Chickpeas (Cicer arietinum L.) in animal nutrition: A review

Animal Feed Science and Technology 168 (2011) 1–20

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Animal Feed Science and Technology journal homepage: www.elsevier.com/locate/anifeedsci

Review

Chickpeas (Cicer arietinum L.) in animal nutrition: A review V.A. Bampidis a,∗ , V. Christodoulou b a Department of Animal Production, School of Agricultural Technology, Alexander Technological Educational Institute of Thessaloniki, P.O. Box 141, 57400 Thessaloniki, Greece b Animal Research Institute, National Agricultural Research Foundation (N.AG.RE.F.), 58100 Giannitsa, Greece

a r t i c l e

i n f o

Article history: Received 17 August 2010 Received in revised form 19 March 2011 Accepted 5 April 2011

Keywords: Chickpeas Nutritional value Ruminants Pigs Poultry Fish Performance Product quality

a b s t r a c t Chickpeas can be used as a high energy and protein feed in animal diets to support milk, meat and/or egg production. In common with other grain legumes, chickpeas may contain secondary compounds such as trypsin and chymotrypsin inhibitors which can impair utilization of the nutrients by non-ruminants. Heat treatment is an effective method to increase the amount of protein available for intestinal digestibility. Moreover, chickpea straw can be used as an alternative forage in ruminant diets. This review evaluates chickpeas relative to their nutrient composition, content of secondary compounds, and their impact on animal performance. Possible reasons and implications of these results to use chickpeas as a feed are discussed. © 2011 Elsevier B.V. All rights reserved.

Contents 1. 2.

3.

4.

5.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Chemical composition of chickpeas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Chemical composition of chickpea grain and straw . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Factors influencing chickpea grain protein utilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Biological evaluation of chickpeas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Biological value, protein efficiency ratio and digestibility of chickpeas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Effect of chickpeas on ruminal degradability and fermentation characteristics . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Improving the nutritional value of chickpeas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Effect of processing techniques on the SC of chickpeas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.2. Effect of processing techniques on nutritional properties of chickpeas . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Use of chickpeas in animal nutrition . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.1. Growing and lactating ruminants. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.2. Pig . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.3. Broilers and layers . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5.4. Fish . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

2 2 2 2 4 4 5 8 8 10 11 11 14 15 17

Abbreviations: ADF, acid detergent fiber; BW, body weight; CKP, chickpea; CP, crude protein; DFC, daily feed consumption; DM, dry matter; EM, egg mass; EP, egg production; EW, egg weight; FCR, feed conversion ratio; FE, feed efficiency; GE, gross energy; ME, metabolizable energy; NDF, neutral detergent fiber; OM, organic matter; SBM, soybean meal; SC, secondary compounds; TMR, total mixed ration; VFA, volatile fatty acids. ∗ Corresponding author. Tel.: +30 231 0013313; fax: +30 231 0791325. E-mail address: [email protected] (V.A. Bampidis). 0377-8401/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.anifeedsci.2011.04.098

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6.

Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

18 18 18

1. Introduction Chickpea (Cicer arietinum L.) is one of the world’s most important grain legumes (FAO, 1993) because it is a valuable source of protein, minerals and vitamins, and plays a very important role in human diets in many areas of the world. More than 70% of the world’s chickpea production and consumption is in India, but it is important in many other countries in Asia, Africa, Europe and the Americas (Singh, 1988; Chavan et al., 1989). Based on seed color and geographic distribution, the chickpea is grouped into two types: Kabuli (Mediterranean and Middle Eastern origin) and Desi (Indian origin; Chavan et al., 1989). Kabuli cultivars are white to cream colored and are used almost exclusively by cooking whole seeds as a vegetable for humans. The seeds of Desi cultivars are wrinkled at the beak with brown, light brown, fawn, yellow, orange, black or green color. This chickpea is cultivated principally as a legume crop, since it is well adapted to semi-arid conditions with some irrigated varieties yielding up to 3.5 t/ha of seed in autumn seeding (Iliadis, 2001). Although most chickpeas are produced for human consumption, they provide the livestock industry with an alternative protein and energy feedstuff. In addition, chickpea straw is used as a ruminant feed. The objective of this review is to summarize data on the nutrient profile of chickpeas, and examine data on their nutritive value in animal diets.

2. Chemical composition of chickpeas 2.1. Chemical composition of chickpea grain and straw The chemical composition of Kabuli and Desi chickpea grain is in Table 1. Kabuli chickpea grain exhibits lower neutral detergent fiber (NDF) and acid detergent fiber (ADF), and higher crude fat and starch, compared to Desi chickpea grain, without differing in other components. The crude protein (CP) content of chickpeas, which ranges from 137 to 340 g/kg dry matter (DM), is highly dependant on the cultivation system (El-Hardallou and Salih, 1981; Singh, 1985; Chavan et al., 1989; Abreu and Bruno-Soares, 1998). The sulfur amino acids are the first limiting nutritionally, followed by valine, threonine and tryptophan (Singh, 1985; Chavan et al., 1989; Iqbal et al., 2006). Chickpeas contain 562–788 g/kg DM of total carbohydrates, with starch, total sugars and fiber being the major components (Chavan et al., 1989). The total lipid content of chickpeas ranges from 34 to 82 g/kg DM (Chavan et al., 1989). Triglycerides are the major components of neutral lipids, whereas lecithin is the major component of polar lipids. Among the fatty acids, unsaturated fatty acids constitute 746 g/kg DM (oleic acid 243 g/kg DM, linoleic acid 481 g/kg DM, and linolenic acid 22 g/kg DM), while saturated fatty acids make up 116 g/kg DM (palmitic acid 104 g/kg DM and stearic acid 13 g/kg DM; Chavan et al., 1989). Chickpeas are also a good source of minerals, such as Ca, P, Mg, Fe and K (Chavan et al., 1989). The gross energy (GE) content of chickpea is 18.5 MJ/kg DM (Hadjipanayiotou et al., 1985; Sommerfeldt and Lyon, 1988; Abreu and BrunoSoares, 1998; Thacker et al., 2002), while the metabolizable energy (ME) content is 12.3 MJ/kg DM (Viveros et al., 2001; Maheri-Sis et al., 2008). The GE and ME contents of chickpea straw are 18.4 MJ/kg DM (Hadjipanayiotou et al., 1985) and 7.7 MJ/kg DM (Ramalho Ribeiro and Portugal Melo, 1990; López et al., 2005), respectively (Table 1). Its relative high nutritive value, for a straw, can make it an important dietary ingredient for ruminants.

2.2. Factors influencing chickpea grain protein utilization Chickpeas, like other legumes, contain a variety of secondary compounds (SC), such as protease and amylase inhibitors, as well as lectins, polyphenols and oligosaccharides (Table 2), which impair nutrient absorption from the gastrointestinal tract and can result in detrimental effects on animal health and growth (Singh, 1988; Chavan et al., 1989; Van der Poel, 1990; Saini, 1993; Perez-Maldonado et al., 1999). It has been reported that some organs (i.e., liver, pancreas, and gizzard) may become hypertrophic in monogastrics due to SC in legume seeds (Huisman and Van der Poel, 1989; Rubio et al., 1999; Viveros et al., 2001; Christodoulou et al., 2006b). Relative to other legumes, such as soybeans, peas, and common beans, chickpeas contain relatively small amounts of trypsin and chymotrypsin inhibitors, creating fewer problems in nonruminant nutrition (Singh, 1988; Saini, 1989; Savage and Thompson, 1993), while Chavan et al. (1989) reported similar SC contents for chickpeas and soybeans. However, in ruminants, the SC, which are present in chickpeas and other grain legumes (Singh, 1988; Friedman, 1996), appear to be inactivated by 12–24 h of in vitro incubation with rumen liquor (Holmes et al., 1993), and do not have a substantive effect on nutrient absorption from the small intestine of sheep (Woldetsadick et al., 1991).

