Caballero B. (ed.) Encyclopaedia of Food Science, Food Technology and Nutrition. Ten-Volume Set

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Molds See Mycotoxins: Classifications; Occurrence and Determination; Toxicology; Spoilage: Chemical and

Enzymatic Spoilage; Bacterial Spoilage; Fungi in Food – An Overview; Molds in Spoilage; Yeasts in Spoilage

Molluscs See Shellfish: Characteristics of Crustacea; Commercially Important Crustacea; Characteristics of

Molluscs; Commercially Important Molluscs; Contamination and Spoilage of Molluscs and Crustaceans;

Aquaculture of Commercially Important Molluscs and Crustaceans

Monosodium Glutamate See Taste Enhancers

MULTIPLE SCLEROSIS – NUTRITIONAL

MANAGEMENT

R Cichon and L Wadolowska, Warmia and Masuria

University in Olsztyn, Olsztyn, Poland

Background

0001 Multiple sclerosis (MS) belongs to the demyelinating

diseases, which comprise a group of neurologic dis-

orders. Demyelinating diseases have in common the

pathologic feature of local or patchy destruction of

myelin sheaths in the central nervous system accom-

panied by an inflammatory response. Destruction of

the myelin sheaths leads to dysfunction of the central

nervous system (CNS) in transmission of electrical

nerve impulses.

0002 The term ‘sclerosis’ is applied to the hardening of

the CNS and is called ‘multiple,’ because multiple

areas of optic nerves, brain and spinal cord undergo

sclerosis, whereby myelin is replaced with sclera and/

or scar tissue. The disease was first described by

Cruveilhier in 1835 under the name ‘sclerose en

plaque,’ in that the disease is marked by the appear-

ance of hard patches throughout the brain and spinal

cord. Its outstanding symptoms are weakness,

muscular incoordination, jerky movements of the

eyeballs, paralysis, and a curious, deliberate way of

speaking, known commonly as ‘scanning speech.’

The condition has periodic remissions and on the

whole tends to become worse, but is seldom an im-

mediate threat to life. The disease most commonly

strikes between the ages of 20 and 40 years, and

females account for 60–70% of cases. The average

age of onset of the first clinical episode of MS is in the

third and fourth decades. It is rare for the disease to

begin in childhood or beyond the sixth decade, but it

is not unknown.

Features of Multiple Sclerosis

0003MS is pleomorphic in its presentation. The clinical

picture is determined by the location of foci of

demyelination within CNS. Classic features include

impaired vision, nystagmus, dysarthria, decreased

perception of vibration and position, ataxia and in-

tension tremor, weakness or paralysis of one or more

limbs, spasticity, and bladder problems. Diagnosis is

based on the clinical presentation, neurological tests

and magnetic resonance imaging (MRI, to reveal the

presence of plaques). There are two main forms and

two subtypes of the disease: relapsing-remitting

MS (RRMS), chronic progressive MS (CPMS), and

secondary progressive and benign MS. In RRMS,

periods of acute worsening of symptoms are followed

by spontaneous improvement. In CPMS, there are no

clear-cut attacks, and the symptoms become steadily

worse. This form of MS might progress rapidly,

4034 MULTIPLE SCLEROSIS – NUTRITIONAL MANAGEMENT

causing severe disability and even premature death

within a few years. Secondary progressive MS is

described when RRMS becomes progressive, and

benign MS when an initial attack is never followed

by another. The criteria for the diagnosis of clinically

definite MS include a reliable history of at least two

episodes of neurologic deficit and objective clinical

signs of lesions at more than one site within the CNS.

Clinically probable MS is defined as either two

attacks with clinical evidence of one lession or one

attack with clinical evidence of two lesions. However,

classifications of MS are based on clinical phenomen-

ology, and the definitions of relapse, remission, and

progression are still imprecise.

0004 MS usually presents in the form of recurring

attacks of focal or multifocal neurologic disfunction,

reflecting lesions within the CNS. The disease begins

most commonly in early adult life. The frequency of

flare-ups is greatest during the first 3–4 years of the

disease, but a first attack may be so mild as to escape

medical attention, for example, blurred or double

vision. Once the initial symptoms disappear, they

may never recur, and a period of months or years

may pass before other symptoms appear, such as

weakness of certain muscles, unusual tiring of a

limb, minor interference with walking, muscle stiff-

ness, dizziness, loss of bladder control, and disturb-

ances in the senses of touch, pain, and heat. Each

symptom may appear and then disappear, only to

be followed by another. The disease continues to

progress, and eventually, the patient becomes

crippled and even bedridden. However, the progres-

sion and remission of MS are different for every indi-

vidual. Although occasional patients die within the

first few years of disease onset, most do not, and the

average survival from MS is more than 30 years after

the onset of disease.

