Sorghum , an alternative cereal for gluten-free product Sorgo , un cereal alternativo para productos sin gluten

Corresponding author: Davy Chávez. Universidade Federal Rural do Rio de Janeiro, Department of Food Science and Technology, Rodovia Br 465, km 7, 23890-000, Seropédica, RJ, Brazil. E-mail: davyhw76@gmail.com ABSTRACT There is a growing demand for health foods, indicated by the number of searches including the terms “celiac disease” and “gluten free products”. Most information is designed not only for celiac and gluten intolerant patients, but by others interested in obtaining additional health benefits from foods. Sorghum has been recently recognized as a cereal with functional properties, able to improve human health, but still of low direct human consumption. This review aims to illustrate the publication trends relating to sorghum for gluten free products and celiac disease. The scientific literature available in databases from the last twenty years was used. We perceived the need for further sensorial studies in order to understand the consumer expectations of gluten free products, considering the large varieties of colored sorghum grains that could be used to prepare different gluten free products.


INTRodUCTIoN
In the beginning of the 21st century, food security became a public priority concern led by social, political and environmental problems at different scales 1 .The movement is founded on the idea of adequate nutrition, freedom from hunger and that the government has the obligation to provide food security for vulnerable groups, as part of international and regional conventions, agreements and protocols 2 .It is important that vulnerable groups may also be assisted by food safety protocols, as it refers to the reduction of the probability that certain food products may result in illness, injury, or even death.
Gluten-related disorders (GRDs) are triggered in certain individuals when products that contain gluten are consumed.Gluten is found in some cereals, such as wheat, barley or rye 4 .These individuals belong to a particular vulnerable group that is genetically and/or immunologically predisposed to suffer from GRD.This group can be subdivided into individuals suffering from allergies (wheat allergy), autoimmune diseases (celiac disease (CD) and diseases that are likely to be immune mediated (Non-celiac gluten sensitivity) 5,6 .
Consumers with different GRDs require more options to eat.On the other hand, the number of gluten free products (GFP) is growing due to an increase of consumers with gluten intolerance and others that avoid products containing gluten and follow a GFP diet for lifestyle reasons.Nevertheless, there are not enough GFP options and quality and quantity of these products have not kept up with the rising demand 7,8 .Improvement of GFP is a challenge for the food industry and the number of studies on this topic has been on the rise.
Currently, non-conventional cereals such us sorghum and millet are not considered important plants for human nutrition in most countries of Europe, and North and South America.In those regions they are produced mainly for animal feed.In contrast, sorghum and millet are major food sources in many African and Asian countries, not only for human consumption, but because they have been considered as interesting crops due to their agronomical characteristics.They are drought resistant and have a low fertilizer requirement 10,11 , which make them suitable to adapt in the new global warming scenario.In addition, sorghum is an interesting alternative for celiac patients and gluten intolerant consumers 1 .
In developed countries, the consumption of sorghum, especially varieties with tannin, may promote intake of low calories associated with high antioxidant, dietary fiber content, with the consequent benefits for celiac disease, obesity and diabetes-related health problems 11,14,15 .Also, in developing countries, sorghum could represent an important income reduction mechanism in foreign grain import costs, hence the use of sorghum as a food for human consumption could help local economies additionally to their health benefits 1 .
This work evaluates the current knowledge and ongoing information on CD and sorghum.It examines three important aspects: 1) CD; 2) Sorghum, as an alternative for human nutrition and health and 3) a metadata analysis regarding CD, sorghum and sensorial publications in order to understand the reasons why GFP are not sufficiently available worldwide.

data collecting
FAOSTAT was used to collect the latest (2014) available crop information regarding sorghum production; the search was performed in June 2017.The Google trends search engine, accessed in June (2017), was used to find the terms "gluten free" and "Celiac disease" from 2004 to 2016.Also, the Scopus bibliographic database was consulted for the period 1997 to 2016, using the words: "sorghum", "celiac", "sensorial analysis", "food" and additional combinations.These terms were searched in the title, abstract and keywords.

