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

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restrictions on the food groups and foods that are

consumed, the willingness to use fortified foods or

nutrient supplements, and to accept medical advice,

and the physiological state of the individual. Vegetar-

ians who consume unplanned regimens or feed them

to their children are no more immune to nutritional

problems of excess, inadequacy, and imbalance than

are omnivores. Particular risks arise when many food

groups and foods are eliminated without due care

being given to providing alternative sources of nutri-

ents either from other conventional foods, fortified

foods, nutrient supplements, or a combination of

these. This is a particular problem for those who by

virtue of their increased nutritional needs or their

health status are especially nutritionally vulnerable.

A vegetarian diet, which might suffice for good health

in other groups, may not meet their nutritional needs

and may be inappropriate for them. Such groups

include the very young (weanlings and young

children), those who are growing rapidly (adoles-

cents), those likely to become pregnant, pregnant

and lactating women, the very old, and the sick. For

example, infants who are weaned to vegan diets may

develop rickets, iron-deficiency anemia, protein-

calorie malnutrition, and other dietary deficiency

diseases. There is also a small minority of vegetarians

whose convictions and practices place them at in-

creased health risk. They refuse to use prescription

drugs, reject immunizations using animal antiserum,

medications using recombinant products such as

epoietin-a, human recombinant insulin, and blood

transfusions, or avoid or delay other conventional

medical care. Such practices may increase disease

risks or severity. They may self-treat using unproven

remedies including herbal and botanical preparations

without due caution to make sure that they are safe.

Therefore not only dietary patterns but also associ-

ated health behaviors need to be assessed.

0025 The most common dietary deficiencies observed

on unplanned vegetarian diets are iron-deficiency

anemia (particularly in weanlings, young children,

and pregnant women), rickets in weanlings and

young children, megaloblastic anemia due to vitamin

deficiency (in pregnant and lactating women,

infants and young children, and the aged), and osteo-

malacia and low bone density in vegan adults and the

elderly.

Dietary Planning

0026 Table 2 presents some key points for dietary planning

for each of the common vegetarian dietary patterns.

Well-planned vegetarian diets that meet the dietary

standards for nutrients as determined by scientific

expert groups are in line with current dietary

recommendations. Balance, variety, and moderation

are essential and can be achieved by focusing on

alternative sources for nutrients high in foods that

are excluded on the vegetarian pattern. The use of a

wide variety of plant foods, the advent of nutrient-

fortified plant foods, and the judicious use of vitamin

and mineral supplements at times of particularly high

needs may be helpful. Sound vegetarian dietary

guides have been published that assure adequacy of

nutrient intakes, and these facilitate dietary planning,

especially for vegans. Since periods of rapid growth or

physiological stress are times when risks of nutri-

tional deficiencies are greatest, special attention is

warranted to planning dietary intakes during these

nutritionally vulnerable times during the life cycle,

especially for those who consume vegan diets. Be-

cause diets that permit good health in adults may

not do so during these times of particular stress,

special guidance from a dietitian is often helpful as

tbl0002Table 2 Considerations in dietary planning for vegetarian

patterns

Dietarypattern Keyissues andcomments

Meatless, partial or

semivegetarian

These diets are similar in most respects

to nonvegetarian diets and fit well with

dietary recommendations to decrease

risks of chronic degenerative diseases

Lactoovo vegetarian Liberal amounts of vitamin D-fortified

dairy products and some eggs in the

diet allow for adequate intakes of

nutrients, with the possible exception

of iron, which can be obtained from

fortified cereals. Low-fat dairy products

are preferred to keep intakes of

saturated fat and total fat moderate

Lactovegetarian Same as above

Macrobiotic Current variations of this diet are less

restrictive than versions used two

decades ago, but deficiencies of

energy, iron, calcium, vitamin B

vitamin D, and other nutrients may still

arise in weanlings, pregnant women,

and young children, especially if diets

are unplanned

Vegans or

‘pure vegetarian’

Without careful planning, energy and

vitamins B

, D, and bioavailable

sources of iron may be low.