Pathology

0005 In 1961, Swank proposed the hypothesis that a

dysfunction of the blood–brain barrier is a primary

damage defect in MS. Current opinion holds that

autoimmunity or viral infection is likely to be impli-

cated in their pathogenesis.

0006 Many scattered, discrete areas of demyelination,

termed plaques, are the pathologic hallmark of MS.

Plaques vary in size and may be found anywhere

in the white matter but typically occur in the para-

ventricular areas of the cerebrum and subpially,

and within the brainstem and spinal cord. The per-

ipheral nervous system is not affected. Many plaques

are clinically silent. In fact, some autopsy studies

indicate that 20% of MS cases are clinically silent

during life.

0007Active MS lesions feature T-lymphocyte and mono-

cyte–macrophage accumulations about venules and

at plaque margins is being destroyed. The invasion

of white matter by inflammatory cells is held respon-

sible for the myelin breakdown. They also function as

scavengers of myelin debris; fat-laden macrophages

may persist for months, perhaps years, after the acute

inflammatory response has subsided. Despite much

research, viral inclusions have not been detected.

Only limited regeneration of myelin occurs, and the

reason is unclear. There are probably several mechan-

isms responsible for recovery from an MS attack. The

pathologic features of MS fail to account for hour-to-

hour and day-to-day waxings and wanings in func-

tion so characteristic of the disease. Conduction of

impulses through demyelinated nerve is compromised

and is further altered by transient changes in the

internal milieu such as functuations in temperature

and electrolyte balance or by stress.

Etiology

0008The causes of MS remain unknown. A role for

immune-mediated or infectious factors has been pro-

posed, but data to support these postulates are incon-

clusive. Epidemiological studies have implicated an

interplay between genetic and environmental factors

in the etiology of MS. It has been suggested that

nutrition and food pattern, particularly high con-

sumption of animal fat and low intake of fish prod-

ucts may play a role in the etiology of MS. Recently,

studies have focused on long-chain polyunsaturated

fatty acids (LCPUFA) and vitamin D.

Epidemiology

0009Epidemiologic studies have established several facts

that ultimately will have to be incorporated into any

coherent theory of the disease. Neuroepidemiology

has played a fundamental role in the study of multiple

sclerosis by providing some etiologic clues, although

a definitive basis for the conclusive resolution of its

enigma is still lacking. Epidemiologic and genetic

studies have indicated that MS is probably caused

by multiple factors, both genetic and environmental,

none of which is individually sufficient, and appear to

act before adolescence – or possibly later – in genetic-

ally susceptible individuals. This unifying hypothesis

emphasizes the role of a genetic–racial susceptibility,

the importance of environmental factors, a possible

etiologic heterogeneity, and a lack of specificity of the

unknown endogenous and exogenous agents. Situ-

ations or events with biological plausibility, such

as childhood or adolescent infectious diseases, ex-

posures to geographic and sociocultural factors,

MULTIPLE SCLEROSIS – NUTRITIONAL MANAGEMENT 4035

nutritional habits, hypersensitivity, significant head

and spinal trauma, and other factors may contribute,

at different times, to the putative acquisition of MS,

trigger its onset, and modify its subsequent course.

0010 In general, the incidence in temperate climates

exceeds that in tropical zones, but variations within

regions with similar climates do exist; hence, the

effect is not simply one of latitude or temperature.

Geographically, MS describes three frequency zones.

High-frequency areas (characterized by a prevalence

of 30þ per 100 000) now comprise most of Europe,

Israel, Canada, northern USA, southeastern Australia,

New Zealand, and eastern Russia. Medium-frequency

areas include the southern USA, most of Australia,

South Africa, the southern Mediterranean basin,

Russia into Siberia, the Ukraine and parts of Latin

America. Prevalence rates of less than 5 per 100 000

are found in the rest of Asia, Africa, and northern

South America. The incidence of MS in northern

Europe, Canada, and the northern USA is approxi-

mately 10 new cases each year per 100 000 persons

between the ages of 20 and 50, two to three times

higher than that in Australia, New Zealand, and the

southern USA. MS is rare in Japan, elsewhere in the

Orient, and Africa. Some epidemiologic evidence also

suggests that persons emigrating from high- to low-

risk regions as children may be partially protected

from MS. Immigrants from high- to lower-risk areas

retain the MS risk of their birth place only if they are

at least 15 years old at the time of emigration. Those

from low- to high-risk areas increase their risk

even beyond that of the natives, with susceptibility

extending from about 11 to 45 years of age. MS

occurred in epidemic form in the North Atlantic

islands, particularly in the Faroe Islands, where the

first symptom onset was in 1943, heralding the first of

four successive epidemics at 13-year intervals. What

was transmitted is thought to be a specific, wide-

spread, persistent infection called primary multiple

sclerosis affection (PMSA), which only rarely leads

years later to clinical MS. The search for PMSA is best

attempted on the Faroes, where there are regions still

free of MS after 50 years. The data are consistent with

the existence of an environmental factor, possibly a

virus, and perhaps geographically restricted, that

influences the development of MS. Immunologic,

epidemiologic, and genetic data indicate that tissue

injury in MS results from an abnormal immune re-

sponse to one or more myelin antigens that develop in

genetically susceptible individuals after exposure to

an as-yet undefined causal agent.

