12
This article appeared in a journal published by Elsevier. The attached copy is furnished to the author for internal non-commercial research and education use, including for instruction at the authors institution and sharing with colleagues. Other uses, including reproduction and distribution, or selling or licensing copies, or posting to personal, institutional or third party websites are prohibited. In most cases authors are permitted to post their version of the article (e.g. in Word or Tex form) to their personal website or institutional repository. Authors requiring further information regarding Elsevier’s archiving and manuscript policies are encouraged to visit: http://www.elsevier.com/copyright

Nutritional value of leafy vegetables of sub-Saharan Africa and their potential contribution to human health: A review

  • Upload
    up-za

  • View
    0

  • Download
    0

Embed Size (px)

Citation preview

This article appeared in a journal published by Elsevier. The attachedcopy is furnished to the author for internal non-commercial researchand education use, including for instruction at the authors institution

and sharing with colleagues.

Other uses, including reproduction and distribution, or selling orlicensing copies, or posting to personal, institutional or third party

websites are prohibited.

In most cases authors are permitted to post their version of thearticle (e.g. in Word or Tex form) to their personal website orinstitutional repository. Authors requiring further information

regarding Elsevier’s archiving and manuscript policies areencouraged to visit:

http://www.elsevier.com/copyright

Author's personal copy

Critical Review

Nutritional value of leafy vegetables of sub-Saharan Africa and their potentialcontribution to human health: A review

Nangula P. Uusiku a, Andre Oelofse a, Kwaku G. Duodu b,*, Megan J. Bester c, Mieke Faber d

a Centre for Nutrition, Department of Food Science, Faculty of Natural and Agricultural Sciences, University of Pretoria, Pretoria, 0002, South Africab Department of Food Science, Faculty of Natural and Agricultural Sciences, University of Pretoria, Pretoria, 0002, South Africac Department of Anatomy, School of Medicine, Faculty of Health Sciences, University of Pretoria, Pretoria, 0002, South Africad Nutritional Intervention Research Unit, Medical Research Council, P O. Box 19070, Tygerberg, 7505, South Africa

1. Introduction

Rural people of sub-Saharan Africa include indigenous andtraditional vegetables in their diet. African leafy vegetables (ALVs),also known generically as African spinach, contribute significantlyto household food security and add variety to cereal-based staplediets (Van den Heever, 1997). Traditionally, these vegetables arecooked and eaten as a relish together with a starchy staple food,usually in the form of porridge (Vainio-Mattila, 2000). Leafyvegetable (LV) dishes may be prepared from a single plant speciesor from a combination of different species, and the combinationseaten vary daily (Marshall, 2001). When the ALVs are cooked, salt isusually added to enhance the taste. Oil, butter, groundnuts,coconut, milk, bicarbonate of soda, tomato and onion are also

added depending on availability and preference (Nguni and Mwila,2007; Ogoye-Ndegwa and Aagaard-Hansen, 2003).

The consumption pattern of ALVs is different among house-holds within different countries. In South Africa, the consumptionpattern is highly variable and depends on factors such as povertystatus, degree of urbanization, distance to fresh produce marketsand season of the year (Jansen Van Rensberg et al., 2007). Poorhouseholds use these leafy vegetables (LVs) more than theirwealthier counterparts (Jansen Van Rensberg et al., 2007). In asurvey done in Nairobi (Kenya), ethnicity was shown to stronglyinfluence households’ choice and consumption of LVs (Kimiyweet al., 2007). In Bulamogi County of Uganda, the consumption ofwild food plants is limited to casual encounters, periods of foodshortages and as supplements to major food crops (Tabuti et al.,2004).

The frequency of consumption of ALVs has decreased over theyears, probably because ALVs are often considered to be inferior intheir taste and nutritional value compared to exotic vegetables

Journal of Food Composition and Analysis 23 (2010) 499–509

A R T I C L E I N F O

Article history:

Received 15 October 2009

Received in revised form 6 May 2010

Accepted 17 May 2010

Keywords:

Leafy vegetables

Wild foods

Indigenous foods

Sub-Saharan Africa

Nutritional value

Nutrient retention after processing

Antinutrients

Species differences

Human health

Nutritional status

Undernutrition

Protein-energy malnutrition

Micronutrient deficiencies

Horticulture and biodiversity

Food analysis

Food composition

A B S T R A C T

This paper reviews the literature on African leafy vegetables (ALVs) consumed in sub-Saharan Africa. The

aim is to evaluate the nutritional value of these plant species and their potential impact on the

nutritional status of the people living in sub-Saharan Africa. Processing and the presence of

antinutritional factors are taken into consideration as they adversely affect the nutritional content of

the ALVs. The role of dietary fiber and other important components found in ALVs is also discussed due to

their importance in the prevention of chronic and lifestyle diseases. Many of the ALVs are good sources of

micronutrients, especially Manihot esculenta which contains 1970 mg retinol equivalents/100 g edible

portion and 311 mg/100 g of vitamin C, as well as Chenopodium album with up to 6 mg/100 g iron,

18.5 mg/100 g zinc, 226 mg/100 g calcium and up to 211 mg/100 g magnesium. These vegetables may

help to meet daily requirements of these and other essential nutrients, especially in individuals with

marginal nutritional status. Furthermore, ALVs such as Arachis hypogea and Bidens pilosa are good

sources of dietary fibre, while Nasturtium aquatica, Urtic dioica and Xanthosoma mafaffa are excellent free

radical scavengers. In many instances ALVs have levels of these components that are higher than those of

exotic vegetables such as spinach and cabbage. Factors such as storage, cooking methods and drying

influence the micronutrient, antioxidant and antinutritional factor content of these vegetables. The

consumption, cultivation and possibly the commercialization of these ALVs should therefore be

promoted.

� 2010 Elsevier Inc. All rights reserved.

* Corresponding author. Tel.: +27 12 420 4299; fax: +27 12 420 2839.

E-mail address: [email protected] (K.G. Duodu).

Contents lists available at ScienceDirect

Journal of Food Composition and Analysis

journa l homepage: www.e lsev ier .com/ locate / j fca

0889-1575/$ – see front matter � 2010 Elsevier Inc. All rights reserved.

doi:10.1016/j.jfca.2010.05.002

Author's personal copy

such as spinach (Spinacea oleracea) and cabbage (Brassica

olearacea) (Weinberger and Msuya, 2004). In addition, preferenceof ALV species differs depending on the gender and age ofconsumers, as well as cultural background and geographicallocation (Jansen Van Rensberg et al., 2004). When available, theALVs are preferred over exotic vegetables (Marshall, 2001;Shackleton et al., 1998). Several studies have indicated that theALVs contain micronutrient levels as high as or even higher thanthose found in most exotic LVs (Kruger et al., 1998; Odhav et al.,2007; Steyn et al., 2001; Weinberger and Msuya, 2004). LVs arecooked using traditional methods, and the excess is often dried andstored for consumption during the off-season (Vainio-Mattila,2000). The cooking or preparation methods and period of cookingmay affect the nutritional value as well as the bioavailability ofmany nutrients (Gupta and Bains, 2006; Leskova et al., 2006).

This paper reviews studies on LVs in sub-Saharan Africa. Thepurpose of this paper is to determine whether these ALVs canpotentially contribute to the alleviation of protein-energy malnu-trition and micronutrient deficiencies while taking into accountthe effect of antinutrients. Furthermore, the role of antioxidantsfound in these ALVs in the prevention of diseases will be discussed.An additional purpose of this review is to encourage furtherresearch into the nutritional as well as antioxidant content andactivity of ALVs in order to promote the consumption, cultivationand commercialization of these vegetables.

2. Undernutrition in sub-Saharan Africa

The sub-Saharan African region covers an area of 24.3 millionsquare kilometers and consists of 48 countries, with an estimatedpopulation of around 788 million, just over 10% of the world’spopulation (UNAIDS, 2007).

Sub-Saharan Africa has the highest prevalence of undernutri-tion in the world, with one in three people being chronicallyhungry (FAO, 2008), the majority of whom live in the rural areas.Poverty in the region is associated with unemployment, worseningof the HIV/AIDS pandemic, as well as natural- and human-induceddisasters (FAO, 2006; FAO/WFP, 2007). Three-quarters of thenearly 11 million children in developing countries that die beforetheir fifth birthday are in sub-Saharan Africa and South Asia (FAO,2005). Nutrient deficiencies of vitamin A, iron and zinc arewidespread (FAO, 2001). Worldwide, an estimated 33.3%, or 190million children younger than 5 years are at risk of vitamin Adeficiency, with Africa and South-East Asia having the highestprevalence of vitamin A deficiency, 44.4% and 49.9%, respectively(WHO, 2009). In 1999, the National Food Consumption Surveyconducted in South Africa found that a significant majority ofchildren aged 1–9 years consumed a diet deficient in energy and ofpoor nutrient density (MacIntyre and Labadarios, 2000). Thedeficiency of one micronutrient can exacerbate the deficiency ofanother, thus there is likely to be concomitant deficiencies of morethan one micronutrient in individuals (Black, 2003; Scrimshaw andSangiovanni, 1997).

A large proportion of households in sub-Saharan Africa is poorand exists on a diet composed primarily of staple foods preparedfrom cereals (maize, millet, sorghum, teff), tubers (cassava,cocoyam, yam) and plantains (Oniang’o et al., 2003), which aregenerally low in micronutrients. These households rely mostly onthe consumption of LVs to fulfill their daily requirements ofbioavailable micronutrients. A study done on the consumption offruits and vegetables in 10 sub-Saharan African countries by Ruelet al. (2005) found that none of the countries reached the WHO/FAO recommended minimum daily intake. The study further foundthat, with the exception of Kenya, the mean consumption in mostcountries did not even reach half of the recommended intake. Alow intake of vegetables and fruit does not only put people at risk

for micronutrient deficiencies, but it is also among the top 10 riskfactors contributing to mortality worldwide (Ezzati et al., 2002).Smith and Eyzaguirre (2007) argued that in sub-Saharan Africancountries ALVs could play an important role in the WHO globalinitiative on increased consumption of vegetables and fruit.

3. ALVs and their potential contribution to health

Vegetables are a rich source of vitamins and other componentsthat contribute to antioxidant activity in the diet (Gupta and Bains,2006), while no single vegetable provides all the nutrient require-ments. A diversified diet is needed to meet daily micronutrientrequirements (Grusak and Dellapenna, 1999). The role of ALVs in thediet is often difficult to capture using conventional dietaryassessment methodologies (Grivetti and Ogle, 2000). Available datafor the micronutrient content and antioxidant activity of some ALVsare for raw samples. Processing such as cooking and drying can affectthe nutritional content and antioxidant activity (Agte et al., 2000)and therefore further studies determining these effects are essential.