Concentrated sources of energy can

increase caloric intakes. Vitamin B

,D,

and calcium can be supplied through

use of soy milk, cereals, and/or

supplements of these nutrients. A

variety of protein food sources assures

adequate complementary proteins. Iron

intakes may be enhanced by iron-

fortified cereals, green leafy

vegetables, and iron supplements if

these are acceptable. A vegan food

guide can be helpful

5978 VEGETARIAN DIETS

well. If there is doubt as to the nutritional adequacy

and healthfulness of vegetarian diets, the assistance of

a dietitian and dietary assessment of food records

of typical intake is warranted. Many computerized

dietary assessment programs are available that can

assist in this task.

Conclusion

0027 Plant-only (vegan, macrobiotic, and fruitarian),

plant-based (lactovegetarian, lactoovo vegetarian,

meatless), and plant-rich omnivorous diets that are

planned to insure dietary adequacy and minimize

chronic disease risk are compatible with good nutri-

tional status and health.

Acknowledgment

0028 This review was supported in part by contract

number 53/3 K06-10 from the US Department of

Agriculture to Tufts University.

See also: Anemia (Anaemia): Iron-deficiency Anemia;

Megaloblastic Anemias; Calcium: Properties and

Determination; Cholecalciferol: Properties and

Determination; Cobalamins: Properties and

Determination; Dietary Fiber: Properties and Sources;

Folic Acid: Properties and Determination; Functional

Foods; Iron: Properties and Determination; Macrobiotic

Diets; Protein: Food Sources; Riboflavin: Properties and

Determination; Rickets and Osteomalacia; Zinc:

Properties and Determination

Further Reading

American Dietetic Association (1993) Position of the

American Dietetic Association on vegetarian diets.

Journal of the American Dietetic Association 11:

1317–1319.

Dagnelie P, Van Staveren W, Vergate F, Dingan D, Van

den Berg H and Hautvast J (1989) Increased risk of

vitamin B

and iron deficiency in infants on macrobi-

otic diets. American Journal of Clinical Nutrition 50:

818–824.

Duyff RL (1997) The vegetarian way. In: Duyff RL (ed.)

The American Dietetic Association’s Complete Food

and Nutrition Guide, pp. 553–572, 595. Minneapolis:

Chronimed Publishing.

Dwyer JT (1996) Vegetarianism for women. In: Krummel D

and Kris-Etherton PM (eds) Nutrition in Women’s

Health, pp. 232–263. Gaithersburg, MD: Aspen.

Dwyer JT and Loew FM (1994) Nutritional risks of vegan

diets to women and children: are they preventable?

Journal of Agricultural and Environmental Ethics 7:

87–109.

Haddad EH (1994) Development of a vegetarian food

guide. American Journal of Clinical Nutrition 59

(suppl.): 1248–1254.

Haddad EH, Sabate J and Whitten CG (1999) Vegetarian

food guide pyramid: a conceptual framework. American

Journal of Clinical Nutrition 70 (suppl.): 615S–619S.

Harper AE (ed.) (2000) Physiologically active food com-

ponents. American Journal of Clinical Nutrition 71:

1651S–1743S.

Herbert V (1997) Vitamin B

. In: Ziegler EE and Filer

LJ (eds) Present Knowledge in Nutrition, 7th edn, pp.

191–206. Washington, DC: ILSI Press.

Hodgkin G and Mahoney S (eds) (1995) Seventh-Day Ad-

ventist Diet Manual Including a Vegetarian Plan, 7th

edn, pp. 1–559. Loma Linda, CA: Seventh-Day Advent-

ist Dietetic Association.

Johnston PK (ed.) (1994) Vegetarian nutrition: proceedings

of a symposium held in Arlington VA. American Journal

of Clinical Nutrition 59 (suppl.): 1099S–2362S.

Johnston PA (1999) Nutritional implications of vegetarian

diets. In: Shils ME, Olson JA, Shike M and Ross AC (eds)

Modern Nutrition in Health and Disease, 9th edn, pp.

1755–1768. Baltimore: Williams and Wilkins.

Johnston PK and Sabate J (eds) (1999) Third International

Congress on Vegetarian Nutrition. American Journal of

Clinical Nutrition 70: 429S–634S.

Key TF, Fraser GE, Thorogood M et al. (1998) Mortality in

vegetarians and nonvegetarians: a collaborative analysis

of 8300 deaths among 76 000 men and women in five

prospective studies. Public Health Nutrition 1: 33–41.

