Review article

A review of the potential of Lathyrus sativusL. and L. cicera L. grain for use as animal feed

C.D. Hanburya,*, C.L. Whiteb, B.P. Mullanc, K.H.M. Siddiquea,c

aCentre for Legumes in Mediterranean Agriculture (CLIMA), University of Western Australia,

Nedlands 6907, AustraliabCSIRO, Division of Animal Production, Private Bag, PO Wembley 6014, Australia

cAgriculture Western Australia, Locked Bag No. 4, Bentley Delivery Centre, Bentley 6983, Australia

Received 28 December 1999; received in revised form 3 July 2000; accepted 19 July 2000

Abstract

The use of two closely related species, Lathyrus cicera and L. sativus, as grain legumes for

human and animal consumption, dates to the Neolithic period. Due to its tolerance to harsh

environmental conditions L. sativus is still used widely for human food in Ethiopia and the Indian

sub-continent, although cultivation has diminished in many other regions.

The grain of both L. cicera and L. sativus contains a neurotoxin, 3-(-N-oxalyl)-L-2,3-diamino

propionic acid (ODAP), which can cause a paralysis of the lower limbs (lathyrism). Due to the

occurrence of lathyrism in humans recent plant breeding has produced cultivars with low ODAP

concentrations. The susceptibility of animal species to lathyrism is poorly understood, although

horses and young animals are more susceptible. Older published animal feeding studies are of

limited use, since the presence and role of ODAP was unknown until the 1960s. More recent

feeding studies indicate that low ODAP lines of L. cicera or L. sativus can be safely incorporated at

inclusion rates up to 40, 30 and 70% of the diet of poultry, pigs and sheep, respectively, without

growth reductions.

The compositions of both L. cicera and L. sativus are similar to other commonly used feed grain

legumes, respective protein contents are 25 and 27%. Antinutritional factors (ANFs), other than

ODAP, are present in both L. cicera and L. sativus at concentrations similar to those found in other

grain legumes; including trypsin inhibitors, chymotrypsin inhibitors, amylase inhibitors, lectins,

tannins, phytate and oligosaccharides. The effect of ANFs in L. cicera and L. sativus on animal

performance is not well understood and sometimes confounded with ODAP effects. Heating of

grain will reduce levels of the proteinaceous ANFs and in some cases ODAP as well.

Variation recorded in the germplasm of L. cicera and L. sativus has not been greatly utilised in

plant breeding to lower levels of ANFs, with the exception of ODAP, leaving considerable potential

for rapid improvement of cultivars. L. cicera and L. sativus are low production cost legumes

Animal Feed Science and Technology

87 (2000) 1±27

* Corresponding author. Tel.: �61-8-9368-3744; fax: �61-8-9368-2165

E-mail address: chanbury@agric.wa.gov.au (C.D. Hanbury).

0377-8401/00/$ ± see front matter # 2000 Elsevier Science B.V. All rights reserved.

PII: S 0 3 7 7 - 8 4 0 1 ( 0 0 ) 0 0 1 8 6 - 3

adapted to low rainfall environments and have considerable potential as good quality, cheap protein

sources. As world demand for legume feed protein is likely to increase, due to increasing demand

for animal food products, both L. cicera and L. sativus are crops that should be considered in

regions with suitable environments. # 2000 Elsevier Science B.V. All rights reserved.

Keywords: Lathyrus; Protein; ODAP; Antinutritional factors; Lathyrism

1. Introduction

The use of legumes as sources of protein for the animal feed industry is expected to

increase further in the near future. Rising incomes in the Asian region are increasing the

demand for meat products, and hence the requirement for animal feeds. There have been

changes in public perception and some unfortunate developments, such as the

consequences of `mad cow' disease (i.e. bovine spongiform encephalopathy or BSE) in

UK. This has resulted in many feed compounders either choosing to, or being banned

from, using animal by-products as a source of protein (Farrell, 1997). The amino acid

requirement of animals often differ with species and bodyweight, hence no single source

of plant protein will provide the exact amino acids required for all animals. It is,

therefore, preferable to include a range of protein sources in diet formulations, each

complementing the other. For these reasons, the demand for grain legumes, such as

Lathyrus spp., by the feed industry is expected to increase. Any feedstuff is likely to be

used in diets for animals if it supplies the required nutrients, if it is cost competitive with

other available ingredients, and if the user is con®dent it will produce the desired result.

Soybean (Glycine max) meal is used widely as a source of protein for animal feeds, and

the price of most other protein meals and grain legumes are set relative to this

commodity. In Europe there has been increasing emphasis on local production of legumes

for animal feed in order to supply some of this protein demand (Gatel, 1994), rather than

relying on imported soybean meal. Subsidies have resulted in increasing production of,

particularly, ®eld peas (Pisum sativum) and faba beans (Vicia faba). This expansion has

been partly at the expense of previously grown legume crops, such as Lathyrus spp.,

which do not have subsidies (Franco Jubete, 1991).

It has been demonstrated in recent studies that two Lathyrus spp. (L. sativus L. and L.

cicera L.) have considerable potential as grain legume crops on ®ne textured, neutral to

alkaline, soil types in southern Australian Mediterranean-type environments (Hanbury

et al., 1995; Siddique et al., 1996, 1999; Siddique and Hanbury, 1998). In Australia the

adaptation of the two species is slightly different, L. cicera seeming better adapted to

lower rainfall (250±350 mm annually) regions and L. sativus to medium rainfall (350±

600 mm annually). They are being evaluated as low input, multi-purpose crops for green

manuring, animal feed and fodder. In Australia, animal feed is seen as the primary use of

the grain of these species, both on and off farm. Animal feeding with both species has a

long history and is still practised in some parts of the world. However, published studies

are scattered and frequently dif®cult to access. This review aims to summarise the animal

feeding literature and demonstrate the potential for the two species as animal feed.

2 C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27

The genus Lathyrus is a large one, comprising 189 species and sub-species according

to Allkin et al. (1985), and approximately 150 species according to Kupicha (1983). Of

these only a small number are cultivated. The closely related L. sativus (grass pea) and L.

cicera (dwarf chickling) both belong to the same section: Lathyrus. Jackson and Yunus

(1984) suggest that the similarities between semi-domesticated L. cicera and

domesticated L. sativus may be a result of hybridisation or common ancestry. Some

interspeci®c crosses between the two have been successful (Yunus and Jackson, 1991).

Archaeobotanical evidence shows that both L. sativus and L. cicera were cultivated on the

Iberian peninsula in the Neolithic period (PenÄa-Chocarro and Zapata PenÄa, 1999).

Evidence also suggests that L. sativus is possibly the most ancient domesticated crop in

Europe, the Neolithic expansion of its cultivation into what is now Spain led to the

cultivation of a local native species, L. cicera (Kislev, 1989). Erskine et al. (1994) suggest

that L. sativus was originally domesticated as a secondary crop as a result of being a weed

of lentil (Lens culinaris) crops.

2. Lathyrism

Lathyrus species, particularly L. sativus, have been known since classical times to be

implicated in a paralysis of humans and animals (Hugon et al., 2000) known as

`̀ lathyrism'' or more speci®cally `̀ neurolathyrism''. Both ruminants and monogastric

species can be affected, some literature indicates that monogastrics can be more affected.

It was only in the later half of the 20th century that the compound responsible was

identi®ed (Murti et al., 1964; Rao et al., 1964).

There are two forms of lathyrism, neurolathyrism and osteolathyrism. Osteolathyrism

is characterised by skeletal deformities and can be caused by consumption of the species

L. odoratus (sweet pea), L. hirsutus, L. pusillus and L. roseus (Roy, 1981). Osteolathyrism

has been recorded experimentally in a wide range of animals (Barrow et al., 1974). The

principal compound responsible was found to be b-aminopropionitrile (BAPN; Fig. 1),

although the related nitriles aminoacetonitrile (AAN) and methylene aminoacetonitrile

(MAAN) also have some osteolathyritic activity (Barrow et al., 1974). Although BAPN is

not found in either L. sativus or L. cicera (Bell, 1962, 1964), there is evidence that a

BAPN precursor (2-cyanoethyl-isoxazolin-5-one) is present in L. sativus seedlings but not

in seed (Lambein et al., 1993). Consumption of L. sativus seedlings and shoots as

vegetables has been blamed as the cause of osteolathyritic symptoms found in a small

proportion of people with chronic neurolathyrism (Haque et al., 1997). Incidents of

osteolathyrism from feeding of L. sativus or L. cicera have not been reported in animal

studies, either under natural grazing or experimental conditions, and consequently the

following discussion will focus on neurolathyrism.

Neurolathyrism is the term used to describe the symptoms shown after heavy

consumption of several different Lathyrus species and some Vicia species. The symptoms

are weakness of the hind limbs and paralysis or rigidity of the muscles. Within the

Lathyrus genus, the category of neurolathyrism has been further divided into two sub-

categories. One is caused by the compound L-2,4-diaminobutyric acid (DABA; Fig. 1),

primarily in the perennial species L. sylvestris (Foster, 1990) and L. latifolius (Barrow

C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 3

et al., 1974). However, DABA is not found in L. cicera or L. sativus (Bell, 1962, 1964;

Padmanaban, 1980). The form of neurolathyrism most pertinent to this discussion is that

caused by the non-protein amino acid 3-(-N-oxalyl)-L-2,3-diamino propionic acid (ODAP,

also referred to as b-N-oxalylamino-L-alanine or BOAA; Fig. 1): which has been recorded

in humans and animals following consumption of L. sativus, L. cicera, L. ochrus and L.

clymenum (Barrow et al., 1974; Padmanaban, 1980; Franco Jubete, 1991). The seed of a

number of other uncultivated Lathyrus species have been found to contain ODAP (Bell,

1962, 1964). Historically the consumption of L. sativus has been most often linked with

lathyrism in humans and animals, primarily because of all Lathyrus species it is the most

widely utilised as grain and fodder. Lathyrism is the term mostly used to refer to

neurolathyrism caused by ODAP, therefore this term will be used in this review from this

point onward.

Lathyrism in humans has received more attention than that in animals, due to the social

cost. Symptoms in humans are most often initial painful spasms in the muscles of the

lower limbs with accompanying weakness, followed by chronic spastic paraplegia of

various degrees (Spencer et al., 1986), and can lead to total loss of use of the legs (Attal

et al., 1978). The paralysis is rarely reversible (and then only in early stages of the

symptoms; Hugon et al., 2000) and the consequences for poor communities who depend

upon L. sativus as a primary food source at times of food scarcity can be devastating.

Lathyrism still occurs, with a 1997 outbreak during food shortages in Ethiopia crippling

2000 people (Getahun et al., 1999). Lathyrism is endemic to the areas of the world which

have signi®cant areas of L. sativus cultivation; India, Bangladesh, Ethiopia and Nepal.

However, in the 20th century outbreaks were also reported in Afghanistan, Algeria,

China, France, Germany, Italy, Pakistan, Romania, Russia, Spain and Syria (Trabaud and

MouhaÈrram, 1932; Barrow et al., 1974; Roy and Spencer, 1989; Hugon et al., 2000).

