Abstract
Although sorghum has been used for centuries as a food-crop in Africa and India, researchers in the United States and Europe have only relatively recently become interested in the potential of this unique cereal. Much of this interest focuses on the potential use of sorghum in food product development for individuals with allergies to foods containing wheat-based flours. Because it lacks gluten, sorghum is considered safe for people diagnosed with celiac disease, a condition marked by intolerance to gluten. Recent studies have shown that certain sorghum varieties, tan-plant sorghums, can be used to produce high-quality food and beverage products including cookies, waffles, flour, bread, noodles and beer. The intention is to promote the use and marketing of these sorghums in the Italian Campania Region for sorghum flours suitable as food for celiac patients.
Introduction
Celiac disease (CD) is an autoimmune condition that requires a gluten-free diet for the rest of one's life. Celiac patients must avoid wheat and related grains such as barley, rye, spelt, and triticale because, like wheat, they contain gluten (Kasarda Citation2001). Gluten ingestion in celiac patients causes a variety of gastrointestinal and non-gastrointestinal symptoms and biochemical abnormalities (Sollid Citation2002; Green and Jabri Citation2003) which ameliorate after gluten withdrawal. Diagnosis is often made in adulthood and in patients with a long personal history of disease can run misdiagnosed for years (Ciacci et al. Citation1995). The highest reported prevalence is in Northern Europe and in countries of European ancestry with the overall prevalence in the general population as high as 1% (Catassi et al. Citation1996; Fasano and Catassi Citation2001; Green and Jabri Citation2003).
Sorghum (Sorghum bicolor [L.] Moench) is a drought-resistant and heat tolerant cereal grain that grows in semi-arid conditions. While sorghum has traditionally been used primarily as animal feed in Western countries, nearly 40% of the world sorghum production is used for human food in Africa and India. (Dendy Citation1995; Rooney and Waniska Citation2000).
Sorghum is considered a safe food for celiac patients because it is more closely related to maize than to wheat, rye and barley (Kasarda Citation2001). Sorghum might, therefore, provide a good basis for gluten-free breads and other baked products such as pasta, cookies, and snacks although no direct testing has been conducted on its safety for celiac patients. Significant research has been conducted on sorghum-wheat composite foods and sorghum can be added to wheat flour to produce acceptable breads and other foods (Hulse et al. Citation1980; Dendy Citation1992; Munck Citation1995; Cauvain Citation1998; Carson et al. Citation2000). However, such composite foods could not be consumed by persons with celiac disease.
Several types of wheat-free food products have been made from sorghum including: breads (Satin Citation1988; Cauvain Citation1998; Schober et al. Citation2005), parboiled sorghum (Young et al. Citation1990), sorghum tortillas (Choto et al. Citation1985), snack foods (Serna-Saldivar et al. Citation1988), cookies (Badi and Hoseney Citation1976; Morad et al. Citation1984) and flatbreads (Lindell and Walker Citation1984; Morad et al. Citation1984). These studies have demonstrated that sorghum can be used to produce high quality human food products. Recently, in the US sorghum hybrids that produce white grain from a tan plant (often called ‘food grade’ sorghum) are being used for the production of wheat-free foods for persons with celiac disease. The development of white food grade sorghum lines means that white, neutral tasting flour can be produced from sorghum. These flours are useful in food products because they do not impart unusual colors or strong flavors and may be desired over corn flours for these reasons (Waniska and Rooney Citation2002). The present study was planned to evaluate the impact of pure sorghum food products on celiac patients with the aim to promote sorghum cultivation and flour production in the Italian Campania Region and use as valuable food for humans in Western countries which traditionally use sorghum mostly for animal feed.
Materials and methods
Sorghum field trials
Field trials of tan-plant sorghum cultivars were performed according to Nagaraj et al. (Citation2005).
Sorghum food production
Sorghum bread was produced as described in Schober et al. (Citation2005) with the addition of olive oil and cookies as described in Badi and Hoseney (Citation1976). All sorghum food products were made from a commercially-available white food grade sorghum flour (Twin Valley Mills, Ruskin, NE, USA).
Market analysis
The market analysis for gluten-free food was performed using the Italian Association of Celiacs (IAC) database Citation2004.
