathways and type II as building blocks of tissue, energy is the fuel that is burnt to power the process; "energy" is not a nutrient, per se; it is a measure of total food intake. Pure energy deficiency rises when there is insufficient food available (famine). However, a low energy (food) intake is frequently a result of loss of appetite rather than lack of available food of some sort; low energy intake is then not a primary Cause of malnutrition but secondary to the anorexia of type II nutrient deficiency, infections or other illnesses that similarly affect metabolism such as liver disease. Provision of more of the type of food that is already available within the household will not correct a low energy intake and weight loss due to anorexia, rather the underlying cause should be identified and corrected - unrecognised type II nutrient deficiency may be a common cause of this anorexia, and should be addressed by changing the quality of the food available rather than simply its quantity.

References

1. Golden, M.H. (1988) The Role of Individual Nutrient Deficiencies in Growth Retardation of Children as Exemplified by Zinc and Protein. In: Linear Growth Retardation in Less Developed Countries, pp. 143-163. Ed. Waterlow, J.C. Raven Press, New York.

2. Golden, M.H. (1991) The Nature of Nutritional Deficiency in Relation to Growth Failure and Poverty. Acta Paediatrica Scandanavica, 374, 95-110.

3. Williams, R.B. & Mills, C.F. (1970) The Experimental Production of Zinc Deficiency in the Rat. British Journal of Nutrition, 24, 989-1003.

4. Rudman, D., Millikan, W.J., Richardson, T.J.. Bixler II, T.J., Stackhouse, W.J. & McGarrity, W.C. (1975) Elemental Balances During Intravenous Hyperalimentation of Underweight Adult Subjects. Journal of Clinical Investigation, 55, 94-104.

5. McCance, R.A. (1936) Experimental Human Salt Deficiency. Lancet, 1, 823-830.

6. Krebs, N.F., Hambidge, K.M. & Walravens, P.A. (1984) Increased Food Intake of Young Children Receiving a Zinc Supplement. American Journal of Diseases of Childhood, 138, 270-273.

7. Beaton, G.H. & Ghassemi, H. (1982) Supplementary Feeding Programs for Young Children in Developing Countries. American Journal of Clinical Nutrition, 35, 864-916.

8. Orr, J.B. (1928) Milk Consumption and the Growth of School Children. Lancet, 1, 202-203.

9. Spies, H., Dreizen, S., Snodgrasse, R.M., Arnett, C.M. & Webb-Peploe, H. (1959) Effect of Dietary Supplement of Non Fat Milk on Human Growth Failure. American Journal of Diseases of Childhood, 98, 187-197.

10. Lampl, M., Johnston, F.E. & Malcolm, L.A. (1978) The Effects of Protein Supplementation on the Growth and Skeletal Maturation of New Guinean School Children. Annals of Human Biology, 5, 219-227.

11. Nicol, B.M. (1959) The Protein Requirements of Nigerian Peasant Farmers. British Journal of Nutrition, 13, 307-320.

12. Fomon, S.J., Filer, L.J., Thomas, L.N.. Anderson, T.A. & Nelson, S.E. (1975) Influence of Formula Concentration on Caloric Intake and Growth of Normal Infants. Acta Paediatrica Scandanavica, 64, 172-181.

13. Fomon, S.J., Filer, L.J., Ziegler, E.E., Bergmann, K.E. & Bergmann, R.L. (1977) Skim Milk in Infant Feeding. Acta Paediatrica Scandanavica, 66, 17-30.

14. Salmenpera, L., Perheentupa, J. & Siimes, M.A. (1985) Exclusively Breast Fed Healthy Infants Grow Slower than Reference Infants. Pediatric Research, 19, 307-312.

15. Walravens, P.A. & Hambidge, K.M. (1976) Growth of Infants Fed a Zinc Supplemented Formula. American Journal of Clinical Nutrition, 29, 1114-1121.

16. Gibson, R.S., Vanderkooy, P.D.S., MacDonald, A.C., Goldman, A., Ryan, B.A. & Berry, M. (1989) A Growth-Limiting, Mild Zinc-Deficiency Syndrome in Some Southern Ontario boys with Low Height Percentiles. American Journal of Clinical Nutrition, 49, 1266-1273.