Fig. 1. Chemical diagrams of b-aminopropionitrile (BAPN), L-2,4-diaminobutyric acid (DABA), 3-(-N-oxalyl)-L-2,3-diamino propionic acid (ODAP or BOAA) and glutamate.

4 C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27

Boiling has been found to reduce ODAP levels in several cases, however, there are mixed

reports on other forms of cooking (Tekle Haimanot et al., 1993; Akalu et al., 1998).

Padmajaprasad et al. (1997) reported that boiling grain and discarding the water reduced

ODAP levels by up to 90%.

3. ODAP toxicity

Following its isolation and identi®cation (Murti et al., 1964; Rao et al., 1964) the

neurolathyritic action of ODAP was soon demonstrated in adult monkeys (Macaca

radiata; Rao et al., 1967). Cheema et al. (1969) administered ODAP intraperitoneally to

rats. Young rats showed lathyrism symptoms and had 0.11 mmol gÿ1 ODAP in the brain,

adult rats showing trace or nil ODAP and no symptoms. Olney et al. (1976) found some

indication of exclusion of ODAP by the blood-brain barrier in mice. Padmanaban (1980)

suggested that the hypothesis of less ODAP exclusion by the blood-brain barrier in young

animals should be re-examined, as greater excretion of ODAP by older animals may be

an important factor. Spencer et al. (1986) showed unequivocally that ODAP, either

naturally present in L. sativus or when added to other food sources, was the cause of

corticospinal dysfunction in monkeys (Macaca fascicularis), with symptoms of hind limb

motor dif®culties.

ODAP acts as a glutamate (Fig. 1) analogue in the nervous system and probably acts by

binding strongly to a-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)-

type glutamate receptors. Permanent damage probably occurs with excitotoxic

degeneration of neurons, although there are other possible neurotoxic effects. The

ultimate fate of ODAP and the distribution in the brain and spinal cord is not known

(Hugon et al., 2000). ODAP was not detected in pig loin tissue following feeding for an

extended period (Castell et al., 1994; see Section 4.3).

In human populations young men are widely reported as the most susceptible to

lathyrism (McCarrison, 1926; Shourie, 1945; Attal et al., 1978; Hamid et al., 1986;

Getahun and Tekle Haimanot, 1997), although the reasons for this are not understood

(Hugon et al., 2000). The production and susceptibility to ODAP may be linked to Zn

de®ciency in plants and humans, respectively (Lambein et al., 1994; Lambein and Kuo,

1997). ODAP has also been found to inhibit growth of some insects and yeasts (Rao et al.,

1964; Mehta et al., 1972), and so may have a plant protective role.

4. The nutritive value of Lathyrus for animals

4.1. Chemical composition of the seed

Note: All concentrations in grain are expressed as received unless speci®ed otherwise.

4.1.1. Proximate composition

The proximate compositions of L. cicera and L. sativus are generally very similar to

®eld pea and faba bean (Table 1). Both Lathyrus spp. have low fat and high starch

C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 5

Table 1

Composition of L. cicera and L. sativus in comparison to ®eld pea (P. sativum), faba bean (V. faba) and lupin (L. angustifolius)a

L. cicera L. sativus Field pea Faba bean Lupin

i ii iii iv Mean iii iv v vi vii viii ix x xi xii Mean i xiii i xiii i xiii

No. lines 1 1 4 1 ± 8 1 3 1 3 1 1 25 1 1 ± 1 24±3788 1 5±355 1 111±3782

Component (% DM)

Protein 21.7 27.2 33.0 26.4 29.6 34.3 30.1 30.9 26.4 32.6 26.3 31.3 27.3 35.9 26.9 29.4 21.0 25.7 23.7 26.9 29.1 35.1

Ash 2.9 3.1 3.8 3.1 3.5 3.9 3.1 3.3 2.8 2.6 3.2 3.1 2.0 2.7 2.9 2.6 3.3 2.8 3.8 3.0 2.6 3.0

Fat 1.4 0.7 ± ± 1.1 ± ± 0.9 1.7 5.3 0.7 1.0 1.4 1.2 0.8 1.6 1.7 1.2 1.4 1.4 7.2 6.5

Crude ®bre 7.3 6.7 ± ± 7.0 ± ± ± 6.0 8.3 5.5 10.0 8.3 5.3 5.9 8.0 7.2 6.6 10.0 9.4 16.1 16.8

ADF 10.7 10.6 10.7 11.0 10.7 9.0 12.2 ± ± ± ± ± ± ± 8.3 9.3 8.1 10.3 13.1 11.0 22.9 21.6

NDF 22.1 24.3 17.8 18.2 19.4 15.5 16.0 ± ± ± ± ± ± ± ± 15.6 14.6 14.7 20.2 14.3 26.9 25.8

Lignin 0.6 0.2 ± ± 0.4 ± ± ± ± ± ± ± ± 1.5 0.8 1.2 1.1 0.6 2.4 ± 2.8 0.9

Starch 44.2 ± ± ± 44.2 ± ± ± ± ± ± ± 41.2 ± ± 41.2 45.3 ± 40.0 ± 0.8 ±

Dry matter (% ar) ± 89.7 90.3 89.5 90.1 90.9 89.0 90.0 ± ± 90.0 87.6 91.9 ± 91.1 91.3 ± 90.2 ± 89.7 ± 91.1

a Source: (i) Abreu and Bruno-Soares (1998), (ii) Hanbury (unpublished), (iii) Aletor et al. (1994), (iv) Farhangi (1996), (v) Adsule et al. (1989), (vi) Infascelli et al.

(1995), (vii) Shobhana et al. (1976), (viii) Dhiman et al. (1983), (ix) Latif et al. (1975), (x) Urga et al. (1995), (xi) Kuo et al. (1995), (xii) Low et al. (1990), (xiii) Mean

values from Petterson et al. (1997).

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contents, similar to ®eld pea and faba bean, conversely lupin has high fat and low starch

content. The composition of the lipid fraction (Table 2) shows in most cases that the fatty

acid pro®le is similar to other grain legumes, concentrations of stearic and linoleic acid

are a little higher and oleic acid slightly lower. The data of Senatore and Basso (1994)

differ from other data in both L. cicera and L. sativus, they found levels of oleic acid

considerably higher and levels of linoleic acid considerably lower than all other reports.

Whether this difference is due to the methods of Senatore and Basso (1994) or a

difference in the Italian Lathyrus ecotypes examined is unclear, their results also differ

from those for other grain legumes species (Table 2).

4.1.2. Mineral content

The data on L. cicera mineral content are more complete than those for L. sativus

(Table 3). Mineral contents of both species are similar and compare to other agriculturally

important grain legumes. On the basis of the available data it does not appear that either

species will be markedly different to the other grain legumes widely used.

4.1.3. Protein content and quality

The mean protein content in L. cicera and L. sativus is 25 and 27%, respectively, from

samples across a wide range of locations (Table 4). These are higher than protein contents

in ®eld pea (23%) or faba bean (24%), but lower than in lupin (32%) (Petterson et al.,

1997) or soybean (42%; Ravindran and Blair, 1992). Chandna and Matta (1994) found

the composition of seed protein in L. sativus to be: albumins (14%), globulins (66%),

Table 2

Fatty acid composition of L. cicera and L. sativus (compared to ®eld pea (P. sativum), faba bean (V. faba) and

lupin (L. angustifolius))a

L. cicera L. sativus Field

pea

Faba

bean

Lupin

i ii ii iii iv v vi vi vi

No. lines 2 2 3 1 1 1 5±16 3±8 3±174

Fatty acid (% of total fats)

Mystiric ± 0.4 0.6 ± 0.8 0.5 0.3 0.5 0.1

Palmitic 15.4 5.3 8.1 25 14.8 16.8 12.5 14.0 11.0

Palmitoleic ± 0.3 0.4 ± 0.3 ± ± ± 0.1

Stearic 7.9 18.7 13.8 2 7.5 4.6 1.2 2.3 3.7

Oleic 12.1 57.7 58.3 1 16.7 18.6 25.1 21.0 33.5

Linoleic 46.2 12.1 14.1 67 56.0 38.9 42.3 45.0 37.1

Non-adecanoic 0.8 ± ± ± ± ± ± ± ±

Linolenic 8.6 0.7 1.1 3 2.2 8.0 9.7 4.7 5.3

Arachidic 2.4 1.2 0.5 ± ± ± 0.7 1.8 0.9

Eicosadienoic 2.7 ± ± ± ± ± ± ± 0.4

Behenic ± 0.9 0.4 Trace ± ± 0.3 0.9 1.9

Total 96.1 97.3 97.3 98 98.3 87.4 91.8 89.3 92.1

a Source: (i) Hanbury (unpublished), (ii) Senatore and Basso (1994), (iii) Choudhury and Rahman (1973),

(iv) Kuo et al. (1995), (v) Grela and GuÈnter (1995), (vi) Mean values from Petterson et al. (1997).

C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 7

Table 3

Mineral content (as received) of L. cicera and L. sativus (includes comparison with ®eld pea (P. sativum), faba bean (V. faba) and lupin (L. angustifolius))a

L.cicera L. sativus Field pea Faba bean Lupin

i ii Mean ii iii iv v vi vii Mean viii viii viii

No. of lines 2 1 ± 1 1 25 1 1 3 ± 5±84 4±23 355±677

Mineral (mg/kg)

Se 0.12 ± 0.12 ± ± ± ± ± ± ± 0.07 0.05 0.08

Cu 7.6 5.6 6.9 8.2 ± ± ± 7.7 ± 8.0 4.8 10.3 4.9

Fe 70 78 73 38 ± 95 ± 63 74 89 53 77 75

Mn 11 12 12 15 ± ± ± ± ± 15 14 30 17

Zn 22 15 20 27 ± ± ± ± ± 27 30 28 35

B 9 14 11 11 ± ± ± ± ± 11 ± ± ±

Mineral (%)

P 0.30 0.27 0.29 0.34 0.31 0.44 0.26 0.32 0.41 0.42 0.34 0.41 0.30

K 0.88 0.86 0.87 ± ± ± ± 0.64 ± 0.64 0.91 0.96 0.81

Na 0.07 0.06 0.07 0.02 ± ± ± 0.04 ± 0.03 0.01 0.01 0.05

Ca 0.16 0.27 0.20 0.12 0.14 0.16 0.28 0.09 0.18 0.16 0.07 0.12 0.22

Mg 0.12 0.13 0.13 0.12 ± ± 0.11 0.09 ± 0.11 0.12 0.10 0.16

S 0.16 0.17 0.17 0.18 ± ± ± 0.14 ± 0.16 0.18 0.13 0.23

Ca:P 0.53 1.0 0.69 0.53 0.45 0.36 1.1 0.28 0.43 0.38 0.21 0.29 0.73

a Source: (i) Hanbury (unpublished), (ii) Farhangi (1996), (iii) Low et al. (1990), (iv) Urga et al. (1995), (v) Latif et al. (1975), (vi) Adsule et al. (1989), (vii)

Shobhana et al. (1976), (viii) Mean values from Petterson et al. (1997).

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glutelins (15%) and prolamins (5%); similarly; Duke (1981) also quotes values of 26, 53,

15 and 6%, respectively.