Mangels R (1995) Nutrition section. In: Wasserman D (ed.)

Simply Vegan, 2nd edn. Baltimore: Vegetarian Resource

Group.

Messina M and Messina V (1996) The Dietitian’s Guide to

Vegetarian Diets. Gaithersburg, MD: Aspen.

Mutch PB and Johnston PK (eds) (1988) Proceedings of the

First International Congress on Vegetarian Nutrition.

American Journal of Clinical Nutrition 48 (suppl.):

707–927.

Sanders TAB (1999) Essential fatty acid requirements of

vegetarians in pregnancy, lactation and infancy. Ameri-

can Journal of Clinical Nutrition 70: 555S–559S.

Sanders TAB and Reddy S (1994) Vegetarian diets and

children. American Journal of Clinical Nutrition 59

(suppl.): 1176–1181.

Smith J and Dwyer JT (1998) Vegetarian diets for children.

In: Dershewitz RA (ed.) Ambulatory Pediatric Care, 3rd

edn, pp. 106–112. Philadelphia: Lippincott Raven.

Wasserman D and Mangels R (1995) Simply Vegan, 2nd

edn. Baltimore: Vegetarian Resource Group.

Young VR and Pellett PL (1994) Plant proteins in relation to

human protein and amino acid nutrition. American

Journal of Clinical Nutrition 59 (suppl.): 1203–1212.

VEGETARIAN DIETS 5979

VERMOUTH

P Liddle and L Boero, Martini & Rossi, Pessione,

Torino, Italy

History

0001 The origins of vermouth date back to ancient Medi-

terranean history. The maceration of herbs and spices

in wine was common practice in antiquity, and the

invention of aromatized wine, the ancestor of ver-

mouth, has been attributed to Hippocrates. Greece

abounds in aromatic plants and Crete in particular

provided the plants dittany and wormwood, both of

which possess tonic and digestive properties. It is

reported that Hippocrates macerated the flowers of

these plants in strong, sweet Greek wine, thereby

obtaining a satisfying and digestive beverage which

throughout antiquity and the Middle Ages was called

‘Hippocratic wine’ or vinum absinthianum. Later, the

Romans elaborated on the production of such wines

by introducing other herbs such as thyme, rosemary,

myrtle, and celery.

0002 In the Middle Ages the Venetians, who had the

monopoly of the spice trade, introduced aromatic

plants into Italy which until then were unknown in

that country, and they were used in the preparation of

Hippocratic wine. These plants (cardamom, cinna-

mon, myrrh, cloves, rhubarb, ginger, and sandal-

wood) came from East Africa, India, and Indonesia.

0003 Turin, along with Florence and Venice, was one of

the major Italian centers of production of Hippo-

cratic wines and liqueurs from the late eighteenth

century. Piedmont in particular possessed two assets:

aromatic plants abounded in the Piedmont Alps and

their foot-hills, and the bouquet of Piedmont dry and

sweet white wines combined very well with the fra-

grance of herbs. These two factors doubtless explain

why this area became the major center of the ver-

mouth industry in the nineteenth century, when the

leading names in that sector emerged.

0004 The term ‘vermouth’ derives etymologically from

Wermut, the German name for wormwood. While

the latter English term refers to the use of the plant

as a vermifuge, the German name is supposedly

derived from Wer (man) and Mut (courage, spirit).

When it was introduced into Bavaria in the first half

of the seventeenth century by the Piedmont producer

Alessio, vinum absinthianum was probably translated

literally as Wermutwein, which when it reached

France became vermouth.

0005Today, most of the world’s vermouth is produced

in Europe (essentially in Italy, France, and Spain)

and to a lesser extent in South America, but local

varieties are always to be found in all wine-producing

countries.

Definition

0006In basic terms, vermouth is a combination of wine,

aromatic plants (hereafter referred to as ‘botanicals’),

sugar, sometimes grape must in limited quantities,

and alcohol. Caramel is the only coloring substance

authorized, and is used for red vermouths.