Enrichment of Food Staples Through Plant Breeding. A New Strategy for Fighting Micronutrient Malnutrition

Howarth Bouis of the International Food Policy Research Institute (IFPRI) presents arguments for investing in a new strategy for reducing micronutrient malnutrition, through plant breeding.

by Howarth Bouis, Research Fellow, International Food Policy Research Institute, Washington, D.C.

The four, broad, widely-recognized strategies for reducing micronutrient malnutrition are supplementation, fortification, dietary diversification, and disease reduction. This note introduces arguments for investing in a fifth, broad, concurrent strategy - plant breeding. Plant breeding not only holds great promise for making a significant, low-cost, and sustainable contribution to reducing micronutrient, particularly mineral, deficiencies in humans, it also may well have important spinoff effects for increasing farm productivity in developing countries in an environmentally-beneficial way. Trace minerals are important not only for human nutrition, but for plant nutrition as well.

An underlying cause and fundamental constraint to solution of the micronutrient problem is that non-staple foods, particularly animal products, tend to be the foods richest in bioavailable micronutrients, which the poor in many developing countries desire to eat. but cannot afford. Their diets consist mostly of staple foods, primarily cereals - in fact, per capita direct consumption of staple foods overall varies little according to income level. For the poor, these staple foods are primary sources of what micronutrients they are able to consume, particularly minerals. This also means that micronutrient deficiencies are likely to be more common than energy deficiency.

The plant breeding strategy seeks to take advantage of this existing human consumption behavior by developing staple food crops that, in some sense, fortify themselves - breeding staple crop genotypes that load high amounts of minerals and vitamins into their seeds.

The initial steps in the long-term effort to bring this strategy to a successful conclusion have already been taken by the Consultative Group on International Agricultural Research (CGIAR), a group of seventeen internationally-funded agricultural research centers seeking to raise farm productivity and food consumption in developing countries. Over the past two years, a coordinated plan has been developed involving collaborative research on five major staple food crops (rice, wheat, maize, beans, and cassava) between five core research institutes: three CGIAR Centers - (The International Center for Tropical Agriculture[CIAT], The International Center for Maize and Wheat Improvement [CIMMYT], and The International Rice Research Institute [IRRI]); the Waite Agricultural Research Institute of the University of Adelaide in Australia; and the Plant, Soil, and Nutrition Laboratory (PSNL) run by the USDA-ARS and located on the Cornell University campus - and a number of other collaborating institutes and scientists in developing and developed countries. The project was initiated and is being coordinated by a fourth CGIAR Center, the International Food Policy Research Institute (IFPRI). Initial screening for promising germplasm has already commenced, drawing on extensive germplasm banks located at CIAT, CIMMYT, and IRRI. and seeds provided by collaborating agricultural research organizations in developing countries.

Five Core Questions

A strategy of breeding plants that enrich themselves, that load high amounts of minerals and vitamins into their edible parts, has the potential for substantially reducing recurrent costs that are associated with other strategies, such as fortification and supplementation. However, this approach will work only if farmers are willing to adopt such varieties, if the edible parts of these varieties are palatable and acceptable to consumers, and if the extra micronutrients can be absorbed by the human body. In examining the feasibility of a plant breeding strategy, it is imperative to address five core questions, which are discussed below. Readers are referred to various references for more detailed justifications of the abbreviated answers provided.

Is it scientifically feasible to breed for staple food varieties whose seeds are micronutrient-dense? If so, how long will it take to develop such varieties?

There are at least three cases of agricultural research projects in developed countries which have successfully manipulated the efficiency of mineral uptake of plants and the mineral content of plant seeds, all of which have been commercially successful: zinc-dense wheat varieties, developed at the Waite Agricultural Research Institute of the University of Adelaide to improve plant nutrition in zinc "deficient" soils, are already being grown on a commercial basis in Australia; in the United States, an iron-efficient soybean has been developed to overcome problems of iron "deficient" soils; and also in the United States, cadmium levels in durum wheats have been reduced through plant breeding so as to meet quality standards in countries importing U.S. wheat.