In this review of the literature, research pertaining to a total of193 plant species belonging to 108 families found in 12 sub-SaharanAfrican countries have been studied with regards to aspects suchas their ethnobotany, trade, dietary and medicinal use, as well astheir nutritional value, antioxidant activity and antinutritionalfactors. Nutritional data are available for 31 plant species (Tables 1, 2and 4). It is, however, difficult to compare data from different studiesdue to differences in the methods used for quantification, units ofmeasurement, source, time of collection, seasonal conditions andgeographical regions. From the literature search, various analyticalprocedures have been used for the determinations of proximatecompositions, and micronutrients, as well as other importantcomponents of ALVs. Proximate compositions have been deter-mined using AOAC methods (crude protein content using theKjedahl method with a nitrogen to protein conversion factor of 6.25,fibre content determined as either dietary fibre (non-starchpolysacharrides and lignin) or crude fibre (cellulose, lignin andhemicellulose), carbohydrate determined either by difference or byenzyme extraction method for total available carbohydrates, fatusing the soxhlet method (Table 1), vitamins by HPLC withfluorometry procedures (Table 3) and minerals by using atomicabsorption spectrophotometry (Table 4).

4. Protein content of ALVs and contribution to health

The protein content of ALVs range between 1 and 7 g/100 gedible portion (Table 1). Some ALVs have higher protein contentthan exotic LVs. FAO (1990) and Odhav et al. (2007) reported thatthe crude protein content of both Senna occidentalis and M.

esculenta, was 7 g/100 g edible portion (fresh weight basis), whichis greater than that reported for Brassica oleracea subsp. capitata

(Mosha and Gaga, 1999) and S. oleracea (Kruger et al., 1998) withvalues of 1 g/100 g and 3 g/100 g. However, compared to legumes,ALVs are not very good sources of protein. Thermal processingenhances the digestibility of proteins (Gibson et al., 2006), but canalso lead to protein degradation that lowers the protein content ofLVs. Differences in the agro-climatic conditions may account forthe variation in protein content for Bidens pilosa observed by FAO(1990), Kruger et al. (1998) and Odhav et al. (2007).

Protein-energy malnutrition (PEM) manifests as marasmus(mostly energy deficient), kwashiorkor (mostly protein deficient)or a combination of the two (marasmic-kwashiorkor) (Muller andKrawinkel, 2005). In sub-Saharan Africa, 28% of children under-5years are moderately or severely underweight (underweight is anindicator for PEM) (UNICEF, 2006). The relatively low level ofprotein in ALVs necessitates supplementation with animal proteinor proteins from legumes to have an impact on PEM.

N.P. Uusiku et al. / Journal of Food Composition and Analysis 23 (2010) 499–509500

Author's personal copy

Table 3Vitamin content of selected African leafy vegetables (values per 100 g edible portion, fresh weight basis).

African leafy vegetables Vitamin A (mg RE) Ascorbic acid (mg) Riboflavin (mg) Folate (mg)

Adansonia digitata – 52b – –

Amaranthus sp. 327a 46–126a,c 0.1–0.4a,b 64a

A. hypogea – 87d – –

B. pilosa 301–985a,b 23a,c 0.2a 351a

Brassica sp. – 30–113a,d 0.0–0.2a,d 16a

C. album 917a 31a 0.3a 30a

Cleome sp. 1200a 13–50a,b 0.1a 346a

Cucurbita pepo 194a 11a 0.1a 36a

I. batatas 103–980a,b 11–70a,b,d 0.3–0.4a,d 80a

M. esculenta 1970b 311b 0.6b –

Momordica sp. – 4c – –

Solanum nigrum 1070a 2a 0.3a 404a

Sonchus oleraceus 985a 25a – –

S. oleracea 669a 28a 0.2a 194a

Vernonia sp. – 51–198b,e 0.3a 457a

V. unguiculata 99a 50a 0.2a 141a

‘–’ represent not determined.a Kruger et al. (1998).b FAO (1990).c Steyn et al. (2001).d Mosha and Gaga (1999).e Ejoh et al. (2007).

Table 1Energy, moisture and macronutrient content of selected African leafy vegetables (values per 100 g edible portion, fresh weight basis).

African leafy vegetables Energy kJ (kcal) Moisture (g) Protein (g) Fibre (g) Fat (g) Carbohydrates (g)

Adansonia digitata 289 (69)a 77a 4a 3§a 0.3a 16yaAmaranthus sp. 113–222 (27–53)b 83–91b 4–6b 3§b 0.2–0.6b 4–8ybArachis hypogea 297 (71)c 82c 4c 8§c 0.5c 13ycBidens pilosa 163–222 (39–53)a,b,d 85–88a,b,d 3–5a,b,d 3–6§a,b,d 0.4–0.6a,b,d 2zd, 8ya,b

Brassica sp. 100–142 (24–34)c 92–94c 1–2c 2–4§c 0.1–0.3b 5–6ycCeratotheca triloba 259 (62)b 85b 2b 2§b 2.1b 8ybChenopodium album 212–247 (44–59)b,d 83–85b,d 4–5b,d 2§b,d 0.8b 2zd, 8ybCleome sp. 142–218 (34–52)a,b,d 85–88a,b,d 5a,b,d 1–5§a,b,d 0.3–0.9a,b,d 2zd, 5ya,b

Cucurbita pepo 109 (26)d 93d 3d 2§d 0.7d 0.4zdEmex australis 151 (36)b 89b 5b 2§b 0.6b 3ybGalinsoga parviflora 171 (41)b 89b 4b 1§b 0.5b 5ybIpomoea batatas 188–276 (45–66)a,c,d 83–88a,c,d 4–5a,c,d 2–5§a,c,d 0.2–1.1a,c,d 4zd, 10ycJusticia flava 213 (51)b 84b 3b 1§b 0.4b 9ybLesianthera africana 305 (73)e 77e 3e 4**e 1.1e –

Manihot esculenta 381 (91)b 72b 7b 4§b 1.0a 18ybMomordica sp. 222 (53)a 85a 5a 3§a 5.0b 7ya

Portulaca oleracea 96 (23)b 93b 3b 1§b 0.3b 3ybSenna occidentalis 351 (84)b 77b 7b 3§b 2.2b 9ybSolanum sp. 228–241 (55–58)b,d,g 83–90b,d,g 3–5b,d,g 1**g, 2–6§b,d 0.6b 2zd, 9ybSpinacea oleracea 125 (30)d 92d 3d 3§d 0.4d 1zdVernonia sp. 167–343 (40–82)a,f 79–89a,f 3–5a,f 2–5§a,f – –

Vigna unguiculata 180 (43)d 86d 5d 4§d 0.4d 2zd

‘§’ represent dietary fibre, ‘**’ represent crude fibre, ‘y’ represent carbohydrate value by difference, ‘z’ represent available carbohydrate, ‘–’ represent not determined.a FAO (1990).b Odhav et al. (2007).c Mosha and Gaga (1999).d Kruger et al. (1998).e Isong and Idiong (1997).f Ejoh et al. (2007).g Oboh et al. (2005).

Table 2Recommended daily nutrient intakes (RNI) of selected micronutrients for different age groups as released by the FAO/WHO (2001).

Age

(yrs)

Sex Vitamin A

(mg RE)

Vitamin

C (mg)

Riboflavin

(mg)

Folate

(mg)

Irona

(mg)

Zincb

(mg)

Calcium

(mg)

Magnesium

(mg)

1–3 400 30 0.5 150 5.8 8.3 500 60

4–6 450 30 0.6 200 6.3 9.6 600 76

7–9 500 35 0.9 300 8.9 11.2 700 100

10–18 Male 600 40 1.3 400 14.6 (10–14 yrs) 17.1 1300 230

18.8 (15–18 yrs)

Female 600 40 1.0 400 32.7 (10–14 yrs) 14.4 1300 220

31.0 (15–18 yrs)

19–65 Male 600 45 1.3 400 13.7 14.0 1 000 260

Female 500 45 1.1 400 29.4 9.8 1 000 220

a Based on a diet with 10% iron bioavailability.b Based on a diet with low zinc bioavailability.

N.P. Uusiku et al. / Journal of Food Composition and Analysis 23 (2010) 499–509 501

Author's personal copy

5. Dietary fibre

Dietary fibre content of ALVs ranges from 1 g/100 g edibleportion in Galinsoga parviflora, Justicia flava and Portulaca oleracea

to 8 g/100 g in A. hypogea (Table 1). The total dietary fibre contentof ALVs may vary due to differences in stages of plant maturity,seasonal variation, fertilizers or chemicals used, variety of plant,geographical location and the method used for analysis (Aletoret al., 2002; Punna and Parachuri, 2004). Furthermore, cooking ofplant tissues alters the physical and chemical properties of plantcell walls, which in turn affects their performance as dietary fibre(McDougall et al., 1996). The increased temperature duringcooking leads to breakage of weak bonds between polysaccharidesand the cleavage of glycosidic linkages, which may result insolubilization of the dietary fibre (Svanberg et al., 1997). Thereseems to be very little known about the effect of cooking on totaldietary fibre (TDF) content of ALVs. However, it may behypothesised that the effects noted above could also occur inALVs. Kala and Prakash (2004) reported that cooking (not pressurecooking) caused a slight increase in the total dietary fibre (TDF)content of Indian LVs, which was attributed to the hydration orpolymerization of TDF fractions. Puupponen-Pimia et al. (2003)reported no significant change in soluble, insoluble and totaldietary fibre contents of blanched and freezer stored spinach. Thiscould be due to the stability of dietary fibre components found inthis vegetable species.

Increased migration of communities from rural areas to cities isoften associated with significant changes in diet, and an increase indiseases associated with a high sugar and fat and low fibre contentsuch as diabetes, cardiovascular disease and cancer (Walker et al.,

2002). Inclusion of ALVs in the urban diet can potentially increasedietary fibre intake.