0011 There is some evidence for genetic factors in mul-

tiple sclerosis. The evidence comes from epidemiolo-

gic studies, racial predilection, risk in family members

(sibs, half sibs, adoptees), and twin studies. MS is not

a Mendelian inherited disease; only the susceptibility

to the disease is inherited. MS seems to be an oligo-

or multigenic disorder with an apparently similar

phenotype for the different genes involved. A genetic

component in MS is indicated by an increased relative

risk to siblings compared with the general population

and an increased concordance rate in monozygotic

compared with dizygotic twins. Whole genome

screens conducted in different populations have

identified discrete chromosomal regions potentially

harboring MS-susceptibility genes.

Nutrition and Multiple Sclerosis

0012Specific nutritional therapy has been advocated for

a number of neurologic diseases of undetermined

etiology. In some of the disorders, improper or

inadequate nutrition is implicated. Therefore, dietary

manipulation constitutes the main therapeutic mode.

For instance, a low-fat diet has been recommended as

an effective means of reducing the incidence of

exacerbations in patients suffering from MS. How-

ever, objective evaluation of the efficacy of this treat-

ment modality has not yet been possible. In MS, a

combination of genetic and environmental factors,

including dietary factors, underlies the symptoms

and signs of neurologic dysfunction that can be ameli-

orated by changes in the diet and/or vitamin supple-

mentation.

0013Epidemiologic studies relating MS to nutritional

factors have revealed a possible link between the

incidence of the disease, total fat intake, and percent-

age of calories (of animal origin) consumed. A long-

term study carried out by Swank showed significantly

less deterioration and much lower death rates among

MS patients when they consumed less fat (20 g of fat

per day).

0014The results of prospective case-control studies

showed that some foods consumed at certain ‘critical’

ages could play a causal role in the oneset of MS. An

association was suggested between MS and high

consumption of bread and ‘pasta,’ butter and lard,

legume soup, horse flesh, coffee and tea in the period

from infancy to adolescence, and of eggs and wine

during adulthood. A possible autoimmune demyeli-

nating disease with lipid changes suggests a deficiency

of PUFA.

0015MS tends to be more prevalent in countries where

the use of animal fat is high. It has also been suggested

that the administration of unsaturated fatty acids,

such as linoleic or arachidonic acid, may reduce the

number and severity of MS attacks. This idea is based

on the observation that brain and spinal cord

obtained from patients who have died of MS is defi-

cient in unsaturated fatty acids and that linoleic and

4036 MULTIPLE SCLEROSIS – NUTRITIONAL MANAGEMENT

arachidonic acids tend to inhibit the lymphocyte–

antigen interaction, the cellular mechanism that may

enhance demyelination. Sensitized lymphocytes prob-

ably interact with myelin components in the affected

parts of the nervous system during an attack of MS.

That the ingestion of unsaturated fatty acids, such

as linoleic acid, affects the course of MS remains

unproved.

0016 Early epidemiological studies demonstrated a low

incidence of atheroslerotic, inflammatory, and auto-

immune diseases in Greenland Eskimos who con-

sumed diets high in marine-derived (n-3) PUFA.

Human studies have consistently demonstrated a de-

crease in production of pro-inflammatory cytokines

when moderate to high levels of marine-derived (n-3)

PUFA are taken orally. The decrease in production of

pro-inflammatory cytokines and eicosanoids contrib-

utes to the beneficial effect of fish oil in reducing the

pathogenesis of inflammatory and atherosclerotic dis-

eases. Essential fatty acids (EFA) are necessary for

normal immune function of humans and animals.

EFA deficiency impairs B- and T-cell-mediated re-

sponses. These impairments can be ameriorated by

the inclusion of EFA in the diet. The possibility that

polyunsaturated fatty acids have an immunosup-

pressant effect has led to the evaluation of

high-polyunsaturated fatty acids diets in MS, as neu-

rologic disorders of immune-inflammatory etiology

that affect CNS. a-Linolenic acid (C18:3 n-3) can be

converted to EPA (C20:5 n-3), which can replace

arachidonic acid in membrane phospholipids and

can be preferentially used by cyclooxygenase. This

results in the reduced production of prostaglandins

(PG) of the 2 series and leukotrienes of the 4 series.

