Protein intake adequacy

The studies conducted in Nigeria on protein intake cover only a small part of the Nigerian population. Most data available were obtained from the richer southern parts of Nigeria (Table 2 and Fig. 1). Protein-rich foods are usually expensive and not all households have the purchasing power to acquire them^{(Reference Akerele, Ibrahim and Adewuyi4)}. Therefore, it can be speculated that protein deficiency is more prevalent in northern Nigeria since there are fewer financial resources available to buy protein-rich foods. Altogether twenty articles were included for examining protein intake adequacy. A total of four studies (19 %) focused on school children (aged 2–12 years), seven articles (43 %) on adolescents (aged 10–19 years), three studies (14 %) concentrated on women including pregnant and lactating women, while six articles (29 %) addressed complete households.

Table 2. Adequacy of protein intake in different states in Nigeria

EAR, estimated average requirement; FFQ, food frequency questionnaire; RDA, recommended daily allowance; 24hR, 24 h recall.

* Mean weight expressed in kg, weight used as reported in an article if available, if not a reference weight was used. Average reference weights were calculated when a study covered multiple age groups. When only household data were available, a mean weight of 27·0 kg was calculated from all the reference weights for men and (non-pregnant) women for all ages.

† EAR = sum of protein needed for maintenance and growth⁽¹⁹⁾ = ‘the intake that meets the estimated nutrient needs of half the individuals in a group’. RDA (safe intake level) = average protein requirement plus twice the standard deviation, meeting the needs of 97–98 % of the population⁽²⁾.

‡ Level of satisfaction (%) calculated as protein in g/d consumed by study population divided by the calculated EAR/RDA in g/d × 100.

§ Adapted from FAO⁽¹⁹⁾.

║ Adapted from WHO/FAO/UNU⁽²⁾.

¶ Adapted from Walpole et al. ^{(Reference Walpole, Prieto-Merino and Edwards20)}.

Fig. 1. Map of Nigeria showing the individual states where protein intake was assessed, with the circle indicating a study area studied in one study rather than one state. Blank map adapted from D-Maps⁽⁹³⁾.

It is important to realise the limitations of the present review due to the quality of the reported data. The protein intake values as reported in our review were mean protein intake values. These values are valid to determine average protein intake adequacy; however, they do not take a distribution of intake into account. Furthermore, studies conducted on Nigerian pregnant and lactating individuals were scarce. Due to lack of data (we found only one study; Table 2) on the protein intake among diseased (for example, HIV/AIDS, respiratory diseases, etc.) target populations, we did not analyse this further. Some studies did report a percentage of stunted/wasted children, but most gave no separate protein intake value for this group. Other studies did not provide information on whether the study population included pregnant, lactating or diseased individuals. Also, many studies did not report the actual weights of the participants, making it difficult to calculate a precise EAR/RDA based on their actual body weight.