6. Micronutrients

In this review, the contribution of ALVs to the dietaryrequirements of selected micronutrients namely, vitamin A andC, folate and riboflavin as well as zinc, iron, calcium andmagnesium will be evaluated. It is not possible to specify anaverage portion size for ALVs, as serving sizes of food even within acountry vary considerably depending on season, availability, foodtraditions in different parts of the country, people’s knowledge,capacity and economy (Stangeland et al., 2009). The Recom-mended Nutrient Intakes (RNI) for these micronutrients forchildren and adults (males and females) are presented inTable 2. In the studies reviewed, the micronutrient content hasbeen determined using extracts of fresh ALVs and the effects ofcooking have not been taken into consideration. Cooking hasvariable effects on micronutrients in ALVs ranging from no effecton iron and zinc content, increases in b-carotene bioavailability,and reduction in vitamin C due to leaching. Therefore, theproportion of the recommended intake obtained from the freshmaterial is used to obtain the potential beneficial effect asindicated in this paper.

6.1. Vitamin A

In plants, vitamin A occurs in the form of provitamin Acarotenoids such as lutein, b-carotene, violaxanthin and neox-anthin (Rodriquez-Amaya, 2001). Beta-carotene is the most

Table 4Mineral content of selected African leafy vegetables (values per 100 g edible portion, fresh weight basis).

African leafy vegetables Calcium (mg) Iron (mg) Magnesium (mg) Zinc (mg)

Adansonia digitata 410a – – –

Amaranthus sp. 253–425a,b,c 0.3–3.8b,d 105–224b,c 0.02–8.4b,d

A. hypogea – 1.0e – 2.9e

Aystasia gangetica – 0.6–3.7b,f – 0.1–1.1b,d

B. pilosa 162–340a,b,c 2.0–6.0b,c 79–135b,c 0.9–2.6b,c

Brassica sp. 27–31c,d 0.5–3.5e 13c 0.9–1.3e

Ceratotheca triloba – 2.9b – 0.5b

C. album 15–226c,d 2.2–6.1b,c 155–211b,c 1.4–18.5b,c

Cleome sp. 31–288a,b,c 2.6–2.9b,c 44–76b,c 0.6–0.8b,c

Colocasia esculenta – 0.4–0.5d,f – 0.06–0.6d,f

Corchorus olitorius – 2.0d – 0.05d

Crotalaria sp. – 0.5d – 0.05d

Cucurbita sp. 39c 1.5d 38c 0.06–0.2c,d

Emex australis – 1.7b – 2.2b

G. parviflora – 3.0b – 1.5b

I. batatas 37–158a,c,d 0.6–1.0c,e 61c 0.03–3.1c,e

J. flava – 2.6b 225b 1.8b

L. africana – 0.2g – 0.1g

M. esculenta 30–303a,d – – –

Momordica sp. – 3.5b – 1.8b

P. oleracea – 2.9b – 2.4b

Senna occidentalis 513b 2.5b – 2.1b

Solanum nigrum 278–310b,c 8.5 –12.8b,c 84c 0.8–3.5b,c,i

S. oleracea 99c 2.7c 79c 0.5c

Urica urens 668c – 133c –

Vernonia sp. 145a 0.8–3.2h – 0.08d

V. unguiculata 188c 0.3–3.0c,d 60c 0.23d

‘–’ represent not determined.a FAO (1990).b Odhav et al. (2007).c Kruger et al. (1998).d Orech et al. (2007).e Mosha and Gaga (1999).f Mepba et al. (2007).g Isong and Idiong (1997).h Ejoh et al. (2007).i Oboh et al. (2005).

N.P. Uusiku et al. / Journal of Food Composition and Analysis 23 (2010) 499–509502

Author's personal copy

important of the provitamin carotenoids in terms of its relativeprovitamin A activity and quantitative contribution to the diet(SACN, 2005). Vitamin A levels in the diet depends on the b-carotene content of the ALVs, amount consumed, bioavailabilityand bioefficacy (West et al., 2002). The levels of vitamin A are givenin retinol equivalents (RE), with 1 RE being equivalent to 6 mg of b-carotene or 12 mg of other provitamin A carotenoids such as a-carotene, g-carotene, and b-cryptoxanthin. The recommendeddaily intake for vitamin A as given by the RNI is also expressed interms of RE. In the most recent edition of the Dietary ReferenceIntakes (DRI) for the United States and Canada, the U.S. Institute ofMedicine (IOM, 2001) introduced the term ‘‘retinol activityequivalent’’ (RAE) to replace the RE used by FAO/WHO to takeinto account new research on vitamin A activity (bioefficacy) ofcarotenoids. The IOM (2001) proposed using the following vitaminA equivalency factors for provitamin A carotenoids from mixedfoods, namely, 1 mg RAE is equivalent to 1 mg of preformed retinol,2 mg of supplemental b-carotene in oil, 12 mg of b-carotene or24 mg of other provitamin A carotenoids such as a-carotene, g-carotene, and b-cryptoxanthin.

The b-carotene content of ALVs is highly species dependent andvaries from 99 mg RE in Vigna unguiculata to 1970 mg RE (per 100 gedible portion) for M. esculenta (Table 3). In the most recent editionof Recommended Nutrient Intakes (RNI), 1 RE is defined as 6 mg b-carotene (FAO/WHO, 2001). Using the RNI in Table 2, 300 g freshALVs would fulfill the dietary requirements of vitamin A forchildren. For adults, 300 g of fresh Cucurbita pepo would contribute116% of female RNI and 97% of males RNI, whereas 300 g of fresh V.unguiculata would contribute only 59% and 50% of female and maledaily requirements, respectively.

The stability and retention of carotenoids in food is influencedby their chemical nature, the method and severity of processing,food particle size, storage time and storage conditions (Cheynier,2005). Cooking LVs increases the bioavailability of a- and b-carotene (Khachik et al., 1992). Carotenoids are bound by protein,thus heat treatment such as boiling and steaming helps to releasebound carotenoids and enables them to be readily extracted(Howard et al., 1999). Masrizal et al. (1997) observed a greaterretention of b-carotene in the vegetables prepared by microwavesteaming and stir-frying with oil than those stir-fried with water orboiled. Adding oil to Manihot sp. and Ceiba sp. has been shown toenhance serum retinol in Ghanaian preschool children (Takyi,1999). Consumption of cooked and pureed spinach leads to higherplasma total b-carotene concentrations, compared to when thesevegetables are consumed raw (Rock et al., 1998). This could beattributed to the increased extractability on cooking due todestruction of enzymes which otherwise could cause carotenedegradation (Kala and Prakash, 2004).

The role of ALVs as sources of vitamin A is even more pertinentgiven the prevalence of vitamin A deficiency in developingcountries. As many as 190 million young children and more than15 million pregnant women living in developing countries arevitamin A deficient (WHO, 2009). An estimated 42.4% of youngchildren in sub-Saharan Africa are vitamin A deficient (Aguayo andBaker, 2005). Lately, emphasis has been put on increasing theintake of b-carotene vegetables, including dark-green LVs, toimprove vitamin A intake. ALVs can therefore play a significant rolein this regard. Consumption of foods rich in b-carotene is regardedas more beneficial than taking antioxidant supplements. Two mainstudies conducted on the effect of supplemental b-carotene on therisk of developing lung cancer are the Alpha-Tocopherol Beta-Carotene (ATBC) trial on Finnish heavy smokers (The ATBC CancerPrevention Study Group, 1994; Albanes et al., 1996), and the Beta-Carotene and Retinol Efficacy Trial (CARET) on asbestos workersand heavy smokers (Omenn et al., 1996) in which the subjects tooka-tocopherol, b-carotene and retinyl palmitate supplements. In

these trials, there was an increase in incidences of or mortalityfrom lung cancer among participants who received either a-tocopherol or b-carotene or b-carotene combined with retinylpalmitate. The CARET had to be halted following these observa-tions. Both trials concluded that taking the supplements providedno protection against lung cancer.

Concerns with respect to the bioavailability of vitamin A fromgreen LVs have been raised (De Pee et al., 1995). The authorsattributed the reduction in bioavailability to physical inaccessibil-ity of carotenoids in plant tissues which may have prevented therelease of b-carotene from the matrix, as well as to competition forabsorption with other carotenoids. Nonetheless, consumption ofcooked and pureed green LVs was shown to have a beneficial effecton vitamin A status (Haskell et al., 2004). It stands to reason thatALVs could have a similar beneficial effect. Takyi (1999) indeedshowed that an increased intake of ALVs, with fat added,contributed significantly to improving the vitamin A status inchildren.

6.2. Ascorbic acid

Table 3 indicates that ascorbic acid in the selected unprocessedALVs range from 2 to 311 mg (per 100 g edible portion) in Solanum

nigrum and M. esculenta, respectively. It is however difficult tocalculate their contribution towards dietary vitamin C require-ments as this vitamin is greatly affected by processing. A decreasein ascorbic acid by 19% in cooked amaranth, 61% in dried Vernonia

amygdalina and by almost 100% in dried Adonsonia digitata hasbeen reported (FAO, 1990). The storage of dehydrated LVs shouldbe at low temperature because it effectively reduces degradation ofascorbic acid and browning (Negi and Roy, 2001).

In sub-Saharan Africa, the intake of ascorbic acid from LVs isoften determined by seasonal factors, as well as postharveststorage, time and temperature of storage, cooking practices andchlorination of water (FAO, 2001). Losses of ascorbic acid fromvegetables are large during blanching procedures and relativelysmall during frozen storage, suggesting that losses duringblanching occur primarily by leaching rather than by chemicaldegradation (Howard et al., 1999). Mepba et al. (2007), Sreeramuluet al. (1983) and Wallace et al. (1998) found a significant reductionin ascorbic acid of several ALVs after thermal processing. Steamblanching, followed by dehydration have been reported as themost effective preservation methods in retaining ascorbic acid(Schippers, 2000). Freeze-drying also retains most ascorbic acid incomparison with shade-, sun-, and vacuum-drying of ALVs(Shitanda and Wanjala, 2006).

Ascorbic acid promotes absorption of soluble non-haem iron bychelation or by maintaining the iron in the reduced form (FAO,2001). In addition, it also significantly counteracts the inhibition ofiron absorption by phytates in the diet. Besides its ability toscavenge free radicals, ascorbic acid can regenerate otherantioxidants such as tocopheroxyl and the carotene radical cationfrom their radical species (Halliwell and Gutteridge, 1999).