Thus, the consumption of oils containing C18:3 n-3

might be associated with immunological changes.

This opinion is supported by many studies that have

shown immunological modulation following marine

oil consumption.

0017 Evidence on etiology in MS suggests that the preva-

lence depends on the interaction of two factors, diet

and exposure to visible sunlight. The dietary features

that may be beneficial include supplementation with

fish oils, avoidance of saturated fats, and the associ-

ated intake of antioxidants with unsaturated fatty

acids. Inhibition, by antioxidants, of the enzyme

lipoxygenase inhibits leukotriene synthesis, and the

presence of fish oils leads to the production of leuko-

trienes with less inflammatory properties. This is of

particular importance in the retina, where leuko-

trienes might be the underlying cause of retrobulbar

neuritis.

0018 A significant protective effect has been observed

with other nutrients, including vegetable protein,

dietary fiber, vitamin C, thiamin, riboflavin, calcium,

and potasium. With respect to specific foods (as op-

posed to nutrients), a higher intake of fruit juices was

inversely associated with risk. A protective effect was

also observed with cereal/bread intake; pork/hot dogs

and sweets/candy were positively associated with

risk. The study generally supports a protective role

for components commonly found in plants (fruit/

vegetable and grains) and increased risk with high-

energy and animal food intake.

0019An epidemiologic study on the relationship be-

tween mortality rates from MS for the period 1983–

1989 for 36 countries has shown that saturated fatty

acids, animal fat, animal minus fish fat, and latitude

correlated independently and positively with MS

mortality. The ratio of polyunsaturated fatty acids

to saturated fatty acids (P/S ratio) and the ratio of

unsaturated to saturated fatty acids (U/S ratio) correl-

ated independently and negatively with MS mortality.

The results support the data, at least partially, on an

association between certain dietary factors and MS.

0020For MS patients, good nutrition has the potential

to enhance the quality of life and reduce the risk of

lifestyle diseases and secondary conditions. Eating

patterns in patients with MS showed the need for

interventions to promote good nutrition among per-

sons with MS. Usually, nutritional intake for MS

patients is not optimal in many important areas.

0021Acute and chronic neurologic diseases of nonnutri-

tional origin that impair consciousness of motor func-

tions essential to adequate nutritional intake, such

as paralysis or weakness of the facial muscles, the

tongue, the pharynx, and the muscles of deglutition,

frequently require the temporary or permanent use of

a nasogastric tube or gastrostomy for the patient’s

well-being. These measures make possible proper

enteral nutrition and may, in fact, prove to be life-

saving. In most of these disorders, nutritional support

does not affect the basic pathogenesis of the disease.

The use of B-complex vitamin preparations for a

variety of acute and chronic neurologic diseases of

cryptic origin continues to be common medical prac-

tice. To date, however, there is no objective evidence

that this practice has any effect on the speed of recov-

ery of the afflicted nervous tissue.

0022Despite significant advances over previous decades

in the field of nutrition, large gaps remain in our

understanding of the role in the normal and abnormal

activity of the nervous system. More sensitive and

critical methods for the assessment of the nutritional

status of the nervous system and for the evaluation

of the dietary management of MS are essential for

more rational and effective therapeutic manipulation

(treatment).

0023Nutritional therapy consisting of vitamins and

other nutrients continues to be used in neurologic

MULTIPLE SCLEROSIS – NUTRITIONAL MANAGEMENT 4037

disorders of unknown cause, in spite of a total lack of

scientific rationale. The popularity of administering

large doses of vitamins (and other nutrients) as ther-

apy for chronic neurologic diseases of uncertain eti-

ology stems from the fact that experimentally induced

deficiencies of this nutrients in animals frequently

result in symptoms caused by reversible lesions of the

CNS. In most instances, the far-advanced lesions show

demyelination, a frequent finding in many human

neurologic diseases. However, considering the large

doses of vitamins consumed daily, for a variety of

reasons, by an ever–increasing number of people, vita-

min toxicity affecting the nervous system is relatively

rare. Of all the vitamins, only two – vitamin A and

pyridoxine – are known to produce adverse neurolo-

gic reactions when ingested in pharmacologic, rather

than recommended, nutritional doses.

0024 Patients who are being treated with drugs may

incur a significant degree of vitamin deficiency (D,

, and folic acid). The prolonged administration of

drugs may lead to a decrease in bone mineral content.

The drugs interact with the vitamin D and its active

forms, decreasing intestinal calcium absorption

and redistribution. The severity of demineralization

appears to be related to the dose of the drugs, a

deficiency of physical activity, and a lack of exposure

to sunlight. In general, the problem does not appear

to be of sufficient clinical importance to warrant the

routine vitamin D supplementation of patients with

MS drugs; however, the possibility should be borne in

mind, and vitamin D metabolites should be estimated

periodically in long-term patients with poor intake or

malabsorption.