The amino acid pro®les of L. cicera and L. sativus (Table 5) are similar to those

reported for many grain legumes (Petterson et al., 1997; Ravindran and Blair, 1992). For

monogastric species most grain legumes are de®cient in the sulphur containing amino

acids (methionine and cystine) but are rich in lysine (Gatel, 1994; Ravindran and Blair,

1992), this is also the case in L. cicera and L. sativus. In mixed diets, grain legumes,

therefore, complement cereals, which have higher levels of methionine and cystine but

lower levels of lysine. The mean lysine concentration in L. cicera is slightly lower than in

L. sativus, 6.16 (n � 3) cf. 6.8 g/16 g N (n � 12). Lysine contents per 16 g N are �5%

lower than in ®eld pea, and �30% higher than in lupins (Table 5). On the basis of the

protein composition both Lathyrus spp. have similar application to other legumes used as

animal feed.

Little information is published on L. sativus and L. cicera amino acid availabilities in

monogastric and protein degradability in ruminant species. The protein degradability

estimates from in sacco studies in three ruminant species (Table 6) showed both L. sativus

and L. cicera to be similar to ®eld pea and faba bean. Protein degradabilities in both

Lathyrus spp. were usually slightly greater than lupin; and usually slightly less than in

faba bean or ®eld pea.

4.1.4. Energy

For both L. cicera and L. sativus, measures of energy are similar to those for many

other common feed grain legumes. However, L. cicera and L. sativus have consistently

lower gross energy (GE) than lupin (which has a much higher fat content, Table 1) but are

similar to ®eld pea and faba bean (Table 7).

Table 4

Protein concentrations (as received) reported in L. cicera and L. sativus

Species Mean protein (%) No. lines Location Source

L. cicera 25 128 Spain Franco Jubete (1991)

26 51 ± Petterson et al. (1997)

23 20 Australia Laurence (1979)

24 17 Australia Hanbury (unpublished)

27 16 Syria Aletor et al. (1994)

L. sativus 24 114 Bangladesh Kaul et al. (1982)

28 76 Chile Tay et al. (2000)

29 41 ± Petterson et al. (1997)

26 40 Australia Laurence (1979)

31 36 Syria Aletor et al. (1994)

25 25 Ethiopia Urga et al. (1995)

30 15 India Ramanujam et al. (1980)

25 12 Australia Hanbury (unpublished)

25 10 Spain Franco Jubete (1991)

27 3 Canada Rotter et al. (1991)

29 3 India Shobhana et al. (1976)

C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 9

Table 5

Amino acid concentrations (g/16 g N) and protein (as received) in L. cicera and L. sativus (includes comparison with ®eld pea (P. sativum), faba bean (V. faba) and lupin

(L. angustifolius))a

L. cicera L. sativus Field pea Faba bean Lupin

i ii Mean ii iii iv v vi vii viii Mean ix ix ix

No. of lines 2 1 ± 1 1 3 1 4 1 1 ± 37 6 30

Amino acids (g/16 g N)

Cystine 1.26 ± 1.26 ± 1.39 1.53 ± 1.2 ± ± 1.4 1.49 1.37 1.48

Aspartic acid 9.54 11.81 10.30 10.45 11.8 ± 8.53 ± 14.6 9.97 11.07 10.16 10.53 9.29

Methionine 0.75 ± 0.75 ± 0.82 1.00 0.24 0.6 0.61 0.59 0.7 0.85 0.78 0.72

Threonine 3.31 3.99 3.54 3.55 4.08 4.04 2.59 2.6 5.15 3.82 3.5 3.35 3.54 3.36

Serine 4.58 4.95 4.70 4.75 4.73 ± ± ± 5.08 4.40 4.74 4.13 5.04 4.85

Glutamic acid 16.26 17.46 16.66 16.37 17.43 ± 13.40 ± 17.47 13.99 15.73 15.88 16.03 20.77

Proline 4.10 ± 4.10 ± 4.00 ± 3.07 ± 4.42 3.50 3.75 4.24 3.82 4.28

Glycine 3.74 4.00 3.83 3.43 4.20 ± 3.45 ± 3.91 3.91 3.78 4.13 4.20 4.12

Alanine 3.67 4.31 3.88 3.62 4.53 ± 3.20 ± 2.19 3.92 3.49 4.00 4.17 3.19

Valine 4.30 4.66 4.42 4.00 4.90 ± 3.91 4.4 5.08 5.88 4.6 4.29 4.30 3.91

Isoleucine 3.68 4.08 3.82 3.69 4.41 ± 3.41 5.0 4.82 3.89 4.5 3.89 3.80 3.97

Leucine 6.50 6.53 6.51 5.76 6.90 ± 5.93 6.6 8.60 6.42 6.7 6.54 7.27 6.61

Tyrosine 2.93 ± 2.93 ± 2.45 ± 2.39 ± 2.92 1.44 2.30 2.87 3.39 3.46

Phenylalanine 4.11 ± 4.11 ± 4.49 ± 3.26 4.2 3.89 2.95 3.9 4.17 4.12 3.65

Lysine 5.98 6.52 6.16 5.37 6.73 7.10 4.08 7.0 6.27 9.65 6.8 6.81 6.29 4.66

Histidine 2.18 ± 2.18 ± 2.61 ± 2.82 2.5 3.47 2.70 2.7 2.37 2.54 2.41

Arginine 7.90 7.96 7.92 7.28 8.04 ± 6.13 8.0 6.11 3.29 7.0 10.04 9.46 12.03

Protein (% ar) 26.8 23.6 25.7 26.8 24.5 26.9 27.4 ± 32.3b 25.6 27.2 23.0 24.1 32.2

a Source: (i) Hanbury (unpublished), (ii) Farhangi (1996), (iii) Low et al. (1990), (iv) Rotter et al. (1991), (v) Latif et al. (1975), (vi) Adsule et al. (1989), (vii) Kuo

et al. (1995), (viii) Ronda Lain et al. (1963), (ix) Mean values from Petterson et al. (1997).b Estimated as 0.90% DM.

10

C.D

.H

an

bury

eta

l./An

ima

lF

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cience

an

dTech

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87

(2000)

1±27

Table 6

In sacco degradability parameters for protein and dry matter in L. cicera and L. sativus grain fed to ruminant

species (compared to ®eld pea (P. sativum), faba bean (V. faba) and lupin (L. angustifolius))a

Animal Feed grain Parameter Degradability

(at r � 0:05)Soluble

fraction (a)

Potentially

degradable

fraction (b)

Rate of

degradation

(c)

Protein Cattleb L. cicera 0.53 0.46 0.36 0.93

Field pea 0.56 0.44 0.35 0.95

Faba bean 0.59 0.41 0.39 0.95

Lupin 0.51 0.50 0.22 0.92

Cattlec L. cicera 0.39 0.61 0.20 0.78

Field pea 0.52 0.48 0.18 0.87

Faba bean ± ± ± ±

Lupin 0.38 0.62 0.17 0.84

Buffalod L. sativus 0.52 0.48 0.17 0.88

Field pea ± ± ± ±

Faba bean 0.79 0.18 0.10 0.91

Lupin 0.34 0.66 0.17 0.84

Sheepd L. sativus 0.62 0.37 0.14 0.89

Field pea ± ± ± ±

Faba bean 0.70 0.28 0.11 0.89

Lupin 0.52 0.46 0.12 0.84

Dry matter Cattleb L. cicera 0.45 0.48 0.25 0.85

Field pea 0.50 0.49 0.22 0.90

Faba bean 0.47 0.46 0.29 0.86

Lupin 0.37 0.61 0.13 0.81

Cattlec L. cicera 0.34 0.62 0.16 0.72

Field pea 0.41 0.59 0.13 0.80

Faba bean ± ± ± ±

Lupin 0.33 0.67 0.14 0.80

Buffalod L. sativus 0.43 0.54 0.12 0.81

Field pea ± ± ± ±

Faba bean 0.6 0.34 0.09 0.82

Lupin 0.17 0.80 0.18 0.80

Sheepd L. sativus 0.59 0.37 0.07 0.81

Field pea ± ± ± ±

Faba bean 0.64 0.30 0.16 0.81

Lupin 0.14 0.83 0.14 0.75

a The parameters describe the non-linear equation: fractional loss � a� b�1ÿ eÿct�; t is the time (h).

Degradabili ty is determined at 0.05 fract ional rumen out¯ow rate (r) according to:

degradability � a� bc=�c� r�, where a is the water soluble fraction, b the potentially degradable fraction, c

the rate of loss of b and t is the time (h).b White (unpublished).c Guedes and Dias da Silva (1996) incorporates a lag phase and is recalculated from r � 0:044 to r � 0:05.d Infascelli et al. (1995).

C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 11

The metabolisable energy (ME) of L. cicera may be slightly higher than L. sativus

(Table 8). The ME for both Lathyrus spp. in sheep are approximately 13 MJ/kg DM,

similar to ®eld pea and faba bean. The sheep ME data of Farhangi (1996) are consistently

lower than all other sources, the in vitro dry matter digestibility (DMD) method used to

calculate ME is not recommended for grain (SCA, 1990). The single record for ME in

cattle shows L. sativus to be similar to ®eld pea and faba bean (Table 8). In chickens,

Table 7

Gross energies (GE; MJ/kg as received) of L. cicera and L. sativus compared to ®eld pea (P. sativum), faba bean

(V. faba) and lupin (L. angustifolius)

L. cicera L. sativus Field pea Faba bean Lupin Source

16.6a ± ± 17.0a ± Flores and Castanon (1991)

16.6a ± 16.6a 16.3a 18.1a Abreu and Bruno-Soares (1998)

16.7 16.9 17.1 16.7 18.4 Farhangi (1996)

16.2 16.7 16.6 16.7 18.3 Hughes (unpublished)

± 15.9 16.2 15.9 ± Duke (1981)

± 16.1 16.6 16.5 ± Guada Vallepuga (1972)

± 16.1 ± ± ± Low et al. (1990)

± ± 16.8 16.8 18.1 Petterson et al. (1997)

16.5 16.3 16.6 16.6 18.2 Mean

a Estimated as 0.90 MJ/kg DM.

Table 8

Metabolisable energy (ME), digestible energy (DE), available metabolisable energy (AME) and true

metabolisable energy (TME) of L. cicera and L. sativus, all in MJ/kg DM, for sheep, cattle and poultry

(compared to ®eld pea (P. sativum), faba bean (V. faba) and lupin (L. angustifolius))a

Energy measure

(MJ/kg DM)

Source L. cicera L. sativus Field pea Faba bean Lupin

ME sheep i 11.4 11.0 11.0 11.4 10.7

ii 14.2 ± ± ± 14.4

iii ± 14.0 13.9 13.3 ±

iv ± ± 12.0 11.5 12.2

v ± 14.4 13.1 13.7 ±

vi ± 12.9 11.8 12.3 ±

DE sheep vii 16.2 ± 16.5 16.3 16.5

v ± 17.5 15.8 16.7 ±

vi ± 15.8 14.2 15.0 ±

ME cattle and sheep viii ± ± 13.5 13.1 ±

ME cattle iii ± 12.9 12.7 12.7 ±

ME poultry ix ± 11.3 ± ± ±

AME poultry x 13.4 11.3 12.0 ± 7.9

iv ± ± 11.7 11.2 10.4

TME poultry xi 11.5 ± ± 12.5 ±

a Source: (i) Farhangi (1996), (ii) White (unpublished), (iii) Kearl (1982), (iv) Petterson et al. (1997), (v)

Guada Vallepuga (1972), (vi) Zorita et al. (1972), (vii) Abreu and Bruno-Soares (1998), (viii) ARFC (1993), (ix)

Latif et al. (1975), (x) R.J. Hughes, personal communication, (xi) Flores and Castanon (1991).