V.A. Bampidis, V. Christodoulou / Animal Feed Science and Technology 168 (2011) 1–20

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Table 1 Chemical composition (g/kg dry matter, unless otherwise stated) of chickpea (CKP) grain and straw summarized from several sources.a , b . Kabuli CKP grain c

n DMd (g/kg) OM Ash CP Crude fat Crude fiber NDF ADF Lignin(sa) Total carbohydrates Starch Total NSP Arabinose Galactose Glucose Mannose Rhamsose Uronic acid Xylose Total oligosaccharides Raffinose Stachyose Sucrose Verbascose GE (MJ/kg DM) DE (MJ/kg DM) ME (MJ/kg DM) Calcium Phosphorus Magnesium Potassium Sodium Copper (mg/kg DM) Iron (mg/kg DM) Manganese (mg/kg DM) Zinc (mg/kg DM) Niacin (mg/kg DM) Pyridoxine (mg/kg DM) Riboflavin (mg/kg DM) Thiamine (mg/kg DM) Alanine Arginine Aspartic acid Cystine Glutamic acid Glycine Histidine Isoleucine Leucine Lysine Methionine Phenylalanine Proline Serine Threonine Tryptophan Tyrosine Valine

9 1 12 15 14 10 8 7 5 4 9 2 2 2 2 2 2 2 2 1 3 2 3 2 7 2 3 5 4 3 3 3 2 3 2 2 1 1 1 1 3 5 3 5 3 3 7 7 7 7 7 7 3 3 7 3 6 7

Desi CKP grain

Mean

SEM

908 978 34 225 62 47 126 54 13 637 394 106 33.4 8.2 30.5 3.7 1.9 22.6 5.3 71 12.4 25.2 21.3 1.0 18.54 16.47 12.95 1.69 3.42 1.78 11.13 0.77 10.65 90.00 22.43 42.2 16.03 4.66 1.77 4.53 10.2 17.8 24.0 3.2 34.3 10.4 5.5 9.1 17.0 14.9 2.8 13.1 7.6 12.8 8.6 1.9 6.8 9.8

6.7 1.3 7.7 3.8 4.1 11.5 3.4 4.7 31.1 15.5 7.8 8.55 0.45 2.60 1.05 0.35 1.20 0.25

n

Mean

5 1 9 11 11 6 6 6 3 2 5

897 971 34 230 48 88 214 132 12 580 334

3.13 0.35 1.89 0.95 0.69 1.13 0.40 0.19 0.67 0.01 1.24 0.34 0.35 16.48 1.33 0.95

1 1 1 1 7 1 2 2 2 1 1 1

7.7 23.8 17.0 0.7 18.38 16.90 11.75 1.50 3.90 2.20 12.10 0.20

1.37 1.91 3.07 0.46 10.13 1.69 0.77 0.70 1.30 0.85 0.28 1.05 0.70 2.23 0.71 0.55 0.75 0.82

3 4 3 5 3 3 6 6 6 6 6 6 2 3 6 2 5 6

9.0 20.6 24.4 4.2 38.5 8.0 5.8 8.9 16.2 14.3 3.0 13.3 10.0 12.6 7.9 1.6 5.6 9.0

CKP straw SEM 6.8 1.3 5.2 3.3 11.3 13.9 5.3 6.0 106.3 18.3

0.80 1.25 0.00 0.10

n

Mean

SEM

3 1 2 5 3 2 4 4 3

896 924 68 65 12 390 694 516 111

17.9

1 1 2 1 1 1

18.4 8.3 7.7 13.0 0.5 4.1

25.5 10.0 1.9 20.0 50.6 34.4 15.8

0.55

0.03 0.58 0.63 0.52 2.53 0.03 0.42 0.53 0.23 0.63 0.37 1.44 0.00 0.40 0.19 0.05 0.42 0.44

a CKP grain sources: El-Hardallou and Salih, 1981; Visitpanich et al., 1985; Batterham et al., 1993; Attia et al., 1994; Akmal Khan et al., 1995; Abreu and Bruno-Soares, 1998; Rubio et al., 1998; Allan et al., 2000; Mustafa et al., 2000; Booth et al., 2001; Salgado et al., 2001; Viveros et al., 2001; El-Adawy, 2002; Thacker et al., 2002; Rubio, 2003; Christodoulou et al., 2006b; Brenes et al., 2008; Maheri-Sis et al., 2008. b CKP straw sources: Hadjipanayiotou et al., 1985; Ramalho Ribeiro and Portugal Melo, 1990; S¸ehu et al., 1998; Bruno-Soares et al., 2000; López et al., 2005. c Number of sources. d ADF, acid detergent fiber; CP, crude protein; DE, digestible energy; DM, dry matter; GE, gross energy; ME, metabolizable energy; NDF, neutral detergent fiber; NSP, non-starch polysaccharides; OM, organic matter.

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Table 2 Secondary compounds and toxic substances of chickpea grain (Singh, 1988). Constituent

Range

Protease inhibitors Trypsin (units/mg) Chymotrypsin (units/mg) Amylase inhibitor (units/g) Oligosaccharides (g/100 g) Raffinose Stachyose Stachyose + verbascose Polyphenols (mg/g) Total phenols Tannins Phytolectins (units/g) Cyanogens (Glycosides) Mycotoxins (␮g/kg)

6.7–14.6 5.7–9.4 0–15.0 0.36–1.10 0.82–2.10 1.90–3.00 1.55–6.10 Traces 400 Traces Traces–35

3. Biological evaluation of chickpeas 3.1. Biological value, protein efficiency ratio and digestibility of chickpeas Biological evaluation of chickpea protein is essential because chemical analyses do not always reveal how much of a protein is biologically available and utilized by animals (Chavan et al., 1989). Both growth methods (PER, protein efficiency ratio) and N balance methods (BV, biological value; NPU, net protein utilization; TD, true digestibility) are used for this purpose (Chavan et al., 1989; Friedman, 1996). Chickpea protein quality was described by Friedman (1996) as being equivalent to that of soybean meal (SBM). Several researchers have studied the nutritional value of chickpeas, and their results support the CP and energy equivalency of chickpeas and SBM. For raw chickpeas, PER values ranged from 1.2 to 2.8 (Newman et al., 1987; Sotelo et al., 1987; Fernandez and Berry, 1988; Chavan et al., 1989; Mitchell et al., 1989; Wang and McIntosh, 1996; Milán-Carrillo et al., 2002; Singhai and Shrivastava, 2006), BV ranged from 0.520 to 0.850 (Chavan et al., 1989; Savage and Thompson, 1993), NPU values ranged from 0.556 to 0.920 (Chavan et al., 1989; Savage and Thompson, 1993; Rubio et al., 1998, 2002), and TD values ranged from 0.760 to 0.928 (Chavan et al., 1989; Savage and Thompson, 1993). According to Chavan et al. (1989), this considerable variation in BV, PER, TD and NPU indicates that genetic diversity in protein quality exists in chickpea cultivars. In vitro CP digestibility of raw chickpeas ranged from 0.631 to 0.890 (Singh and Jambunathan, 1981; Newman et al., 1987; Milán-Carrillo et al., 2002; Monsoor and Yusuf, 2002; Table 3), and the in vitro organic matter (OM) digestibility of chickpeas Table 3 In vitro nutrient digestibility of chickpea (CKP) grain and straw summarized from several sources. Feedstuff

CKP processing

In vitro digestibility a

Kabuli CKP grain Desi CKP grain Kabuli CKP grain Kabuli CKP grain CKP grain

CKP grain CKP grain CKP grain CKP grain

CKP grain

CKP straw a

Raw Raw Raw Boiled Raw Autoclaved Raw Boiled Autoclaved Microwave cooked Germinated Raw Raw Extruded Raw Boiled Raw Extruded Germinated Raw Pressure cooked Microwave cooked Raw

Reference

DM

OM

CP

NDF

Starch

– – – – – – – – – – – – – – – – – – – – – – 0.610

– – – – – – – – – – – 0.923 – – – – – – – – – – –

0.727 0.631 0.697 0.769 0.718 0.835 0.836 0.885 0.900 0.894 0.876 – 0.677 0.824 0.890 0.969 0.740 0.788 0.748 – 0.801 0.741 –

– – – – – – – – – – – – – – – – – – – – – – 0.398

– – – – – – – – – – – – – – – – – – – 0.450 0.436 0.433 –

CP, crude protein; DM, dry matter; NDF, neutral detergent fiber; OM, organic matter.