In the Australian case, this breeding strategy was motivated by previous, more basic scientific research at Waite involving the trace minerals manganese and copper, which suggested that genetic variation between plant varieties was affecting the levels of uptake and grain content of these and other microelements and was associated with tolerance to low plant availability of the element in the soil.

Plant breeders associated with the CGIAR project estimate that, if the genetic inheritance is relatively simple as argued by Graham and Welch (1994), improved varieties could be developed within four years of having the essential facts and tools necessary for genetic improvement, but this time could double if genetic inheritance turns out to be unexpectedly complex and linked to undesirable traits. In either case, two to three years need to be added to this for national government agricultural research programs to test the new varieties before their release. Thus, ten years may be required before nutritionally-improved varieties could be available for commercial production by farmers in developing countries. A more optimistic estimate is six years, if exploratory work with promising genetic material identified at the beginning of the project proves successful.

What effect will breeding for micronutrient-dense seeds have on plant yields? Will farmers adopt such varieties?

Results from research at Waite and elsewhere show that where the soil is deficient in a particular micronutrient, seeds containing more of that nutrient have better germination, better seedling vigor, and/or more resistance to infection during the vulnerable seedling stage. These benefits to crop establishment can result in higher crop yield. Thus, the specific breeding goals for human and plant nutrition largely coincide. There is the expectation, therefore, that the new cultivars with higher contents of micronutrients will have an agronomic advantage to ensure they are competitive in the market place. In box 1 a summary of the main points made in a keynote paper presented by Drs. Robin Graham of Waite and Ross Welch of PSNL (1994) at an organizational workshop held in January 1994 is given, outlining the reasons to expect positive impacts on plant yields of crop varieties that are efficient in the uptake of mineral micronutrients from soils and that load high amounts of these minerals into seeds. Readers are referred to that paper for descriptions of studies and experiments undertaken to support the conclusions cited.

Will breeding for micronutrient-dense seeds change processing or consumer characteristics of staple foods?

Mineral micronutrients comprise a tiny fraction of the physical mass of a seed, perhaps ten parts per million. Dense seeds may contain perhaps as many as fifty parts per million. It is not expected that such small amounts will alter the appearance, taste, texture, or cooking quality of foods.

Betacarotene is associated with an orange or yellow color. Increasing the content of betacarotene in the seed will alter its color, which initially might well reduce consumer preference. However, through nutrition education, the potential drawback of a deep orange or yellow color clearly marking a nutrient-dense product, possibly could be turned to an advantage.

Will micronutrient intakes be increased to a significant degree? To what extent will the extra micronutrients in staple foods consumed be bioavailable?

An underlying cause and fundamental constraint to solution of the micronutrient problem is that non-staple foods, particularly animal products, tend to be the foods richest in bioavailable micronutrients, which the poor in developing countries cannot afford. Their diets consist mostly of staple foods, primarily cereals; in fact, per capita direct consumption of staple foods in the aggregate varies little by income level. For the poor, these staple foods already are primary sources of what micronutrients they are able to consume, particularly minerals.

Evidence on food staple consumption behavior suggests that, if the presently low iron content of food staples could be increased by a factor of 3.5 (say from 12 to 42 parts per million), this would double iron intakes, as suggested by data from the Philippines shown in table 1 (Bouis 1991). However, would this double the amount of bioavailable iron?

FAO/WHO recommends that people who obtain less than 10 percent of their calories from animal foods (this applies to the surveyed Philippine population as shown in table 1) need more iron because perhaps only 5 percent of total intake is absorbed. While doubling iron intakes would not allow the surveyed Philippine females to attain this RDA, particularly at very low income levels, there is no reason to think that the degree of absorption of additional iron would be lower than the present rate of absorption. Thus, bioavailable iron would also double, which should be of substantial benefit.

