Production , consumption and nutritional value of cassava ( Manihot esculenta , Crantz ) in Mozambique : An overview

Both soils and climate in Mozambique suit cassava cultivation and nine million tons fresh weight is produced annually, with a consumption of 85 kg per person per year. The roots are a staple carbohydrate and cooked leaves are served as a vegetable. Cassava is essential to food security, as it is a subsistence crop. Roots and leaves contain vitamin C and some minerals but are deficient in proteins and amino-acids. Although cassava is cultivated by about 63% of the population, cyanogenic glycosides and other anti-nutritional factors, threaten food safety. There are more than 100 varieties, but the more drought and insect resistant bitter types predominate. Traditional products made from cassava that rely on sun-drying, cooking or fermentation to reduce toxicity include “rale”, “xinguinha”, “karakata” “mahewu” and “oteka”. Cassava flour has replaced up to 20% of wheat flour in bread, for economic reasons. An overview of the distribution, consumption patterns and nutritional value of cassava in Mozambique could contribute to knowledge, as much of the existing data has not been published. Food safety and nutritional value could be improved by commercializing the production of traditional products or fortifying the affordable staple carbohydrate. This could improve the health of vulnerable rural populations.


INTRODUCTION
Mozambique, one of the poorest countries in Africa (UNDP, 2010) is located in the south east of the continent.The country covers an area of about 799,380 km 2 which includes 36 million hectares of arable soil and a coastline of 2,740 km (FAO, 2011b).The climate in Mozambique is tropical and humid with two distinct seasons.Winter (April to September) is normally cold and dry, while the summer (October to March) period is warm and rainy.The annual ambient temperature is between 23 and 26°C for the coastal zones of southern and *Corresponding author.E-mail: cheryl.mccrindle@up.ac.za;Tel +27827877823.Author(s) agree that this article remain permanently open access under the terms of the Creative Commons Attribution License 4.0 International License northern Mozambique with a mean annual rainfall of approximately 1200 mm (Hoguane, 2007).
The most recent census data was published in 2009 by the National Institute of Statistics (INE) following the last National Population Census, done in 2007.The population of Mozambique was recorded as 21 284 701, with more than 70% living in rural areas.Population density was 27 per km 2 , growing at a rate of 1.7% per year.The gross birth ratio in the country was 42.2 per 1000 inhabitants, with an infant mortality of 94 deaths per 1000 live births and life expectancy of 49.4 years.About 80% of Mozambicans depended on agriculture for their livelihood and the agricultural sector remained the key for social and economic growth (INE, 2009).
Mozambique has been ranked 8 th in the world and 5 th among African countries with regards to cassava production (FAO, 2011a).It is an important staple food in Mozambique, second only to maize (Walker et al., 2006).Maize does not grow easily in certain regions of Mozambique (Tostao and Wade, 2005).The transportation of maize from high production areas to consumers in other areas is not cost effective (Nielson, 2009).Imported maize originates mainly from South Africa and it is significantly more expensive than cassava (Howard et al., 2003;Tschirley et al., 2006).Mozambique was involved in a protracted war which ended in 1992.This war impacted negatively on food production and bitter cassava was sometimes consumed without further processing, causing acute and chronic poisoning due to cyanogenic glycosides (Cliff, 1994).In the two decades since the war ended, efforts have been made to increase local crop production to reduce imports and improve foreign exchange (Mader, 2005;FAOSTAT, 2011b).Cassava is easily cultivated as a subsistence crop in Mozambique, with more than 90% being produced for human consumption (FAOSTAT, 2011b).Consumption has been estimated as 85kg per person per year (IOF, 2008(IOF, /2009)).Cassava is drought-tolerant and mature roots maintain their nutritional value for up to three years (Montagnac et al., 2009b;Gbadegesin et al., 2013).It is a multiple year crop and roots can be kept in the ground until needed, thus increasing food security (El-Sharkawy, 2004;Donovan et al., 2011;Gbadegesin et al., 2013).Cyanogenic glycosides and other anti-nutritional factors are a threat to human health that is well recognized in Mozambique (Ministry of Health Mozambique, 1984;Essers et al., 1992;Cliff, 1994;Cliff et al., 1997;Nhassico et al., 2008;Cliff et al., 2011).However, a less recognized threat is the poor nutrient quality, which because of the high level of consumption of this staple carbohydrate, threatens a large proportion of the population with malnutrition and poor quality of life.
Fermentation of cassava is known to reduce the toxicity of cyanogenic glycosides.It also results in higher levels of vitamins, especially the B group, and essential amino acids and improves digestibility of protein (Amoa-Awua and Frisvad, 1997;Oyewole, 2001;Boonnop et al., 2009).Traditional foods made from fermented cassava in Mozambique include rale, karakata, mahewu, ottaca and oteka.(Tivana et al., 2009;Donovan et al., 2011;Tivana, 2012;Hagglades et al., 2012;Salegua et al., 2012).This overview aims to consolidate knowledge on the production, consumption and nutritional value of cassava in Mozambique, with a view to stimulating research to improve food safety and nutrition, particularly in vulnerable rural populations.