In vivo protocol
Two female celiac patients from the hospital staff were asked to consume sorghum products for five days. They were both known to be strictly compliant to their gluten-free diet. Before the challenge, a routine haematology and laboratory set of analyses was performed, including analysis for anti-transglutaminase antibodies (2,3 and 3,4 UL, respectively, normal range 1–5). Sorghum flour products were administered daily per os in two celiac patients after informed consent. An expert in the preparation of gluten-free food was asked to prepare three different products: bread, cookies, and small cakes. Patients were asked to consume bread and cookies in the quantity of 150 g per day for 5 days. Patients were asked to answer a questionnaire on palatability and quality of food (visual analogue scales) and a 20-item questionnaire on gastrointestinal and non-gastrointestinal symptoms during the 5 days challenge and after an additional 7 days (day 12). Serum was analyzed for the presence of anti-tissue-transglutaminase antibodies (Ciacci et al. Citation2002) before the challenge and at day 5 and 15.
Results
Sorghum
Sorghum is a genus of numerous species of grasses, some of which are raised for grain and many of which are utilized as fodder plants either cultivated or as part of pasture land. Sorghum is native to tropical and subtropical regions and is grown on all continents in addition to Oceania and Australasia.
Sorghum bicolor (L.) Moench is an important cereal grain with 54 million metric tons harvested from 42 million hectares in 2002 (FAO Citation2004). It is extremely important in the semi-arid zones, where frequently little else can be grown. It is thus an important staple in Africa (Nigeria, Sudan, Burkina Faso, Ethiopia), Asia (India, China), and the drier parts of central and South America. It is estimated that 40% of the worldwide sorghum production is used for human food consumption (Rooney and Waniska Citation2000).
However, the bulk of studies dealing with leavened breads containing sorghum have focused on composite breads from wheat and sorghum, in which a maximum of only 30% sorghum are regarded as acceptable (Munck Citation1995). While such breads have been found acceptable by consumers (Carson et al. Citation2000), they are inappropriate for celiac patients.
Sorghum field trials in Foggia (South of Italy)
Sorghum (Sorghum bicolor [L.] Moench) has a well developed root system including large numbers of root hair able to easily absorb water and nutrients. In addition to this subterranean root system sorghum forms strong aerial roots permeating through the soil and ensuring good stability. The stem is strong, hard, and smooth divided by nodes and grain forms grow up to 1–1.5 m. Sorghum leaves are 50–100 mm wide and 0.5–0.8 m long. Both the leaves and stem are covered with a wax layer. The inflorescence of sorghum is a very characteristic part of the plant and is usually formed in different shapes and sizes. Panicles can be erect, drooping or reflexed. Spikelets contain one flower and are gathered in 2, 3 or 4 on secondary branches. Sorghums are allogamous but their pollen is good enough to pollinate themselves. Seeds of sorghum are round, oval or heart-shaped and can occur in white, creamy, yellow, pink, brown or violet colour. For all these reasons sorghum is a desirable plant in Mediterranean countries that have dry climates during sorghums growth period such as that found in south Italy. Furthermore, this crop belongs among plants suitable for individuals suffering from celiac disease because its seed does not contain gluten causing the digestion malfunction characteristic of celiac disease.
Here we report a preliminary experimental-study aimed at evaluating the agronomic performance of selected white sorghum hybrids and pure lines grown under typical Mediterranean conditions. Field trials were conducted in southern Italy at the Experimental Institute for Cereal Research of Foggia (41°28′ N, 15°32′ E and 75 m a.s.l) on a clay-loam soil (Typic Chromoxerert) during two growing seasons (2005 and 2006).
On the basis of their potential to produce better quality bread than others, five hybrid and four pure lines were chosen during the first and second study-year, respectively. Statistical designs used to analyze the field data included a complete randomized design replicated three times with plots of 45 m2 size. Individual plots were 15 rows wide. Row length was 1.5 m. The test plots were planted and harvested with equipment designed for small-plot work. The sowing dates were on May 2, in 2005 and on May 8, in 2006, respectively, and the plots were harvested on September 2, in 2005 and on October 4, in 2006, respectively. Nitrogen (120 kg N ha−1) was split applied, at the rate of 1/3 before sowing (incorporated by disk harrowing) as ammonium phosphate, and 2/3 N top-dressed applied at the tillering stage as ammonium nitrate. Weeds within the growing season were controlled by means of specific herbicides. Agronomic characteristics were evaluated at harvest date. Field trials results are summarized in and . Data have been tabulated on crop yield, phenological (heading date) and morphological characteristics. In 2005 two white sorghum hybrids, Warner and ATX631, showed the best performances with an average grain yield of 3.31 t ha−1. In the second year the genotypes evaluated showed a lower mean grain yield (2.22 t ha−1) although the climatic condition were better with abundant precipitation from August to October allowing flowering and maturity to proceed without water stress for plants. This report is a contribution of the CRA – Experimental Institute for Cereal Research of Foggia, Italy, that began its performance testing program for white grain sorghum in 2005 to select commercial hybrids or cultivars for producing bread from sorghum flour and to permit valid comparisons among suitable gluten-free cultivars.