0007The difference between the various types of ver-

mouth lies essentially in the presence or absence of

certain botanicals in their formulas. Broadly speak-

ing, there are two main families – sweet and dry –

which differ in their sugar content. Sweet vermouths

contain around 150 grams of sugar per liter, while the

dry varieties contain less than 50 g l

1

. Dry vermouths

are all white, and serve mainly as a base for well-

known cocktails, although they may also be drunk

straight.

0008In the European Union (EU), vermouth is defined

within the European Council Regulation 1601/91

and subsequent amendments. This Regulation applies

to ‘the definition, description and presentation of

aromatized wines, aromatized wine-based drinks,

and aromatized wine-product cocktails.’ Article 2 (1)

(a) of the Regulation states:

0009aromatized wine shall mean a drink:

0010– obtained from wines defined in points 12 to 18 of

Annex I to Regulation (EEC) No. 822/87 (11), as

last amended by Regulation (EEC) No. 1325/90

(12), with the exception of retsina table wine, and

possibly with added grape must, grape must in fer-

mentation and/or fresh grape must with fermentation

arrested by the addition of alcohol, as defined by

Community legislation,

– to which alcohol has been added as defined in Article 3

(d), and

– which has been flavoured with the aid of:

– natural flavouring substances and/or natural flavour-

ing preparations as defined in Article 1 (2) (b) (i) and

– aromatic herbs and/or spices and/or flavouring food-

stuffs,

– which has generally been sweetened and, subject to the

exceptions provided for in paragraph 2, has possibly

been coloured with caramel,

– which has a minimum actual alcoholic strength by

volume of 14.5% vol or more and a maximum actual

alcoholic strength by volume of less than 22 % vol . . .

0011

0012

0013

0014

0015

0016

5980 VERMOUTH

The wine used in the preparation of an aromatized

wine must conform to the relevant EU wine legisla-

tion (in particular as far as the minimum alcohol

content is concerned), and be present in the finished

product in a proportion of not less than 75%.

0017 Vermouth itself is further defined in Article 2 (2) (a)

as an:

0018 aromatized wine . . . the characteristic taste of which is

obtained by the use of appropriate derived substances, in

particular of the Artemisia species, which must always

be used; this drink may be sweetened only by means of

caramelized sugar, sucrose, grape must, rectified concen-

trated grape must and concentrated grape must.

Denominations relating to the sugar contents, e.g.,

sweet, extra-dry, are defined in Article 2 (5). In add-

ition, EU Regulation 122/94 allows for the use of the

pure flavoring substance vanillin, identical to that

found in natural sources.

0019 Definitions in other parts of the world are broadly

similar, with slight variations on the minimum wine

content (70% in some cases), and minimum/max-

imum alcohol contents. In all cases, the base wine

and botanicals used must comply with the relevant

local legislation concerning these ingredients.

0020 Finally, contrary to some popular beliefs, vermouth

is not a ‘vin cuit’ (cooked wine), and, to put to rest

another long-standing rumor, it is not a particularly

acidic product – in fact, the acidity is often less than

that of the average table wine.

Ingredients

Wine

0021 Quantitatively, wine is the most important ingredient

of vermouth, since in the EU it accounts for at least

75% of its volume. The quality of the final product

therefore depends on the quality of the wine

employed. Generally speaking, only neutral white

wines that do not oxidize are employed; they must

be low in tannin if they are not to maderize with age,

and turn a darker color.

Botanicals

0022 The botanicals (leaves, flowers, fruits, seeds, roots,

and barks) are the natural sources of flavor which

characterize vermouth. There are so many of these

that it would be impossible to list them exhaustively

and, of course, the composition of the mixture is a

closely guarded secret of each producer, but some

examples are given in Table 1, together with their

respective Latin botanical names.

0023 As with other foods and beverages, use of

traditional botanicals may introduce trace levels of

compounds which in their pure (or, at least, more

concentrated) form may be suspected of negative

effects on the health of consumers, based on toxico-

logical studies. These compounds, usually present at

or below the mg l

1

level, are hence subject to quan-

titative limitation by the legislation of different coun-

tries. In Europe, these limits are set by the Directive

88/388/EEC, and limits of similar magnitude are

found in other national or international legislation.