Area cultivated and yield
The cropping season for cassava is described as flexible, because roots can be harvested between eight months and three years after planting (FAO/WFP, 2010).In 2011 the total cultivated area was estimated as 5 632 781 ha.The greater proportion of this was used by small scale farmers (96.4%).The remainder was cultivated by medium (2.3%) and larger scale (1.3%) farmers (INE, 2011).Approximately 2 425 240 ha (43%) of this total cultivated area was used for cassava production.Similar to other food crops in Mozambique, cassava is grown mainly (99.7%) by subsistence and small scale family farmers.Medium scale farmers use only 0.3% of the available land and large scale farmers only 0.01% (INE, 2011).
According to the Agriculture and Livestock Census 2009 to 2010, cassava is cultivated throughout the country.The three provinces with the highest production are Nampula Province, in the northern region (29.27%);Zambesia Province in the central region (26.76%); and Inhambane Province (8.80%) in the southern region (ine, 2011).The estimated production per region is shown in Figure 1.Cassava production increased between 2002 and 2008, when the average production was estimated as six million tons.It rose further to nine million tons in 2010 (FAOSTAT, 2011b).Overall, between 2005 and 2012, the yield of cassava in hectogram per hectare increased from 43.155 to 131.804 (Factfish, 2014).By 2012, the production of cassava had escalated to 10.05 million tons (Factfish, 2014).

Munhaça variety being most common in the Southern
Region; Inciricano and Bedo in the Central Region and Nikwaha, Tomo and Cororo varieties, in the Northern Region (MIC, 2007).Consumer preferences influence the variety consumed and are based on the color of the plant, sharpness of the leaf lobe and the color of the root peel (MIC, 2007;Gbadegesin et al., 2013).

Climate and production areas
In Mozambique there are ten agro ecological zones (Figure 2).The classification of these zones is based on climate, vegetation, altitude, soil and farming systems.It can be seen from Table 1 that the majority of cassava is grown in the poor and marginal zones of Mozambique (INIA, 1994).

Cassava consumption
The form in which cassava is consumed varies in the different regions of the country.In the Northern Region cassava flour (71% of production) is mainly boiled with water to make porridge.In this region the consumption of dried cassava accounts for 21% and fresh cassava for 8%, while the consumption of roasted cassava (rale) is not common (IOF, 2008(IOF, to 2009;;Donovan et al, 2011;Hagglades et al., 2012).

Cooked cassava
Approximately 10% of total consumption is cooked cassava, from mainly sweet varieties (Donovan et al., 2011).Due to the high temperature achieved during boiling, the enzyme linamarase can inactivate cyanide in bitter cassava roots (Nambisan andSundareson, 1985, 1994).Traditionally, in Southern Mozambique, cassava is cooked with other vegetables and peanuts, in a dish known as xinguinha.Boiled cassava root, either sweet or bitter, is traditionally served with a green salad and tea.Cassava leaves are generally cooked to make a dark green vegetable that looks like spinach and can be flavored with different spices.

Cassava flour
About 67% of cassava root harvested, is processed into flour (IOF, 2008(IOF, to 2009)).The roots are first peeled and chipped or fermented, then sun dried before milling at community flour-mills.Direct sun-drying is commonly used for preparation of sweet varieties; whereas fermenting followed by sun drying is used in the preparation of bitter varieties (Zvauya et al., 2002;Tivana et al., 2007;Tivana et al., 2009).The inclusion of the fermentation process reduces or removes cyanogenic glycosides, as well as anti-nutritional factors, such as phytates and polyphenols (Montagnac et al., 2009a).In the Northern Region, cassava flour is mainly used to make a stiff porridge known as karakata (Tivana et al., 2007;Tivana, 20012), which is served with vegetables, fish or meat.Cassava flour is used to bake bread and has replaced between 10 and 20% of wheat flour in Mozambique (Salegua et al., 2012).It is also used to bake cakes, as it is more affordable and available than wheat.