6.3. Riboflavin and folate

ALVs contain reasonably good concentrations of both riboflavinand folate (Table 3). The range of riboflavin in ALVs varies from0.04 mg/100 g in some species of Brassica (Kruger et al., 1998) to0.6 mg/100 g in M. esculenta (FAO, 1990), while folate ranges from16 to 457 mg/100 g in Brassica sp. and Urtica urens, respectively.Consumption of 300 g of fresh Cleome sp. would provide 33–60%RNI of riboflavin for children, 30% for adult women and 23% foradult men, while 300 g of fresh M. esculenta would provide up to200% RNI for children and 138% for adult men. With regard tofolate, 300 g of Brassica sp. would provide 16–32% RNI for children,

N.P. Uusiku et al. / Journal of Food Composition and Analysis 23 (2010) 499–509 503

Author's personal copy

while 300 g of fresh U. urens would provide more than 300% RNI foradults.

Riboflavin deficiency commonly occurs with lactose intolerance(FAO/WHO, 2001), a condition that is highest in African popula-tions. This deficiency is associated with increased risk ofcardiovascular diseases (Powers, 2003). Folate is important forthe prevention of foetal neural tube defects (FAO/WHO, 2001) andfolate requirements are significantly higher during pregnancy(McPartlin et al., 1993). Fortification of these vitamins in the foodsupply has reduced incidences of the respective deficiencies. Thecontribution of ALVs to the dietary requirements of these vitaminsis essential.

6.4. Iron

Some ALVs are excellent sources of iron (Odhav et al., 2007), butthe levels are influenced by factors such as soil type and pH, wateravailability to the plant, climatic conditions, plant variety (Khaderand Rama, 2003), plant age (Gupta et al., 1989) and the use offertilizers (Guil Guerrero et al., 1998). The range of dietary ironcontent of ALVs varies from 0.2 to 12.8 mg/100 g edible portion forLesianthera africana and Solanum nigrum, respectively (Table 4).Consumption of 300 g of fresh L. africana would provide 7% of RNIfor 7–9 years old children and 2% of RNI for adult women, whilethat of S. nigrum would provide 431% and 131% of the children andadult women RNI, respectively.

The absorption of non-haem iron (the type of iron in plantfoods) is dependent on the iron status of the individual and severalfactors in the diet such as the presence of inhibitors (oxalates,phytate and fibre) (Kumari et al., 2004) and enhancers (ascorbicacid, b-carotene, fermentable carbohydrates and organic acids)(Hallberg et al., 1989; Lopez et al., 2002). In comparison tovitamins, minerals have greater stability and their contents do notchange significantly due to cooking (Kala and Prakash, 2004).Cooking LVs in iron utensils increases the total iron andbioavailable iron compared to fresh vegetables and those cookedin other metallic utensils such as stainless steel and aluminum(Kumari et al., 2004) and this could also apply to ALVs.

Africa has the highest proportion of individuals affected byanaemia, with an increase in prevalence from 48% in 1993 to 68% in2005 (WHO, 2008). Women, especially during pregnancy or post-partum, low birth weight babies and malnourished children aremore at risk of developing anaemia (Galloway, 2003). The role ofALVs in the diet in preventing anaemia is not only based on the ironcontent of the vegetable, but also on the content of ascorbic acidthat contributes to its absorption.

6.5. Zinc

The zinc content within the same species is highly variable andranges from 0.02 to 8.4 mg/100 g edible portion for severalAmaranthus species, from 1.4 to 18.5 mg/100 g for C. album and0.03–3.1 mg/100 g for Ipomoea batatas (Table 4). Similar to iron,cooking has little or no effect on zinc levels in LVs generally. Zinc ismostly adversely affected by phytate, where a phytate:zinc molarratio of 15:1 is associated with reduced zinc bioavailability(Turnlund et al., 1984). To evaluate mineral absorption fromphytate-rich products, factors such as vegetal matrix, vegetalphytasic activity, the phytate:mineral ratio and the content offermentable fibres should be taken into consideration (Lopez et al.,2002).

Zinc deficiency is associated with impaired gastrointestinal andimmune functions (Welch, 1993), which is of vital importancebecause as many as 67% of global HIV infections are in sub-SaharanAfrica (UNAIDS, 2008). An estimated 6.8% of deaths in childrenunder-5 years of age in 2004 was due to zinc deficiency (Roth et al.,

2008). In sub-Saharan African areas where iron deficiency has beenreported, nutritional zinc deficiency is also common (Abebe et al.,2007). This occurs because iron and zinc have a similar distributionin the food supply, and some dietary components affect theabsorption of both iron and zinc (Hotz and Brown, 2004). Like iron,most ALVs do not contribute significantly to the RNI requirementsof zinc.

6.6. Calcium and magnesium

Table 4 indicates that the range of calcium in ALVs is between15 mg/100 g edible portion in some species of Chenopodium and668 mg/100 g in U. urens, while that of magnesium is between13 mg/100 g in Brassica sp. and 225 mg/100 g in J. flava. Thebioavailability of these minerals is dependent on the age and sex ofan individual, fat content in the diet and the presence ofantinutrients. Certain ALVs could potentially contribute signifi-cantly towards the dietary requirements of these two minerals.

7. Important non-nutritional components of ALVs

ALVs are rich sources of bioactive compounds with beneficialeffects on health. These vegetables may however also containdietary components that compromise digestion and absorption ofvital nutrients. These components occur in combinations and mayact synergistically or may have contradicting effects with eachother. Understanding the role of these components in themaintenance of health is crucial for managing PEM and chronicdiseases of lifestyle. Dietary diversity is essential to reduce theeffects of the antinutritional factors.

7.1. Phenolic compounds

Polyphenols are quantitatively the main dietary antioxidantsand posses higher in vitro antioxidant capacity than vitamins andcarotenoids (Gardner et al., 2000). Plant phenolics include phenolicacids, coumarins, flavonoids, stilbenes, hydrolysable and con-densed tannins, lignans and lignins (Naczk and Shahidi, 2004).Flavonoids such as myricetin, quercetin, kaempferol, isorhamnetinand luteolin have been reported in LVs (Trichopoulou et al., 2000).To the authors’ knowledge, there seems to have been no workundertaken on the specific flavonoid compounds found in ALVs.The concentration of tannins in ALVs range from 655 mg/100 g inXanthasomas sp. to 1222 mg/100 g in Euphorbia hirta (Table 5).Tannins complex with proteins, starches and digestive enzymes,thereby reducing the nutritional value of foods (Chung et al., 1998;Serrano et al., 2009). Tannins interfere with protein absorption andreduce iron availability (Bravo, 1994). Apart from tannins,flavonoids and phenolic acids also hinder iron absorption (Bruneet al., 1989; Serrano et al., 2009).

Generally, plant extracts that contain a high amount ofpolyphenols also exhibit high antioxidant activity (Wong et al.,2006). Although studies on the antioxidant activity of ALVs arelimited (Akindahunsi and Salawu, 2005; Lindsey et al., 2002; Modi,2007; Odhav et al., 2007; Stangeland et al., 2009), studies involvingplant species from Asia are insightful and provide importantinformation regarding polyphenolic content, antioxidant activityand the effect of processing thereon. A study conducted by Maiet al. (2007) found that extracts from Vietnamese plants used formaking drinks showed the highest polyphenol content andantioxidant activity followed by edible wild vegetables, herbsand dark green vegetables. Maisuthisakul et al. (2007) found adistinct correlation between total phenolic content, total flavonoidcontent and antiradical activity in selected Thai indigenous plantparts. Mai et al. (2007) also found a correlation betweenantioxidant activity and the polyphenol content of several

N.P. Uusiku et al. / Journal of Food Composition and Analysis 23 (2010) 499–509504

Author's personal copy

Vietnamese plants. Meanwhile, no correlation between antioxi-dant activity and total phenolic content was found for selectedIndian LVs (Dasgupta and De, 2007) and commonly consumedvegetables in Malaysia (Ismail et al., 2004). The correlationbetween the phenolic or flavonoid content and antioxidant activitydepends on the methodology used as well as type of vegetables,where variations could be due to different antioxidant componentscontributing to antioxidant activity (Ismail et al., 2004).

From the studies done in sub-Saharan Africa (Table 6), Odhavet al. (2007) found that leaves of P. oleracea, Mormodica balsamina

and J. flava had good antioxidant activity, with 96, 94 and 96%scavenging capacity of the methanolic plant extracts. Akindahunsiand Salawu (2005) also found higher scavenging activities of 99,90, 90% in Xanthosom mafaffa, Celosia argentea, Manihot utilissima,respectively, as well as poor activities of 11 and 22% in Ocimum

grtissimum sp and Stractium sp., respectively. Meanwhile, Stange-land et al. (2009) found that Cleome gynandra, Amaranthus sp. andSolanum macrocarpon showed high antioxidant activity with 1.56,1.0 and 0.87 mmol TE/100 g, respectively.

There is a significant interaction between plant age andgrowth temperature, with respect to antioxidant activity ofboiled Amaranthus. Modi (2007) found that boiled amaranththat was harvested 60 days after sowing displayed higherantioxidant activity compared with those harvested at either 20or 40 days after sowing. Therefore, the stage of plant develop-ment should be considered during harvesting for optimumantioxidant activity.

The effects of food processing on the phenolic content andoverall antioxidant activity of foods are the result of differentevents, which take place consecutively or simultaneously (Nicoliet al., 1999) and also depend on the species of plant. Workingon Japanese leafy vegetables, Yamaguchi et al. (2001) foundboth increases and decreases in flavonoid content after cooking.A decrease in flavonoid content could be due to leaching orheat lability of specific flavonoids. An increase could also be dueto release of flavonoids upon breakdown due to heat ofsubstances such as cell wall material to which the flavonoidsmay be bound and the inhibition of oxidative enzymes (Yamaguchiet al., 2001).

7.2. Oxalic acid

Oxalic acid [(COOH)2] is present in many ALVs such as E. hirta,Ipomoea involucrata, Xanthosomas sp., amaranth, M. esculenta,Celosia argentea, Telfaria occidentalis and Vernonia sp. (Table 5),

Table 5Antinutrient content of selected African leafy vegetables (values per 100 g edible portion, fresh weight basis).