Gluten-related disorders (GRd)
GRD can be classified into three groups: group 1, autoimmune disorders that includes CD, gluten ataxia (neurological manifestation of gluten intolerance) and dermatitis herpetiformis; group 2: allergies, e.g.wheat allergy (respiratory allergy, immediate food allergy, wheat-dependent exercise-induced anaphylaxis WDEIA, and urticaria; group 3: non-autoimmune and non-allergic disorders also called nonceliac gluten sensitivity (NCGS) 5,16 .Nonetheless, the difference the according to Hollon17, a gluten exposure can be resulted in increase in intestinal permeability.
The World Gastroenterology Organization 18 defines CD as a chronic, multiple-organ autoimmune disease that affects the small intestine in genetically predisposed children and adults.CD is a result of both intrinsic (genetic) and extrinsic variables (environmental) 19 , other important factor to be consider is the immune dysregulation 4 .CD affects millions of people around the world and its prevalence is increasing 20 .CD affects 1 in 133 Americans, even though 1% of the U.S. population is thought to be afflicted with CD, with 97% of cases going undiagnosed 21 .On the other hand, CD is considered rare in Africa, China, Japan, Korea, Malaysia and immigrants from these countries, where consumption of wheat products is low 22 .
Concerning the proteins responsible for GRD, prolamin is present in cereal grains, e.g., wheat (gluten), rye (secalin), and barley (hordein) that are known to bring about allergic response or detrimental autoimmune reaction in certain individuals 4,2 .
Patients with GRD must avoid foods containing gluten (prolamin proteins coming from wheat, rye and barley) their entire lives 4 .Adults generally are conscious and able to prevent the consumption of GBP (e.g., baked goods and pasta) in daily life events, such as meetings and birthdays, particularly in Western diets.This situation becomes more difficult when travelling to locations where GFPs are not easily found, requiring persons to take their own food with them.But, the situation is much worse when children are affected, as they do not understand the reasons they must restrict their diets.The relationship with other kids and psychological status may be affected as they see their classmates and friends eating all foods containing gluten.Therefore, the entire family is affected with the restriction, which imposes changes in food habits 21 .
From 2004, an increase in the number of searches using the term "CD" was observed up to 2012 when the number began to decline.The popularity of the term "GFP" in Google steadily increased until 2013 and remained stable to 2016 (Figure 1).The steep increase in CD articles in 2008 may be attributed to the increase of awareness influenced by international media events, mainly occurring in developed countries such as the USA, Italy and United Kingdom.When comparing the percentage of searches of both terms, CD is considerably lower (12 % of the number of searches in google in 2012) whereas GFP reached 89% in 2013 (Figure 1).Although searches for CD decreased, GFP kept increasing, which shows a clear concern and/or influence of health seeking issues of lifestyle change that may or may not be related to CD.According to Witczak 23 , the market for GFPs is growing all over the world, as well as plant alternatives to make GFPs such as corn, potato, cassava, rice, sorghum, millets, buckwheat, amaranth, quinoa, legumes, flaxseed, chestnut, carob germ flour, lupin.
E is cross-linked by repeated gluten peptides (eg, Ser-Gln-Gln-Gln-[Gln-]Pro-Pro-Phe).Additionally, the release of immune mediators such as histamine from basophils and mast cells are induced by non-gluten proteins.On the other hand, CD is an autoimmune disorder, which is diagnosed based on serologic markers such as serum antibodies against tissue transglutaminase-2, followed by intestinal biopsy 5 .

Sorghum
Sorghum is a low cost cereal crop characterized by its efficient use of water, resistance to drought and poor soil requirement fertility, as it originated from arid regions of Africa, although there are reports mentioning that it is also native to India 15 .Currently, it can be found in other arid zones of Australia, Central, South America, and North America 25,26 .Sorghum is the major source of carbohydrates, energy and proteins in African and Asian countries.These regions produce different sorghum food types 27 , including breads, tchapalo or sorghum beer, popped sorghum, and porridge, among others 28 .In most industrialized countries such as the USA, Europe and other developing countries like Mexico, Brazil, Argentina, among others, sorghum is mainly used for feed 8,29 .
Since 1977, sorghum yield has been growing more than any other crop in drought and semiarid areas around the world, as reported by Bookwalter, Warner 26 .In addition, as mentioned by de Mesa-Stonestreet 21 , "sorghum utilization helps in food security issues because it is a drought resistant crop that easily withstands harsh cultivating conditions in impoverished regions of Asia and Africa".This sentence is a clear call for awareness that food security is an urgent topic of discussion with respect to global warming.
Sorghum is currently the fifth most produced cereal, following maize, wheat, rice, and barley.Sorghum belongs to the Poaceae family, like wheat, rye, barley, and oat (Figure 2), but from a different subfamily, Panicoideae.Wheat, rye and barley are classified in the same tribe (triticeae), whereas oat and sorghum are divided in avenae and andropogoneae, respectively.NCGS or simply, gluten sensitivity are reactions against gluten that involved neither allergic nor autoimmune mechanisms, nevertheless, the symptoms of NCGS could be similar to those of CD.The most prevalent NCGS disorders are abdominal pains, skin (eczema), headache, diarrhea, among others 5,6 .The diagnosis is difficult because there are no specific laboratory markers for NCGS.Thus, diagnosis alternative are conducted by exclusion, which begins by eliminating CD, then wheat allergy, following by a GFP.diet.As a result, the diagnosis could be made by an open challenge (monitored re-introduction of gluten containing foods) 5 .
Wheat allergy is defined as an adverse immunologic reaction to wheat proteins which prevails in an average of 18% of food allergies The clinical manifestations are similar to other food allergies that present symptoms on the skin and in the respiratory track 16 .In wheat allergy, immunoglobulin According to Ratnavathi and Patil 29 , sorghum is known for its nutritional quality.Nevertheless, the global direct consumption is low and it is considered a marginal crop when compared rice, wheat and maize.Concerning its nutritional value, in a study of 100 sorghum genotypes, cultivated under controlled water stress condition, Queiroz 30 , reported minimum and maximum values (g/100g) of the following components: carbohydrates (54,6 -77,2), proteins (7,8 -19,0), dietary fiber (8,5 -26,3), lipids (1,6 -5,0) and ash (0,9 -2,8).Sorghum prolamins are named kafirins, which are considered safe for celiac patients 12 .
Consequently, sorghum is considered a functional food 12,14,41 .It has been recently reported that sorghum presents anticarcinogenic and antimutagenic properties 28,32,38 , as well as reducing cardiovascular disease, diabetes and obesity 32 .In addition, the health use of sorghum proteins for CD patients and different levels of gluten intolerant consumers has been extensively reported 8,12,21,26,28,32 .