0025 Studies with animals, tissue cultures, as well as

humans indicate that both the level and degree of

saturation of dietary fats influence inflammatory

and immunologic responses. Some of these immuno-

logic changes are associated with beneficial clinical

effects, for example, reduction in pro-inflammatory

cytokine by marine-derived (n-3) PUFA. Others might

not be desirable, for example, decreased T-cell-

mediated function by marine-derived (n-3) PUFA in

older people.

0026 Recommendations to increase PUFA intake should

be accompanied by appropiate recommendations for

an increase in antioxidant intake, in particular vita-

min E. Without adequate antioxidant protection, the

substitution of membrane fatty acids with highly oxi-

dizable (n-3) PUFA of fish oil, that is, EPA and DHA,

may potentiate the peroxidation of cellular mam-

branes. Foods high in polyunsaturates should contain

at least 0.6 mg of tocopherol equivalents per gram of

polyunsaturated fatty acids. Higher levels may be

necessary for fats rich in fatty acids containing more

than two double bonds.

0027In general, for MS patients, recommendations to

decrease dietary total fat intake, with the inclusion of

moderate amounts of (n-6 and n-3) PUFA with ad-

equate antioxidant nutrients should provide for a

competent immune response. The n-6 and n-3 fatty

acids have critical roles in the membrane structures

and as precursors of eicosanoids, which are potent

and highly reactive compounds. Various eicosanoids

have widely divergent, and often opposing, effects

on inflammatory processes and the immune system.

Since they compete for the same enzymes and have

different biological roles, the balance between the n-6

and n-3 fatty acids in the diet can be of considerable

importance. The ratio of linoleic to a-linolenic acid in

the diet should be between 5:1 and 10:1. Patients with

a ratio in excess of 10:1 should be encouraged to

consume more n-3 rich foods such as green leafy

vegetables, legumes, fish, and other seafood.

Dietary Management of Multiple Sclerosis

0028Although there have not been any valid clinical trials

supporting the efficacy of nutrition in delaying the

progression of MS, it is imperative that the dietitian

evaluates the nutritional health status and arranges a

patient’s diet. The nutritional management of patients

with MS is primarily concerned with ensuring that

their nutrient intake meets the requirements. The spe-

cific dietary modifications that are needed in some

patients, mostly because of drug therapy, are of

secondary importance. The principles of management

have to take in consideration the individual needs,

circumstances and difficulties. The current consensus

is that extreme dietary change should have no place in

the management of MS. Patients with MS should be

encouraged to follow a varied, well-balanced diet

based on good nutritional practice and principles for

the population in general. In order to achieve the

recommended dietary targets, considerable changes

in the dietary habits of the MS patient will be

required, usually necessitating:

0029increased intake of micronutrient-rich foods such

as fruits, vegetables, pulses, seeds, legumes, and

cereals. Leafy green vegetables may contribute

adequate amounts of antioxidative vitamins, e.g.,

vitamins E and C;

0030use of low-fat alternatives for full-fat milk and

dairy products;

0031replacing saturated fat spreads and cooking fats

with low-fat spreads and monounsaturated oils;

0032avoiding sugar-rich/fat-rich food group, such as

meat products, pastries, chips, snakes, cakes and

biscuits;

0033encouraging the consumption of all types of fish

and seafood; two portions of fish or seafood per

4038 MULTIPLE SCLEROSIS – NUTRITIONAL MANAGEMENT

week, including oily fish, are recommended to

secure a moderate increase intake of n-6 and n-3

fatty acids, in particular LCPUFA.

0034 An important consideration in the management of

all patients is their hydration status. The consumption

of at least six to eight glasses of fluid per day usually

meets the adequate fluid intake of a patient.

0035 Nutritional problems associated with MS vary

according to the symptoms of illness and the degree

of physical disability of patients. Dysphasia may

occur as the disease progresses, and the diet consist-

ency may need to be modified from solid to soft or

pure

ed foods and even thick liquids. Other problems

include impaired vision, dysarthria, and poor ambu-

lation, thus making eating less enjoyable because

meal preparation becomes a difficult task. In this

situation, single-serving or convenience foods often

permits independent preparation of meals. Given the

chronic nature of this disease, patients may require

enteral nutrition support.

0036 Neurogenic bladder is common, causing urinary

incontinence, urgency, and frequency. To minimize

these problems, it is helpful to distribute fluids evenly

throughout the waking hours and limit them before

bed. Some patients limit fluid intake severely to

decrease the frequency of urination, thus increasing

the risk of urinary tract infection.

0037 Neurogenic bowel can cause either constipation or

diarrhea, and the incidence of fecal impaction is

increased in MS. A diet that is high in fiber with

additional prunes and adequate fluid intake can mod-

erate these problems.