Based on the reviewed literature, protein intake of the Nigerian population of non-pregnant and non-lactating women and children seems to be mostly adequate (LOS > 100 %). However, notable exceptions were also reported in the study on overall households’ intakes in Edo and Kogi, where protein intake was reported to be inadequate for all family members, with females’ intakes being the lowest^{(Reference Onabolu, Bokanga and Tylleskär23)}. Based on our calculations, protein intake of female adolescents seems to be mostly inadequate (LOS < 100 %). The exceptions of satisfactory intake were reported by Ogechi et al. ^{(Reference Ogechi, Akhakhia and Ugwunna24)} and Anyika et al. ^{(Reference Anyika, Uwaegbute and Olojede25)}, and for adolescents above 13 years by Akinyemi & Ibraheem^{(Reference Akinyemi and Ibraheem26)}. Pregnant and lactating women were another group of concern with inadequate protein intake. This could be due to cultural beliefs that exist in certain parts of Nigeria that extra protein cannot be consumed during pregnancy⁽²⁷⁾ and myths about some forbidden protein-rich foods during pregnancy (for example, eggs, beans, snails and grasscutter meat)^{(Reference Ekwochi, Osuorah and Ndu28)}. Especially, the protein intake of pregnant adolescents was low (LOS_EAR < 70 %^{(Reference Oguntona and Akinyele29)}); these females were not even able to meet the requirements for healthy non-pregnant and non-lactating women (LOS_EAR < 84·0 %; and LOS_RDA < 69·8 %). The adult lactating women could only just meet the EAR (LOS_EAR = 104 %), but not the RDA (LOS_RDA = 86·1 %) for healthy non-pregnant and non-lactating women. This is of concern because inadequate protein intake during pregnancy has both short- and long-term consequences for both the infant and mother. Epidemiological studies in human subjects have shown that protein deficiency during pregnancy gives rise to low birth weight, intra-uterine growth restriction and that these offspring are at greater risk for development of the metabolic syndrome in adult life^{(Reference Oke, Hardy and Oke30)}. Nutritional intervention during pregnancy is necessary to ensure that mothers consume appropriate amounts of dietary protein such that there are no negative effects on fetal growth and development^{(Reference Oke, Hardy and Oke30)}. Adequate nutrition is also important during the lactation period, as the nutritional content of breast milk was shown to be dependent on maternal diet, for example, fatty acid content, water-soluble vitamins, etc. There are also some reports indicating that the protein quality of the mother’s diet is reflected in the amino acid composition of the breast milk^{(Reference Wurtman and Fernstrom31,Reference Lindblad and Rahimtoola32)} . Especially lysine^{(Reference Wurtman and Fernstrom31,Reference Lindblad and Rahimtoola32)} , methionine^{(Reference Lindblad and Rahimtoola32)} and tryptophan^{(Reference Wurtman and Fernstrom31)} were substantially reduced in women with poor protein intake from the diet (for example, by consumption of mostly cereal grains and legumes).

Interestingly, sufficient protein intakes (LOS > 200) were also reported among children classified as protein deficient based on their anthropomorphic measures^{(Reference Stephenson, Amthor and Mallowa13)}. When studies provided their own level of adequacy and reported percentages of individuals with inadequate intakes, a more detailed picture emerged. For example, in the only study with children (2–5 years old) in which such distinction was made, 13 % of the participants were reported to have inadequate protein intake^{(Reference Stephenson, Amthor and Mallowa13)}. Within studies focused on women, inadequate intakes were reported for 18 % of women of childbearing age (15–49 years) in south-east Nigeria^{(Reference Onyeji and Sanusi33)}, 14·4 % of women aged 20–59 years in Osun State^{(Reference Adebukola, Ugwunna and Ekerette34)}, and 22·2 % of adolescent females in Osun^{(Reference Ogunkunle and Oludele17)}.

Nigerian diet and its contribution to protein intake adequacy

Previous literature concluded that dietary diversity was low in six states in Nigeria and should be increased^{(Reference Sanusi35)}. The search into the Nigerian consumption pattern (Table 3; fruits, vegetables, oils and fats, and snacks not shown) shows that all examined food groups in the Nigerian diet were consumed frequently by at least 25 % of the population, with ‘fats and oils’, ‘cereals’ and ‘snacks’ being consumed the most (> 65·0 %). Snack consumption was most often reported in studies assessing adolescents and could be an explanation for the low protein intake of adolescent girls since snacks are often fat- and carbohydrate-rich, but protein-poor. Wheat and rice were the most frequent consumed cereals. Cassava and yam were the most eaten roots and tubers; beans and groundnuts the most frequently consumed legumes. Beef, chicken and fish were frequently eaten animal foods, while dairy products were less frequently consumed.

Table 3. Commonly consumed foods and meals from different food groups and their contribution to meeting the protein requirements

The percentage of the Nigerian population that frequently consumed roots and tubers is 49·5 %. Cereals and grains were on average consumed daily by 81·3 % of the population. Several studies showed a contribution of cereals to the protein intake of approximately 20–40 %^{(Reference Akerele36–Reference Orewa and Iyangbe38)}. Legumes were eaten by 45·5 % of the population on average.