Singh and Jambunathan (1981) Attia et al. (1994) Clemente et al. (1998) El-Adawy (2002)

Hadjipanayiotou (2002) Milán-Carrillo et al. (2002) Monsoor and Yusuf (2002) Abd El-Hady and Habiba (2003)

Khatoon and Prakash (2004)

López et al. (2005)

V.A. Bampidis, V. Christodoulou / Animal Feed Science and Technology 168 (2011) 1–20

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Table 4 Nutrient and energy digestibility of chickpea (CKP) grain and straw calculated by difference. Feedstuff

CKP levela

Animal

Digestibility b

CKP grain CKP straw Kabuli CKP grain Desi CKP grain Desi CKP grain Desi CKP grain Extruded CKP grain a b

300 500 600 600

Wethers Wethers Rams Rams Juvenile silver perch Juvenile silver perch Juvenile rainbow trout

Reference

DM

OM

CP

Energy

0.820 0.490 – – 0.508 0.508 –

0.840 0.510 0.921 0.902 – – –

0.790 0.200 – – 0.822 0.792 0.806

0.790 0.490 0.912 0.889 0.548 0.548 –

Hadjipanayiotou et al. (1985) Hadjipanayiotou et al. (1985) Abreu and Bruno-Soares (1998) Abreu and Bruno-Soares (1998) Allan et al. (2000) Booth et al. (2001) Tiril et al. (2009)

Added g CKP/head/day to the basic ration. CP, crude protein; DM, dry matter; OM, organic matter.

was 0.923 on a DM basis (Hadjipanayiotou, 2002). The in vitro DM and NDF digestibility of chickpea straw were 0.610 and 0.398, respectively (López et al., 2005). According to Hadjipanayiotou et al. (1985), the digestibility of chickpea grain calculated by difference in wethers was 0.82 for DM, 0.84 for OM, 0.79 for CP and 0.79 for GE (Table 4), while OM digestibility of chickpeas was as high as 0.921 in rams (Abreu and Bruno-Soares, 1998). Moreover, the CP digestibility of chickpeas in juvenile fish ranged from 0.792 to 0.822 (Allan et al., 2000; Booth et al., 2001; Tiril et al., 2009). In lamb diets containing chickpeas, the apparent digestibility of DM, OM and CP was higher than in the SBM control diet (Hadjipanayiotou, 2002; Table 5). Moreover, increasing the amount of chickpeas in the diets of steers improved apparent digestibility of CP, crude fat and ash, while apparent DM, NDF, ADF and GE digestibility was similar in diets of heifers and steers (Illg et al., 1987; Sommerfeldt and Lyon, 1988). In another study, Gilbery et al. (2007) reported that steers fed chickpeas and corn (235:175 g/kg DM of the total mixed ration – TMR) resulted in similar apparent digestibility coefficients for OM, CP, NDF and ADF to steers fed canola meal and corn (90:320 g/kg DM of the TMR), field pea and corn (205:205 g/kg DM of the TMR), as well as lentils and corn (163:247 g/kg DM of the TMR). The DM, OM, CP and energy digestibilities of chickpea straw determined in sheep were 0.494–0.600, 0.509–0.620, 0.600 and 0.590, respectively (Hadjipanayiotou et al., 1985; S¸ehu et al., 1998). Mustafa et al. (2000), using an indicator method in barrows with an average body weight (BW) of 30 kg, and Thacker et al. (2002), using a mobile nylon bag technique to barrows with an average BW of 43.5 kg, reported that the digestibility coefficients of DM and GE were higher for Kabuli than Desi chickpeas, while both types of chickpeas had similar CP digestibility coefficients (Table 5). The digestibility coefficients for Kabuli and Desi chickpeas were similar or somewhat lower than those for SBM (Mustafa et al., 2000; Thacker et al., 2002). In addition, Salgado et al. (2001), using male piglets (8.2 kg BW), also found differences in digestibility coefficients of dietary components (i.e., DM, OM, GE, NDF, ADF) between Kabuli and Desi chickpea diets. Moreover, apparent digestibility coefficient for chickpeas in rats ranged from 0.651 to 0.828 for N (Sotelo et al., 1987; Rubio et al., 1998, 2002) and from 0.530 to 0.920 for amino acids (Rubio et al., 2002; Rubio, 2003). Apparent ileal digestibility coefficients of dietary components and amino acids in male piglets fed Kabuli and Desi chickpea diets were particularly high, except for ash, NDF and ADF (Salgado et al., 2001; Table 6). Furthermore, apparent ileal digestibilities in Iberian pigs fed chickpeas were 0.720 for DM (Rubio, 2005), 0.740 for N (Rubio, 2005), 0.850 for starch (Rubio et al., 2005) and 0.670–0.920 for fatty acids (Rubio et al., 2005), while in rats it was 0.803 for N (Rubio et al., 1998). True ileal digestibility in Iberian pigs fed chickpeas was 0.890 for N and 0.830–0.970 for amino acids (Rubio, 2005). Brenes et al. (2008) found that broiler chickens 0–21 days of age fed raw and extruded Kabuli chickpeas had apparent digestibilities for crude fat of 0.847 and 0.871 (Table 5), respectively, and apparent ileal digestibilities for CP of 0.848 and 0.873 (Table 6), respectively. Viveros et al. (2001) reported that inclusion of 300 g/kg raw Kabuli chickpeas in diets of broiler chickens reduced ileal starch digestibility by 3%, ileal CP digestibility by 18% and apparent ME by 9% compared with those fed the control diet without chickpea. Moreover, Ravindran et al. (2005, 2006) found that apparent ileal digestibility for broiler chickens 35–42 days of age fed chickpeas was 0.730 for CP, while it ranged from 0.580 to 0.840 for amino acids. Three recent reports studied the apparent digestibility of DM, CP, crude fat, starch and energy of juvenile European seabass and rainbow trout fed extruded chickpeas to inclusion levels up to 350 g/kg (Adamidou et al., 2009a,b; Tiril et al., 2009). In general, extruded chickpea nutrient digestibilities in fish were higher than those in mammals or birds (Table 5). Overall, results suggest that chickpeas have high nutritional value when fed to animals, equivalent to that of other legumes. 3.2. Effect of chickpeas on ruminal degradability and fermentation characteristics The effective ruminal degradability of chickpea CP was 0.592 (DM basis) in ewes (Hadjipanayiotou, 2002; Table 7), and 0.768 and 0.714 (DM basis) in non-lactating Holstein cows, with Kabuli and Desi chickpeas, respectively (Mustafa et al., 2000). Similarly, in growing heifers, steers and lactating cows, ruminal CP degradability increased with increased dietary chickpea proportion (Illg et al., 1987; Hadsell and Sommerfeldt, 1988; Sommerfeldt and Lyon, 1988). Relative to chickpea

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Table 5 Nutrient and energy digestibility, and N retention, of chickpea (CKP) grain and straw summarized from several sources. Feedstuff

CKP concentrate (g/kg)

CKP straw Desi CKP (g/kg) Kabuli CKP (g/kg) Desi CKP (g/kg) CKP (g/kg) Kabuli CKP Desi CKP CKP concentrate (g/kg)

Kabuli CKP – MNBT Desi CKP – MNBT CKP TMR (g/kg DM) Raw CKP (g/kg)

Extruded CKP (g/kg)

Extruded CKP (g/kg)

Extruded CKP (g/kg)

Extruded CKP (g/kg) a

288 455 0 245 494 752 0 500 978 297 300 300 0 491 478 0 136 329

Animal

Wethers Wethers Heifers

Steers

Lambs Juvenile silver perch Barrows Male piglets

Male lambs

Barrows 0 235 0 100 200 300 100 200 300 0 150 300 0 165 350 0 300

Steers Broiler chickens

European seabass

European seabass

Juvenile rainbow trout

Nutrient digestibility

Energy digestibility

DMa

OM

CP

Crude fat

NDF

ADF

Ash

0.770 0.600 0.774 0.805 0.822 0.801 0.725 0.727 0.747 0.494 0.627 0.753 0.706 0.863 0.868 0.832 0.766 0.792 0.808 0.831 0.725 – – – – – – – – – – – – – – – 0.900 0.846

0.800 0.620 – – – – – – – 0.509 – – – 0.895 0.889 0.852 0.785 0.814 0.824 – – 0.647 0.656 – – – – – – – – – – – – – – –

0.780 0.600 – – – – 0.673 0.691 0.716 – 0.881 0.685 0.668 0.914 0.844 0.830 0.720 0.768 0.764 0.837 0.793 0.553 0.549 – – – – – – – 0.929 0.932 0.930 0.955 0.938 0.953 0.947 0.924

– – – – – – 0.693 0.718 0.791 – – – – 0.852 0.851 0.844 – – – – – – – 0.868 0.856 0.856 0.828 0.858 0.876 0.880 0.967 0.972 0.962 0.979 0.973 0.970 0.972 0.965

– – – – – – 0.523 0.505 0.538 – – – – 0.195 0.639 0.333 – – – – – 0.618 0.611 – – – – – – – – – – – – – – –

– – – – – – 0.495 0.459 0.486 – – – – 0.241 0.567 0.255 – – – – – 0.589 0.577 – – – – – – – – – – – – – – –

– – – – – – 0.515 0.524 0.586 – – – – 0.435 0.591 0.590 – – – – – – – – – – – – – – – – – – – – – –

0.770 0.590 – – – – 0.718 0.718 0.735 – 0.721 0.733 0.689 0.881 0.874 0.845 – – – 0.834 0.748 – – – – – – – – – 0.943 0.950 0.942 0.968 0.956 0.964 0.931 0.884

N retention (g/day) – – – – – – 51.5 49.5 45.1 – – – – – – – 6.7 9.0 7.8 – – – – – – – – – – – – – – – – – – –

ADF, acid detergent fiber; CP, crude protein; DM, dry matter; NDF, neutral detergent fiber; OM, organic matter; MNBT, mobile nylon bag technique; TMR, total mixed ration.