A breeding strategy of lowering the level of inhibiting substances (e.g. phytin) in the grain has often been suggested to increase the bioavailability of minerals already consumed. Phytin, being the primary storage form of phosphorus in most mature seeds and grains, is an important compound required for early seed germination and seedling growth (Welch 1986). Phytin plays an important role in determining mineral reserves of seeds and, thus, contributes to the viability and vigor of the seedling produced (Welch 1986, 1993). Selecting for seed and grain crops with substantially lower phytin content could have an unacceptable effect on production, especially in regions of the world having soils of low phosphorus status and/or poor micronutrient fertility (Graham and Welch 1994).

Such attempts to significantly lower the antinutrient content of seeds and grains requires a major shift in seed or grain composition. Because most of the antinutrients known to occur in seeds and grains are major organic constituents of these organs, they may play additional, but yet unrecognized, beneficial roles in plant growth and human health. Therefore, a breeding strategy of attempting to increase iron bioavailability by reducing antinutrient content is not recommended (Graham and Welch 1994).

Certain amino acids (such as cysteine and lysine, but particularly methionine) enhance iron and/or zinc bioavailability. These amino acids occur in many staple foods, but their concentrations are lower than those found in meat products. A modest increase in the concentrations of these amino acids in plant foods may have a positive effect on iron and zinc bioavailability in humans. Iron and zinc occur only in micromolar amounts in plant foods, so only micromolar increases in the amounts of these amino acids may be required to compensate the negative effects of antinutrients on iron and zinc bioavailability. These amino acids are essential nutrients for plants as well as for humans, so relatively small increases of their concentrations in plant tissues should not have adverse consequences on plant growth. The optimal breeding strategy from the point of view of bioavailability may be to increase levels of promotor compounds (Graham and Welch 1994).

Table 1. Intakes and Adequacy of Iron Intakes by Food Group by Income Group and by Type of Family Member, Bukidnon, Philippines.
Expenditure Quintile	1	2	3	4	5	All
Milligrams of iron per adult equivalent per day
Food Staples	3.5	3.8	4.0	4.0	4.4	3.9
Meat, fish	1.2	1.5	1.7	2.3	3.7	2.0
Other Foods	1.9	2.2	2.4	2.4	2.2	2.3
All	6.6	7.5	8.1	8.7	10.3	8.2
Percent of RDA
Preschoolers	65	78	77	86	107	81
Boys (6-12)	75	84	86	88	124	91
Boys (13-19)	68	69	80	80	89	77
Fathers	110	124	134	147	167	137
Girls (6-12)	70	65	80	84	103	78
Girls (13-19)	43	49	56	54	60	53
Mothers	53	57	62	66	76	63
All Family Members	66	75	81	87	103	82

Are there other lower-cost, more easily sustainable strategies for reducing micronutrient malnutrition?

A plant breeding strategy, if successful, will not eliminate the need for supplementation, fortification, dietary diversification, and disease reduction programs in the future. Nevertheless, this strategy does hold promise for significantly reducing recurrent expenditures required for these higher-cost, short-run programs by significantly reducing the numbers of people requiring treatment.

For example, in treating iron-deficiency in developing countries, Yip (1994) argues that if prevalence rates are above 25%, the best approach is to develop programs to improve the iron nutrition for the entire population. In such situations, which for preschoolers and women in developing countries are the rule rather than the exception, this is cheaper than screening for iron-deficient individuals (in any event, the capacity does not exist to screen such large numbers of people). By increasing the iron content of food staples through plant breeding, the entire distribution curve for iron status (e.g. see figures 1, 3, and 4 in Yip) would be shifted to the right, so that targeting a subsequently smaller group of iron-deficient persons may become feasible. The iron intakes of those who still remain iron-deficient would be increased, and so would be of some benefit.

What is the cost of plant breeding as compared with fortification and supplementation programs? The plant breeding effort can be thought of as a two-stage process. The first five-year phase will involve research primarily (but not exclusively) at the five core agricultural research centers mentioned above. The cost has been estimated at about $2 million per year for research on all five crops. During this initial phase, promising germplasm will be identified and the general breeding techniques will be developed for adapting nutrient-rich, high-yielding varieties produced at these international agricultural research centers to specific growing environments in developing countries during phase two.