Meat, poultry and fish intakes varied widely depending on the study and geographical location, but on average the consumption percentage was 48·5 % for meat and poultry and 49·1 % for fish and shellfish. According to a study conducted in the south-east of Nigeria, animal-source products contributed only 3 % to the total daily energy intake^{(Reference Stephenson, Amthor and Mallowa13)}. Dairy products were found to account for barely 0·9 % of protein intake^{(Reference Akerele36)}. In general, dairy products were only consumed by 38·4 % of the population, with milk being consumed by only 31·9 % (Table 3).

Protein quality of staple foods

Even though most Nigerian population groups seem to have adequate protein intakes in terms of quantity, it does not guarantee high-enough protein quality. The drastic effects of a poor protein quality cassava-based diet were demonstrated in a study among children displaying signs of protein malnutrition despite their overall protein intakes being very high with LOS > 200^{(Reference Ojo and Deane39)}. However, since almost complete protein intake was based on cassava, which has very low protein quality, with leucine being the first limiting amino acid (DIAAS 11–18), it did not cover the children’s nutritional needs, resulting in malnutrition. Overall, the nine major staple foods eaten by Nigerians appear not to deliver protein of good quality (Tables 4–9). For the foods from the cereal group (rice, wheat, maize and sorghum), lysine was the first limiting amino acid for all age groups, resulting in DIAAS being inadequate (< 75). Wheat and rice were shown to be of good protein quality for children and adults when looking at the second limiting amino acids (DIAAS > 75), but not for infants. The digestibility factor we used for calculating DIAAS of yam was the overall crude protein digestibility for cassava since no factor for yam could be found in the literature. Protein quality of yam depended on the way of its processing. Processed yam compared with the two unprocessed species had lower protein quality in terms of limiting amino acids (DIAAS < 75). The unprocessed (and thus uneatable) yam was shown to be of (marginally) better protein quality for the first SAA and second (lysine) limiting amino acids (DIAAS > 75 for population > 3 years of age). For both groundnuts and cowpeas, the first limiting amino acid was also lysine (DIAAS 27–38), the second SAA (groundnut DIAAS 40–58; cowpea DIAAS 33–49). The DIAAS of rice, maize, wheat and sorghum were, respectively, 42–69, 37–53, 30–43 and 18–26. All sources of cereals/grains did not have good-quality proteins based on their amino acid score and digestibility, and the most deficient amino acid appears to be lysine, followed by SAA. The only source of good-quality protein, which is commonly consumed, was fish. Tilapia, which is also frequently eaten in Nigeria, was the only fish for which information was available to calculate DIAAS: DIAAS > 94 for children 6 months–3 years of age, and excellent DIAAS > 100 for individuals above 3 years.

Table 4. Digestible indispensable amino acid score (DIAAS) of cassava and rice*

AA, amino acid; SAA, sulfur amino acids (methionine and cysteine); AAA, aromatic amino acids (phenylalanine and tyrosine).

* Adapted from FAO⁽¹⁹⁾.

† True ileal digestibility = ‘the disappearance of a nutrient between the mouth and the end of the small intestine (terminal ileum)’⁽¹⁹⁾.

‡ Reference ratio calculated as (amino acid content × digestibility)/scoring pattern.

§ Limiting AA calculated as the amino acid(s) with the lowest (red) reference ratio score × 100 %. Also done for the second (orange) and third (yellow) amino acids.

║ Essential amino acids: histidine (His), isoleucine (Ileu), leucine (Leu), lysine (Lys), methionine (Met), cysteine (Cys), phenylalanine (Phe), tyrosine (Tyr), threonine (Thr), tryptophan (Tryp) and valine (Val).

Table 5. Digestible indispensable amino acid score (DIAAS) of maize and wheat*

AA, amino acid; SAA, sulfur amino acids (methionine and cysteine); AAA, aromatic amino acids (phenylalanine and tyrosine).

* Adapted from FAO⁽¹⁹⁾.

† True ileal digestibility = ‘the disappearance of a nutrient between the mouth and the end of the small intestine (terminal ileum)’⁽¹⁹⁾.

‡ Reference ratio calculated as (amino acid content × digestibility)/scoring pattern.

§ Limiting amino acid calculated as the amino acid(s) with the lowest (red) reference ratio score × 100 %. Also done for the second (orange) and third (yellow) amino acids.