Rale (roasted cassava roots)
Rale is the traditional name for roasted fermented cassava root and it is a ready to eat food.It can be consumed as a snack with tea, or used as a basic staple food with cooked vegetables or meat.

Cassava beverages
Oteka and impala are alcoholic cassava beverages.These beverages are prepared by cooking cassava flour with water to make a thin starch porridge, which is then mixed with sorghum and malt.This form of cassava is consumed when there is a family celebration, or as a reward at the end of a working day (Donavan et al., 2011;Hagglades et al., 2012).Mahewu is a nonalcoholic fermented beverage made from sweet and bitter cassava.The preparation of cassava mahewu in Mozambique has not been documented.It was observed that, in Mozambique, fresh cassava root or flour was cooked to form a porridge, which was cooled and then fermented.Traditionally, bread, sorghum, millet malt or wheat flour is fermented to make a starter culture.Fermentation takes 24 to 36 hours at room temperature.Generally sugar was seen to be added to sweeten the mahewu before it was consumed.

Nutritional value of cassava
The nutritional content of cassava depends on the specific plant part (root or leaves), geographic location, variety, age of the plant and environmental conditions (FAOSTAT, 2011a).The cassava root is composed of carbohydrates and is therefore mainly a source of energy.The starch content varies between 32 to 35% of the mass of fresh roots and 80 and 90% of the mass of dried roots (Montagnac et al., 2009b).Amylopectin comprises 83% of the carbohydrate content of cassava roots while amylose comprises 17% (Rawel and Kroll, 2003).The amount of sucrose, glucose, fructose and maltose is usually low (Tewe, 2004), however, in sweet varieties more than 17% of the root content is sucrose (Okigbo, 1980;Charles et al., 2005).Fiber content differs according to the variety and stage of development of the root.In fresh roots it is less than 1.7%, while it comprises4% of cassava flour (Gil and Buitrago, 2002).Lipid content varies between 0.1 and 0.3% of the fresh mass of cassava roots and is present as nonpolar (45%) or glycolipids (52%) (Hudson and Ogunsua, 1974).The protein content is trivial, between 1 and 3% of dry matter (Buitrago, 1990) and about 1.5 mg/100 g of fresh mass (Bradbury and Holloway, 1988).Essential amino acids are present in low quantities, with the exception of arginine, glutamic acid and aspartic acid (Gil and Buitrago, 2002).The mineral content of the roots varies (Table 2).According to Burns at al. ( 2012) in a study in Mozambique (Maputo and Nampula Provinces) iron content of cassava roots, varied from 8 to 24 mg/kg whereas zinc was between 3 to 140 pm (Burns et al., 2012).The vitamin content of the roots is low, except for vitamin C, which is found at relatively high levels of between 15 to 45 mg/100g per edible portion (Okigbo, 1980;Gil and Buitrago, 2002;Charles et al., 2004).The content  Lancaster et al., (1982).
of B vitamins of cassava roots is also found to be trivial (Gil and Buitrago, 2002).
The nutrient density of cassava leaves differs in quantity and quality according to cassava variety, stage of development of the shrub and the relative size of the leaves and stem (Gil and Buitrago, 2002).As can be seen from Table 2, cassava leaves contain a higher amount of protein, essential amino acids, vitamins B 1, B 2, and C and carotenoids than roots (Adewusi and Bradbury, 1993;Okigbo 1980;West at al., 1988) and the starch content varies from 7 to 18 g/100g (Gil and Buitrago, 2002).They also contain more minerals such as calcium, iron, manganese, and magnesium and zinc (Webeto at al., 2006).In Mozambique (Maputo and Nampula Provinces) iron content in cassava leaves ranged from 284 to 93 mg/kg and the zinc concentrations varies between 47,8 and 27,0 mg/kg (Burns et al., 2012).