Sorghum food products
Significant research has been conducted on sorghum-wheat composite foods. Many researchers have demonstrated that sorghum can be added to wheat flour to produce acceptable breads and other foods (Cauvain Citation1998; Carson et al. Citation2000). However, as these foods are not wheat-free, persons with celiac disease cannot eat them.
As sorghum lacks gluten proteins, 100% sorghum flour is incapable of forming a visco-elastic dough. In such cases, a batter type formulation must be used, in which case dough is not kneaded, but the batter is mixed with a paddle-type mixer similar to what be used in mixing cake batter for example (Cauvain Citation1998). In such systems gas retention is achieved via the use of gums, emulsifiers, or pre-gelatinized starch (Satin Citation1988; Cauvain Citation1998). Because of this, baked products made from sorghum without added wheat require a different technology. The properties of batter type dough are more fluid than wheat dough and closer in viscosity to cake batters (Cauvain Citation1998) due to the lack of a gluten network.
Several types of wheat-free food products have been made from sorghum including: breads (Schober et al. Citation2005), parboiled sorghum (Young et al. Citation1990), Sorghum tortillas (Choto et al. Citation1985), sorghum noodles (Suhendro et al. Citation2000), snack foods (Serna-Saldivar et al. Citation1988), cookies (Morad et al. Citation1984), and flatbreads (Lindell and Walker Citation1984; Morad et al. Citation1984). These studies have demonstrated that sorghum can be used to produce high quality human food products. The development of white food grade sorghum lines means that white, bland tasting flour can be produced from sorghum. These flours are useful in food products because they do not impart unusual colors or strong flavors and may be desired over corn flours for these reasons (Waniska and Rooney Citation2002).
Wheat-free foods have been prepared using a number of different flours and additives to improve quality (Gallagher et al. Citation2004). For sorghum, incorporating xanthan gum (Satin Citation1988), carboxy methyl cellulose and skimmed milk powder (Cauvain Citation1998), egg (Keregero and Mbete Citation1994; Cauvain Citation1998), rye pentosans (Casier et al. Citation1977), cysteine (Elkhalifa and El-Tinay Citation2002), and modified proteins (Babiker and Kato Citation1998) have all been attempted to improve sorghum baked food quality. Fermentation has also been used to improve the functionality of sorghum foods (Elkhalifa et al. Citation2005). While these studies have improved sorghum flour functionality somewhat, the quality of sorghum food products still is below that of similar foods prepared from wheat. Thus, improvement in sorghum food quality is still needed.
The business of celiac food products in Italy
The Celiac disease can be considered, at the moment, as the most diffused alimentary pathology. In order to estimate the number of celiac people in Italy, and Campania, we have to start from Italian Association of Celiacs (IAC) data, shown in .
Table 1 IAC Members’ Report from 1994–2004.
The IAC members in 2004 were 35,138, while in 1994 they were 5,957; in 10 years, the number of associates has grown approximately 6 times, due in part to the improvement in diagnostic techniques. Naturally not all the celiacs are members of the Association; the Index of ‘Penetration of associates’, (that is the ratio n associates/n inhabitants), related to 2004, is very variable from one Region to another.
In Campania, the index's value is the lowest in Italy. This value could increase if we consider that in this Region the potential demand, represented by the persons still not aware of their own disease, is very considerable. If we consider the Index of ‘Penetration of associates’ in Italy (equal to 1:1622), and multiply it for the population of the Campania (5,702,000 inhabitants), we obtain the number of 3,515 celiac patients.
According to IAC National Secretariat, the number of celiac patients in Campania is indeed much higher and numbers between 5000 and 8000 units.
However, if we consider that, in developed countries, for every case diagnosed approximately 7 remain without diagnosis, it can be calculated that in Campania, beyond the 6000 diagnosed patients there are about 42,000 still not diagnosed, for a total of approximately 50,000 people.
The business for celiac food products is in constant evolution, with the demand is steadily increasing. Even if we have few data available, it is possible to estimate the present demand. The AGC Campania Sanitary Attendance data show a mean expense per capita of Euro 100.00, related to the monthly contribution granted by local government to the each celiac; on the basis of a survey we conducted on a sample of celiacs living in Campania, the monthly expense per capita for gluten-free products can be estimated in Euro 215.00. Such data are showed in .