Reference

Hadjipanayiotou et al. (1985) Hadjipanayiotou et al. (1985) Illg et al. (1987)

Sommerfeldt and Lyon (1988)

S¸ehu et al. (1998) Booth et al. (2001) Mustafa et al. (2000) Salgado et al. (2001)

Hadjipanayiotou (2002)

Thacker et al. (2002) Gilbery et al. (2007) Brenes et al. (2008)

Adamidou et al. (2009a)

Adamidou et al. (2009b)

Tiril et al. (2009)

V.A. Bampidis, V. Christodoulou / Animal Feed Science and Technology 168 (2011) 1–20

CKP grain TMR (g/kg) CKP straw TMR (g/kg) CKP concentrate (g/kg DM)

CKP level

Feedstuff

CKP level

Animal

Nutrient digestibility a

CKP (g/kg) Kabuli CKP Desi CKP Raw CKP (g/kg)

CKP (g/kg) Raw CKP (g/kg)

Extruded CKP (g/kg)

a

0 491 478 0 150 300 450 731 0 100 200 300 100 200 300

Male piglets

Male broiler chickens

Male castrated pigs Broiler chickens

DM

OM

CP

Crude fat

NDF

ADF

Ash

Starch

0.851 0.796 0.769 – – – – 0.720 – – – – – – –

0.891 0.831 0.805 – – – – – – – – – – – –

0.912 0.848 0.848 0.820 0.690 0.670 0.660 0.740 0.858 0.864 0.849 0.831 0.855 0.887 0.878

0.901 0.880 0.898 – – – – – – – – – – – –

0.144 0.170 0.138 – – – – – – – – – – – –

0.133 0.076 0.047 – – – – – – – – – – – –

0.493 0.565 0.542 – – – – – – – – – – – –

0.996 0.982 0.987 0.910 0.900 0.880 0.870 0.850 – – – – – – –

ADF, acid detergent fiber; CP, crude protein; DM, dry matter; NDF, neutral detergent fiber; OM, organic matter.

Energy digestibility

Reference

0.868 0.823 0.800 – – – – – – – – – – – –

Salgado et al. (2001)

Viveros et al. (2001)

Rubio (2005) and Rubio et al. (2005) Brenes et al. (2008)

V.A. Bampidis, V. Christodoulou / Animal Feed Science and Technology 168 (2011) 1–20

Table 6 Nutrient and energy apparent ileal digestibility of chickpea (CKP) grain summarized from several sources.

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Table 7 Effective degradability of chickpea (CKP) grain. Feedstuff

CKP processing

Animal

Outflow rate (/h)

Effective degradability a

Kabuli CKP grain Desi CKP grain CKP grain a

Raw Autoclaved Raw Autoclaved Raw

Cows Cows Ewes

0.041–0.050 0.027–0.022 0.032–0.038 0.030 0.050

DM

CP

0.732 0.555 0.646 0.537 –

0.768 0.466 0.714 0.477 0.592

Reference

Mustafa et al. (2000)

Hadjipanayiotou (2002)

CP, crude protein; DM, dry matter.

straw, potential DM and NDF degradability, determined in rams, were 0.454 and 0.393, respectively (Bruno-Soares et al., 2000). Summarized effects of chickpeas on rumen fermentation are in Table 8. Ruminal ammonia increased (Gilbery et al., 2007), and acetic acid molar proportion decreased (Sommerfeldt and Lyon, 1988; Gilbery et al., 2007) or increased (Hadsell and Sommerfeldt, 1988) with increasing dietary chickpea inclusion levels. Whereas, pH, total volatile fatty acid (VFA) concentrations, as well as major VFA molar proportions were generally unaffected in cattle fed diets with various inclusion levels of corn, SBM and chickpeas (Illg et al., 1987; Hadsell and Sommerfeldt, 1988; Sommerfeldt and Lyon, 1988; Gilbery et al., 2007). 4. Improving the nutritional value of chickpeas In order to improve the nutritional value, and to provide effective utilization of chickpeas to a maximal level in diets of non-ruminants, it is essential that SC activity is removed to obtain a higher protein and energy digestibility (Van der Poel, 1989, 1990). Processing techniques, including dehulling, germination and thermal treatment, not only remove toxic substances and SC, but also improve intake and digestibility (Singh, 1985; Chavan et al., 1989; Van der Poel, 1990; Khattab et al., 2009). Many SC in legumes are mostly inactivated by heat treatment, the effectiveness of which depends, among other factors, on initial SC level, temperature, heating time, particle size, moisture and, probably, species and variety (Van der Poel, 1989; Gatel, 1994). Heat processing includes extrusion, infrared radiation, micronizing, autoclaving, microwave cooking and steam processing or flaking (Saini, 1989; Nestares et al., 1993; Savage and Thompson, 1993; Gatel, 1994; Wang and McIntosh, 1996; Khattab et al., 2009). Among the available heat processing techniques, extrusion provides very good results in destroying SC in legumes (Saini, 1989; Van der Poel, 1989; Vooijs et al., 1993; Milán-Carrillo et al., 2002). Extrusion is unique among heat processes in that the material, mainly moistened starchy or proteinaceous feeds, is worked into a viscous, plastic-like dough and cooked before being forced through a die (Milán-Carrillo et al., 2002). During extrusion, the nutritional value of the compact folded proteins can be increased if both noncovalent interactions and disulfide bonds are broken, resulting in irreversible protein denaturation (Marsman et al., 1997). This process increases the accessibility of proteins to enzymatic degradation, but overprocessing may decrease the nutritional value of legume seeds due to Maillard reactions (Marsman et al., 1997). Besides inactivation of SC and denaturation of proteins, other results of extrusion include gelatinization of starch, inactivation of many native enzymes, reduced microbial counts, and improvement in digestibility and biological value of proteins (Milán-Carrillo et al., 2002). 4.1. Effect of processing techniques on the SC of chickpeas Trypsin inhibitor and haemagglutination activity of grain legumes (i.e., phaseolus bean) decreased, after extrusion at 145 ◦ C for 16 s, to 0.02–0.22 and 0.02–0.07, respectively, of that determined in raw beans (Van der Poel, 1989), and trypsin inhibitor activity of grain legumes (i.e., phaseolus bean) decreased, after extrusion at 100 ◦ C and 130 ◦ C for 10 s, to 0.06 and 0.03, respectively, of that in raw beans (Vooijs et al., 1993). Marzo et al. (2002) also reported that extrusion reduced condensed tannins, polyphenols, as well as trypsin, chymotrypsin and ˛-amylase inhibitory activity of the phaseolus bean seeds to 0.25, 0.50, 0.064, 0.038 and 0.007 of that in raw beans, respectively, while haemagglutination activity was completely eliminated. Moreover, SC of chickpea were inactivated when ground chickpeas (2 mm) were wet extruded at 120 ◦ C (i.e., the barrel temperature near the exit) for 20 s (Christodoulou et al., 2006c,d). Wang and McIntosh (1996) also reported that trypsin inhibitor activity of chickpeas decreased, after boiling and extrusion, to 0.021 and 0.033, respectively, of that in raw chickpeas (Table 9). Saini (1989) reported that trypsin and chymotrypsin inhibitors in grain legumes (i.e., soybean) retained 0.17 and 0.30 activity, respectively, after dry heating at 120 ◦ C for 15 min. In addition, Nestares et al. (1993) reported that the oligosaccharide and tannin contents of chickpeas decreased, after autoclaving at 120 ◦ C for 15 min, to 0.53 and 0.74, respectively, of that in raw chickpeas, and Savage and Thompson (1993) reported that trypsin inhibitor activity of chickpeas decreased, after soaking in cold water at 12 ◦ C for 18 h and boiling for 40 min, and after germination at 25 ◦ C for 72 h, to 0.15 and 0.26, respectively, of that in raw chickpeas. Moreover, according to Márquez et al. (1998), inactivation of 0.66 of the trypsin inhibitor activity occurred in chickpeas after dry heating at 140 ◦ C for 6 h.