║ Essential amino acids: histidine (His), isoleucine (Ileu), leucine (Leu), lysine (Lys), methionine (Met), cysteine (Cys), phenylalanine (Phe), tyrosine (Tyr), threonine (Thr), tryptophan (Tryp) and valine (Val).

Table 6. Digestible indispensable amino acid score (DIAAS) of yam*

AA, amino acid; SAA, sulfur amino acids (methionine and cysteine); AAA, aromatic amino acids (phenylalanine and tyrosine).

* Adapted from FAO⁽¹⁹⁾.

† True ileal digestibility = ‘the disappearance of a nutrient between the mouth and the end of the small intestine (terminal ileum)’⁽¹⁹⁾.

‡ Reference ratio calculated as (amino acid content × digestibility)/scoring pattern.

§ Limiting amino acid calculated as the amino acid(s) with the lowest (red) reference ratio score × 100 %. Also done for the second (orange) and third (yellow) amino acids.

║ Essential amino acids: histidine (His), isoleucine (Ileu), leucine (Leu), lysine (Lys), methionine (Met), cysteine (Cys), phenylalanine (Phe), tyrosine (Tyr), threonine (Thr), tryptophan (Tryp) and valine (Val).

Table 7. Digestible indispensable amino acid score (DIAAS) of fish (tilapia) and groundnuts*

AA, amino acid; SAA, sulfur amino acids (methionine and cysteine); AAA, aromatic amino acids (phenylalanine and tyrosine).

* Adapted from FAO⁽¹⁹⁾.

† True ileal digestibility = ‘the disappearance of a nutrient between the mouth and the end of the small intestine (terminal ileum)’⁽¹⁹⁾.

‡ Reference ratio calculated as (amino acid content × digestibility)/scoring pattern.

§ Limiting amino acid calculated as the amino acid(s) with the lowest (red) reference ratio score × 100 %. Also done for the second (orange) and third (yellow) amino acids.

║ Essential amino acids: histidine (His), isoleucine (Ileu), leucine (Leu), lysine (Lys), methionine (Met), cysteine (Cys), phenylalanine (Phe), tyrosine (Tyr), threonine (Thr), tryptophan (Tryp) and valine (Val).

Table 8. Digestible indispensable amino acid score (DIAAS) of cowpeas*

AA, amino acid; SAA, sulfur amino acids (methionine and cysteine); AAA, aromatic amino acids (phenylalanine and tyrosine).

* Adapted from FAO⁽¹⁹⁾.

† True ileal digestibility = ‘the disappearance of a nutrient between the mouth and the end of the small intestine (terminal ileum)’⁽¹⁹⁾.

‡ Reference ratio calculated as (amino acid content × digestibility)/scoring pattern.

§ Limiting amino acid calculated as the amino acid(s) with the lowest (red) reference ratio score × 100 %. Also done for the second (orange) and third (yellow) amino acids.

║ Essential amino acids: histidine (His), isoleucine (Ileu), leucine (Leu), lysine (Lys), methionine (Met), cysteine (Cys), phenylalanine (Phe), tyrosine (Tyr), threonine (Thr), tryptophan (Tryp) and valine (Val).

Table 9. Digestible indispensable amino acid score (DIAAS) of sorghum*

AA, amino acid; SAA, sulfur amino acids (methionine and cysteine); AAA, aromatic amino acids (phenylalanine and tyrosine).

* Adapted from FAO⁽¹⁹⁾.

† True ileal digestibility = ‘the disappearance of a nutrient between the mouth and the end of the small intestine (terminal ileum)’⁽¹⁹⁾.

‡ Reference ratio calculated as (amino acid content × digestibility)/scoring pattern.

§ Limiting amino acid calculated as the amino acid(s) with the lowest (red) reference ratio score × 100 %. Also done for the second (orange) and third (yellow) amino acids.

║ Essential amino acids: histidine (His), isoleucine (Ileu), leucine (Leu), lysine (Lys), methionine (Met), cysteine (Cys), phenylalanine (Phe), tyrosine (Tyr), threonine (Thr), tryptophan (Tryp) and valine (Val).