African leafy vegetables Oxalic acid (mg) Phytate (mg) Saponins (mg) Tannins (mg) Trypsin inhibitors (g)

Amaranthus sp. 40–50a 140a – – 4–14f

Boscia senegalensis – – – – 17f

Celosia argentea 20a – – – 7f

Corchorus tridens – – – – –

Crassophalum sp 10–20a – – – –

Euphorbia hirta 1115b 655b 6.7b 1222b –

Gynandropsis sp. – – – – 5f

Hibiscus esculentus 10a – – – –

Ipomoea involucrata 913b 176b 386b 869b –

Launaea sp. 108b 9b 424b 168b –

Leptadenia hastate – – – – 1f

L. africana 2c – – – –

Maerua crassifolia – – – – 82f

M. esculenta 20a 100a – – –

Solanum sp. – 40e – – –

Talinum triangulare 20a 190a – – –

Telfaria occidentalis 40a – – – –

Vernonia sp. 1–2d 120a 0.1–0.3d – –

Xanthasomas sp. 654b 131b 481b 655b –

‘–’ represent not determined.a Aletor and Adeogun (1995).b Wallace et al. (1998).c Isong and Idiong (1997).d Ejoh et al. (2007).e Oboh et al. (2005).f Vanderjagt et al. (2000).

Table 6Antioxidant activity of selected African leafy vegetables (values per 100 g edible

portion, fresh weight basis).

African leafy vegetables Antioxidant activity (%)

Amaranthus sp. 45za, 78–90§b,c

Basella alba 89§c

B. pilosa 54za, 88§b

Celosia argentea 90c

C. album 42za, 82§b

Cleome monophylla 84§b

Corchorus olitorius 45§c

Crassocephalum sp. 89§c

G. parviflora 76§b

Hibiscus esculentus 56§c

J. flava 96§b

Manihot utilissima 90§c

Momordica balsamina 94§b

Nasturtium aquatica 100zaOcimum gratissimum 11§c

Oxygonum sinuatum 92§b

P. oleracea 96§b

Sisymbrium thellungii 99zaSolanum sp. 78–92§b,c

Structium sp. 22§c

Urtica dioica 100zaVernonia amygdalina 56§c

Xanthosoma mafaffa 99§c

Amaranthus sp. 1.0ydCleome gynandra 1.6ydSolanum macrocarpon 0.9yd

‘z’ represent % inhibition of linoleic acid oxidation, ‘y’ represent antioxidant activity

in mmol Trolox equivalents per 100 g, by using the ferric reducing ability of plasma

(FRAP) assay, ‘§’ represent % DPPH radical-scavenging capacity.a Lindsey et al. (2002).b Odhav et al. (2007).c Akindahunsi and Salawu (2005).d Stangeland et al. (2009).

N.P. Uusiku et al. / Journal of Food Composition and Analysis 23 (2010) 499–509 505

Author's personal copy

where it occurs in the cell sap (Champ, 2002). Depending onspecies, oxalate can occur as soluble salts of potassium and sodiumsalts and as insoluble salts of calcium, magnesium and iron or as acombination of the two forms (Noonan and Savage, 1999).Insoluble oxalate is excreted in the faeces while the solubleoxalate is absorbed by the body. Soluble oxalate forms strongchelates with dietary calcium, rendering it unavailable forabsorption and assimilation (Gupta et al., 2005; Radek and Savage,2008). High dietary intake of soluble oxalate can lead to theformation of kidney stones (Radek and Savage, 2008). A diet high inoxalates may require dietary supplementation of the divalentminerals to prevent deficiencies (Ponka et al., 2006). Addition of asource of calcium to vegetables containing high levels of solubleoxalate has been shown to reduce the intestinal available oxalatecontent in such food (Radek and Savage, 2008).

7.3. Phytic acid

Phytic acid (myo-inositol 1,2,3,4,5,6 hexakis-dihydrogen phos-phate) is the major phosphorus storage compound in ALVs(Champ, 2005). Table 5 shows that phytic acid content rangesfrom 9 mg/100 g in Launaea sp. to 655 mg/100 g in E. hirta.Although phytic acid is an antioxidant, it has been shown to inhibitabsorption of minerals. Phytic acid chelates multivalent metal ionssuch as zinc, calcium and iron, thus it is a strong inhibitor of iron-mediated free radical generation (Schlemmer et al., 2009). Thedisadvantage of this is that a diet high in phytate content reducesthe bioavailability of zinc, iron and calcium and has adverse effectson the digestion of proteins and starches (Reddy and Pierson,1994). The beneficial effects of phytic acid are related to its metalchelating abilities, the lower inositol’s involvement in signalingpathways and to their phosphate donor/acceptor capabilities(Bohn et al., 2008; Schlemmer et al., 2009). Lower inositolphosphates can act as antioxidants by inhibiting iron-mediatedoxidative reactions, enhancing immunity by increasing NaturalKiller cell function and activity and stimulating bacterial killing byneutrophils (Bohn et al., 2008).

7.4. Glucosinolates

Glucosinolates are precursors of isothiocyanates, and are alsoon the other hand known for their therapeutic and prophylacticproperties of nutritional or functional glucosinolates (Fahey et al.,2001). Most glucosinolate-containing genera are found in theBrassicaceae, Capparaceae and Caricaceae families, although Isongand Idiong (1997) have also reported presence of glucosinolates inL. africana, which is from the Icacineae family. The majority ofglucosinolates are chemically and thermally stable and thereforehydrolysis is mainly enzymatically, and more specifically myr-osinase driven (Verkerk et al., 2009). Following tissue disruption,myrosinase and glucosinolates come into contact, causinghydrolysis of the thioglucosidic bond and the formation of arange of bioactive compounds (Baghurst et al., 1999; Verkerk et al.,2009). Depending on the ingested dose and bioavailability, somehydrolysis products have chemopreventive and carcinogenicproperties (Fahey et al., 2001; Verkerk et al., 2009).

7.5. Saponins

Table 5 shows higher concentrations of 481, 424 and 386 mg/100 g of saponins in Xanthosomas sp., Launaeae sp. and Ipomoea

involucrata, respectively. Saponins have cholesterol lowering effect(Van Duyn and Pivonka, 2000), as well as haemolytic, molluscicid-al, anti-inflammatory, antifungal/antiyeast, antibacterial/antimi-crobial, antiparasitic, cytotoxicity and antitumour, antiviral andother biological activities (Sparg et al., 2004). Saponins are poorly

absorbed and most of their effects are attributable to theirhydrophilic/hydrophobic asymmetry and consequently theircapacity to reduce interfacial tension (Champ, 2002).

7.6. Alkaloids

The bitterness of some ALVs indicates the presence of alkaloids,which invariably influence the consumer acceptability of suchvegetables (Wallace et al., 1998). The two groups of alkaloids thathave been well studied are the pyrrolizidine and the quinolizidine.Pyrrolizidine are frequently found in members of Asteraceae and inthe Boraginaceae families, rendering these plants toxic, while,quinolizidines occur primarily in the genus Lupinus (Croteau et al.,2000). Amaranth sp., Asystasia mysorensis, Crotalaria ochroleuca,Portulaca quadrifida and Sida acuta tested positive for presence ofalkaloids (Orech et al., 2005). Naturally occurring pyrrolizidinealkaloids are harmless but become highly toxic when transformedby cytochrome P450 monooxygenases in the liver (Croteau et al.,2000). These compounds also possess medicinal properties.Alkaloids that have microbicidal properties are due to their effectson transit time in the small intestine (Cowan, 1998).

7.7. Protease inhibitors

ALVs may also contain significant levels of trypsin andchymotrypsin inhibitors that impairs the utilization of proteinsand the amino acids present (Glew et al., 2005), by interacting withproteolytic enzymes rendering them unavailable for proteindigestion (Mosha and Gaga, 1999). Presence of protease inhibitorshave been reported in Maerua crassifolia, Brassica sp. and Boscia

senegalensis, amongst others (Table 5). The activity of trypsin andchymotrypsin inhibitors is strongly influenced by the presence ofwater, the temperature and the length of heating period (Moshaand Gaga, 1999). Conventional blanching was found to be moreeffective in reducing trypsin and chymotrypsin inhibitor activitiesthan microwave blanching (Mosha and Gaga, 1999). AlthoughVanderjagt et al. (2000) found that in most ALVs, the trypsininhibitory activity was heat-stable after 5 min of boiling, whichmay lead to poor protein utilization in humans.

7.8. Reduction of antinutritional factors through processing

Heat treatment is a reliable method of reducing antinutritionalfactors in ALVs (Mosha and Gaga, 1999), although this could lead toleaching of nutrients (Mepba et al., 2007). Blanching and cookingcauses the rupture of the plant cell walls resulting in the leachingof soluble antinutritional factors into the blanching medium.Blanching and cooking significantly reduce the levels of oxalic andphytic acid in ALVs (Oboh et al., 2005), while drying and storage ofLVs has little effect on these antinutritional factors (Yadav andSehgal, 2003).

7.9. Importance of non-nutritional components of ALVs for health

In many sub-Saharan African populations, changes in diet andenvironmental factors, particularly among urban dwellers havecaused a significant increase in diseases of lifestyle (Walker et al.,2002). Consumption of ALVs usually decreases with urbanization.Owing to the diverse biological activities of the non-nutritionalcomponents of ALVs and the need for dietary chemopreventivecompounds that are able to provide health care to rural people,there is a need to investigate the ability of these compounds toprotect or repair DNA oxidative damage. Although very little isknown regarding the antioxidant status of the sub-Saharanpopulation, the assumption can be made that individuals withmicronutrient deficiency will have a low antioxidant status.

N.P. Uusiku et al. / Journal of Food Composition and Analysis 23 (2010) 499–509506

Author's personal copy

Oxidative stress has been associated with cardiovasculardiseases, certain cancers and neurodegenerative diseases (Govin-darajan et al., 2005). Dietary antioxidants such as phenoliccompounds provide bioactive mechanisms to reduce theselifestyle-related diseases (Hung et al., 2004; Riboli and Norat,2003; Schaffer et al., 2004). The precise nature, mechanism andextent of these positive effects on health are yet to be fullyelucidated. The methods of isolating these components and theirmetabolites from the diet are complex and there is a possiblesynergy between these constituents. The bioavailability of thesecomponents is dependent on their chemical structures, foodmatrix and related associations (Vasioli et al., 2006). Furthermore,the RNI for polyphenol components have not yet been established.Research in this area should therefore be encouraged.

ALV species are plentiful in sub-Saharan Africa and the presenceof high levels of antioxidants and some non-nutritional compo-nents in LVs found elsewhere indicates that the evaluation of theantioxidant content, free radical-scavenging activity and non-nutritional components in these ALVs is necessary.