Supplement Usage

0038 Patients may be taking combinations of different

supplements in large doses, sometimes risking over-

dosage with fat-soluble vitamins. The types of supple-

ments likely to be used include evening primrose oil,

fish oil capsules, cod liver oil, and linseed oil. If a

well-balanced diet containing dietary sources of n-3

and n-6 fatty acids is consumed, additional supple-

ments of LC-PUFA sources, vitamins, and minerals

are unlikely to be necessary or beneficial. Patients

who wish to take supplements should be advised to

restrict these to one multiple multivitamin/mineral

preparation providing no more than the recom-

mended dietary allowance, rather than taking several

different types of supplement. In any case, it is best to

do this after consultation with the dietitian.

See also: Cholecalciferol: Properties and Determination;

Essential Fatty Acids; Fish Oils: Dietary Importance;

Vitamins: Overview

Further Reading

Antel JP and Arnason BGW (1987) Demyelinating diseases.

In: Braunwald E et al. (eds.) Harrison’s Principles of

Internal Medicine, 11th edn, pp. 1995–2000. New

York: McGraw-Hill.

Briony T (ed.) (2001) Manual of Dietetic Practice, 3rd edn.

Oxford: Blackwell Science.

FAO/WHO (1994) Fats and Oils in Human Nutrition. FAO

Food and Nutrition Paper 57. Rome: FAO/WHO.

Hamazaki T and Okuyama H (ed.) (2001) Fatty acids and

lipids – new findings. World Review of Nutrition and

Dietetics 88.

Kahana E (2000) Epidemiologic studies of multiple scler-

osis: A review. Biomedicine and Pharmacotherapy 54:

100–102.

Kurtzke JF (2000) Multiple sclerosis in time and space –

geographic clues to cause. Journal of Neurovirology

6(supplement 2S): 134–140.

Mahan LK and Escott-Stump S (eds) (2000) Krause’s Food,

Nutrition & Diet Therapy, 10th edn. Philadelphia, PA:

W.B. Saunders.

Oksenberg JR and Barcellos LF (2000) The complex genetic

aetiology of multiple sclerosis. Journal of Neurovirology

6(supplement 2S): 10–14.

Muscle See Exercise: Muscle; Metabolic Requirements

MULTIPLE SCLEROSIS – NUTRITIONAL MANAGEMENT 4039

MUSHROOMS AND TRUFFLES

Contents

Classification and Morphology

Use of Wild Mushrooms

Classification and Morphology

S Rajarathnam and M N Shashirekha, Central Food

Technological Research Institute, Mysore, India

Background

0001 Mushrooms constitute a specialized group of fungi

and represent the fruiting bodies with a great diver-

sity in shape, size, color, and texture, bearing the

spores of sexual reproduction. In nature, they serve

the function of production, maturation, and dissem-

ination of spores, for the perpetuation of the species.

Thus, these mushrooms as a group of fungi, are

nonchlorophyllous organisms that cannot utilize

solar energy to manufacture their own food as do

green plants. However, mushrooms can produce a

wide range of enzymes that can degrade the complex

substrates on which they grow, following which they

absorb the soluble substances for their own nutri-

tion. This absorptive nutrition is a characteristic of

fungi. Mushrooms as macrofungi can be either epi-

geous, as in ‘morels’ or ‘field mushrooms,’ or hypo-

geous, as in ‘truffles,’ and large enough to be seen

with the naked eye and to be picked by hand. Mush-

rooms need not be aerial, or fleshy, or edible. Out of

69 000 described species of fungi, there are about

10 000 species of fleshy macrofungi, and only a

handful of these are lethal. There are no simple

ways of distinguishing between edible and poisonous

mushrooms. This will be dealt with in a later

section.

Classification

0002 Mushrooms and truffles fall under the class Basidio-

mycetes and a few orders of Euascomycetes, respect-

ively (Figure 1).

Euascomycetes

0003 Euascomycetes include morels (species of Morchella)

with epigeous fruiting bodies and truffles (species

of Tuber) with hypogeous fruiting bodies and are

characterized by the production of ascospores endogen-

ously inside special club-shaped structures called asci.

Basidiomycetes

0004Basidiomycetes are considered the most highly

evolved group of fungi and are characterized by the

exogenous production of basidiospores borne over

club-shaped structures called basidia.

Subclass: Hymenomycetes

0005This group includes all fungi composed of mem-

branes, fleshy, woody, or gelatinous, whether grow-

ing on the ground or on wood. The spore-bearing

surface, called the ‘hymenium,’ is external at an

early stage in the life cycle. The spores are borne on

basidia, and when the spores ripen, they fall to the

ground or are carried by the wind to a host that

presents all the conditions necessary for germination;

there, they produce the thread-like structures called

mycelia. Within these threads are small knots, which

in time develop into full-grown mushrooms.