During phase two, the research sites will shift towards national agricultural research centers and the focus of the research will shift to adaptive breeding. Total costs for phase 2 are difficult to estimate, but will depend on the number of countries involved and the number of crops worked on in each country. Certainly, the annual costs for a individual country should not be more than the annual costs incurred by the five core agricultural research centers during phase one. After release of the successfully adapted, nutrient-rich varieties for commercial production, some maintenance breeding will be necessary.

To provide some sense of the magnitude of the recurrent annual costs involved in fortification and supplementation, a lower-bound estimate of the cost of iron supplementation is $2.65 per person per year when all administrative costs are taken into account (Levin et. al. 1993). A lower-bound estimate for iron fortification is 10 cents per person per year. Consider a populous country such as India where as many as 28 million pregnant women may be anemic in any given year out of a total population of 880 million.

Box 1. Why Mineral Micronutrient-Efficient Crop Varieties Would Lead to Improved Crop Yields. Summary of the main points made in a keynote paper presented at an organizational workshop on Food Policy and Agricultural Technology to Improve Diet Quality and Nutrition, January 1994, Annapolis, MD. A low amount of a trace mineral in a "deficient" soil is not the problem, but rather the key to better plant growth is making more of the trace mineral that is already in the soil "available" to the plant. A soil is said to be "deficient" in a nutrient when addition of fertilizer containing that nutrient produces better growth. However, the amount of a soil. This is because the major part of the trace mineral in the soil is "unavailable" to plants. The trace mineral is chemically bound to other elements in the soil. An alternative view, therefore, is that there is a genetic deficiency in the plant, rather than a deficiency in the soil. Tolerance to micronutrient-deficient soils, termed micronutrient efficiency, is a genetic trait of a genotype or phenotype that causes it to be better adapted to, or yields more in, a micronutrient deficient soil than can an average cultivar of the species (Graham 1984). Crowing zinc-efficient plants on zinc-deficient soils, for example, represents a strategy of "tailoring the plant to fit the soil" in contrast with the alternative strategy of "tailoring the soil to fit the plant" (terminology according to Foy [1983]). These efficient genotypes exude substances from their roots which chemically unbind trace minerals from other binding elements and so make the trace minerals available to the plant. It is well understood that depletion of soil nitrogen takes only a few years if there is no replacement. Thus it is pointless to breed for greater tolerance to nitrogen-deficient soils. Phosphorus efficiency results in overall improvements in cost-efficiency, but depletion of soil phosphorus will eventually occur without replenishment. By contrast for mineral micronutrients, depletion may take hundreds or thousands of years, or may likely never occur at all, owing to various inadvertent additions and other processes (for example, minerals carried in windblown dust [Graham 1991]). It for which soil availability is low, but for which there are large reserves in the soil. Micronutrient-deficient soils are widespread throughout developing countries. As a guide, based on a number of soil surveys, particularly in China where the most extensive soil surveys have been done, it can be estimated that Iron is the fifth most abundant element in the earth's crust, but the fraction of soil iron that may be in soluble form suitable for absorption by plants may be only 10-13% of total soil iron. Thus, depletion of soil iron is never an issue; rather, the issue is the ability of the plant to mobilise sufficient iron to satisfy its needs. Zinc deficiency is probably the most widespread micronutrient deficiency in cereals. Sillanpaa (1990) found that 49 percent of a global sample of 190 soils in 25 countries were low in zinc. Unlike other micronutrients, it is a common feature of both cold and warm climates, drained and flooded soils, acid and alkaline soils, and both heavy and light soils. Efficiency in the uptake of mineral micronutrients from the soil is associated with disease resistance in plants and so decreased use of fungicides. Good nutritional balance is as important to disease resistance in plants as it is in humans. Micronutrient deficiency in plants greatly increases their susceptibility to diseases, especially fungal root diseases of the major food crops. The picture emerging from physiological studies of roots spanning four decades is that the elements phosphorus, zinc, boron, calcium, and manganese are all required in the external environment of the root for membrane function and cell integrity. In particular, phosphorus and zinc deficiencies in the external environment promote leaking of cell contents such as sugars, amides, and amino acids, which are chematoxic stimuli to pathogenic organisms. In the case of zinc, a high internal zinc content did not prevent leakiness due to a deficiency of zinc external to the membrane. It appears that micronutrient deficiency predisposes the plant to infection, rather than the infection causing the deficiency through its effect on root pruning (Graham and Rovira 1984; Sparrow and Graham 1988; Thongbai et al. 1993). Breeding for micronutrient efficiency can confer resistance to root diseases that had previously been unattainable. This means a lower dependence on fungicides, where they are already being used. Micronutrient-efficient varieties grow deeper roots in mineral deficient soils and so are better able to tap subsoil water and minerals. When topsoil dries, roots in the dry soil zone (which are the easiest to fertilize) are largely deactivated and the plant must rely on deeper roots for further nutrition. Roots of plant genotypes that are efficient in mobilizing surrounding, external minerals, not only are more disease resistant, but are better able to penetrate deficient subsoils and so make use of the moisture and minerals contained in subsoils. This reduces the need for fertilizers and irrigation. Plants with deeper root systems are more drought resistant. Micronutrient-dense seeds are associated with greater seedling vigor that, in turn, is associated with higher plant yield. An important function of the seed is to supply the young seedling with minerals until it has developed a root system large enough to take over this The result is a transient and critical period of deficiency when the seedling is particularly vulnerable. Pathogens and weeds may gain an advantage not otherwise given, so that the plants never regain lost potential. There is substantial genetic variability in the efficiency of uptake of mineral micronutrients from deficient soils and in nutrient loading into seeds; micronutrient efficiency is controlled by major, single gene inheritance. The concentration and content of mineral micronutrients in seeds are the result of transport via living tissues (the phloem) from vegetative parts of the plant. Thus, seed density depends on both the micronutrient density of vegetative tissues and on the efficiency of the transport process itself. plant are high in micronutrients, the levels in the seed are always relatively low. An average view of genetic variation in micronutrient density is probably of the order of a factor of three, while their vegetative parts may vary perhaps 100 times more than that. By far the most extensive survey of efficiency factors was carried out at the International Rice Research Institute by Ponnamperuma (1982). Over a period of 10 years, some 80,000 lines from the world collection were screened for types tolerant of a number of soil stresses, including micronutrient deficiencies. Tolerant types gave a yield advantage of about two tons per hectare under any of seven different soil limitations. Ponnamperuma noted that zinc deficiency was widespread in wet rice and iron deficiency in dryland rice. Linkage of zinc efficiency to other efficiency traits (for example, manganese) is poor, suggesting independent mechanisms and genetic control not linked to gross root system geometry. Zinc-efficient genotypes absorb more zinc from deficient soils, produce more dry matter and more grain yield, but do not necessarily have the highest zinc concentrations in tissue or grain. Although high grain zinc concentration also appears to be under genetic control, it is not tightly linked to agronomic zinc efficiency traits and may have to be selected for independently.