Feedstuff

CKP level

Animal

pH

VFAa (mmol/l)

Acetic acid

Propionic acid

Butyric acid

i-Butyric acid

Valeric acid

i-Valeric acid

CKP concentrate (g/kg DM)

Heifers

CKP concentrate (g/kg DM)

0 245 494 752 0

Cows

6.73 6.65 6.63 6.68 6.40

69.6 73.0 70.0 73.3 103.5

0.670 0.680 0.661 0.659 0.561

0.167 0.164 0.170 0.168 0.288

0.126 0.121 0.128 0.136 0.115

0.084 0.077 0.095 0.086 0.060

0.121 0.125 0.126 0.128 0.180

0.158 0.149 0.182 0.162 0.120

73 88 79 94 99

CKP concentrate (g/kg)

500 978 0

Steers

6.30 6.50 6.50

101.8 96.6 92.7

0.557 0.598 0.641

0.293 0.261 0.182

0.112 0.109 0.145

0.060 0.060 0.070

0.190 0.130 0.120

0.130 0.120 0.130

121 95 103

6.50 6.50 6.42 6.26

95.0 87.0 71.4 76.3

0.605 0.597 0.636 0.588

0.231 0.234 0.165 0.181

0.129 0.130 0.128 0.145

0.070 0.080 – –

0.150 0.160 – –

0.130 0.160 – –

104 130 79 109

CKP TMR (g/kg DM) a

500 978 0 235

Steers

DM, dry matter; VFA, volatile fatty acids; TMR, total mixed ration.

Molar proportions

NH3 N (mg/l)

Reference

Illg et al. (1987)

Hadsell and Sommerfeldt (1988)

Sommerfeldt and Lyon (1988)

Gilbery et al. (2007)

V.A. Bampidis, V. Christodoulou / Animal Feed Science and Technology 168 (2011) 1–20

Table 8 The effect of chickpea (CKP) grain on fermentation characteristics summarized from several sources.

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Table 9 The effect of processing on secondary compounds (SC; g/kg) of chickpea grain summarized from several sources. SC

Tannins Trypsin inhibitor activity Phytic acid Polyphenols Trypsin inhibitor activity Trypsin inhibitor activity Phytic acid Saponin Tannins

Legume processing

Reference

Raw

Boiled

Extruded

Autoclaved

Dry roasted

Microwave cooked

Germinated

1.65 2.71 8.1 3.39 9.4 6.2 12.1 0.91 4.85

0.38 0.42 5.8 1.35 0.2 – 8.6 0.44 2.52

– – – – 0.31 – – – –

– – – – – – 7.1 0.51 2.42

– – – – – 2.1 – – –

– – – – – – 7.5 0.48 2.50

0.59 0.71 – – – – 5.3 0.70 3.73

Chavan et al. (1989) Savage and Thompson (1993) Attia et al. (1994) Wang and McIntosh (1996) Márquez et al. (1998) El-Adawy (2002)

Overall, results suggest that SC included in chickpea grains are inactivated by various processing techniques, with heat treatment, and especially extrusion, offering the best results in destroying these SC. 4.2. Effect of processing techniques on nutritional properties of chickpeas Boiling, autoclaving, microwave cooking and germinating affected the chemical composition of chickpeas (Table 10). However, microwave cooking and germination caused slight losses in vitamins and minerals, while boiling and autoclaving caused significant losses (El-Adawy, 2002). Extrusion also affected the chemical composition of chickpeas, but dry heating did not (Table 11). Monsoor and Yusuf (2002) showed that in vitro CP digestibility of chickpeas was increased by 9% (0.969 versus 0.890) due to inactivation of protease inhibitors when chickpeas were heated at 100 ◦ C in boiling water for 5 min (Table 3). Sotelo et al. (1987) reported no difference for the CP digestibility of raw and boiled chickpeas (0.780 versus 0.773), and Fernandez and Berry (1988) showed that germination of chickpeas for 24 h decreased CP digestibility (0.807 versus 0.869). Moreover, extrusion improved the in vitro CP digestibility of chickpeas by 21.7% (i.e., 0.824 versus 0.677; Milán-Carrillo et al., 2002). Mustafa et al. (2000) reported that heat treatment of chickpeas (i.e., autoclaved at 127 ◦ C for 10 min) reduced ruminal degradability of CP for Kabuli and Desi chickpeas by 39 and 33%, respectively, thereby increasing the protein available for intestinal digestion (Table 7). The PER value of chickpeas, boiled in water for 3 h and dried in an oven at 60–70 ◦ C for 20–24 h, ranged from 2.08 to 2.48 (Del-Angel and Sotelo, 1982; Sotelo et al., 1987; Table 12). Extrusion improved the PER value of chickpeas by 36.9% (1.78 versus 1.30; Milán-Carrillo et al., 2002). However, Wang and McIntosh (1996) reported that extruded or boiled chickpeas increased BW gain of rats, but not PER values, and decreased pancreas and small intestine relative weight, when compared Table 10 The effect of processing on the chemical composition (g/kg dry matter, unless otherwise stated) of chickpea grain (El-Adawy, 2002).

Ash CPa NPN Crude fat Crude fiber Total carbohydrates Starch Raffinose Stachyose Sucrose Verbascose Calcium Phosphorus Magnesium Potassium Sodium Copper (mg/kg DM) Iron (mg/kg DM) Manganese (mg/kg DM) Zinc (mg/kg DM) Niacin (mg/kg DM) Pyridoxine (mg/kg DM) Riboflavin (mg/kg DM) Thiamine (mg/kg DM) a

Raw

Boiled

Autoclaved

Microwave cooked

Germinated

37.2 236.4 18.2 64.8 38.2 623.4 369.1 14.5 25.6 18.9 1.9 1.8 2.3 1.8 8.7 1.2 11.0 77.2 21.1 43.2 16.0 4.7 1.7 4.5

35.2 232.1 14.2 62.2 46.2 624.3 365.1 7.6 15.2 12.3 0.0 1.2 1.9 1.6 3.4 1.1 7.3 68.1 18.0 34.2 0.7 2.7 0.8 1.5

35.6 231.5 13.8 61.7 49.6 621.6 366.9 8.1 14.6 11.9 0.0 1.3 2.1 1.7 4.1 1.2 8.1 71.0 19.0 38.9 0.8 3.1 0.9 1.6

35.1 231.6 15.1 62.1 48.2 623.0 368.1 7.1 14.7 13.6 0.0 1.3 2.2 1.7 4.3 1.2 9.4 73.0 20.3 39.5 2.3 3.7 1.0 1.9

38.1 255.3 28.2 62.2 52.1 592.3 343.7 0.0 0.0 13.5 0.0 1.7 2.4 1.7 5.1 1.2 10.0 79.1 20.0 49.3 15.2 4.8 2.0 2.8

CP, crude protein; DM, dry matter; NPN, non-protein N.

V.A. Bampidis, V. Christodoulou / Animal Feed Science and Technology 168 (2011) 1–20

11

Table 11 Chemical composition (g/kg, as fed basis) of raw, heated and extruded chickpea grain (Christodoulou et al., 2005, 2006b,c,d).

DMa Ash CP Crude fat Crude fiber NDF ADF Arginine Cystine Glycine + serine Histidine Isoleucine Leucine Lysine Methionine Phenylalanine Proline Threonine Tryptophan Tyrosine Valine a

Raw chickpea

Dry heated chickpea

Extruded chickpea

908 27 209 50 38 82 53 17.4 3.7 13.3 5.9 8.8 16.0 14.9 1.5 10.0 5.8 7.3 2.7 6.3 9.7

921 27 211 51 39 – – 17.6 3.7 13.4 6.0 8.9 16.2 15.0 1.5 10.1 5.9 7.4 2.7 6.4 9.8

923 39 239 51 38 – – 20.7 4.4 15.9 7.0 10.7 19.0 17.8 1.8 12.2 6.9 8.9 3.2 7.3 11.3

ADF, acid detergent fiber; CP, crude protein; DM, dry matter; NDF, neutral detergent fiber.