0006The subclass Hymenomycetes is generally classi-

fied in one large order, the Agaricales, which in turn

is divided into six families:

0007Agaricaceae–hymenium with gills;

0008Polyporaceae–hymenium with pores;

0009Hydnaceae–hymenium with spines;

0010Thelephoraceae–hymenium horizontal and mostly

on the under surface;

0011Clavariaceae–hymenium on a smooth club-shaped

surface;

0012Tremellaceae–hymenium even and superior – gel-

atinous fungi.

Subclass: Gastromycetes

0013The word ‘Gastromycetes’ is derived from two Greek

words, ‘gaster’ (stomach) and ‘mycetes’ (fungus). The

hymenium is enclosed in the rind or peridium. The

word ‘peridium’ comes from ‘peridio’ (‘I wrap

around’), because the peridium entirely envelopes

the spore-bearing portion, which eventually sheds

the enclosed spores formed inside the basidia and

spicules. The cavity within the peridium consists of

two parts: a threaded part, called the capillitium,

4040 MUSHROOMS AND TRUFFLES/Classification and Morphology

which can be seen in any dried puff ball, and a cellular

part, called the gleba, which is the spore-bearing

tissue, composed of minute chambers lined with the

hymenium. The peridium breaks in various ways to

permit the spores to escape. When children pinch a

puff ball to ‘see the smoke,’ they are doing just what

the puff ball would have them do, scattering its seeds

to the winds.

0014 Gastromycetes has four orders:

0015 Glebal chambers usually not separating from the

peridium or from each other;

0016 Gleba powdery;

0017 Hymenium present in early stages; spores mostly

light-colored, small – Lycoperdales;

0018 CC. Hymenium lacking or indistinct; spores mostly

dark, large – Sclerodermatales;

0019 BB. Gleba slimy and fetid; exposed on a receptacle –

Phallales;

0020 AA. Glebal chambers forming waxy peridioles, or

entire gleba separating as a unit from the peri-

dium – Nidulariales.

Distribution of Mushroom Species

0021Mushroom species are distributed throughout the

world, some very specific to certain geographic

areas, while others are universal and may occur in

different seasons in the same region. Temperature

plays a critical role in the distribution of mushroom

species, and so their distribution can be categorized

under tropical, subtropical, and temperate belts

(Table 1). The reason for specific distribution of

mushroom species in relation to temperature is to be

Class

Sub-class

Series Discomycetes Hymenomycetes

Agaricales

Gastromycetes

Lycoperdales

E.g. Lycoperdon

Pezizales

E.g. Morchella

Tuberales

E.g. Tuber

Sclerodermatales

E.g. Sclerodendron

Phallales

E.g. Phallus

Nidulariales

E.g. Cyathus

Family Agaricaceae

E.g. Agaricus

Polyporaceae

E.g. Polyporus

Hydnaceae

E.g. Hydnum

Thelephoraceae

E.g. Thelephora

Clavariaceae

E.g. Clavaria

Tremellaceae

E.g. Tremella

Order

Euascomycetes Basidiomycetes

Fungi

fig0001 Figure 1 Location of mushrooms and truffles in the classification of fungi.

tbl0001Table 1 Geographic distribution of various mushroom species

Climatic belt Mushroom species

Tropical Volvariella spp.

Subtropical Agaricus bitorquis

Pleurotus spp.

Temperate Agaricus bisporus

Boletus grevillei

Tricholoma saponaceum

Laccaria laccata

Polyporus squamosus

MUSHROOMS AND TRUFFLES/Classification and Morphology 4041

viewed to the specific enzymes secreted and factors

influencing these enzymes by the mushroom species

under study, in relation to the geographic conditions

of natural occurrence.

Morphology

Natural Habitat

0022 Mushroom species can be found growing on dead and

decaying plant material, humus soil, e.g., Agaricus,

as saprophytes on the dead trunks of live trees, e.g.,

Pleurotus, as parasites on the living trees, e.g., Armil-

laria, or characteristically in symbiotic association

with the roots of pine trees, e.g., Morchella. Species

of Termitomyces grow on the ant hills, again an

example of symbiosis. Tuber species grow under-

ground in certain European climates and their flavour

is often detectable by dogs.

Vegetative Phase

0023 Mushrooms have two phases in their life cycle: a

mycelium that is usually hidden and inconspicuous

with a longer growth phase followed by short-lived

fruiting bodies. The mycelium derives the nutrition

for its growth (which, after a period of establishment,

culminates in the production of fruiting bodies) under

certain defined favorable conditions. The conditions

for mycelial growth are not very specific, in contrast

to the very specific growth conditions required by the

fruiting bodies. The constraints and problems associ-

ated with the latter explain why several mushroom

species have yet not been able to be cultivated artifi-

cially. Mycelia may be uninucleate (monokaryotic) or

binucleate (dikaryotic) (Figure 2), depending on the

species and stage in the life cycle. In nature, generally,

the spore germinates under favorable conditions to

produce the uninucleate mycelium.