These figures imply that treating one-half of the anemic pregnant women in any one year through a well-targeted supplementation program would cost $37 million per year. A fortification program reaching half of the population would cost $44 million per year. Thus, the projected costs of a plant breeding strategy are relatively low. The major part of the cost is the initial one-time cost of development.

One can imagine that there will be unforeseen problems and costs associated with plant breeding not mentioned here. Daily doses of iron from supplementation and fortification programs may be higher than the additional iron likely to be added to the daily intake of food staples through plant breeding. Nevertheless, whatever refinements are necessary to these comparative cost estimates, there is no arguing the tact that the base, fixed costs of plant breeding are sufficiently low, that cost considerations are overwhelmingly on the side of a plant breeding strategy as compared with supplementation and fortification.

Moreover, these comparative costs do not take into account the potential benefits to improved agricultural productivity. For example, a CIMMYT wheat breeder based in Turkey, where soils are particularly zinc-deficient, went to Australia in 1993 to learn about ongoing plant research there, where growing conditions and soil constraints to improved productivity are similar to those in Turkey. He gave a presentation at the organizational workshop in which he estimated that, if the Australian zinc-dense seed varieties were adapted to growing conditions in Turkey, Turkish wheat tanners would save $100 million annually in reduced seeding rates alone (seeding rates could be reduced from an average of 250 to 150 kilograms per hectare on 5 million hectares; a ton of wheat sells for about US$200 on the world market). This does not count the benefit to yield, or the potential benefit of improved zinc status in humans.