with raw chickpea. In this study, chickpea fed rats had lower spleen, thymus and liver relative weights, and higher cecum and colon relative weights, than did rats fed casein supplemented diets (Wang and McIntosh, 1996). Germination of chickpeas for 24 h increased PER by 12.5% (2.7 versus 2.4; Fernandez and Berry, 1988). However, Carías et al. (1998) found a PER of 1.58 and a NPU of 0.598 for chickpeas soaked in water overnight, cooked under pressure at 121 ◦ C for 20 min, and then dried at 70 ◦ C for 48 h. There were also no differences in NPU, BW gain, organ relative weights and apparent ileal digestibility of amino acids in rats fed diets based on raw or germinated chickpeas as the only protein source (Rubio et al., 2002). Overall, results suggest that processing techniques improve the nutritional value of chickpea grains, mainly due to inactivation of included SC. 5. Use of chickpeas in animal nutrition 5.1. Growing and lactating ruminants Using Holstein heifers, Illg et al. (1987) evaluated the nutritional value of chickpeas in diets where chickpeas replaced SBM in the concentrate in proportions of 151:0, 105:245, 54:494 and 0:752 g/kg DM for SBM and chickpeas, respectively. Table 12 The effect of processing on biological parameters of chickpea (CKP) grain summarized from several sources. Feedstuff

CKP grain CKP grain CKP grain

CKP grain

CKP grain

CKP grain CKP grain a

CKP processing

Raw Boiled Raw Germinated Raw Boiled Germinated Raw Boiled Extruded Raw Boiled Autoclaved Microwave cooked Germinated Raw Extruded Raw Germinated

Biological parameters

Reference

BVa

PER

TD

NPU

– – – – 0.648 0.703 0.659 – – – – – – – – – – – –

1.94 2.08 2.40 2.70 – – – 1.55 1.58 1.71 2.32 2.51 2.47 2.50 2.52 1.30 1.78 – –

– – – – 0.859 0.888 0.899 – – – – – – – – – – – –

– – – – 0.556 0.624 0.592 – – – – – – – – – – 0.660 0.690

BV, biological value; NPU, net protein utilization; PER, protein efficiency ratio; TD, true digestibility.

Sotelo et al. (1987) Fernandez and Berry (1988) Savage and Thompson (1993)

Wang and McIntosh (1996)

El-Adawy (2002)

Milán-Carrillo et al. (2002) Rubio et al. (2002)

12

Feedstuff

CKP level

Animal

DMa intake (kg/day)

BW gain (kg/day)

FCR (kg DM intake/ kg BW gain)

CKP concentrate (g/kg DM)

0 245 494 752 0 136 329 0 136 329 0 200 420 0 125 250 0 125 250 0 168

Heifers

– – – – 1.20 1.18 1.17 1.02 1.00 0.99 1.11 1.05 0.88 1.13 1.12 1.15 1.12 1.12 1.10 6.98 7.52

0.98 1.13 1.14 0.95 0.37 0.36 0.36 0.33 0.31 0.31 0.28 0.28 0.22 0.27 0.27 0.28 0.21 0.19 0.21 1.71 1.91

4.72 4.05 3.65 4.01 3.20 3.23 3.26 3.14 3.23 3.18 4.03 3.67 3.90 4.19 4.17 4.06 5.29 5.92 5.33 4.08 3.94

CKP concentrate (g/kg)

CKP concentrate (g/kg)

CKP concentrate (g/kg)

CKP concentrate (g/kg)

CKP TMR (g/kg DM) a

Male lambs

Male kids

Male lambs

Male lambs

Female lambs

Steers

BW, body weight; DM, dry matter; FCR, feed conversion ratio; TMR, total mixed ration.

Carcass yield (kg/100 kg BW) – – – – – – – – – – 52.8 52.5 52.9 48.0 47.6 48.5 52.1 50.8 51.6 – –

Reference Illg et al. (1987)

Hadjipanayiotou (2002)

Hadjipanayiotou (2002)

Lanza et al. (2003)

Christodoulou et al. (2005)

Gilbery et al. (2007)

V.A. Bampidis, V. Christodoulou / Animal Feed Science and Technology 168 (2011) 1–20

Table 13 The effect of chickpea (CKP) grain on performance of growing ruminants summarized from several sources.

Feedstuff

CKP level

Animal

DMa intake (kg/day)

Milk yield (kg/day)

Fat (g/kg)

CP (g/kg)

Lactose (g/kg)

Reference

CKP concentrate (g/kg DM)

0 500 978 0 120 240 0 300

Cows

20.1 20.0 20.6 2.0 2.0 2.0 2.0 2.0

34.5 35.1 35.7 1.6 1.5 1.6 1.1 1.2

30.6 30.9 32.8 59.8 58.6 59.0 75.0 77.0

32.0 30.9 29.6 56.8 56.5 57.4 64.0 64.0

– – – 49.3 49.3 49.4 53.0 53.0

Hadsell and Sommerfeldt (1988)

CKP concentrate (g/kg)

CKP concentrate (g/kg) a

CP, crude protein; DM, dry matter.

Ewes

Ewes

Christodoulou et al. (2005)

Christodoulou et al. (2007)

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Table 14 The effect of chickpea (CKP) grain on performance of lactating ruminants summarized from several sources.

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V.A. Bampidis, V. Christodoulou / Animal Feed Science and Technology 168 (2011) 1–20

They reported that BW gain was higher in heifers fed the 105:245 and 54:494 g/kg DM proportions, compared with the other groups, and that DM intake and feed conversion ratio (FCR) decreased linearly with increasing chickpea inclusion level (Table 13). Furthermore, Gilbery et al. (2007) showed that steers fed chickpeas had higher overall DM intake, final BW and BW gain than controls. Hadjipanayiotou (2002) and Lanza et al. (2003) studied replacement of SBM with chickpeas in diets of male Chios and Barbaresca lambs, respectively. The Chios lambs were fed diets with 0, 136 and 329 g/kg chickpeas (as fed basis), while the Barbaresca lambs diets were 0, 200 and 420 g/kg chickpeas (as fed basis). Hadjipanayiotou (2002) reported no differences in final BW, BW gain and DM intake of either chickpea group compared to the SBM group, and Lanza et al. (2003) reported no differences in final BW, BW gain and DM intake of the lower chickpea inclusion level group, compared to the SBM group, but that Barbaresca lambs in the highest chickpea inclusion group had a 9.7% lower final BW, 18.5% lower BW gain and 21.1% lower DM intake versus the SBM group. Both Hadjipanayiotou (2002) and Lanza et al. (2003) reported no differences in FCR among groups, except for Barbaresca lambs fed diets with the lowest level of chickpea inclusion which had an 8.9% better FCR than the SBM group. Hadjipanayiotou (2002) also reported no differences in performance of male Damascus kids fed diets with 0, 136 and 329 g/kg chickpeas (as fed basis). Moreover, chickpea straw, fed in the TMR of 10 month old camel calves (BW 187–240 kg) with chaffed dry groundnut forage and concentrate (700:150:150 g/kg of the TMR), supported a BW gain of 0.38–0.42 kg/day, with high nutrient utilization (Nagpal et al., 2005). In addition, Christodoulou et al. (2005) studied effects of partial and total replacement of SBM with chickpeas on productivity and meat composition of growing Florina (Pelagonia) lambs. SBM and chickpeas were fed to lambs in proportions of 140:0, 70:125, and 0:250 g/kg, and no differences occurred among chickpea inclusion groups in final BW, BW gain, DM intake or FCR. Christodoulou et al. (2005) also found that lambs slaughtered at ∼140 days of age did not differ in cold carcass weight and carcass yield among chickpea inclusion levels, which is consistent with Lanza et al. (2003) who showed that male Barbaresca lambs slaughtered at 132 day of age had the same dressing proportion among groups fed SBM or 200 or 420 g/kg inclusion levels of chickpeas (as fed basis) in the concentrate. Moreover, there were no differences in physical and chemical characteristics of the longissimus dorsi muscle of male lambs fed concentrate with various inclusion levels of chickpeas (Lanza et al., 2003), while some differences occurred in intramuscular fatty acid composition (Priolo et al., 2003). Hadsell and Sommerfeldt (1988) evaluated the nutritional value of chickpeas in diets of lactating Holstein cows fed concentrates containing SBM and chickpeas in proportions of 285:0, 139:500, and 0:978 g/kg DM, respectively. Cows fed the diet with the 0:978 g/kg DM proportion had higher milk yield than cows fed the 285:0 g/kg DM proportion, and higher milk fat content versus cows fed the 285:0 and 139:500 g/kg DM proportions (Table 14). However, milk protein content declined linearly as chickpea inclusion level increased. Christodoulou et al. (2005) studied effects of partial and total replacement of SBM with chickpeas on milk yield and composition of lactating Chios ewes. The SBM and chickpeas were fed to ewes in proportions of 100:0, 50:120, and 0:240 g/kg and there were no differences among groups in average milk yield (1.57 kg/day), or milk fat (59.1 g/kg), protein (56.9 g/kg), lactose (49.3 g/kg) and ash (9.0 g/kg) contents. In another experiment, Chios ewes fed a concentrate with 300 g/kg chickpeas had similar productive performance to ewes fed the SBM concentrate (Christodoulou et al., 2007). Overall, results suggest that substitution of SBM and cereal grains with chickpea grains results in equal growth of ruminants, as well as equal milk yield and composition in lactating ruminants. 5.2. Pig Visitpanich et al. (1985) reported that BW gain and FCR for growing pigs were not affected when they were fed concentrates containing SBM versus Kabuli and Desi chickpeas in proportions of 186:0 g/kg (control) versus 46:263 and 46:272 g/kg, respectively (Table 15). In another study, Batterham et al. (1993) evaluated the nutritional value of raw chickpeas in diets with growing pigs using concentrates containing SBM versus Kabuli and Desi chickpeas in proportions of 425:0 g/kg (control) versus 325:250, 228:500 and 130:750 g/kg, and 281:250, 140:500 and 0:750 g/kg, respectively, and found that BW gain, daily feed consumption (DFC) and FCR were similar among treatments. Moreover, Mustafa et al. (2000) studied the nutritional value of raw chickpeas in an experiment with 64 growing/finishing pigs. For the finishing, and overall, experimental periods, BW gain, DFC and FCR were similar among treatments, while inclusion of raw chickpeas (300 g/kg) appeared to depress performance relative to the control SBM diet during the growing period. In a study of young pig gut morphology, Salgado et al. (2001) observed moderate villus atrophy and crypt hyperplasia with chickpea diets which was associated with impaired nutrient absorption and decreased performance. In a 17 week experiment, increasing extruded chickpea inclusion levels up to 300 g/kg in pig diets positively influenced BW gain and FCR during the growing period, but did not affect BW, BW gain, DFC and FCR during the overall growing/finishing period (Christodoulou et al., 2006d). The increased performance in growing pigs fed the extruded chickpea containing diets may be attributed to the extrusion which improved the utilization of starch, fat and protein in chickpeas by the pigs (Spais, 1997; Milán-Carrillo et al., 2002). The diet containing 100 g/kg raw chickpeas negatively influenced BW gain and DFC during the finishing period, compared to the SBM diet, suggesting that pigs may have been susceptible to the SC contained in raw chickpeas (Christodoulou et al., 2006d). Pigs slaughtered at 45–50 kg had the same carcass yield (73.1–74.7 kg/100 kg of BW) when chickpeas were added to the diets, even at 750 g/kg (Visitpanich et al., 1985; Batterham et al., 1993). Mustafa et al. (2000) also showed that pigs slaughtered at an average weight of 102 kg had the same carcass yield (76.1 kg/100 kg of BW) and lean yield (59.7 kg/100 kg