Reproductive Phase

0024After a certain amount of vegetative growth depend-

ing on the availability of the compatible strain, the

uninucleate mycelium reaches the dikaryotic phase,

which in turn leads to the production of fruiting bodies,

bearing spores. For clarity, the typical life cycles of

three mushroom varieties are described below.

0025Primary homothallism Here, the basidiospore ger-

minates to produce the mycelium, which in turn is

self-fertile and ultimately can result in the production

of fruiting bodies, which bear gills, basidia terminat-

ing with four basidiospores (per basidium), as a prod-

uct of meiosis, e.g., Volvariella volvacea (Figure 3).

0026Secondary homothallism Agaricus bisporus is an

example of this phenomenon, wherein the basidium

by name itself bears only two spores, and each spore in

turn is binucleate, carrying both the compatible

factors in the same spore, so that the mycelium that

results from germination of the basidium finally yields

to the development of fruiting bodies (Figure 4).

fig0002 Figure 2 Mono- and dikaryotic mycelia. (a) septate without

clamp connections; (b) septate with clamp connections.

fig0003Figure 3 Primary homothallism in Volvariella volvacea. (a)

fruiting body; (b) basidium; (c) basidiospore; (d) mycelium; (e)

fruiting initial; (f and g) developing fruiting body.

4042 MUSHROOMS AND TRUFFLES/Classification and Morphology

0027 Heterothallism Species of Pleurotus are classic

examples of heterothallism, in which each basidium

bears four basidiospores, each genetically different

from the other, so that the degree of inbreeding is

reduced to 25%, with increased scope for outbreed-

ing of 75%. This represents possibly the most highly

evolved life-cycle system of the basidiomycetes and is

strengthened further by the operation of multiple

alleles at the two different loci (Figure 5).

Variations in Mushroom Morphology

0028 The fruiting body is the net result of a certain min-

imum amount of vegetative growth, followed by the

onset of conditions (physical, chemical, or biological)

favoring reproduction. The fruiting body that de-

velops typically has a stem/stalk called a ‘stipe,’ with

or without a basal cup, called a ‘volva,’ and a ring on

the stem known as an ‘annulus’ (Figure 6). The occur-

rence of an annulus/volva is dependent on the charac-

teristic nature of development or morphogenesis

of the fruiting body. The display of annulus and

volva also varies depending on the species (Table 2).

The stipe terminates with a cap, also called a ‘pileus’

varying in shape, size, texture, structure, and color,

and constituting one of the most beautiful objects of

nature on the earth. The great diversity in morph-

ology of the mushroom species is depicted in

Figure 7. The cap is variously colored, bright, or

dull. However, the toxicity of a mushroom bears no

relation to its coloration (Table 3). The cap consists of

a fertile layer called a ‘hymenium’ (Figure 8) compris-

ing gills, which in turn bear basidia with basidios-

pores at the distal end intercalated with sterile

cysitidia. The fruiting body may collapse as a result

of autodigestion, as in Coprinus (inky cap) or may

even have latex-containing tissues as in Lactarius

(milky mushroom).

0029Orientation of gills The morphology of gills con-

tributes to valuable taxonomic criterion in Agaricus,

when the gills are open from the genesis to the shed-

ding of basidiospores. Their attachment to the stipe/

stem varies and is specific to the species. Gills may be

free and detached from the stipe. A mushroom is

described as decurrent when the gills run down the

stem (the usual situation in many funnel-shaped

fruiting bodies), adnate when the gill is attached

along its entire width, adnexed when attachment is

along only a part of the total width, and sinuate when

there is a notch where the gill joins the stem. The

attachment of gills in the cap has a bearing on the

confluency of the cap, and this interrelation is

depicted in the Figure 9.

0030In Euascomycetes, ascospores are formed inside

the club-shaped structures called ‘asci,’ whereas in

fig0004 Figure 4 Secondary homothallism in Agaricus bisporus.

(a) fruiting body; (b) basidium with two basidiospores; (c) basi-

diospore; (d) mycelium; (e and f) developing fruiting body.

fig0005Figure 5 Heterothallic and tetrapolar life cycle in Pleurotus

sajor-caju. (a) fruiting body; (b) basidium with four genetically

different basidiospores; (c) basidiospores; (d) germinating

basidiospores; (e) monokaryotic mycelia; (f) dikaryotization;

(g) dikaryotic mycelia.

MUSHROOMS AND TRUFFLES/Classification and Morphology 4043