Overall, all DIAAS for the scoring pattern for infants were inadequate. However, infants are supposed to be exclusively breastfed, and the protein of human milk meets all the amino acid requirements. Therefore the FAO⁽⁴⁰⁾ based the scoring pattern for infants on breast milk and consequently no foods from either plant- or animal-based foods can satisfy infant amino acid requirements like human breast milk. However, given the worrying possibility that maternal amino acid deficiencies may be reflected in the composition of breast milk protein, we believe that impact of maternal diet on the amino acid pattern in breast milk requires further research to assure the optimal nutrition for breastfed infants^{(Reference Wurtman and Fernstrom31,Reference Lindblad and Rahimtoola32)} .

Foods with high protein quality (DIAAS ≥ 100) are important to bridge the nutritional gaps created by consumption of the low-quality plant-based staple foods. Animal protein sources such as dairy products, beef, chicken and eggs were animal-source foods shown to be such excellent protein sources (DIAAS ≥ 100; Table 10)^{(Reference Ertl, Knaus and Zollitsch41–Reference Rutherfurd, Fanning and Miller43)}. These foods could be of importance in bridging the gap between the lack of lysine from cereals and legumes. Our results showed that about 40 % of the Nigerian population eats beef frequently. Eggs and chicken are eaten frequently by one-quarter of the Nigerian population. Milk was frequently consumed by one-third of the population. It was shown that plant-based foods had an average DIAAS of 61, whereas animal-source foods had an average DIAAS of 114^{(Reference Ertl, Knaus and Zollitsch41)}. If these animal-source foods are consumed daily, they could replenish the amino acids that are consumed in inadequate amounts due to the daily consumption of mainly cereals. A relatively high-quality plant-based food is soya beans which was shown to be an excellent source of protein and could, therefore, be a valuable (plant food) addition to the Nigerian diet (Table 10)^{(Reference Ertl, Knaus and Zollitsch41)}.

Table 10. Digestible indispensable amino acid score (DIAAS) of high-quality protein foods (adapted from Ertl et al. ^{(Reference Ertl, Knaus and Zollitsch41)})

SAA, sulfur amino acids (methionine and cysteine).

* Based on the scoring pattern of 6 months–3 years using pig true ileal digestibility factors.

† Adapted from Rutherfurd et al. ^{(Reference Rutherfurd, Fanning and Miller43)} based on the scoring pattern of 6 months–3 years using rat true ileal digestibility factors.

‡ Adapted from Mathai et al. ^{(Reference Mathai, Liu and Stein42)} based on the scoring pattern of 6 months–3 years using pig true ileal digestibility factors.

§ Adapted from Mathai et al. ^{(Reference Mathai, Liu and Stein42)} based on a scoring pattern of >3 years of age using pig true ileal digestibility factors.

Dietary diversity and protein quality of a food mixture

As a rule, it applies that eating from multiple food groups, being both plant and animal foods, increases the chance of meeting the nutrient requirements^{(Reference Adebukola, Ugwunna and Ekerette34,Reference Ogunba44)} . Dietary diversity is widely recognised as a key component of high-quality diets, as consuming a variety of foods across and within different food groups helps ensure adequate intake levels of essential nutrients^{(Reference Ruel, Harris, Cunningham, Preedy, Hunter and Patel45)}. However, previous literature concluded that dietary diversity was low in all six examined states in Nigeria and should be increased^{(Reference Sanusi35)}. Resource-poor settings are generally characterised by consumption of monotonous diets^{(Reference Ingenbleek, Jazet and Dzossa46)}.

Consumption from animal-source food groups was found to be significantly related to nutrient adequacy in Nigeria^{(Reference Onabolu, Bokanga and Tylleskär23)}. Animal-source foods are still regarded as the best source of good-quality protein, since plant proteins, with the exception of soya, are lacking one or more essential amino acids^{(Reference Ertl, Knaus and Zollitsch41,Reference McLain, Escobar and Kerksick47)} . Plant foods can make a valuable contribution to overall protein intake, with cereals such as rice and wheat providing adequate amounts of all essential amino acids apart from lysine. The addition of small amounts of animal-based proteins such as milk, cheese, eggs and meat to the diet can possibly bridge the lysine gap that legumes (apart from soya beans) and cereals leave behind.