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Table 15 The effect of chickpea (CKP; g/kg) grain on performance of pigs summarized from several sources. Feedstuff

CKP level

Pigs

DFCa (kg/day)

BW gain (kg/day)

FCR (kg DFC/ kg BW gain)

Carcass yield (kg/100 kg BW)

Reference

Raw CKP Kabuli CKP Desi CKP Raw CKP Kabuli CKP

0 263 272 0 250 500 750 250 500 700 0 300 300 0 100 200 300 100 0 100 200 300 100

Pigs

– – – 1.70 1.76 1.72 1.74 1.75 1.74 1.75 2.39 2.20 2.22 2.89 2.85 2.88 2.88 2.82 2.88 2.85 2.85 2.83 2.78

0.63 0.62 0.61 0.93 0.93 0.94 0.88 0.90 0.88 0.86 0.90 0.84 0.83 0.86 0.85 0.87 0.88 0.86 0.84 0.79 0.82 0.77 0.73

2.14 2.16 2.21 1.83 1.91 1.83 1.97 1.95 1.98 2.04 2.64 2.61 2.68 3.37 3.36 3.31 3.27 3.28 3.43 3.60 3.48 3.68 3.81

75.0 74.6 74.7 72.6 72.2 72.3 72.9 74.4 72.3 74.9 75.7 76.0 76.1 78.0 80.9 79.5 77.9 79.0 78.8 77.7 77.3 77.6 78.6

Visitpanich et al. (1985)

Desi CKP

Raw CKP Kabuli CKP Desi CKP Extruded CKP

Raw CKP Extruded CKP

Raw CKP a

Male pigs

Pigs

Male pigs

Female pigs

Batterham et al. (1993)

Mustafa et al. (2000)

Christodoulou et al. (2006d)

BW, body weight; DFC, daily feed consumption; FCR, feed conversion ratio.

of BW) among groups fed SBM or with 300 g/kg inclusion levels of chickpeas or field peas in the concentrate. Moreover, Christodoulou et al. (2006d) reported that pigs slaughtered at approximately 119 kg of fasted BW did not differ in cold carcass weight, carcass yield and lean yield among chickpea inclusion levels. In the Christodoulou et al. (2006d) study, there were no differences in weights of the heart, liver and kidney, while weight of kidney fat had a quadratic effect. Similarly, diet supplementation with chickpeas at inclusion levels of 250, 500 and 750 g/kg had no effect on liver weight of pigs (Batterham et al., 1993). Carcass classification of pigs, slaughter weight and other important meat quality attributes, such as pH, chemical composition, fatty acid composition, as well as odor and taste, remained the same, while physical characteristics of the pork, such as color and cooking loss, as well as sensory characteristics, such as tenderness and juiciness, indicated small differences among dietary treatments containing extruded chickpeas up to 300 g/kg compared to a control group of pigs fed a diet containing SBM (Christodoulou et al., 2006a). Overall, results suggest that substitution of SBM and cereal grains with chickpea grains results in equal growth of pigs for the finishing period, but depresses performance during the growing period. Heat treatment, i.e., extrusion, improves nutritional value of chickpeas increasing performance in growing pigs. 5.3. Broilers and layers Farrell et al. (1999) found a negative effect on BW, DFC and FCR of broiler chickens, during the staring period from 1 to 21 day of age, fed diets containing raw chickpeas up to 360 g/kg of concentrate (Table 16), as well as increased relative pancreas weight when compared to other diets. Performance of broiler chickens, during the finishing period from 21 to 42 day of age, was not impaired with increasing chickpea levels (Farrell et al., 1999). Viveros et al. (2001) studied the nutritional value of raw and autoclaved chickpeas in two experiments with male broiler chickens from 1 to 28 day of age. In the first experiment, broilers received diets with 0, 150, 300 and 450 g/kg raw Kabuli chickpeas, and in the second diets with 0, 75 and 150 g/kg raw and autoclaved Desi chickpeas. They reported that increasing the proportion of raw chickpea in the diet negatively influenced BW gain, DFC and FCR, and that feeding autoclaved chickpeas increased BW gain and DFC, but did not change FCR versus those fed the control diet. Feeding broiler chickens with raw chickpeas at inclusion levels up to 450 g/kg of the diet resulted in increased gizzard, liver and pancreas weights, and with autoclaved chickpeas at inclusion levels up to 150 g/kg of the diet resulted in increased weight of the gizzard and decreased liver weight, compared with those fed the control diet (Viveros et al., 2001). Brenes et al. (2008) studied the nutritional value of raw and extruded Kabuli chickpeas in broiler chickens (Cobb) from 1 to 21 day of age. Increasing chickpea content in the diet did not affect BW gain, DFC and FCR, with no differences between raw and extruded chickpeas, while relative liver weight increased with both raw and extruded chickpeas, but relative pancreas weight increased only with raw chickpeas (Brenes et al., 2008). Christodoulou et al. (2006b) also found that raw chickpeas can partially replace SBM at inclusion levels of 120 g/kg of diet without affecting final BW, DFC and FCR of broiler chickens (i.e., Cobb 500) compared to the SBM diet, while a higher inclusion level of 240 g/kg of diet adversely affected productive performance, suggesting that birds may have been susceptible to the

16

Table 16 The effect of chickpea (CKP; g/kg) grain on performance of broilers summarized from several sources. Feedstuff

CKP level

Poultry

DFCa (g/day)

BW gain (g/day)

FCR (g DFC/g BW gain)

Carcass yield (g/100 g BW)

Reference

Raw CKP

120 180 240 300 360 120 180 240 300 360 0 150 300 450 0 75 150 75 150 0 120 240 120 240 0 200 400 600 800 0 100 200 300 100 200 300 0 120 240 360 480 0 160 200

Male broiler chickens (1–21 days of age)