Anti-nutritional factors in cassava
Cassava contains anti-nutritional compounds that affect the digestibility and absorption of nutrients.Processing techniques are used to counteract or denature antinutritional factors and increase nutritional value of the leaves and roots (Montagnac et al., 2009b).These antinutritional factors include phytates, polyphenols, oxalates, nitrates and saponins.The quantity depends on the variety of cassava and plant maturity (Nambisan and Sundareson, 1994;Montagnac et al., 2009a;Bandna et al., 2012Bandna et al., -2013)).
Phytate content of roots is about 624 mg/100 g in the roots (Marfo et al., 1990).It interferes with the uptake and utilisation of minerals such as calcium, iron, molybdenum and zinc in consumers (Hambidge at al., 2008).Phytate has also been reported to interfere with the enzymatic process of protein digestion in the gut (Singh and Krikorian, 1982).
Polyphenols or tannins, mainly found in cassava leaves, range from 2.1 to 120 mg/100g dry weight (Wobeto et al., 2007).Studies have reported that tannins interfere with the uptake of nonheme-iron in consumers and decrease thiamin absorption and the digestibility of starch (Silva and Silva, 1999).They also interfere with lipid and protein digestibility (Bravo, 1998).Oxalates are found in cassava leaves and it is well known that oxalates interfere with calcium uptake (Wobeto et al., 2007).Oxalate a in cassava leaves varies from 1.35 to 2.88 g/100 g dry weight (Correa, 2000;Wobeto et al., 2007).

Cassava toxicity
The most toxic substances found in both cassava roots and leaves are cyanogenic glycosides.The level depends on the genotype as well as environmental factors, for instance drought.Acute poisoning and death following consumption of cassava is rare.Cases that have been reported are mainly associated with undernourishment, marasmus and kwashiorkor (Cock, 1973;FAO/WHO, 2005).In Mozambique, acute poisoning from cassava consumption has, however, been reported in Nampula Province (Essers et al., 1992).To avoid acute toxicity in humans the level of cyanide should be less than 10 mg equivalent/kg dry matter (FAO/WHO, 1991a).Unfortunately, it is estimated that the level of cyanide from cassava, consumed per person in Mozambique, is 14 to 70 times higher based on bodyweight (Burns et al., 2012), than the safety limit proposed by the World Health Organization (FAO/ WHO, 1991b).
In Mozambique, konzo is the most common cassava intoxication reported.The first case of konzo was reported in 1981 (Ministry of Health Mozambique, 1984).Population groups found to be most vulnerable are women of child bearing age and children up to two years of age (Cliff et al., 2011).All cases reported in the country have been found to be related to consumption of bitter cassava which was poorly processed, collected during a famine period, during the civil war, or to a diet deficient in sulfur amino acids (Ministry of Health Mozambique, 1984;Essers at al., 1992;Tylleskar er al., 1993;Cliff at al., 1997;Ernesto et al., 2002;Cliff at al., 2011). Patients Salvador et al. 35 with konzo have been found to have a high level of thiocyanete in their urine (Ministry of Health Mozambique, 1984;Ernesto et al., 2002;Cliff at al., 2011).Thiocyanate remains in the body as a result of the detoxification of cyanide.It is stored in the stomach and patients with konzo are also at risk to develop stomach cancer (Mirvish, 1983;Maduagwu and Umoh, 1988).Like anti-nutritional factors, cyanogenic glycosides can be reduced or removed by processing.Processing methods include drying, roasting, boiling, soaking, wetting, and fermentation (Zvauya et al., 2002;Cardoso et al., 2005;Tivana et al., 2007;Cumbana et al., 2007;Tivana et al., 2009).Detoxification processes can be used singularly or in combination.In most cases the combined use of processes results in better nutrient quality (Ikemefuna et al., 1991).A long term approach to the removal of cyanogenic glycosides would be by genetic manipulation to breed less toxic cassava plants (Soetan, 2008).However, this would not solve the problem completely, as environmental factors also play a role.

CONCLUSIONS
This overview consolidates recent publications on the production, consumption and nutritional value of cassava in Mozambique.Many rural parts of Mozambique are remote and lack infrastructure.It is mainly in these deep rural areas that cassava plays an essential role in food security.It is well recognized that the toxic and antinutritional factors in cassava threaten food safety in vulnerable populations, particularly during famine or civil unrest in Mozambique.Yet there are affordable traditional ways of reducing and eliminating these toxic compounds and improving the health of rural populations, using traditional cassava products such as karakata, rale, mahewu and oteka.On a positive note, cassava provides an affordable and accessible source of carbohydrates in Mozambique, as it is easily cultivated, even at subsistence level and is resistant to drought and insects.The macro-economic impact of cassava flour is particularly important to make bread more affordable, as imported wheat is expensive in a country with a very low Gross Domestic Product and a high level of poverty.More research is required on ways to enrich cassava products, to meet the need for essential nutrients in vulnerable populations, particularly growing children and women of childbearing age, possibly including fortification with essential nutrients such as iron.
and 100 varieties have been documented in Mozambique (INIA/IITA/SARRNET, 2002).Varieties grown in Mozambique are known to vary according to region; the

Table 1 .
Agro ecological zones for cassava growth with their agro-climatic conditions.