8. Conclusion

African leafy vegetables (ALVs) contain significant levels ofmicronutrients that are essential for human health. The micro-nutrients are affected differently by processing, depending on thetype of processing, as well as the type of vegetable species. Thermalprocessing of LVs reduces the level of ascorbic acid but enhancesthe bioavailability of vitamin A. The bioavailability of mineralssuch as iron and zinc from plant sources is low in the presence ofantinutritional factors like phytates, while the presence of vitaminC and protein improves their efficacy. High levels of antinutritionalfactors in the diet may lead to mineral deficiencies, especially if thediet is largely plant-based. Some compounds with antinutritionalfactors may have beneficial effects to human health, depending onthe dose and bioavailability. Adding small amounts of foods ofanimal origin will help to improve the bioavailability of certainnutrients in plant-based diets.

Raw ALVs have been shown to possess antioxidant activity andthus have the potential to be used as cheap natural sources forreducing cellular oxidative damage, and consequently reducingdegenerative conditions such as cardiovascular diseases andcancers. Antioxidant capacity may also be affected by processing;therefore it is necessary to determine the antioxidant potential, aswell as the specific phenolic compounds contributing to totalantioxidant activity, in cooked ALVs. Further research should look atantioxidant activity in cooked ALVs and their effects on degenerativediseases. Limited quantities of and often only incomplete data areavailable on the nutritional value of these plants. Thorough andcomplete investigations into the nutritional value of these plants areessential. These data can then be used to develop strategies topromote the utilization, cultivation and commercialization of thesesources of nutrients and important non-nutritional components.

Acknowledgement

Authors thank the Schlumberger Foundation and Third WorldOrganization for Women in Science (TWOWS) for financialassistance.

References

Abebe, Y., Bogale, A., Hambidge, K.M., Stoecker, B.J., Bailey, K., Gibson, R.S., 2007.Phytate, zinc, iron and calcium content of selected raw and prepared foodsconsumed in rural Sidama, Southern Ethiopia, and implications for bioavail-ability. Journal of Food Composition and Analysis 20, 161–168.

Agte, V.V., Tarwadi, K.V., Mengale, S., Chiplonkar, S.A., 2000. Potential of tradition-ally cooked green leafy vegetables as natural sources for supplementation of

eight micronutrients in vegetarian diets. Journal of Food Composition andAnalysis 13, 885–891.

Aguayo, V.M., Baker, S.K., 2005. Vitamin A deficiency and child survival in sub-Saharan Africa: a reappraisal of challenges and opportunities. Food and Nutri-tion Bulletin 26, 348–355.

Akindahunsi, A.A., Salawu, S.O., 2005. Antioxidant indices of some green leafyvegetables. Tropical Science 45, 33–35.

Albanes, D., Heinonen, O.P., Taylor, P.R., Virtamo, J., Edwards, B.K., Rautalanti, M.,Hartman, A.M., Palmgren, J., Freedman, L.S., Haapakoski, J., Barrett, M.J., Pietinen,P., Malila, N., Tala, E., Liippo, K., Salomaa, E.R., Tangrea, J.A., Teppo, L., Askin, F.B.,Taskinen, E., Erozan, Y., Greenwald, P., Huttunen, J.K., 1996. Alpha-Tocopheroland beta-carotene supplements and lung cancer incidence in the alpha-tocoph-erol, beta-carotene cancer prevention study: effects of baseline characteristicsand study compliance. Journal of the National Cancer Institute 88, 1560–1570.

Aletor, O., Oshodi, A.A., Ipinmoroti, K., 2002. Chemical composition of common leafyvegetables and functional properties of their leaf protein concentrates. FoodChemistry 78, 63–68.

Aletor, V.A., Adeogun, O.A., 1995. Nutrient and antinutrient components of sometropical leafy vegetables. Food Chemistry 53, 375–379.

Baghurst, P., Beaumont-Smith, N., Baghurst, K., Cox, D., 1999. The relationshipbetween the consumption of fruits and vegetables and health status. Reportto Department of Health and Aged Care and the Strategic IntergovernmentalNutrition Alliance, CSIRO Health Sciences and Nutrition, Adelaide, Australia.

Black, R., 2003. Micronutrient deficiency – an underlying cause of morbidity andmortality. Bulletin of the World Health Organization 81, 79.

Bohn, L., Meyer, A.S., Rasmussen, S.K., 2008. Phytate: impact on environment andnutrition. A challenge for molecular breeding. Journal of Zhejiang UniversityScience 9, 165–191.

Bravo, L., 1994. Polyphenols: chemistry, dietary sources, metabolism, and nutri-tional significance. Nutrition Reviews 56, 317–333.

Brune, M., Rossander, L., Hallberg, L., 1989. Iron absorption and phenolic com-pounds: importance of different phenolic structures. European Journal ofClinical Nutrition 43, 547–558.

Champ, M.M.-J., 2002. Non-nutrient bioactive substances of pulses. British Journalof Nutrition 88, S307–S319.

Cheynier, V., 2005. Polyphenols in food are more complex than often thought. TheAmerican Journal of Clinical Nutrition 81, 223S–229S.

Chung, K.T., Wong, T.Y., Wei, C.I., Huang, Y.W., Lin, Y., 1998. Tannins and humanhealth: a review. Critical Reviews in Food Science and Nutrition 36, 421–464.

Cowan, M.M., 1998. Plant products as antimicrobial agents. Clinical MicrobiologyReviews 12, 564–582.

Croteau, R., Kutchan, T.M., Lewis, N.G., 2000. Natural products (secondary meta-bolites). In: Buchanan, B., Gruissem, W., Jones, R. (Eds.), Biochemistry andMolecular Biology of Plants. American Society of Plant Physiologists, pp.1250–1318.

Dasgupta, N., De, B., 2007. Antioxidant activity of some leafy vegetables of India: acomparative study. Food Chemistry 101, 471–474.

De Pee, S., West, C.E., Muhilal, Daryadi, D., Hautvast, J.G.A.J., 1995. Lack of improve-ment in vitamin A status with increased consumption of dark green leafyvegetables. Lancet 346, 75–81.

Ejoh, R.A., Nkonga, D.V., Inocent, G., Moses, M.C., 2007. Nutritional components ofsome non-conventional leafy vegetables consumed in Cameroon. PakistanJournal of Nutrition 6, 712–717.

Ezzati, M., Lopez, A.D., Rodgers, A., Van der Hoorn, S., Murray, C.J.L., 2002. Selectedmajor risk factors and global and regional burden of disease. Lancet 360, 1347–1360.

Fahey, J.W., Zalcmann, A.T., Talalay, P., 2001. The chemical diversity and distributionof glucosinolates and isothiocyanates among plants. Phytochemistry 56, 5–51.

FAO (Food and Agriculture Organization of the United Nations), 1990. Utilization oftropical foods: fruits and leaves. FAO Food and Nutrition Paper No. 47/7. Rome,Italy.

FAO, 2005. The state of food insecurity in the world: eradicating world hunger – keyto achieving the Millennium Development Goals. Rome, Italy.

FAO, 2006. The state of food insecurity in the world: eradicating world hunger –taking stock ten years after the World Food Summit. Rome, Italy.

FAO, 2008. The state of food insecurity in the world: high food prices and foodsecurity – threats and opportunities. Rome, Italy.

FAO/WFP, 2007. FAO/WFP crop and food supply assessment mission to Lesotho.Rome, Italy.

FAO/WHO, 2001. Human Vitamin and Mineral Requirements, 2nd ed. Geneva,Switzerland.

Galloway, R., 2003. Anemia Prevention and Control – What Works? Part 1. ProgramGuidance. USAID, World Bank, PAHO/WHO, Micronutrient Initiative, FAO, andUNICEF, Washington, DC.

Gardner, P.T., White, T.A.C., Mcphail, D.B., Duthie, G.G., 2000. The relative contribu-tions of vitamin C, carotenoid and phenolics to the antioxidant potential of fruitjuices. Food Chemistry 68, 471–474.

Gibson, R.S., Perlas, L., Hotz, C., 2006. Improving the bioavailability of nutrients inplant foods at the household level. Proceedings of the Nutrition Society 65, 160–168.

Glew, R.S., Vanderjagt, D.J., Bosse, R., Huang, Y.-S., Chuang, L.-T., Glew, R.H., 2005.The nutrient content of three edible plants of the Republic of Niger. Journal ofFood Composition and Analysis 18, 15–27.

Govindarajan, R., Jijayakumar, M., Pushpangadan, P., 2005. Antioxidant approach todisease management and the role of ‘Rasayana’ herbs of Ayurveda. Journal ofEthnopharmacology 99, 165–178.

N.P. Uusiku et al. / Journal of Food Composition and Analysis 23 (2010) 499–509 507

Author's personal copy

Grivetti, L.E., Ogle, B.M., 2000. Value of traditional foods in meeting macro andmicronutrient needs – the wild plant connection. Nutrient Research Reviews 13,31–46.

Grusak, M.A., Dellapenna, D., 1999. Improving the nutrient composition of plants toenhance human nutrition and health. Annual Reviews of Plant Physiology andPlant Molecular Biology 50, 133–161.

Guil Guerrero, J.L., Gimenez Martinez, J.J., Torija Isasa, M.E., 1998. Mineral nutrientcomposition of edible wild plants. Journal of Food Composition and Analysis 11,322–328.

Gupta, S., Bains, K., 2006. Traditional cooked vegetable dishes as important sourcesof ascorbic acid and b-carotene in the diets of Indian urban and rural families.Food and Nutrition Bulletin 27, 306–310.

Gupta, K., Barat, G.K., Wagle, D.S., Chawla, H.K.L., 1989. Nutrient contents andantinutritional factors in conventional factors in conventional and non-con-ventional leafy vegetables. Food Chemistry 31, 105–116.

Gupta, S., Lakshmi, A.J., Manjunath, M.N., Prakash, J., 2005. Analysis of nutrient andantinutrient content of underutilized green leafy vegetables. LWT 38, 339–345.

Hallberg, L., Brune, M., Rossander, A.B., 1989. Iron absorption in man: ascorbic acidand dose-dependant inhibition by phytate. The American Journal of ClinicalNutrition 49, 140–144.

Halliwell, B., Gutteridge, J.M.C., 1999. Free Radicals in Biology and Medicine. OxfordUniversity Press, Oxford.

Haskell, M.J., Jamil, K.M., Hassan, F., Peerson, J.M., Hossain, M.I., Fuchs, G.J., Brown,K.H., 2004. Daily consumption of Indian spinach (Basella alba) or sweet potatoeshas a positive effect on total body vitamin A stores in Bangladeshi men. TheAmerican Journal of Clinical Nutrition 80, 705–714.