12 C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27

available ME is slightly higher in the Lathyrus spp. than in lupin, but otherwise similar to

®eld pea and faba bean (Table 8).

4.1.5. Digestibility

Only a few studies have determined in vitro DMD and organic matter digestibilities

(OMD). Similarly, little has been done on in vivo digestibilities. Generally, but not

consistently, digestibilities of L. cicera are slightly lower than for L. sativus. Both are,

however, broadly similar to other commonly used grain legumes (Table 9). In vivo

measures were usually higher than in vitro measures.

Several studies that have examined in sacco dry matter degradabilities have shown that

L. cicera and L. sativus have similar values to other commonly used grain legumes

(Table 6). However, the parameters differ, particularly with lupin, which had a small

water soluble fraction.

4.2. Antinutritional factors

In common with all grain legumes there are a range of antinutritional factors (ANFs)

found in L. cicera and L. sativus grain. The ANFs commonly found in grain legumes

include: tannins, phytic acid, oligosaccharides, protease inhibitors (trypsin and

chymotrypsin inhibitors), amylase inhibitors and lectins (Liener, 1989). ODAP is also

an ANF and is almost unique to the Lathyrus genus. There are only a small number of

published studies of levels and activities of ANFs, other than ODAP, in L. sativus (Latif

et al., 1975; Deshpande and Campbell, 1992; Aletor et al., 1994; Urga et al., 1995;

Srivastava and Khokhar, 1996; Wang et al., 1998), and less on L. cicera (Aletor et al.,

1994).

Table 9

In vitro dry matter digestibilities (DMD), in vitro organic matter digestibilities (OMD), in vivo DMD and in vivo

OMD in sheep of L. cicera and L. sativus (compared to ®eld pea (P. sativum), faba bean (V. faba) and lupin

(L. angustifolius))a

Digestibility

measure (%)

Sourceb L. cicera L. sativus Field pea Faba bean Lupin

In vitro DMD i 82.1 ab 79.9 ab 82.7 a 80.3 ab 78.7 b

ii 88.6 a 92.9 b ± ± ±

In vitro OMD i 85.5 a 89.3 b 85.4 a 83.2 c 85.4 a

ii 85.5 a 90.3 b ± ± ±

In vivo DMD i 93.6 a ± ± ± 96.7 a

iii 93.0 a ± ± ± 95.5 a

iv ± 95.9 a 85.7 b 90.9 b ±

In vivo OMD iii 94.5 a ± ± ± 96.5 a

iv ± 95.6 a 86.9 b 91.8 ab ±

v 90.0 a ± 91.1 a 91.7 a 86.0 b

a Within each row the values with different letters are signi®cantly different (P < 0:05).b Source: (i) Farhangi (1996), (ii) Aletor et al. (1994), (iii) White (unpublished), (iv) Zorita et al. (1972), (v)

Abreu and Bruno-Soares (1998).

C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 13

4.2.1. Proteinaceous ANFs

The proteinaceous ANFs are (i) trypsin and chymotrypsin inhibitors (both protease

inhibitors), respectively measured as trypsin inhibitor activity (TIA) and chymotrypsin

inhibitor activity (CTIA), (ii) amylase inhibitors and (iii) lectins. ODAP will also be

included under this heading, although ODAP is a non-protein amino acid and not strictly

a proteinaceous ANF.

4.2.1.1. ODAP. Until recent times animal feeding studies with L. sativus or L. cicera have

been performed with no knowledge of the role of ODAP in lathyrism. Therefore, in all

older studies of animal feeding (i.e. pre 1960s) the concentration of ODAP is unknown.

Recent studies have shown that ODAP concentrations can vary widely both within and

between the two species, however, environmental conditions are not as important as

genotype (Hanbury et al., 1999). Nonetheless, stresses such as salinity and drought

(Hussain et al., 1997) have been found to increase ODAP concentrations but are little

understood. Generally L. cicera has lower seed ODAP concentrations than L. sativus

(Table 10). Concentrations of ODAP in the seed can be particularly high in L. sativus land

races, up to 1.50% (Table 10).

1. TIA and CTIA

These inhibitors are destroyed in the rumen and so are not a problem for ruminant

animals. In monogastric species they can result in hypertrophy of the pancreas if

present in suf®cient quantities. There is often an increased production of S-containing

enzymes which are lost due to forming indigestible complexes. Animal growth rate is

commonly depressed by TIA and CTIA (Deshpande and Damodaran, 1990).

Due to different assay conditions, making comparisons between reported levels of

TIA and CTIA (Table 11) are dif®cult. The reported ranges are lower in L. cicera than

L. sativus (Aletor et al., 1994). Urga et al. (1995) claimed that measured TIA in

Table 10

ODAP content (% as received) mean and range of a number of lines of L. cicera and L. sativus grown at various

locations

L. cicera L. sativus Location Source

Mean (range) No. Mean (Range) No.

0.15 (NA)a 128 0.20 (0.16±0.25) 10 Spain Franco Jubete (1991)

0.16 (0.10±0.22) 24 0.49 (0.07±0.75) 70 Syria Abd El-Moneim (1994)

0.13 (0.09±0.16) 16 0.49 (0.33±0.59) 36 Syria Aletor et al. (1994)

0.18 (0.08±0.34) 96 0.39 (0.04±0.76) 407 Australia Hanbury et al. (1999)

± ± 0.88 (0.45±1.40) 172 Bangladesh Kaul et al. (1982)

± ± 0.72 (0.37±1.04) 10 Ethiopia Tekle Haimanot et al. (1993)

± ± 0.44 (0.28±1.50) 1187 India Pandey et al. (1995)

± ± 0.32 (0.18±0.52) 76 Chile Tay et al. (2000)

± ± NA (0.08±0.99) 73 China Chen cited by Campbell (1997)

0.16 0.46 Grand mean

a Not available.

14 C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27

L. sativus (Table 11) was considerably lower than for soybeans, common beans and

cowpeas, but higher than found in chickpeas, although the values in these species were

not reported.

The TIA data can be compared to that of other feed legumes (measured by similar

methods) to estimate a ranking for both L. cicera and L. sativus (Table 12). In

summary, the species rank in likely order of increasing TIA: ®eld pea, faba bean,

L. cicera, L. sativus, P. vulgaris, soybean. Soybean is widely used for animal feeding

but must be heated to destroy the protease inhibitors prior to feeding to monogastric

animals.

2. Amylase inhibitor activity

Amylase is the enzyme primarily involved in starch digestion in mammals.

Amylase inhibitors are thought to reduce amylase activity, but the extent to which they

are important is debated (Deshpande and Damodaran, 1990). Deshpande and

Campbell (1992) found in 100 lines of L. sativus that the range of amylase inhibitor

activity (AIA) was 3.6±91.4 units gÿ1 DM, substantially lower than the 330±

675 units gÿ1 DM found in P. vulgaris cultivars (Deshpande et al., 1982).

Table 11

Measured TIA and CTIA (units mgÿ1 DM) of L. cicera and L. sativus

L. cicera No. lines L. sativus No. lines Source

TIA 12.6±20.4 16 20.1±44.1 36 Aletor et al. (1994)

9.15±15.1 2 ± Hanbury (unpublished)

± 16.7±26.2 25 Urga et al. (1995)

± 133±174 100 Deshpande and Campbell (1992)

CTIA 21±31 2 ± Hanbury (unpublished)

± 0±23 100 Deshpande and Campbell (1992)

Table 12

Relative comparisons (%) of measured TIA of L. sativus and L. cicera in relation to ®eld pea (P. sativum), faba

bean (V. faba), Phaseolus vulgaris and soybean (G. max) (each relative comparison is made between similar

measurement techniques)a

Relative comparison Species TIA (%)

Field pea Faba bean L. cicera L. sativus P. vulgaris Soybean

1 ± ± ± 30 (i) 36 (i) 100 (i)

2 ± ± 32 (ii) 61 (ii) ± 100 (iii)

3 7 (iv) 18 (iv) ± ± 28 (iv) 100 (iv)

4 18 (v) 11 (v) ± ± 44 (v) 100 (v)

5 7 (vi) ± ± ± ± 100 (vi)

6 13 (vii) 5 (vii) 22 (viii) ± 100 (vii) ±

7 ± ± ± 56 (ix) 100 (x) ±

a Source: (i) Latif et al. (1975), (ii) Aletor et al. (1994), (iii) Smith et al. (1980), (iv) Deshpande and

Damodaran (1990), (v) Elkowicz and Sosulki (1982), (vi) Saini (1989), (vii) Petterson et al. (1997), (viii)

Hanbury (unpublished), (ix) Deshpande and Campbell (1992), (x) Deshpande et al. (1982).

C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 15

3. Lectins

Lectins are present in most legumes (Liener, 1989), they interfere with nutrient

digestion and absorption and increase wasteful protein synthesis, resulting in reduced

ef®ciency of nutrient utilisation. Levels in L. cicera and L. sativus are unknown,

however, Srivastava and Khokhar (1996) detected lectins in all of four lines of

L. sativus.

4.2.1.2. Proteinaceous ANF conclusions. Rotter et al. (1990) found that autoclaving feed

containing 82% L. sativus increased feed consumption and increased the efficiency of feed

utilisation by chickens. In a separate sample autoclaving for 2 h decreased the concen-

tration of ODAP from 0.24 to 0.11%. Such effects of heating are commonly known to occur

for lectins, TIA and CTIA (Saini, 1989; Wiryawan and Dingle, 1999). Latif et al. (1975)

found that heating could totally inhibit TIA in L. sativus. The extrusion of L. sativus (which

involves heating) before feeding to pigs removed any inhibitory effect on proteolytic

activity, including trypsin activity, in pancreatic homogenates (Kapica et al., 1998).

The effect of various kinds of heating on the levels of ODAP are not clear. Boiling

treatments seem to consistently reduce ODAP concentration by 30±90% (Tekle Haimanot

et al., 1993; Srivastava and Khokhar, 1996; Padmajaprasad et al., 1997; Akalu et al.,

1998). However, the effect of boiling is largely (though not wholly) due to the water

solubility of ODAP. Roasting has been reported to both increase ODAP concentration

(Tekle Haimanot et al., 1993) and to reduce it by 87% (Akalu et al., 1998). Akalu et al.

(1998) found that heating induced isomerisation of b-ODAP (the neurotoxically active

form) to a-ODAP (the benign form), however, there appeared to be an equilibrium of

�60% of total ODAP in the b-ODAP form, irrespective of heating time. From the human

nutrition perspective further research on reducing ODAP content during Lathyrus food

preparation is warranted. Given the variable results and the techniques required (possibly

boiling) the pre-treatments are probably not practical for animal feeding purposes. The

availability of low ODAP cultivars also reduces the need for such pre-treatment of animal

feeds.