To demonstrate this in the present review we examined an example of a mixture of commonly eaten plant- and animal-based foods: rice, cowpeas and tilapia (Table 11). The combination of rice, beans and fish is frequently eaten in Nigeria. Portion sizes for rice (51·9 g) and beans (cowpeas) (54·9 g) were obtained from a study in southwestern Nigeria^{(Reference Sanusi and Olurin22)}. A portion size of 50 g was assumed for tilapia. The same true ileal digestibility factors and amino acid contents of the foods as for the individual food calculations (Tables 4, 7 and 8) were used. The first limiting amino acids were tryptophan and valine. However, the tryptophan content of cowpeas was not determined. Therefore, the DIAAS based on the second limiting amino acids (isoleucine, lysine and tryptophan) was also determined. If we exclude tryptophan, the DIAAS for infants, children and others were, respectively, 51, 76 and 84 %. For young children and individuals older than 3 years the protein quality for this mixture was good (> 75 %). Where rice and cowpeas individually had lysine as the first limiting amino acid for individuals older than 3 years, this mixture of foods is of good protein quality in terms of lysine (reference ratio = 0·90) for this age group and tilapia bridged the lysine gap that rice and cowpeas left behind. It should still be examined whether the addition of such foods is feasible in terms of availability, affordability and sustainability. Importantly, when a similar exercise was performed by Suri et al. in 2014^{(Reference Suri, Tano-Debrah and Ghosh48)}, without the addition of an animal protein source, it was shown that both the addition of groundnuts and cowpeas to cereals like maize, millet and sorghum did not yield good protein quality blends (PDCAAS = 42–67 %). The addition of milk (DIAAS > 116) to the diet might be also valuable for increasing linear growth in stunted children^{(Reference Hoppe, Mølgaard and Michaelsen49)} and could be easily achieved by adding milk to pap given to young children.

Table 11. Digestible indispensable amino acid score (DIAAS) of a mixture of rice, cowpeas and tilapia (mixed meal) using the method of the FAO⁽¹⁹⁾

AA, amino acid; SAA, sulfur amino acids (methionine and cysteine); AAA, aromatic amino acids (phenylalanine and tyrosine); n.d., not determined.

* Portion sizes (single serving) for rice and cowpeas were adapted from Sanusi & Olurin^{(Reference Sanusi and Olurin22)} and the portion size of tilapia was set at 50·0 g.

† Protein content of raw foods adapted from Stadlmayr et al. ^{(Reference Stadlmayr, Charrondiere and Enujiugha82)}.

‡ Calculated as portion (g) × protein (g/100 g)/100.

§ Calculated as (amino acid content of foods (mg/g protein) × true ileal digestibility factors of amino acids in the same food) × (protein content in portion per food). The amino acid contents of rice and fish were adapted from Shaheen et al. ^{(Reference Shaheen, Islam and Munmun71)} and for cowpeas from Olaleke et al. ^{(Reference Olaleke, Olorunfemi and Akintayo91)}. The true ileal digestibility factors were adapted from Gilani et al. ^{(Reference Gilani, Tomé and Moughan85)}.

║ Calculated as the sum of each amino acid content per food/total protein content in the mixture (24·7 g).

¶ Calculated as total in mixture mg of each amino acid in total protein/scoring patterns. Scoring patterns for infants (birth–6 months), children aged 6 months to 3 years and other individuals older than 3 years were adapted from FAO⁽¹⁹⁾.

** Digestible indispensable amino acid score (DIAAS) determined by multiplying the reference ratio of the first (marked red) and second (marked yellow) limiting amino acid by 100 %.