Sorghum-made food product
Most products produced with sorghum are found in India and some African countries 25,39 .In West Africa the consumption of sorghum beverages (alcoholic and nonalcoholic) is common.Examples include: Dolo (Burkina Faso), Burukutu (Ghana), Pito (Ghana), Gowé (Benin) and Ran-noodo 42 .The combination of soghum and maize is called Kunu and is found mainly in northern Nigéria 43 .In a review by Ratnavathi and Patil 29 , the authors compiled a list of foods made from sorghum and its mixture with other cereals.Some of them are described below: Tortillas are a traditional Mexican food, conventionally based on calcium oxide treated maize, also called nixtamalization, this same process is also carried out with sorghum to produce very fine circles that is baked 44 .
Roti or bhakri is made with a fine whole sorghum flour that is baked on rolling 45 .
Injera is a bread made from fermented dough for about 48 h and baked for 2-3 min 46 .
Kanji or ambali is a porridge prepared from whole sorghum flour of low consistency that is consumed in the southern parts of India, Africa and Central America 47 .
Tô is made from decorticated soghum grain that is milled into a flour, that is cooked for about one hour in water (1:4) with small amount of tamarind or lemon juices and allowed to cool (1 h) 48 .
Annam is made of dehulled boiled sorghum grains in water (1:3) until grain softness is achieved, and then the excess of water is drained off 45 .
Upma is a breakfast food or snack prepared with wheat semolina and polished milled sorghum.It is made with a little oil in a sauce pan and seasoned with grains like chickpeas along with mustard and cumin seeds 47 .
Sankati is a type of thick porridge made from grits or flour of milled sorghum grain that is boiled for 10 min with water (1:3).Then, fine flour is added by stirring for about 3 min and 10 cm diameter balls are made, eaten fresh or stored overnight 43 .
Dosa and Idli are fermented breakfast foods.Idli is made in molds and steam cooked, while Dosa is a thin, oily pan cake 47 .
Muruku, chakkalu and namak (Snack foods) are made by frying blended sorghum flour.These products could compete with snacks made from corn, rice and wheat 29 .
Ugali is main made of brown sorghum, but also with white grains that is served as a stiff porridge 49 .
Ogi is made from dehulled or whole milled sorghum and is cooked with water, vegetables, meat and other ingredients to produce a type of soup 50 .
Kisra is prepared by mixing 60% whole sorghum flour and 40% water and then fermented for 12-24 h until a sour taste is obtained 51 .
Couscous is a coarse granulated sorghum flour (whole or dehulled) with water it is turned into agglomerated particles that are consumed with milk and other sauces 49 .
The partial or total substitution of wheat with local flours originated a basted bakery product like bread (whole sorghum), plum cake and biscuits, noodles and pasta.Popping sorghum is a common product too.On the other hand, the extrusion cooking technology has opened a wide variety of products with high commercial values based on the good extrusion qualities of sorghum (in some cases it presents similar properties of extruded corn and rice products) 29 .