The results of heat treatment of L. sativus indicate that the protease inhibitors are

inactivated as observed in other grain species. It would be desirable not to require heat

treatment, however possible reductions in ODAP content could also occur. The presence

of lines of negligible TIA indicates the potential for further reductions through breeding.

There is insuf®cient data on the range of CTIA in either L. sativus or L. cicera, although

with wider testing variation is highly likely to be found, given the variation present in

other grain legume species. Such variation can be exploited in breeding programs.

4.2.2. Tannins

Tannins are polyphenolic compounds of two classes: low molecular weight

hydrolysable and higher molecular weight non-hydrolysable (or condensed). It is

postulated that condensed tannins bind to proteins in the digestive tract and form

complexes which are frequently indigestible (Marquardt, 1989). The hydrolysable tannins

are often found to have little effect on digestibility.

Tannins in faba beans and ®eld peas are frequently localised in the seed coat

(Marquardt, 1989; Gatel and Grosjean, 1990), with high tannin levels in darker seed coats

16 C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27

than lighter ones. Similarly, Deshpande and Campbell (1992) found that white or cream

coloured seeds of L. sativus were associated with low tannin levels (both condensed and

total), whereas seed with darker seed coats generally had high tannin levels. Similar

observations regarding L. sativus were made by Urga et al. (1995) and Wang et al. (1998).

In L. sativus lighter seeds are associated with white ¯ower colour (Jackson and Yunus,

1984), consequently the selection of white ¯ower colour could be used to reduce tannin

contents.

The range of condensed tannins in the literature is from undetectable to 0.77%

(Table 13), with a smaller range in L. cicera than in L. sativus. This may be a result of the

smaller number of measurements and/or little selection of L. cicera in comparison to

L. sativus lines. Unlike L. sativus, ¯ower colour in L. cicera does not vary greatly (Franco

Jubete, 1991; Hanbury et al., 1995) and may be related to the small variation in tannin

content. There is considerable scope for improvement of varieties with negligible condensed

tannin levels. In the case of L. sativus, much suitable germplasm is already identi®ed.

4.2.3. Phytate

Phytate is a cyclic compound that chelates with mineral ions (e.g. Ca, Mg, Zn, Fe) and

forms compounds not readily absorbed in the intestine (Liener, 1989), thereby reducing

animal performance. It is destroyed in the rumen and so is not a nutritional problem for

ruminants. The range 0.49±1.09% in the two Lathyrus spp. (Table 14) is high in

comparison to ®eld pea (0.15±0.70%) and faba bean (<0.01±1.04%; Petterson et al.,

1997).

Table 13

Condensed tannins contents (catechin equivalents, % as received) in L. cicera and L. sativus

Species Condensed tannins No. lines Source

Mean Range

L. cicera 0.36 0.27±0.55 16 Aletor et al. (1994)

0.68 0.59±0.77 2 Hanbury (unpublished)

L. sativus 0.12 0.00±0.44 100 Deshpande and Campbell (1992)

0.21 0.00±0.50 36 Aletor et al. (1994)

0.64 0.46±0.77 25 Urga et al. (1995)

0.31a 0.08±0.47a 9 Wang et al. (1998)

a Estimated as 0.90 of % DM.

Table 14

Phytate concentrations (% as received) in L. cicera and L. sativus

Species Phytate (%) No. lines Source

Mean Range

L. cicera 0.80 0.80±0.81 2 Hanbury (unpublished)

L. sativus 0.71 0.49±0.96 25 Urga et al. (1995)

1.07 1.03±1.09 4 Srivastava and Khokhar (1996)

C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 17

4.2.4. Oligosaccharides

Oligosaccharides are digested in the rumen but are indigestible to monogastric animals

and lead to ¯atulence. High levels of oligosaccharides can impair nutrition and lead

to distress and discomfort in animals. In two lines of L. cicera, oligosaccharide levels

were both 3.6% (Hanbury, unpublished), comparable to a range 3.0±4.8% in ®eld pea

and 2.6±3.3% in faba bean (Petterson et al., 1997). Kuo et al. (1995) found

oligosaccharide content in L. sativus to be 6.1% which they compared to faba bean

with a mean of 3.4%.

4.2.5. ANF conclusions

The presence of ANFs is ubiquitous in grain legumes, consequently ANFs do not

preclude the use of L. cicera and L. sativus as feed grain. However, improvement on

cultivars is desirable and, on the basis of variation that exists in the germplasm, there is

considerable scope for rapid improvement. Total reduction of ANFs may not be desirable

as they can also function as protection against disease and pest attack.

In the case of trypsin inhibitors, chymotrypsin inhibitors, tannins and phytate in L.

cicera and L. sativus variation within the germplasm is already available, or likely to be

available on the basis of known variation among other grain legume species. This

indicates that substantial improvements in L. cicera and L. sativus cultivars can be made.

Most of the ANFs, other than ODAP, currently identi®ed are in quantities less than those

already encountered in other common grain legumes and are consequently unlikely to

cause any serious concerns when used as animal feeds. Heating may be used to reduce the

level of proteinaceous ANFs and ODAP. The degree that this is necessary needs to be

determined by feeding studies. It is highly likely that improvements in cultivars will

lessen any need for heat treatments.

4.3. Animal feeding studies

4.3.1. General

As for human food there are many historical references to the use of Lathyrus spp. as

animal feed or fodder, principally L. sativus, L. cicera, L. ochrus and L. clymenum. Use of

L. sativus and L. cicera is referred to by Columella in the ®rst century A.D. (PenÄa-

Chocarro and Zapata PenÄa, 1999).

Because of concerns of human lathyrism there has been an emphasis in many

countries to develop L. sativus cultivars with lower ODAP levels (Roy et al., 1993;

Campbell et al., 1994) with some success. Consequently, recent animal feeding studies

have been able to both quantify the amount of ODAP in the diet and provide a low ODAP

intake at higher inclusion rates of L. sativus. Few studies of L. cicera as animal feed have

been conducted. Due to the possible high variability in ODAP content in the lines used in

older studies their results should be interpreted cautiously. Lathyrism can occur in both

monogastrics and ruminants. Whether this can be avoided in low ODAP Lathyrus

spp. lines and what constitutes a safe dose of ODAP in any species of animal is not

certain.

Observations on the effects on different animal species when fed on Lathyrus spp. of

unknown ODAP content differ. There is some evidence that rumen micro-organisms may

18 C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27

be able to degrade ODAP. Horses are noted as being very susceptible to lathyrism with

symptoms of paralysis of the hind limbs and sometimes dying, following heavy grazing

or feeding on Lathyrus spp. seed (Stockman, 1932; Steyn, 1933; LoÂpez Bellido, 1994).

There is anecdotal evidence of pigs, sheep and cattle having died due to lathyrism after

being turned into Lathyrus spp. ®elds (Stockman, 1932). He also claims that pigs may

thrive on a pure diet of Lathyrus spp. seed, despite developing weakness in the hind legs.

Monkeys can be affected similarly to humans by consumption of L. sativus and death

sometimes results (Rao et al., 1967). It is reported that many species of birds are readily

affected by lathyrism when consuming Lathyrus spp. seed (Stockman, 1932), although

Franco Jubete (1991) reported that in Spain doves fed avidly on L. cicera with no obvious

ill-effects. Lewis et al. (1948) fed L. sativus and L. cicera to young rats at 50% of food

intake for 7±21 weeks and did not induce any lathyritic symptoms, growth rates were

similar to those fed a diet based on ®eld peas. Basu et al. (1937) found no lathyrism

symptoms in rats fed 15% L. sativus for 8 weeks, growth rates were lower than those fed

®eld peas.

According to reports from Spain (LoÂpez Bellido, 1994) occasional consumption of

L. sativus or L. cicera grain does not harm horses or sheep. In small areas of Spain, where

these species are still cultivated both L. sativus and L. cicera grain is fed to stock,

sometimes with the exception of pigs (PenÄa-Chocarro and Zapata PenÄa, 1999). In sheep

both L. sativus and L. cicera grain are often used for gestating females, fattening lambs

and serving males; L. cicera can be included at up to 50% of the feed ration with no

symptoms of lathyrism (LoÂpez Bellido, 1994). Up to 350 g of L. cicera seed per day is

fed to lactating ewes by Spanish shepherds without harmful effects (Franco Jubete, 1991).

Tekle Haimanot et al. (1997) reported that in a small study most horses, donkeys, goats

and sheep developed spasticity in the hind limbs after 1±3 years feeding on L. sativus

grain. They noted that the new born goats and sheep were quite sensitive to lathyrism, the

symptoms being evident after 1±3 months. Cattle producers in northern Spain have used

L. cicera grain widely, with the peak area of production 24 000 ha in 1983±1986 (Franco

Jubete, 1991).

Although levels of ODAP were not reported in the above mentioned studies, evidence

exists indicating that rumen micro¯ora adapt to ODAP and break it down. Bacteria have

been isolated from soil sludge which can use ODAP as their sole carbon and nitrogen

source (Yadav et al., 1992). In sheep, tolerance to L. sylvestris in their diet seems due to

changes in the rumen contents (Rasmussen et al., 1992), presumably increasing

breakdown of DABA, a neurotoxin chemically similar to ODAP (Fig. 1). Fermenting

L. sativus seeds with Aspergillus oryzae and Rhizopus oligosporus for 48 h each has been

shown to reduce ODAP concentration by >90% (Kuo et al., 1995). Farhangi (1996)

incubated L. sativus and L. cicera grain in sheep rumen ¯uid and reported a rapid

disappearance of ODAP (>90% in 4 h), supporting the idea that certain rumen micro-

organisms can destroy the toxin.

There are only a small number of feeding studies in which ODAP levels have been

measured or estimated, and each of these will be discussed. Using L. sativus lines of seed

with a ODAP content of �0.08%, no symptoms of lathyrism were observed in donkeys,

pigs or sheep when fed as 50±80% of daily intake for 180±250 days (Chen referred by

Campbell, 1997); details are not available.

C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 19

4.3.2. Chickens

Low et al. (1990) found that inclusion of low ODAP L. sativus grain at 82% of the diet

for up to 4 weeks (commenced at age 7 days) did not induce any symptoms of lathyrism

in chickens. Control chickens fed a wheat/soybean based diet grew more rapidly. The

ODAP concentration in the seed used was not measured, although the line was known to

have low levels (mean 0.13%), low variation within a line is consistent in both L. sativus

and L. cicera (�30%; Hanbury et al., 1999).

Rotter et al. (1991) fed high (0.27%), medium (0.22%) and low (0.13%) ODAP lines of

L. sativus to chickens at 20±80% of the diet. They found that an increased proportion of

L. sativus seed in the diet of young chickens decreased weight gain, feed intake and

ef®ciencies of feed conversion (feeding commenced at age 7 days). At 20 and 40%

proportions there were minor or no differences to a wheat/soybean diet. However, using

0.27% ODAP seed generally resulted in decreased weight gain, feed intake and

ef®ciencies of feed conversion, compared to lower ODAP seed. Since increasing the

proportion of L. sativus above 40% (irrespective of ODAP concentration) also affected

the chickens it can be concluded that there were ANFs in the seed (other than ODAP)

which were not characterised.