39.4 38.4 38.4 38.8 38.1 94.5 92.0 95.7 94.8 93.4 40.2 39.2 37.2 34.8 47.5 46.7 43.0 46.8 45.8 101.6 99.1 93.8 100.3 94.1 225.7 229.0 237.6 240.4 241.0 43.0 41.3 41.6 41.8 43.4 44.5 41.2 89.8 92.3 91.2 89.5 89.8 132.3 117.2 112.5

30.6 30.4 30.4 29.7 28.8 49.6 47.5 53.7 50.6 48.9 30.5 26.6 24.4 21.1 31.5 29.9 27.7 31.8 28.4 49.9 48.1 42.6 49.0 43.5 92.0 92.2 84.7 85.0 84.9 31.9 29.5 28.9 29.8 31.8 32.1 30.3 56.5 57.4 57.9 56.7 56.2 45.8 40.3 39.5

1.29 1.27 1.27 1.32 1.33 1.96 2.00 1.93 1.90 2.00 1.32 1.47 1.53 1.65 1.50 1.56 1.55 1.47 1.61 2.08 2.10 2.24 2.09 2.21 2.46 2.48 2.81 2.83 2.84 1.35 1.40 1.44 1.41 1.37 1.39 1.36 1.59 1.60 1.58 1.58 1.60 2.89 2.91 2.85

– – – – – – – – – – – – – – – – – – – 75.2 74.5 72.3 75.0 73.1 77.1 76.3 78.8 76.2 76.6 – – – – – – – 66.7 67.1 67.4 66.9 67.2 70.6 71.3 68.9

Farrell et al. (1999)

Raw CKP

Raw CKP

Autoclaved CKP Raw CKP

Heated CKP Extruded CKP

Raw CKP

Extruded CKP

Raw CKP

Raw CKP

a

Male broiler chickens

Male broiler chickens

Male broiler chickens Broiler chickens

Broiler chickens Male broiler turkeys

Broiler chickens

Broiler chickens

Broiler chickens

BW, body weight; DFC, daily feed consumption; FCR, feed conversion ratio.

Farrell et al. (1999)

Viveros et al. (2001)

Viveros et al. (2001)

Christodoulou et al. (2006b)

Christodoulou et al. (2006c)

Brenes et al. (2008)

Garsen et al. (2008)

Katogianni et al. (2008)

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Raw CKP

Male broiler chickens (21–42 days of age)

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Table 17 The effect of chickpea (CKP; g/kg) grain on performance of layers summarized from several sources. Feedstuff

CKP level

Poultry

DFCa (g/day)

EP (eggs/hen/day)

EW (g)

EM (g/hen/day)

FE (g feed/g EM)

Reference

Raw CKP Raw CKP

250 0 110 210 310 410

Laying hens Laying hens

115.4 118.2 117.6 118.7 117.1 114.8

0.824 0.718 0.726 0.722 0.742 0.724

56.9 71.7 69.8 71.6 71.0 73.4

46.7 51.8 53.2 53.3 53.3 53.5

2.47 2.28 2.21 2.23 2.20 2.15

Perez-Maldonado et al. (1999) Garsen et al. (2007)

a

DFC, daily feed consumption; EM, egg mass; EP, egg production; EW, egg weight; FE, feed efficiency.

Table 18 The effect of chickpea (CKP; g/kg) grain on performance of growing fish summarized from several sources. Feedstuff

CKP level

Fish

FIa (g/100 g BW)

Initial BW (g)

Final BW (g)

FCR (g FI/ g BW gain)

Extruded CKP

0 165 350 0 300

European seabass

1.08 1.14 1.11 – –

102.4 95.0 96.3 50.8 49.7

250.5 268.4 238.0 90.0 88.3

1.34 1.24 1.36 1.09 1.24

Extruded CKP a

Juvenile rainbow trout

Fillet yield (g/100 g BW) 41.0 – 42.5 – –

Reference Adamidou et al. (2009b)

Tiril et al. (2009)

BW, body weight; FCR, feed conversion ratio; FI, feed intake.

SC contained in raw chickpeas. Carcass yield traits and internal organs weights of broiler chickens were not affected when raw chickpeas were incorporated at inclusion level of 120 g/kg of diet, but negatively influenced with the higher inclusion level of 240 g/kg of diet (Christodoulou et al., 2006b). In contrast, Garsen et al. (2008) found that partial replacement of SBM with raw chickpeas resulted in similar performance and carcass characteristics of broiler chickens (i.e., Ross) when chickpeas were supplemented to their diet in gradually increasing levels up to 480 g/kg with respect to the birds age (i.e., 160 g/kg for 1–14 days of age, 240 g/kg for 15–28 days, 480 g/kg for 29–42 days). Moreover, Katogianni et al. (2008) showed that gradual substitution of 0.50 and 0.75 of raw chickpeas for SBM in the organic fattening of broilers (i.e., Cobb 500) until 81 days of age (i.e., 0 g/kg for 1–21 days of age, 200 and 280 g/kg for 12–49 days, 160 and 200 g/kg for 50–81 days, respectively) led to FCR and proportions of carcass parts similar to those of control birds, although carcasses and carcass parts were lighter. Christodoulou et al. (2006c) showed that partial replacement of SBM with extruded chickpeas (i.e., 200 g/kg of diet) resulted in similar performance of male broiler turkeys (i.e., B.U.T. 9). Diets containing higher inclusion levels of extruded chickpeas (i.e., 400, 600, 800 g/kg of diet) did not affect DFC at 84 days of age, but negatively influenced final BW and FCR, compared to the control diet. Carcass yield traits and meat quality were not affected with inclusion of extruded chickpeas in diets of broiler turkeys at levels up to 800 g/kg (Christodoulou et al., 2006c, 2009). Available information on the nutritional value of chickpeas for layers is limited (Table 17). Perez-Maldonado et al. (1999) studied the nutritional value of chickpeas, field peas, faba beans and sweet lupins in an experiment with laying hens from 18 to 58 week of age. Chickpeas supported excellent production, when included at 250 g/kg of the diet of laying hens, but increased relative pancreas weight when compared to other diets (Perez-Maldonado et al., 1999). Moreover, Garsen et al. (2007) showed that partial and total replacement of SBM with raw chickpeas resulted in similar productive performance and egg quality of laying hens (i.e., Lohmann), except for yolk color which decreased with increasing chickpea levels. Overall, results suggest that supplementation of poultry diets with chickpea grains results in equal growth of broilers for the finishing period, as well as equal egg production in layers, but depress broiler performance during the starting period. Heat treatment improves nutritional value of chickpeas increasing performance in broilers. 5.4. Fish The use of plant proteins to replace traditional protein sources such as fish meal in aquaculture diets has become more common in recent years. However, information on the nutritional value of chickpeas for fish is limited (Table 18). Adamidou et al. (2009b) evaluated the nutritional value of extruded chickpeas, field peas and faba beans in a 14 week experiment with growing European seabass fish. Extruded chickpeas were fed to fish in proportions of 0, 165, and 350 g/kg in total replacement of wheat and partial replacement of SBM and sunflower cake, and no differences occurred among chickpea, or other legumes, inclusion groups in final BW, feed intake or FCR. In addition, Tiril et al. (2009) showed that the productive performance of juvenile rainbow trout was not affected by inclusion of extruded chickpeas at 300 g/kg of the diet in partial replacement of fish meal, SBM, maize gluten, wheat and fish oil. In the later study, both diets had the same PER and inclusion of extruded chickpeas in fish diets resulted in no (Tiril et al., 2009) or minor (Adamidou et al., 2009b) differences in chemical composition of fish muscle versus the controls. Overall, results suggest that substitution of SBM and cereal grains with extruded chickpea grains results in equal growth of fish.

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6. Conclusions In general, raw chickpeas can be used in ruminant diets at inclusion levels up to 300 g/kg, or more, because the secondary compounds in chickpeas and other grain legumes appear to be inactivated by rumen fermentation. In contrast, raw chickpeas can be used in diets of non-ruminants at inclusion levels up to 200 g/kg to support growth and egg production without detrimental effects on pigs and birds. Higher inclusion levels of chickpeas in pig, poultry and fish diets can be used after removal of the secondary compounds using heat treatments which improves the nutritional value of chickpeas. As a heat treatment, extrusion destroys most secondary compounds, thereby improving the utilization of starch, fat and protein in chickpeas by pigs, poultry and fish. Chickpea straw has relatively high nutritional value, for a straw, and can be used as a ruminant feed. Acknowledgement The authors thank Dr. P.H. Robinson (UC Davis, Davis, CA, USA) for proof-reading the typescript. 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