Metadata analysis
The number of scientific publications regarding the term "celiac" was higher (Figure 3a) than any other, totalizing 24.239 (from 1997 to 2014).When the term "celiac and food" (Figure 3a) was used, the number of publications drastically reduced from thousands to hundreds per year totaling 2.382, which represented about 10% of the search term "celiac".Although the number of publications was low when "food" term was considered, there is a steady increase in publications that it is believed traditional and nontraditional foods have been investigated and/or develope.
When compared to "celiac", the term "sorghum" appeared in 13.594 research articles (Figure 3b), whereas "sorghum" and "food" terms totaled 2.210 published works, indicating that sorghum for food uses are comparably low and still deserves attention.By combining "sorghum" and "celiac" terms, only 54 articles were found (Figure 3d).The first articles that considered these terms appeared in 2004 and in 2016 the just three mentioned the term.
In order to develop a food product, it is very important to have it evaluated by sensory analyses.By following a market rule, "sensorial" and "food" terms were also searched for in scientific publications.As expected, a considerable number of articles was found (1,608) from 1997 to 2016 and expressive growth over the years (Figure 3c).
When "sorghum" and "sensorial food" terms were searched, only 200 articles were found (Figure 3c).It is worth noting that only 17 articles were found when "celiac" and "sensorial" were searched together (Figure 3d), indicating a strong need to develop new sorghum food products for CD patients with good quality and acceptance 23 .Sensorial studies and characterization are the key to evaluate and develop products 52 .
The USA, India, Brazil and China are the countries with almost 55% of published articles on sorghum (Figure 4a).The countries with research based on developing food for humans using sorghum are USA, India, Nigeria, South Africa, China and Brazil with almost 45% of articles (Figure 4b).The USA and European countries appear to be mainly concerned with CD (Figure 4c), as opposed to African and countries from the Indian sub-continent, where CD is believed to be scarce18.Data analysis also revealed three countries where sensorial analysis in food is emphasized (Figure 4d): Spain (13,7%), Brazil (12,5 %) and Italy (12,1%).
A list of published data from the last few years (2015-2017) on the use of sorghum food applications is displayed in Table 1.It is worth noting that only recently, a growing concern on producing acceptable foods using sorghum that combine good sensorial appeal and health benefits is observed.The list shows a scarce number of technical publications that evaluate sorghum products using sensorial techniques.

CoNClUSIoNS
The consumption of GFPs has experienced an exponential increase in the last few years, particularly from 2006.This outstanding increase was not only caused by the rise in incidence of CD and gluten intolerance, but also due to the consumer´s concern for eating healthy foods-absent of gluten, but with beneficial increments of dietary fiber, bioactive compounds and antioxidant capacity.In this review, we have shown that sorghum grain has important functional food characteristics.Thus, it can be considered a health food alternative for the population, particularly, for persons with CD and those with lower levels of gluten intolerance.However, it was also observed and demonstrated here, based on the online search engines, that there are limited number of GFP.Also, more sensorial studies are the key to meet the challenge of developing palatable GFP based in sorghum.

Figure 1 .
Figure 1.Trends in search related terms: "Gluten free products" and "Celiac disease" (www.google.com.trends),accessed in June, 2017.* Searched terms are relative to the total number of Google searches.

Figure 3 .
Figure 3. Number of scientific articles from 1997 to 2016 using Scopus metadata.This search was carried out in June, 2017.

Figure 4 .
Figure 4. Top ten countries in publications regarding the searched terms: a) "sorghum", b) "sorghum and food", c) "celiac" and d) "sensorial and food" by employing Scopus metadata.This search was carried out in June, 2017.

Table 1 .
An overview of recent (last two years) publications using sorghum as directly consumed food product.Peroxidases from root exudates ofMedicago sativa and Sorghum bicolor: No Dubrovskaya et al. 54 Catalytic properties and involvement in PAH degradation Resistant starch content among several sorghum (Sorghum bicolor) genotypes and No Teixeira et al. 15 the effect of heat treatment on resistant starch retention in two genotypes Physicochemical properties of sorghum and technological aptitude for popping.No Llopart and Drago 13 Nutritional changes after popping Nutritional composition of sorghum [Sorghum bicolor (L.) Moench] genotypes No Queiroz et al. 31 cultivated without and with water stress Composition, in vitro digestibility, and sensory evaluation of extruded whole Yes Mkandawire et al. 33 grain sorghum breakfast cereals Proline over-accumulation alleviates salt stress and protects photosynthetic and No Reddy et al. 55 antioxidant enzyme activities in transgenic sorghum [Sorghum bicolor (L.) Moench] Tocochromanols and carotenoids in sorghum (Sorghum bicolor L.): Diversity and No Cardoso et al. 56 stability to the heat treatment Dual modification of native white sorghum (Sorghum bicolor) starch via No Mehboob et al. 57 acid hydrolysis and succinylation Process optimization for a ready-to-serve breakfast smoothie from a composite Yes Rani et al. 58 milk-sorghum base Sorghum-cowpea composite porridge as a functional food, part II: Antioxidant No Apea-Bah et al. 59 properties as affected by simulated in vitro gastrointestinal digestion Effect of heat treatment of sorghum flour on the functional properties of Yes Marston et al. 60 gluten-free bread and cake Utilization of sorghum, rice, corn flours with potato starch for the Yes Ferreira et al. 61 preparation of gluten-free pasta