4.3.3. Pigs

Castell et al. (1994) fed starter pigs (15±35 kg liveweight) high ODAP (0.30% in the

seed) L. sativus at up to 40% of the feed ration. The increased inclusion rate of L. sativus

reduced average daily weight gain (ADG) by up to 25%, decreased ef®ciency of feed

conversion by up to 10% and reduced voluntary feed intake (VFI) by up to 19% in linear

dose responses. Heart and spleen weights as a proportion of liveweight were also

signi®cantly reduced by the increased level of L. sativus. Castell et al. (1994) also fed

L. sativus to grower-®nisher pigs (25±100 kg liveweight) and reported a signi®cant linear

reduction in ADG and VFI with increasing proportion of L. sativus (up to 30% of intake).

In two experiments, both high (0.27%) and low (0.09%) ODAP lines were used, and it

was found that increased concentration of ODAP signi®cantly reduced ADG and VFI

independently of the inclusion rate of L. sativus in the diet. There was a signi®cant

linear effect of increased L. sativus inclusion rate on increases in liver and kidney

weight relative to liveweight, differing from observations in starter pigs. Scores for visual

appeal of meat fell slightly with increased inclusion rates. Following slaughter no

evidence could be seen of degeneration of the spinal cord or nerve tissue indicative

of neurolathyrism. No trace of ODAP could be found in loin samples at a detection

level of 100 ng gÿ1. It can be concluded from this work that increased ODAP

concentration (as varied by concentration of ODAP in L. sativus) probably reduced

pig performance. However, other ANFs may possibly have been at higher levels in

the higher ODAP L. sativus. The inclusion rate of L. sativus had a much greater effect

than ODAP level, implying that ANFs other than ODAP were more important in reducing

growth rates.

In contrast with the results of Castell et al. (1994) using L. sativus, Mullan et al. (1999)

fed L. cicera (0.09% ODAP) to pigs from 15 to 110 kg liveweight at substitution rates up

to 30% of the diet, diets were matched for sulphur amino acids. In comparison to the

standard soybean based diet there was no difference in ADG, VFI or feed conversion ratio

20 C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27

(FCR) at any substitution rate. Liver and kidney weights were also unaffected. No

indications of lathyrism were observed. Weaner pigs (5±13 kg liveweight) showed

no signs of lathyrism and no difference in ADG, VFI and FCR to controls, when fed

L. cicera (0.10% ODAP) at up to 15% of their diet (Mullan, unpublished). When

fed L. cicera at 20% of the diet ADG was 10% lower with similar increases in FCR,

probably due to the high levels of plant protein in their immature digestive systems.

4.3.4. Sheep

Farhangi (1996) compared effects of whole L. cicera grain (0.17% ODAP) to lupin

(Lupinus angustifolius) grain in two experiments with sheep. In experiment 1, 12 mature

Merino wethers were fed diets containing 15% either whole L. cicera or lupin grain for 17

days. No signs of toxicity were observed and there were no differences in VFI due to the

treatments. In experiment 2, a total of eight immature Merino wethers were fed diets of

25% L. cicera or lupin for 73 days. No gross signs of neurolathyrism were reported.

However, feed intake and growth rate were reduced by 7 and 30%, respectively, and wool

growth by 19% in sheep fed the L. cicera diet. The small number of sheep in the

experiments was a problem in obtaining signi®cant results, and only the wool growth

differences were statistically signi®cant (P < 0:05) in experiment 2.

White (unpublished) compared immature Merino wethers fed L. cicera cv. Chalus

(0.10% ODAP) or lupin, ad libitum over a 10-week period. L. cicera and lupin were fed at

two rates, 35 and 70% of the diet, the remainder being hay. There were 20 sheep per diet

group, fed individually. The sheep fed L. cicera showed greater liveweight gains, dressed

carcass weights, VFI and ef®ciencies of feed conversion than those fed lupins.

Ef®ciencies of feed conversion for 35 and 70% lupin diets were 10.6 and 11.5,

respectively, and for 35 and 70% L. cicera diets were 11.6 and 13.2%, respectively. There

were no indications of animal ill health in behaviour, carcasses or biochemical analyses

conducted throughout the experiment. Quality testing of meat showed equal or better

results for L. cicera than lupins and wool growth was similar for all diets. Overall, the

results indicated that sheep fed the L. cicera diets performed better than those fed the

lupin diets.

5. Conclusions

5.1. Animal feeding conclusions

The pig feeding studies indicate that grain of Lathyrus spp. of low ODAP

concentrations can be fed at 30% of the diet without any effect on animal performance.

However, L. sativus may have higher levels of ANFs (possibly TIA and CTIA, Table 11)

since similar inclusion rates at the same ODAP concentration (0.09%) reduced growth

rates using L. sativus (Castell et al., 1994) but not using L. cicera (Mullan et al., 1999).

Younger pigs do not perform optimally if fed more than 15% L. cicera (0.09% ODAP),

but this is probably due to sensitivity to plant protein, not to ODAP.

Poultry seem able to tolerate up to 40% of their diet of L. sativus of moderate ODAP

concentrations (0.27%) with minor reductions in growth. Above 40% there appears to be

C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 21

signi®cant effects of ANFs other than ODAP. There are no data on poultry performance

using L. cicera.

Both pigs and poultry showed depressed performance when high ODAP (0.27%)

L. sativus line were fed. Whether this was due to ODAP or other ANFs in the Canadian

varieties used is unclear. Further characterisation of the ANFs in both L. sativus and

L. cicera is necessary to separate the effects of ODAP from those of other ANFs. Until

this is performed higher ODAP lines (�0.15% or higher) should be avoided.

Sheep, and presumably other ruminants, can tolerate high levels of inclusion (up to

70% of 0.09% ODAP L. cicera) with no reduction in performance. ODAP and other

ANFs are probably broken down in the rumen. It is unlikely that ANFs other than ODAP

in any lines of L. sativus and L. cicera will signi®cantly affect ruminants. Since a 70%

inclusion rate is unlikely to be used in practical ruminant feeding higher ODAP varieties

could certainly be tolerated at inclusion rates below 70% (i.e. in this case if the intake of

ODAP does not exceed 0.063% of the diet in sheep of 35±48 kg liveweight).

Caution should be taken when using L. cicera or L. sativus in the diet of young animals

because they are thought to be more susceptible to ODAP than older animals. However,

the evidence for this is inconclusive, and needs to be veri®ed by experiment. Young pigs

can tolerate low ODAP (0.09%) L. cicera at rates (up to 15% of diet) used for other grain

legumes, but they may not be tolerant to higher levels of ODAP. Further comparisons

between Lathyrus spp. and other grain legumes considered safe (e.g. ®eld peas) need to

be performed using young animals.

5.2. General conclusions

The serious consequences of lathyrism for animals means that caution must be

exercised in feeding recommendations. There is suf®cient evidence to justify the

conclusion that safe feeding levels (summarised in Section 5.1) over extended periods are

possible with the reduced ODAP levels of cultivars and germplasm now available.

However, reduction in animal growth rates due to both ODAP and other ANFs have been

recorded. Similarly to other commonly used grain legumes, the heating of L. cicera and

L. sativus will reduce the level and activities of the proteinaceous ANFs, which are

particularly important for the monogastric species, also with possible reductions in ODAP

content. Little improvement in ANFs (other than ODAP) has been attempted in breeding

of either L. cicera or L. sativus. The improvement of cultivars is possible in a short time

frame, given the variation already recorded and available to breeding programs,

particularly in L. sativus. Experience with other species of grain legumes indicates that

variation in the known ANFs will be present in the germplasm. The germplasm for both

Lathyrus species is large, to date relatively unutilised and, particularly for L. sativus,

highly variable.

Compositions of both L. cicera and L. sativus are generally similar to ®eld pea; apart

from the presence of ODAP, and their generally higher protein and ANF levels. Feeding

data already shows that current cultivars can perform as well as industry standard

ingredients. This indicates that rapid exploitation of these species in the feed industry

is possible given experimentally established feeding recommendations. Since both

L. sativus and L. cicera are well adapted to large areas of southern Australia and other

22 C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27

Mediterranean-type environments the potential of a rapidly developed market for grain

would be one incentive for growers in these areas to adopt these crop options, particularly

for those attempting to replace pasture legume rotations with low input grain legume

crops.

Acknowledgements

We would like to thank Mr. Bob Hughes and Mr. Peter Zviedrans, South Australian

Research and Development Institute and Mr. Miyan Shahajahan, University of Adelaide

for GE and AME data. We would also like to thank the Grains Research and Development

Corporation, CLIMA, Agriculture Western Australia and CSIRO, Division of Animal

Production for providing funds and facilities.

References

Abd El-Moneim, A.M., 1994. Evaluation of BOAA content in new lines of Lathyrus spp. International Centre

for Agricultural Research in the Dry Areas Annual Report 1994, Germplasm Program Legumes. ICARDA,

Aleppo, pp. 206±207.

Abreu, J.M.F., Bruno-Soares, A.M., 1998. Chemical composition, organic matter digestibility and gas

production of nine legume grains. Anim. Feed Sci. Technol. 70, 49±57.

Adsule, R.N., Kadam, S.S., Salunkhe, D.K., 1989. Lathyrus bean. In: Salunkhe, D.K., Kadam, S.S. (Eds.), CRC

Handbook of World Food Legumes: Nutritional Chemistry, Processing Technology, and Utilization, Vol. 2.

CRC Press, Boca Raton, FL, pp. 115±130.

Akalu, G., Johansson, G., Nair, B.M., 1998. Effect of processing on the content of b-N-oxalyl-a,b-

diaminopropionic acid (b-ODAP) in grasspea (Lathyrus sativus) seeds and ¯our as determined by ¯ow

injection analysis. Food Chem. 62, 233±237.

Aletor, V.A., Abd El-Moneim, A., Goodchild, A.V., 1994. Evaluation of the seeds of selected lines of three

Lathyrus spp. for b-N-oxalylamino-L-alanine (BOAA), tannins, trypsin inhibitor activity and certain in vitro

characteristics. J. Sci. Food Agric. 65, 143±151.

Allkin, R., MacFarlane, T.D., White, R.J., Bisby, F.A., Adey, M.E., 1985. The geographical distribution of

Lathyrus: issue 1. Vicieae Database Project Publication No. 6. University of Southampton.

ARFC, 1993. Energy and Protein Requirements of Ruminants. CAB International, Wallingford.

Attal, H.C., Kulkarni, S.W., Choubey, B.S., Palkar, N.D., Deotale, P.G., 1978. A ®eld study of lathyrism-some

clinical aspects. Indian J. Med. Res. 67, 608±615.

Barrow, M.V., Simpson, C.F., Miller, E.J., 1974. Lathyrism: a review. Quart. Rev. Biol. 49, 101±128.

Basu, K.P., Nath, M.C., Mukherjee, R., 1937. Biological value of the proteins of soyabean, ®eld pea, and

Lathyrus sativa. By the balance sheet and growth methods. Indian J. Med. Res. 24, 1001±1026.

Bell, E.A., 1962. Associations of ninhydrin-reacting compounds in the seeds of 49 species of Lathyrus.

Biochem. J. 83, 225±229.

Bell, E.A., 1964. Relevance of biochemical taxonomy to the problem of lathyrism. Nature 203, 378±380.