Table 2 Estimation of present and potential demand for celiac food products in Campania, 2004.
The data show clearly that the potential demand for these products is very high, up to 130,00 million Euro; the present supply, instead, is absolutely inadequate to satisfy neither the present demand, nor the potential demand. From present IAC data in Campania, there is lack of companies specialized in gluten-free products; only few companies have diversified their supply, offering also gluten free products; they are small companies, and offer only a limited range of such products.
Gluten-free products are sold directly by the companies, or through the pharmacies; some gluten-free products are also sold by big distribution (COOP, DESPAR, GS), even if such phenomenon turns out much more diffused in the North compared to the South of Italy.
In vivo test
On the first day of the challenge, the patients were given a 20-item clinical questionnaire which did not disclose any particular symptoms and an evaluation scale for the palatability of the sorghum food products. Patients judged cookies and cakes as excellent whereas bread was rated not as high. The recipe for bread was therefore changed with the addition of olive oil and a longer fermentation and the new bread was available from the second day. At day five the clinical questionnaire was re-administered with results similar to day one. Blood tests for anti-transglutaminase antibodies were repeated. Palatability of food stored at room temperature was still excellent although, obviously, the bread was dry and the patients toasted it before eating. The clinical questionnaire and blood test were repeated after 7 days (day 12 from first food administration) and no difference in symptoms or serum anti-transglutaminase levels were noticed at 7 and again at 15 days after the last intake (2.7 and 3.5 UL and 2.1 and 3.0 UL, respectively). The patients declared that they would have included sorghum-derived food in their diet if available.
Discussion
The development of a sorghum chain, from production to consumer in the Campania Region, presupposes the establishment of a baking business enterprise producing white sorghum food products for celiac patients.
Very recently a small-sized enterprise named Celi.net has been established in Campania region (Naples, Italy). Dr Scott Bean of the US Department of Agriculture in Kansas has conducted research in collaboration with Celi.net. Celi.net has started preliminary work using white sorghum in gluten-free baking for celiac patients. Bread and cookies were produced by Celi.net from white sorghum flour supplied by Twin Valley Mills (USA). The latter sorghum foods produced were safely consumed by celiac patients under clinical control (Ciacci et al. Citation2007).
The aim of Celi.net and its activity will be centralized on the theme of research, development and production of new foods for celiac patients in Italy and particularly in the Campania Region. In this context, the interest of Celi.net will be addressed on widely used sorghum food products, those highly requested by many celiac patients, such as bread, biscuits, cookies, waffles, noodles, and pizza crust. In addition, the Celi.net research and development will identify, through tests made in laboratory by qualified people utilizing white sorghum flour, new high quality sorghum food products for celiac patients.
The number of celiac patients in the Campania Region is continually on the increase. The only treatment for celiac disease is to follow a gluten-free diet. Sorghum is an excellent choice for gluten-free food because it has a similar color, flavor, texture and nutrient profile to wheat. The market for sorghum gluten-free food in the US is also growing. In Italy, food for celiac patients is very expensive and as many patients have low earnings, which places many celiacs in a difficult position and causes unnecessary stress. On the other hand, it is very likely that sorghum flour products will be less expensive with respect to other foods for celiac patients sold in Italy. Poor peoples both in Asia and Africa primarily use sorghum as food.
Prof. Del Giudice's research team in the Campania Region started three years ago with a close collaboration with Dr Scott Bean and Prof. Mitchell Tuinstra from USDA-Kansas for developing in the Campania Region and in Italy a sorghum chain from production to consumer. In this project is inserted, as a spin-off project to industry, the establishment of a small firm named Celi.net for producing food from sorghum flour. The clinical control of celiac patients as consumers in that sorghum chain is foreseen.
In the future we are going to organize in Italy and in the Campania Region the sorghum chain in close collaboration with research institutes in the US, exchanging experimental data with the final aim to produce a high quality food at a low cost to give all celiac patients an easier life.
Acknowledgements
We thank both Prof. Scott Bean for critical reading of the manuscript and Prof. Mitchell Tuinstra for very generously providing food-grade sorghum hybrids and pure line cultivars. The research was partly supported by Compagnia di San Paolo special grant ‘iniziativa’ to L. Del Giudice. Paola Pontieri was supported by a postdoctoral grant from the Istituto Banco di Napoli, Fondazione.
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