Conclusion

Because of the comparatively long lead times involved in bringing the results of plant breeding research to bear on the mineral deficiency problem in humans, these efforts will not contribute to meeting the end-of-decade goals for reducing micronutrient malnutrition set out in the World Declaration on Nutrition and endorsed by 158 countries at the International Conference on Nutrition. However, the timing of the CGIAR project is such that the mineral-dense seed technologies could come "on-line" just after the major push to meet the end-of-decade goals through higher-cost strategies has run its course.

It would seem prudent to invest now in a plant breeding strategy to sustain the gains made by the end of the decade and to maintain momentum for further reductions in iron and other mineral deficiencies.

Very significant progress has been made in terms of (i) putting much of the requisite network of people and institutions in touch with one another, (ii) obtaining consensus among an interdisciplinary group of scientists that this research strategy looks promising in terms of its scientific feasibility and potential for improving human nutrition in developing countries, (iii) obtaining agreement on specific activities that scientists and institutions must undertake in coordination to make this happen, and (iv) initiating the research activities.

The key issues are not those of cost, or whether plant breeders eventually will be successful in developing micronutrient dense seeds if the relatively modest resources required are found to develop them. Rather the two key issues are:

(1) Will the agronomic advantages of the mineral-dense seeds be sufficiently strong that they will be widely adopted by farmers in developing countries?

(2) Will the additional nutrients contained in the seeds be of a sufficient magnitude and sufficiently bioavailable so as to have an appreciable impact on micronutrient status?

References

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Foy, C. D. (1983). Plant Adaptation to Mineral Stress in Problem Soils. Iowa State Journal of Research. 57. 355-391.

Graham, R. D. (1984). Breeding for Nutritional Characteristics in Cereals. Advances in Plant Nutrition, 1, 57-102.

Graham. R. D. (1991). Breeding Wheats for Tolerance to Micronutrient Deficient Soil: Present Status and Priorities. In: Wheat for the Nontraditional Warm Areas, ed. D. A. Saunders, 315-332. Mexico City, Mexico: Centro Internacional de Mejoramiento de Maiz y Trigo.

Graham. R. D., & Rovira, A.D. (1984). A Role for Manganese in the Resistance of Wheat to Take-all. Plant Soil, 78, 441-444.

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Ponnamperuma, F. N. (1982). Genotypic Adaptability as a Substitute for Amendments on Toxic and Nutrient-Deficient Soils. In: Plant Nutrition 1982. Proceedings of the Ninth International Plant Nutrition Colloquium, ed. A. Scaife, 467-473. Slough: Commonwealth Agricultural Bureaux.

Sillanpaa, M. (1990). Micronutrient Assessment at the Country Level: An International Study. FAO Soils Bulletin, 63. Rome: Food and Agriculture Organization of the United Nations.

Sparrow, D. H., & Graham, R.D. (1988). Susceptibility of Zinc-Deficient Wheat Plants to Colonization by Fusarium graminearum Schw. Group 1. Plant Soil, 112, 261-266.

Thongbai, P., Hannam, R.J., Graham, R.D. & Webb, M.J. (1993). Zn Nutrition and Rhizoctonia Root Rot of Cereals. Plant Soil (in press).

Welch. R. M. (1986). Effects of Nutrient Deficiencies on Seed Production and Quality. Advances in Plant Nutrition, 2, 205-247.

Welch, R. M. (1993). Zinc Concentrations and Forms in Plants for Humans and Animals. In: AD Robson, ed, Zinc in soils and plants, ed. A. D. Robson, 183-195. Dordrecht, Netherlands; Boston, Mass., U.S.A.: and London: Kluwer Academic Publishers.

Yip, R. (1994). Iron Deficiency: International Programmatic Approaches. Journal of Nutrition.