Campbell, C.G., 1997. Grass Pea. Lathyrus sativus L. Promoting the conservation and use of underutilized and

neglected crops. 18. Institute of Plant Genetics and Crop Plant Research, Gatersleben/International Plant

Genetic Resources Institute, Rome.

Campbell, C.G., Mehra, R.B., Agrawal, S.K., Chen, Y.Z., Abd El-Moneim, A.M., Khawaja, H.I.T., Yadov, C.R.,

Tay, J.U., Araya, W.A., 1994. Current status and future research strategy in breeding grasspea (Lathyrus

sativus). Euphytica 73, 167±175.

Castell, A.G., Cliplef, R.L., Briggs, C.J., Campbell, C.G., Bruni, J.E., 1994. Evaluation of lathyrus (Lathyrus

sativus L.) as in ingredient in pig starter and grower diets. Can. J. Anim. Sci. 74, 529±539.

C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 23

Chandna, M., Matta, N.K., 1994. Studies on changing protein levels in developing and germinating seeds of

Lathyrus sativus L. J. Plant Biochem. Biotechnol. 3, 59±61.

Cheema, P.S., Malathi, K., Padmanaban, G., Sarma, P.S., 1969. The neurotoxicity of b-N-oxalyl-a,b-

diaminopropionic acid, the neurotoxin from the pulse Lathyrus sativus. Biochem. J. 112, 29±33.

Choudhury, K., Rahman, M.M., 1973. Fatty acids in different pulses produced and consumed in Bangladesh. J.

Sci. Food Agric. 24, 471±473.

Deshpande, S.S., Campbell, C.G., 1992. Genotype variation in BOAA, condensed tannins, phenolics and

enzyme inhibitors of grass pea (Lathyrus sativus). Can. J. Plant Sci. 72, 1037±1047.

Deshpande, S.S., Damodaran, S., 1990. Food legumes: chemistry and technology. Adv. Cereal Sci. Technol. 10,

147±241.

Deshpande, S.S., Sathe, S.K., Salunkhe, D.K., Cornforth, D.P., 1982. Effects of dehulling on phytic acid,

polyphenols and enzyme inhibitors of dry beans (Phaseolus vulgaris L.). J. Food Sci. 47, 1846±1850.

Dhiman, T.R., Sharma, V.K., Narang, M.P., 1983. Evaluation of `Khesari dhal' (Lathyrus sativus) in calf starter.

Agric. Wastes 8, 1±8.

Duke, J.A., 1981. Handbook of Legumes of World Economic Importance. Plenum Press, New York.

Elkowicz, K., Sosulki, F.W., 1982. Antinutritive factors in eleven legumes and their air-classi®ed protein and

starch fractions. J. Food. Sci. 47, 1301±1304.

Erskine, W., Smartt, J., Muehlbauer, F.J., 1994. Mimicry of lentil and the domestication of common vetch and

grass pea. Econ. Bot. 48, 326±332.

Farhangi, M., 1996. The nutritional value of Lathyrus cicera grain for sheep. M.Sc. (Animal Production) Thesis.

University of Adelaide.

Farrell, D.J., 1997. Where in the world will we ®nd the ingredients to feed our livestock by the year 2007? In:

Corbett, J.L., Choct, M., Nolan, J.V., Rowe, J.B. (Eds.), Recent Advances in Animal Nutrition in Australia.

University of New England, Armidale, pp. 136±145.

Flores, M.P., Castanon, J.I.R., 1991. Effect of level of feed input on true metabolizable energy values and their

additivity. Poult. Sci. 70, 1381±1385.

Foster, J.G., 1990. Flatpea (Lathyrus sylvestris L.): a new forage species? a comprehensive review. Adv. Agron.

43, 241±313.

Franco Jubete, F., 1991. Los Titarros: El cultivo de Lathyrus en Castilla y LeoÂn. Junta de Castilla y LeoÂn.

Valladolid.

Gatel, F., 1994. Protein quality of legume seeds for non-ruminant animals: a literature review. Anim. Feed Sci.

Technol. 45, 317±348.

Gatel, F., Grosjean, F., 1990. Composition and nutritive value of peas for pigs: a review of European results.

Livest. Prod. Sci. 26, 155±175.

Getahun, H., Tekle Haimanot, R., 1997. Psychosocial assessment of lathyrism patients in rural Estie sub-district

of South Gondar administrative zone, northern Ethiopia. In: Tekle Haimanot, R., Lambein, F. (Eds.),

Lathyrus and Lathyrism, a Decade of Progress. University of Ghent, Belgium, pp. 35±37.

Getahun, H., Mekonnen, A., Tekle Haimanot, R., Lambein, F., 1999. Epidemic of neurolathyrism in Ethiopia.

Lancet 354, 306±307.

Grela, E.R., GuÈnter, K.D., 1995. Fatty acid composition and tocopherol content of some legume seeds. Anim.

Feed Sci. Technol. 52, 325±331.

Guada Vallepuga, J.A., 1972. Energia digestible y metabolizable de las semillas de leguminosas para los ovidos,

Vol.18. Anales de la Facultad de Veterinaria de Leon, Universidad de Oveido, pp. 401±471.

Guedes, C.M., Dias da Silva, A., 1996. CineÂtique de la deÂgradation dans le rumen de la matieÁre seÁche et de

l'azote de graines de leÂgumineuses meÂditerraneÂennes. Ann. Zootechnol. 45, 423±435.

Hamid, M.A., Kaul, A.K., Akanda, R.U., 1986. Lathyrism in Bangladesh. An agro-economic survey of two

lathyrism prone areas. Department of Economics, Rajshahi University, Rajshahi and Ford Foundation,

Dhaka.

Hanbury, C.D., Sarker, A., Siddique, K.H.M., Perry, M.W., 1995. Evaluation of Lathyrus germplasm in a

Mediterranean type environment in south-western Australia. CLIMA Occasional Publication No. 8, Perth.

Hanbury, C.D., Siddique, K.H.M., Galwey, N.W., Cocks, P.S., 1999. Genotype±environment interaction for seed

yield and ODAP concentration of Lathyrus sativus L. and L. cicera L. in Mediterranean-type environments.

Euphytica 110, 45±60.

24 C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27

Haque, A., Hossain, M., Lambein, F., Bell, E.A., 1997. Evidence of osteolathyrism among patients suffering

from neurolathyrism in Bangladesh. Nat. Toxins 5, 43±46.

Hugon, J., Ludolph, A.C., Spencer, P.S., 2000. b-N-oxalylamino-L-alanine. In: Spencer, P.S., Schaumburg, H.

(Eds.), Experimental and Clinical Neurotoxicology, 2nd Edition. Oxford University Press, New York,

pp. 925±938.

Hussain, M., Chowdhury, B., Haque, R., Lambein, F., 1997. Effect of water stress, salinity, interaction of cations,

stage of maturity of seeds and storage devices on the ODAP content of Lathyrus sativus. In: Tekle Haimanot,

R., Lambein, F. (Eds.), Lathyrus and Lathyrism, a Decade of Progress. University of Ghent, Belgium,

pp. 107±112.

Infascelli, F., Di Lella, T., Piccolo, V., 1995. Dry matter, organic matter and crude protein degradability of high

protein feeds in buffaloes and sheep, Zoot. Nutr. Anim. 21 (Suppl.), 89±94.

Jackson, M.T., Yunus, A.G., 1984. Variation in the grass pea (Lathyrus sativus L.) and wild species. Euphytica

33, 549±559.

Kapica, M., Valverde Piedra, J.L., Studzinski, T., Grela, E.R., 1998. Effect of dietary supplementation of raw and

extruded grass pea seeds (Lathyrus sativus L.) on activity of pancreatic enzymes in pigs. J. Anim. Feed Sci. 7

(Suppl. 1), 253±257.

Kaul, A.K., Islam, M.Q., Begum, K., 1982. Variability for various agronomic characters and neurotoxin content

in some cultivars of khesari (Lathyrus sativus L.) in Bangladesh. Bangladesh J. Bot. 11, 158±167.

Kearl, L.C., 1982. Nutrient requirements of ruminants in developing countries. International Feedstuffs Institute,

Utah State University, Logan.

Kislev, M.E., 1989. Origins of the cultivation of Lathyrus sativus and L. cicera (Fabaceae). Econ. Bot. 43, 262±

270.

Kuo, Y.-H., Bau, H.-M., Quemener, B., Khan, J.K., Lambein, F., 1995. Solid-state fermentation of Lathyrus

sativus seeds using Aspergillus oryzae and Rhizopus oligosporus sp. T-3 to eliminate the neurotoxin ODAP

without loss of nutritional value. J. Sci. Food Agric. 69, 81±89.

Kupicha, F.K., 1983. The infrageneric structure of Lathyrus. Notes from the Royal Botanic Garden Edinburgh

41, 209±244.

Lambein, F., Kuo, Y.-H., 1997. Factors affecting human susceptibility to neurolathyrism. In: Tekle Haimanot, R.,

Lambein, F. (Eds.), Lathyrus and Lathyrism, a Decade of Progress. University of Ghent, Belgium, pp. 9±13.

Lambein, F., Khan, J.K., Kuo, Y.-H., Campbell, C.G., Briggs, C.J., 1993. Toxins in the seedlings of some

varieties of grass pea (Lathyrus sativus). Nat. Toxins 1, 246±249.

Lambein, F., Haque, R., Khan, J.K., Kebede, N., Kuo, Y.-H., 1994. From soil to brain: zinc de®ciency increases

the neurotoxicity of Lathyrus sativus and may affect the susceptibility for the motorneurone disease

neurolathyrism. Toxicon 32, 461±466.

Latif, M.A., Morris, T.R., Jayne-Williams, D.J., 1975. Use of khesari (Lathyrus sativus) in chick diets. Br. Poult.

Sci. 17, 539±546.

Laurence, R.C.N., 1979. A comparison of the grain and protein yield potential of some annual grain legume

species in South Australia. Aust. J. Exp. Agric. Anim. Husb. 19, 495±503.

Lewis, H.B., Fajans, R.S., Esterer, M.B., Shen, C., Oliphant, M., 1948. The nutritive value of some legumes.

Lathyrism in the rat. The sweet pea (Lathyrus odoratus), Lathyrus sativus, Lathyrus cicera and some other

species of Lathyrus. J. Nutr. 36, 537±559.

Liener, I.E., 1989. Antinutritional factors in legume seeds: state of the art. In: Huisman, J., Van der Poel, T.F.B.,

Liener, I.E. (Eds.), Recent Advances of Research in Antinutritional Factors in Grain Legume Seeds. Pudoc,

Wageningen, pp. 6±13.

LoÂpez Bellido, L., 1994. Grain legumes for animal feed. In: HernaÂndez Bermejo, J.E., LeoÂn, J. (Eds.), Neglected

Crops: 1492 from a Different Perspective. FAO Plant Production and Protection Series No. 26. FAO, Rome,

pp. 273±288.

Low, R.K.-C., Rotter, R.G., Marquardt, R.R., Campbell, C.G., 1990. Use of Lathyrus sativus L. (var. Seminis

albi) as a foodstuff for poultry. Br. Poult. Sci. 31, 615±625.