Hotz, C., Brown, K., 2004. Assessment of the risk of zinc deficiency in populationsand options for its control. Food and Nutrition Bulletin 25, S96–S203.

Howard, L.A., Wong, A.D., Perry, A.K., Klein, B.P., 1999. b-carotene and ascorbic acidretention in fresh and processed vegetables. Journal of Food Science 64, 929–936.

Hung, H.C., Joshipura, K.J., Jiang, R., Hu, F.B., Hunter, D., Smith-Warner, S.A., Colditz,G.A., Rosner, B., Spiegelman, D., Willett, W.C., 2004. Fruit and vegetable intakeand risk of major chronic disease. Journal of the National Cancer Institute 96,1577–1584.

Institute of Medicine, 2001. Dietary Reference Intakes: Vitamin A, Vitamin K,arsenic, Boron, Chromium, Copper, Iodine, Iron, Manganese, Molybdenum,Nickel, Silicon, Vanadium, and Zinc. National Academy Press, Washington.

Ismail, A., Marjan, Z.M., Foong, C.W., 2004. Total antioxidant activity and phenoliccontent in selected vegetables. Food Chemistry 87, 581–586.

Isong, E.U., Idiong, U.I., 1997. Comparative studies on the nutritional and toxiccomposition of three varieties of Lesianthera africana. Plant Foods for HumanNutrition 51, 79–84.

Jansen Van Rensberg, W.S., Van Averbeke, W., Slabbert, R., Faber, M., Van Jaarsveld,P., Van Heeden, I., Wenhold, F., Oelofse, A., 2007. African leafy vegetables inSouth Africa. Water SA 33, 317–326.

Jansen Van Rensberg, W.S., Venter, S.L., Netshiluvhi, R., Van Den Heever, E., Voster,H.J., De Ronde, J.A., 2004. Role of indigenous leafy vegetables in combatinghunger and malnutrition. South African Journal of Botany 70, 52–59.

Kala, A., Prakash, J., 2004. Nutrient composition and sensory profile of differentlycooked green leafy vegetables. International Journal of Food Properties 7, 659–669.

Khachik, F., Goli, M.B., Beecher, G.R., Holden, J.H., Lusby, W.R., Tenario, M.D., Barrera,M.R., 1992. Effect of food preparation on qualitative and quantitative distribu-tion of major carotenoid constituents of tomatoes and several green vegetables.Journal of Agriculture and Food Chemistry 40, 390–398.

Khader, V., Rama, S., 2003. Effect of maturity on macromineral content of selectedleafy vegetables. Asia Pacific Journal of Clinical Nutrition 12, 45–49.

Kimiywe, J., Waudo, J., Mbithe, D., Maundu, P., 2007. Utilization and medicinal valueof indigenous leafy vegetables consumed in urban and peri-urban Nairobi.Retrieved September 2008 from the African Journal of Food, Agriculture,Nutrition and Development on the World Wide Web: http://www.ajfand.net/vol7no4.html.

Kruger, M., Sayed, N., Langenhoven, M., Holing, F., 1998. Composition of South AfricanFoods: Vegetables and Fruit. Medical Research Council, Cape Town, South Africa.

Kumari, M., Gupta, S., Lakshmi, J., Prakash, J., 2004. Iron bioavailability in green leafyvegetables cooked in different utensils. Food Chemistry 86, 217–222.

Leskova, E., Kobıkova, J., Kovacikova, E., Kosicka, M., Porubska, J., Holcıkova, K., 2006.Vitamin losses: retention during heat treatment and continual changesexpressed by mathematical models. Journal of Food Composition and Analysis19, 252–276.

Lindsey, K.L., Motsei, M.L., Jager, A.K., 2002. Screening of South African food plantsfor antioxidant activity. Journal of Food Science 67, 2129–2131.

Lopez, H.W., Leenhardt, F., Coudray, C., Remesy, C., 2002. Minerals and phytic acidinteractions: is it a real problem for human nutrition? International Journal ofFood Science and Technology 37, 727–739.

MacIntyre, U., Labadarios, D., 2000. Chaper 6: Dietary intake: quantitative foodfrequency method. In: Labadarios, D. (Ed.), The National Food ConsumptionSurvey (NFCS): Children Aged 1–9 Years, South Africa, 1999. Retrieved Septem-ber 2006 from the Department of Health home page on the World Wide Web:http://www.sahealthinfo.org/nutrition/foodconsumption.htm.

Mai, T.T., Thu, N.N., Tien, P.G., Chuyen, N.V., 2007. Alpha-glucosidase inhibitory andantioxidant activities of Vietnamese edible plants and their relationships withpolyphenol contents. Journal of Nutrition Science and Vitaminology 53, 267–276.

Maisuthisakul, P., Suttajit, M., Pongsawatmanit, R., 2007. Assessment of phenoliccontent and free radical-scavenging capacity of some Thai indigenous plants.Food Chemistry 100, 1409–1418.

Marshall, F., 2001. Agriculture and use of wild and weedy greens by the Piik Ap OomOkiek of Kenya. Economic Botany 55, 32–46.

Masrizal, M.A., Giraud, D.W., Driskell, J.A., 1997. Retention of vitamin C, iron and b-carotene in vegetables prepared using different cooking methods. Journal ofFood Quality 20, 403–418.

McDougall, G.J., Morrison, I.M., Stewart, D., Hillman, J.R., 1996. Plant cell walls asdietary fibre: range, structure, processing and function. Journal of the Science ofFood and Agriculture 70, 133–150.

McPartlin, J., Halligan, A., Scott, J.M., Darling, M., Weir, D.G., 1993. Accelerated folatebreakdown in pregnancy. Lancet 341, 148–149.

Mepba, H.D., Eboh, L., Banigo, D.E.B., 2007. Effects of processing treatments on thenutritive composition and consumer acceptance of some Nigerian edible leafyvegetables. Retrieved April 2008 from the African Journal of Food, Agriculture,Nutrition and Development on the World Wide Web: http://www.ajfand.net/vol7no1.html.

Modi, A.T., 2007. Growth temperature and plant age influence on nutritional qualityof Amaranthus leaves and seed germination capacity. Water SA 33, 369–375.

Mosha, T.C., Gaga, H.E., 1999. Nutritive value and effect of blanching on the trypsinand chymotrypsin inhibitor activities of selected leafy vegetables. Plant Foodsfor Human Nutrition 54, 271–283.

Muller, O., Krawinkel, M., 2005. Malnutrition and health in developing countries.Canadian Medical Association Journal 173, 279–286.

Naczk, M., Shahidi, F., 2004. Extraction and analysis of phenolics in food. Journal ofChromatography A 1054, 95–111.

Negi, P.S., Roy, S.K., 2001. Effect of drying conditions on quality of green leavesduring long term storage. Food Research International 34, 283–287.

Nguni, D., Mwila, G., 2007. Opportunities for increased production, utilization andincome generation from African leafy vegetables in Zambia. Retrieved Septem-ber 2008 from the African Journal of Food, Agriculture, Nutrition and Develop-ment on the World Wide Web: http://www.ajfand.net/vol7no4.html.

Nicoli, M.C., Anese, M., Parpinel, M.T., 1999. Influence of processing on the antioxi-dant properties of fruit and vegetables. Trends in Food Science and Technology10, 94–100.

Noonan, S., Savage, G., 1999. Oxalate content of food and its effect on humans. AsiaPacific Journal for Clinical Nutrition 8, 64–74.

Oboh, G., Ekperigin, M.M., Kazeem, M.I., 2005. Nutritional and haemolytic proper-ties of eggplants (Solanum macrocarpon) leaves. Journal of Food Compositionand Analysis 18, 153–160.

Odhav, B., Beekrum, S., Akula, Us., Baijnath, H., 2007. Preliminary assessment ofnutritional value of traditional leafy vegetables in KwaZulu-Natal, South Africa.Journal of Food Composition and Analysis 20, 430–435.

Ogoye-Ndegwa, C., Aagaard-Hansen, J., 2003. Traditional gathering of wild vege-tables among the Luo of Western Kenya – a nutritional anthropology project.Ecology of Food and Nutrition 42, 69–89.

Omenn, G.S., Goodman, G.E., Thornquist, M.D., Balmes, J., Cullen, M.R., Glass, A.,Keogh, J.P., Meyskens J.L.JJr., Valanis, B., Williams J.H.JJr., Barnhart, S., Cherniack,M.G., Brodkin, C.A., Hammar, S., 1996. Risk factors for lung cancer and forintervention effects in CARET, the Beta-Carotene and Retinol Efficacy Trial.Journal of the National Cancer Institute 88, 1550–1559.

Oniang’o, R.K., Mutuku, J.M., Malaba, S.J., 2003. Contemporary African food habitsand their nutritional and health implications. Asia Pacific Journal of ClinicalNutrition 12, 231–236.

Orech, F.O., Akenga, T., Ochora, J., Friis H., Aagard-Hansen, J., 2005. Potential toxicityof some traditional leafy vegetables consumed in Nyang’oma division, WesternKenya. African Journal of Food, Agriculture, Nutrition and Development on theWorld Wide Web: http://www.ajfand.net/vol5no1.html.

Orech, F.O., Christensen, D.L., Larsen, T., Friis, H., Aagaard-Hansen, J., Estambale, B.A.,2007. Mineral content of traditional leafy vegetables from western Kenya.International Journal of Food Sciences and Nutrition 58, 595–602.

Ponka, R., Fokou, E., Fotso, M., Tchouanguep, F.M., Leke, R., Souopgui, J., Bih, M.A.,2006. Composition of dishes consumed in Cameroon. International Journal ofFood Science and Technology 41, 361–365.

Powers, H.J., 2003. Ribiflavin (vitamin B-2) and health. American Journal of ClinicalNutrition 77, 1352–1360.

Punna, R., Parachuri, U.R., 2004. Effect of maturity and processing on total, insolubleand soluble dietary fiber contents of Indian green leafy vegetables. InternationalJournal of Food Sciences and Nutrition 55, 561–567.

Puupponen-Pimia, R., Hakkinen, S.T., Aarni, M., Suortti, T., Lampi, A.-M., Eurola, M.,Pirronen, V., Nuutila, A.M., Oksman-Caldentey, K.-M., 2003. Blanching and long-term freezing affect various bioactive compounds of vegetables in differentways. Journal of the Science of Food and Agriculture 83, 1389–1402.