Strengths

Nigeria is one of the major countries in the West African region and has a complex and diverse food culture; therefore the results of the present review on Nigeria may be also applicable to other countries in West Africa^{(Reference Adegboye, Smith and Anang11)}. The methodology of this review can be applied to other low- and middle-income countries since the diets are often, just like the Nigerian diet, mostly plant-based (for example, due to costs) and lack variety, which might influence protein intake adequacy. Diet pattern and protein intake as assessed in the present review reflect recent estimates from the year 2000 and onwards. This review considered both the quantity of protein intake and the protein quality of some major staple foods of the Nigerian diet and a mixture of these foods. Moreover, our review used DIAAS, which is the most recent measure for protein quality and can be considered superior to the old measure (PDCAAS). This was, to our knowledge, the first review that calculated DIAAS of foods such as yam and cassava.

Limitations

The lack of information in the literature on amino acid contents of foods and on true ileal digestibility factors for calculating DIAAS was a major limitation for the present review. Many true ileal digestibility factors are determined in animals, such as pigs, and it is still unsure if these results and methods are also applicable to humans^{(Reference Fuller21)}. Many studies did not measure the tryptophan content of foods and we could therefore not calculate a score for this essential amino acid. Given the above, DIAAS was calculated only for nine Nigerian foods, which does not reflect the total diet. The measure for protein quality, DIAAS, does not take quantity into account since it calculates protein quality based on the amounts of amino acid (mg) per 1 g of food protein⁽¹⁹⁾. Furthermore, our review did not take anti-nutritional factors, such as trypsin inhibitors (legumes), tannins (legumes and cereals) and phytates (cereals), both present naturally in the food or formed during processing, into account that may possibly interfere with the absorption of nutrients from the diet. The FAO⁽¹⁹⁾ reported that the methods for determining true ileal digestibility factors might not always fully account for anti-nutritional factors.

Recommendations and future research

We calculated protein quality for a mixture of foods, but information on protein quality of more foods should be determined to calculate DIAAS for complete meals (for example, soups, stews with vegetables, etc.), which play an important role in the Nigerian diet. Also, it is advised to determine the protein quality for more mixtures of foods to examine the role of animal-source proteins in bridging the essential amino acid gaps that plant-based foods leave. To do this, more research should be conducted on amino acid contents of such foods and true ileal digestibility factors to broaden the DIAAS calculations. Also, research should examine whether animal-source proteins can increase the dietary diversity score of Nigerian individuals. Related to this, future research should aim at studying the effects of dietary diversity on protein and amino acid adequacy. The distinction between protein quality v. quantity should be made clearer. This might help in determining portion sizes of (mixtures) of foods for meeting the essential amino acid requirements.

Another attention point for future research might be the development of specific products that address the protein and amino acid needs for those individuals that currently do not consume enough protein. For example, for adolescent girls, it may be beneficial to enrich often consumed snacks with good-quality proteins from, for example, soyabean flour^{(Reference Hyelsinta, Ebere and Kwary50)} or dairy products. Also, possibilities of enriching complementary foods for children, like pap, with good-quality proteins such as soya beans, fish or milk could be explored further^{(Reference Ojofeitimi, Abiose and Ijadunola51,Reference Ijarotimi and Ogunsemore52)} . Providing children with a good-quality protein-rich lunch that will account for about one-third of the protein recommendations in the context of a school feeding programme, for example, might help in eradicating PEM^{(Reference Akarolo-Anthony, Odubore and Yilme53,Reference Awogbenja54)} .

Previous Nigerian studies have suggested affordable and available protein-rich foods such as rabbit meat^{(Reference Kalio, Etela and Ginika55)}, insects^{(Reference Ebenebe, Amobi and Udegbala56)}, wild plant species^{(Reference Lockett, Calvert and Grivetti57)}, indigenous leafy vegetables^{(Reference Omoyeni, Olaofe and Akinyeye12)} and goat milk^{(Reference Belewu and Adewole58)}. Some studies have already been conducted on determinants (for example, socio-economic factors, education, infections) of protein intake and PEM, and it is advised to extend this knowledge to better understand the context of protein malnutrition^{(Reference Akerele, Ibrahim and Adewuyi4,Reference Odebode and Odebode59,Reference Ene-Obong, Enugu and Uwaegbute60)} . Also, we believe further research into the effects of maternal diets deficient in essential amino acids on the breast milk amino acid composition is warranted. Finally, we suggest applying the methodology of this review to other developing countries to examine if there is a trend in protein intake adequacy across these countries.