Marquardt, R.R., 1989. Dietary effects of tannins, vicine and convicine. In: Huisman, J., Van der Poel, T.F.B.,

Liener, I.E. (Eds.), Recent Advances of Research in Antinutritional Factors in Grain Legume Seeds. Pudoc,

Wageningen, pp. 141±155.

McCarrison, R., 1926. A note on lathyrism in the Gilgit agency. Indian J. Med. Res. 14, 379±381.

C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 25

Mehta, T., Hsu, A.-F., Haskell, B.E., 1972. Speci®city of the neurotoxin from Lathyrus sativus as an amino acid

antagonist. Biochemistry 11, 4053±4063.

Mullan, B.P., Hanbury, C.D., Hooper, J.A., Nicholls, R.R., Hagan, C.R., Siddique, K.H.M., 1999. Lathyrus

(Lathyrus cicera): a potential new ingredient in pig grower diets. In: Corbett, J.L. (Ed.), Recent Advances in

Animal Nutrition in Australia, Vols. 12, 12A. University of New England, Armidale.

Murti, V.V.S., Seshadri, T.R., Venkitsubramanian, T.A., 1964. Neurotoxic compounds of the seeds of Lathyrus

sativus. Phytochemistry 3, 73±78.

Olney, J.W., Misra, C.H., Rhee, V., 1976. Brain and retinal damage from lathyrus excitotoxin, b-N-oxalyl-L-a,b-

diaminopropionic acid. Nature 264, 659±661.

Padmajaprasad, V., Kaladhar, M., Bhat, R.V., 1997. Thermal isomerisation of b-N-oxalyl-L-a,b-diaminopro-

pionic acid, the neurotoxin in Lathyrus sativus, during cooking. Food Chem. 59, 77±80.

Padmanaban, G., 1980. Lathyrogens. In: Liener, I.E. (Ed.), Toxic Constituents of Plant Foodstuffs, 2nd Edition.

Academic Press, New York, pp. 239±263.

Pandey, R.L., Chitale, M.W., Sharma, R.N., Kashap, O.P., Agrawal, S.K., Geda, A.K., Chandrakar, H.K.,

Agrawal, K.K., 1995. Catalogue on grasspea (Lathyrus sativus L.) germplasm. Department of Plant Breeding

and Genetics, Indira Gandhi Agricultural University, Raipur, Madhya Pradesh.

PenÄa-Chocarro, L., Zapata PenÄa, L., 1999. History and traditional cultivation of Lathyrus sativus L. and Lathyrus

cicera L. in the Iberian peninsula. Veget. Hist. Archaeobot. 8, 49±52.

Petterson, D.S., Sipsas, S., Mackintosh, J.B., 1997. The chemical composition and nutritive value of Australian

pulses. Grains Research and Development Corporation, Canberra.

Ramanujam, S., Sethi, K.L., Rao, S.L.N., 1980. Stability of neurotoxin content in khesari. Indian J. Genet. Plant

Breed. 40, 300±304.

Rao, S.L.N., Adiga, P.R., Sarma, P.S., 1964. The isolation and characterization of b-N-oxalyl-L-a,b-

diaminopropionic acid: a neurotoxin from the seeds of Lathyrus sativus. Biochemistry 3, 432±436.

Rao, S.L.N., Sarma, P.S., Mani, K.S., Rao, T.R.R., Sriramachari, S., 1967. Experimental neurolathyrism in

monkeys. Nature 214, 610±611.

Rasmussen, M.A., Foster, J.G., Allison, M.J., 1992. Lathyrus sylvestris (¯atpea) toxicity in sheep and ruminal

metabolism of ¯atpea neurolathyrogens. In: James, L.F., Keeler, R.F., Bailey, E.M., Cheeke, P.R., Hegarty,

M.P. (Eds.), Poisonous Plants. Proceedings of the Third International Symposium. Iowa State University

Press, Ames, IA, pp. 377±381.

Ravindran, V., Blair, R., 1992. Feed resources for poultry production in Asia and the Paci®c. II. Plant protein

sources. World Poult. Sci. J. 48, 205±231.

Ronda Lain, E., Morales Gallego, J.F., Otero CoreteÂs, J., 1963. ProporcioÂn de aminoaÂcidos contenidos en las

leguminosas en grano cultivadas en Espana. Rev. Nutr. Anim. 1, 24±32.

Rotter, R.G., Marquardt, R.R., Low, R.K.-C., Briggs, C.J., 1990. In¯uence of autoclaving on the effects of

Lathyrus sativus fed to chicks. Can. J. Anim. Sci. 70, 739±741.

Rotter, R.G., Marquardt, R.R., Campbell, C.G., 1991. The nutritional value of low lathyrogenic Lathyrus

(Lathyrus sativus) for growing chicks. Br. Poult. Sci. 32, 1055±1067.

Roy, D.N., 1981. Toxic amino acids and proteins from Lathyrus plants and other leguminous species: a literature

review. Nutr. Abstr. Rev. Ser. A 51, 691±707.

Roy, D.N., Spencer, P.S., 1989. Lathyrogens. In: Cheeke, P.R. (Ed.), Toxicants of Plant Origin, Vol. III. Proteins

and Amino Acids. CRC Press, Boca Raton, FL, pp. 169±201.

Roy, P.K., Ali, K., Gupta, A., Barat, G.K., Mehta, S.L., 1993. b-N-oxalyl-L-a,b-diaminopropionic acid

in somaclones derived from internode explants of Lathyrus sativus. J. Plant Biochem. Biotechnol. 2,

9±13.

Saini, H.S., 1989. Activity and thermal inactivation of protease inhibitors in grain legumes. In: Huisman, J., Van

der Poel, T.F.B., Liener, I.E. (Eds.), Recent Advances of Research in Antinutritional Factors in Grain

Legume Seeds. Pudoc, Wageningen, pp. 249±253.

SCA (Standing Committee on Agriculture), 1990. Recommended procedures for the examination of the

degradability of feed proteins by the arti®cial ®bre bag (in sacco) method. Feeding Standards for Australian

Livestock, Ruminants. CSIRO, Melbourne.

Senatore, F., Basso, F., 1994. Fatty acid and sterol composition from seeds of some Lathyrus ecotypes. Riv. Ital.

Sostanze Grasse 71, 567±569.

26 C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27

Shobhana, S., Sangawan, P.S., Nainwatee, H.S., Lal, B.M., 1976. Chemical composition of some improved

varieties of pulses. J. Food Sci. Technol. 13, 49±51.

Shourie, K.L., 1945. An outbreak of lathyrism in central India. Indian J. Med. Res. 33, 239±247.

Siddique, K.H.M., Hanbury, C.D., 1998. Introduction, evaluation and utilization of Lathyrus germplasm in

Australia. In: Mathur, P.N., Ramanatha Rao, V., Arora, R.K. (Eds.), Lathyrus Genetic Resources Network in

Asia. IPGRI, New Delhi, pp. 42±45.

Siddique, K.H.M., Loss, S.P., Herwig, S.P., Wilson, J.M., 1996. Growth, yield and neurotoxin (ODAP)

concentration of three Lathyrus species in Mediterranean-type environments of Western Australia. Aust. J.

Exp. Agric. 36, 209±218.

Siddique, K.H.M., Loss, S.P., Regan, K.L., Jettner, R.L., 1999. Adaptation and seed yield of cool season grain

legumes in Mediterranean environments of south-western Australia. Aust. J. Agric. Res. 50, 375±387.

Smith, C., Twaalfhoven, L., Van Megen, W., Hitchcock, C., 1980. The determination of trypsin inhibitor levels

in foodstuffs. J. Sci. Food Agric. 31, 341±350.

Spencer, P.S., Ludolph, A., Dwivedi, M.P., Roy, D.N., Hugon, J., Schaumburg, H.H., 1986. Lathyrism: evidence

for role of the neuroexcitary amino acid BOAA. Lancet ii, 1066±1067.

Srivastava, S., Khokhar, S., 1996. Effects of processing on the reduction of b-ODAP (b-N-oxalyl-L-2,3-

diaminopropionic acid) and anti-nutrients of khesari dhal, Lathyrus sativus, J. Sci. Food Agric. 71, 50±58.

Steyn, D.G., 1933. Lathyrus sativus L. (chickling vetch khesari Indian pea) as a stock food. Onderstepoort J. Vet.

Sci. 1, 163±171.

Stockman, R., 1932. The poisonous principle of Lathyrus and some other leguminous seeds. J. Hyg. 31, 550±

562.

Tay, J., Valenzuela, A., Venegas, F., 2000. Collecting and evaluating Chilean germplasm of grasspea (Lathyrus

sativus L.). FABIS Newsletter, in press.

Tekle Haimanot, R., Abegaz, B.M., Wuhib, E., Kassina, A., Kidane, Y., Kebede, N., Alemu, T., Spencer, P.S.,

1993. Pattern of Lathyrus sativus (grass pea) consumption and beta-N-oxalyl-a,b-diaminopropionic acid (b-

ODAP) content of food samples in the lathyrism endemic region of northwest Ethiopia. Nutr. Res. 13, 1113±

1126.

Tekle Haimanot, R., Getachew, T., Doyle, D., Kriek, N.P.J., Spencer, P.S., 1997. Preliminary report on the

development of an animal model for human neurolathyrism. In: Tekle Haimanot, R., Lambein, F. (Eds.),

Lathyrus and Lathyrism, a Decade of Progress. University of Ghent, Belgium, pp. 27±29.

Trabaud, J., MouhaÈrram, 1932. Le lathyrisme syrie est du au Lathyrus sativus. Lathyri syriens et libanals. Rev.

Med. FrancËaise 13, 449±450.

Urga, K., Fite, A., Kebede, B., 1995. Nutritional and antinutritional factors of grass pea (Lathyrus sativus)

germplasms. Bull. Chem. Soc. Ethiop. 9, 9±16.

Wang, X., Warkentin, T.D., Briggs, C.J., Oomah, B.D., Campbell, C.G., Woods, S., 1998. Total phenolics and

condensed tannins in ®eld pea (Pisum sativum L.) and grass pea (Lathyrus sativus L.). Euphytica 101, 97±

102.

Wiryawan, K.G., Dingle, J.G., 1999. Recent research on improving the quality of grain legumes for chicken

growth. Anim. Feed Sci. Technol. 76, 185±193.

Yadav, V.K., Santha, I.M., Timko, M.P., Mehta, S.L., 1992. Metabolism of the Lathyrus sativus L. neurotoxin, b-

N-oxalyl-L-a,b-diaminopropionic acid, by a pure culture of a soil-borne microbe. J. Plant Biochem.

Biotechnol. 1, 87±92.

Yunus, A.G., Jackson, M.T., 1991. The gene pools of the grass pea (Lathyrus sativus L.). Plant Breed. 106, 319±

328.

Zorita, E., Guedas, J.R., SuaÂrez, A., Guada, J.A., 1972. Digestibilidad y valor nutritivo de las semillas de ocho

leguminosas cultivadas para grano, Vol. 18. Anales de la Facultad de Veterinaria de Leon, Universidad de

Oveido, pp. 551±560.

C.D. Hanbury et al. / Animal Feed Science and Technology 87 (2000) 1±27 27