Radek, M., Savage, G.P., 2008. Oxalates in some Indian green leafy vegetables.International Journal of Food Sciences and Nutrition 59, 246–260.

Reddy, N.R., Pierson, M.D., 1994. Reduction in antinutritional and toxic componentsin plant foods by fermentation. Food Research International 27, 281–290.

Riboli, E., Norat, T., 2003. Epidemiologic evidence of the protective effect of fruit andvegetables on cancer risk. American Journal of Clinical Nutrition 78, 559S–569S.

Rock, C.L., Lovalvo, J.L., Emenhiser, C., Ruffin, M.T., Flatt, S.W., Schwartz, S.I., 1998.Bioavailability of b-carotene is lower in raw than in processed carrots andspinach in women. Journal of Nutrition 128, 913–916.

Rodriquez-Amaya, 2001. A Guide to Carotenoid Analysis in Foods. ILSI press,Washington, DC.

Roth, D.E., Caulfield, L.E., Ezzati, M., Black, R.E., 2008. Acute lower respiratoryinfections in childhood: opportunities for reducing the global burden throughnutritional interventions. Bulletin of the World Health Organization 86, 356–364.

N.P. Uusiku et al. / Journal of Food Composition and Analysis 23 (2010) 499–509508

Author's personal copy

Ruel, M.T., Minot, N., Smith, L., 2005. Patterns and determinants of fruit andvegetable consumption in sub-Saharan Africa: a multicountry comparison.Background Paper for the Joint FAO/WHO Workshop on Fruit and Vegetablesfor Health, September 1–3, 2004, Kobe, Japan. WHO, Geneva, Switzerland.

SACN (Scientific Advisory Committee on Nutrition), 2005. Review of Dietary Adviceon Vitamin A. TSO, London, UK.

Schaffer, S., Eckert, G.P., Muller, W.E., Llorach, R., Rivera, O., Grande, S., Galli, C.,Visioli, F., 2004. Hypochlorous acid scavenging properties of local Mediterra-nean plant foods. Lipids 39, 1239–1247.

Schippers, R.R., 2000. African Indigenous Vegetables, An Overview of CultivatedSpecies. Natural Institute ACP – EU Technical Centre for Agricultural and RuralCooperation, Chatham, UK.

Schlemmer, U., Frølich, W., Prieto, R.M., Grases, F., 2009. Phytate in foods andsignificance for humans: food sources, intake, processing, bioavailability, pro-tective role and analysis. Molecular Nutrition and Food Research 53, S330–S375.

Scrimshaw, N.S., Sangiovanni, J.P., 1997. Synergism of nutrition, infection andimmunity: an overview. The American Journal of Clinical Nutrition 7, 464S–477S.

Serrano, J., Pupponen-Pimia, R., Dauer, A., Aura, A.-M., Saura-Calixto, F., 2009.Tannins: current knowledge of food sources, intake, bioavailability and biolog-ical effects. Molecular Nutrition and Food Research 53, S310–S329.

Shackleton, S.E., Dzerefos, C.M., Shackleton, C.M., Mathabela, F.R., 1998. Use andtrading of wild edible herbs in the central lowveld savanna region, South Africa.Economic Botany 52, 251–255.

Shitanda, D., Wanjala, N.V., 2006. Effect of different drying methods on the quality ofjute (Corchorus olitorius L.). Drying Technology 24, 95–98.

Smith, I.F., Eyzaguirre, P., 2007. African leafy vegetables: their role in the WorldHealth Organization’s global fruit and vegetable initiative. African Journal ofFood, Agriculture, Nutrition and Development 7 (3). Retrieved June 2007 fromthe World Wide Web: http://www.ajfand.net.index.html.

Sparg, S.G., Light, M.E., Van Staden, J., 2004. Biological activities and distribution ofplant saponins. Journal of Ethnopharmacology 94, 219–243.

Sreeramulu, N., Ndossi, G.D., Mtotomwema, K., 1983. Effect of cooking on thenutritive value of common food plants in Tanzania. Part 1. Vitamin C in someof the wild green leafy vegetables. Food Chemistry 10, 205–210.

Stangeland, T., Remberg, S.F., Lye, K.A., 2009. Total antioxidant activity in 35Ugandan fruits and vegetables. Food Chemistry 113, 85–91.

Steyn, N.P., Olivier, J., Winter, P., Burger, S., Nesamvuni, C., 2001. A survey of wild,green, leafy vegetables and their potential in combating micronutrient defi-ciencies in rural populations. South African Journal of Science 97, 276–278.

Svanberg, S.S.M., Nyman, E.M.G.-L., Andersson, R., Nilsson, T., 1997. Effects of boilingand storage on dietary fiber and digestible carbohydrates in various cultivars ofcarrots. Journal of the Science of Food and Agriculture 73, 245–254.

Tabuti, J.R.S., Dhillion, S.S., Lye, K.A., 2004. The status of wild food plants in BulamogiCounty, Uganda. International Journal of Food Sciences and Nutrition 55, 485–498.

Takyi, E.E.K., 1999. Children’s consumption of dark green leafy vegetables withadded fat enhances serum retinol. Journal of Nutrition 129, 1549–1554.

The ATBC Cancer Prevention Study Group, 1994. The effect of vitamin E and beta-carotene on the incidence of lung cancer and other cancers in male smokers.New England Jounal of Medicine 330, 1029–1035.

Trichopoulou, A., Vasilopoulou, E., Hollman, P., Chamalides, Ch., Foufa, E., Kaloudis,Tr., Kromhout, D., Miskaki, Ph., Petrochilou, I., Poulima, E., Stafilakis, K., Theo-philou, D., 2000. Nutritional composition and flavonoid content of edible wildgreens and green pies: a potential rich source of antioxidant nutrients in theMediterranean diet. Food Chemistry 70, 319–323.

Turnlund, J.R., King, J.C., Keyes, W.R., Gong, B., Michel, M.C., 1984. A stable isotopestudy of zinc absorption in young men: effects of phytate and alpha-cellulose.The American Journal of Clinical Nutrition 40, 1071–1077.

UNAIDS, 2007. Sub-Saharan Africa. Retrieved March 2008 from the UNAIDS home-page on the World Wide Web: http://www.unaids.org/en/CountryResponses/Regions/SubSaharanAfrica.asp.

UNAIDS, 2008. Report on the Global AIDS Epidemic. Geneva, Switzerland.UNICEF, 2006. The State of the World’s Children 2007 – Executive Summary.

Women and Children, the Double Dividend of Gender Equality. New York, USA.Vainio-Mattila, K., 2000. Wild vegetables used by the Sambaa in the Usambara

Mountains, NE Tanzania. Annales Botanici Fennici 37, 57–67.Van den Heever, E., 1997. The use and conservation of indigenous leafy vegetables

in South Africa. In: Guarino, L. (Ed.), Traditional Vegetables in Africa: Conser-vation and Use, August 29–31, 1997, Nairobi, Kenya. International Plant GeneticResources Institute, Rome, Italy, pp. 154–158.

Vanderjagt, D.J., Freiberger, C., Vu, H.-T.N., Mounkaila, G., Glew, R.S., Glew, R.H.,2000. The trypsin inhibitor content of 61 wild edible plant foods of Niger. PlantFoods for Human Nutrition 55, 335–346.

Van Duyn, M.A.S., Pivonka, E., 2000. Overview of the health benefits of fruit andvegetable consumption for the dietetics professional: selected literature. Jour-nal of the American Dietetic Association 100, 1511–1521.

Vasioli, F., Bogani, P., Grande, S., Detopoulou, V., Manios, Y., Galli, C., 2006. Local foodand cardioprotection: the role of phytochemicals. In: Heinrich, M., Muller, W.E.,Galli, C. (Eds.), Local Mediterranean Food Plants and Nuetraceuticals, vol. 59, pp.116–129.

Verkerk, R., Schreiner, M., Krumbein, A., Ciska, E., Holst, B., Rowland, I., De Scrijver, R.,Hansen, M., Gerhauser, C., Mithen, R., Dekker, M., 2009. Glucosinolates in Brassicavegetables: the influence of the food supply chain on intake, bioavailability andhuman health. Molecular Nutrition and Food Research 53, S219–S265.

Walker, A.R.P., Walker, B.F., Adam, F., 2002. Variations in occurrences of nutrition-related diseases in sub-Saharan Africans in stages of transition: what of thefuture? Nutrition 18, 71–74.

Wallace, P.A., Marfo, E.K., Plahar, W.A., 1998. Nutritional quality and antinutritionalcomposition of four non-conventional leafy vegetables. Food Chemistry 61, 287–291.

Weinberger, K., Msuya, J., 2004. Indigenous Vegetables in Tanzania – Significance andProspects. AVRDC – The World Vegetable Center, Technical Bulletin No. 31,Taiwan.

Welch, R.M., 1993. Zinc concentrations and forms in plants for humans and animals.In: Dobson, A.D. (Ed.), Zinc in Soils and Plants. Proceedings of the InternationalSymposium on ‘Zinc in Soils and Plants’ at The University of Western Australia.Kluwer Academic Publishers, London, UK.

West, C.E., Eilander, A., Van Lieshout, M., 2002. Consequences of revised estimates ofcarotenoid bioefficacy for dietary control of vitamin A deficiency in developingcountries. Journal of Nutrition 132, 2920S–2926S.

WHO, 2008. Worldwide Prevalence of Anaemia 1993–2005: WHO Global Databaseon Anaemia. Geneva, Switzerland.

WHO, 2009. Global Prevalence of Vitamin A Deficiency in Populations at Risk 1995–2005: WHO Global Database of Vitamin A Deficiency. Geneva, Switzerland.

Wong, S.P., Leong, L.P., Koh, J.H.W., 2006. Antioxidant activities of aqueous extractsof selected plants. Food Chemistry 99, 775–783.

Yadav, S.K., Sehgal, S., 2003. Effect of domestic processing and cooking on selectedantinutrient contents of some green leafy vegetables. Plant Foods for HumanNutrition 58, 1–11.

Yamaguchi, T., Mizobuchi, T., Kajinawa, H., Miyabe, F., Terao, J., Takamura, H.,Matoba, T., 2001. Radical-scavenging activity of vegetables and the effect ofcooking on their activity. Food Science and Technology Research 7, 250–257.

N.P. Uusiku et al. / Journal of Food Composition and Analysis 23 (2010) 499–509 509