0024In the particular case of vermouth, the use of Arte-

misia species forms part of the EU definition of the

product, and virtually all of the Artemisia species

contain thujone, a compound often associated with

the negative aspects of the drink absinthe. However,

the most common source of thujone in foodstuffs

is sage, a botanical whose name and history are

synonymous with good health, and which is widely

and traditionally used as a culinary herb in many

countries.

0025The EU Directive, for example, currently fixes a

maximum limit for thujone of 5 mg kg

1

in alcoholic

beverages of less than 25% alcohol. Sweet vermouths

are well within these limits, generally containing less

tbl0001Table 1 English and Latin botanical names of examples of

natural sources of flavor used in the production of vermouth

Englishname Latin botanicalname

Angelica Angelica archangelica

Artemisia species Various

Bay Pimenta racemosa

Camomile Anthemis nobilis

Cardamom Elettaria cardamomum

Cinchona Cinchona species

Cinnamon Cinnamomum zeylanicum

Citrus species Various (orange, lemon, etc.)

Clary sage Salvia sclarea

Clove Eugenia caryophyllus

Coriander Coriandrum sativum

Dittany of Crete Origanum dictamnus

Elder Sambucus nigra

Gentian Gentiana lutea

Ginger Zingiber officinale

Hops Humulus lupulus

Juniper Juniperus communis

Lemon balm Melissa officinalis

Licorice Glycyrrhiza glabra

Marjoram Origanum vulgare

Nutmeg and mace Myristica fragrans

Orris Iris florentina

Quassia Quassia amara

Raspberry Rubus idaeus

Rhubarb Rheum officinale

Rose Rosa damascena

Saffron Crocus sativus

Sage Salvia officinalis

Savory Satureia hortensis

St John’s wort Hypericum perforatum

Star anise Illicium verum

Thyme Thymus vulgaris

Vanilla Vanilla planifolia

VERMOUTH 5981

than 1 mg kg

1

, a level considerably lower than those

in past or current versions of absinthe; most dry

vermouths contain even less.

0026 Other such compounds may be introduced into

traditional flavored alcoholic beverages by botanicals

that also often have long-standing histories of culin-

ary use. In all cases, careful selection of raw materials,

and if necessary the mode of preparation of the

botanical extracts, results in products which respect

current limits. In addition, it should be remembered

that the very presence of alcohol in flavored wines

and spirits constitutes an ‘automatic’ limiting factor

on the ingestion of such compounds during moderate

consumption of these products.

Alcohol

0027 Ethyl alcohol also enters into the composition of

vermouth, both to fortify the wine and as a means

of extracting the flavoring substances from the bota-

nicals. It must be of agricultural origin, very pure, and

conform to standards laid down by legislation (e.g.,

concerning the maximum level of methanol and other

natural fermentation byproducts). In Europe, such

specifications are given in Annex I to Regulation

1601/91.

Water

0028 Although not a major ingredient, the water used

(mainly together with alcohol for the botanical ex-

tracts) must usually conform to the standards for

drinking water. This is the case in Europe, as em-

bodied in the current and future requirements of EU

Directives concerning potable water (80/778/EEC

and 98/83/EC).

Sugars

0029 In order to give vermouth its required sugar content,

mistelle (muted grape must) or a good dessert wine

may be added to the base wine, as well as the neces-

sary amount of good-quality white sugar. The sugars

slightly attenuate the bitterness of certain substances

that would otherwise be too strong on the palate.

They give the vermouth body, firmness, and smooth-

ness, and thus play a very important role in the prep-

aration. As mentioned above, sweet vermouths

contain about 150 g l

1

of sugar, and dry vermouths

less than 50 g l

1

Caramel

0030 Red vermouth generally owes its amber hue to caramel,

which in Europe is the only coloring matter authorized

under Regulation 1601/91. Apart from imparting

color, it also confers a special flavor specific to red

vermouth, contributing to the body and smoothness.

Production

0031Prior to the marriage of the ingredients of vermouth,

the base-wine blend and the botanical extracts must

be prepared.

Base-wine blend

0032The preparation of the base-wine blend is performed

using traditional processing aids common to all wines

and wine-based products, e.g., gelatin, bentonite,

charcoal, etc. Colloid formation and coagulation

reduce the levels of high-molecular-weight com-

pounds and of traces of iron and other metals, all of

which could compromise the clarity and stability of

the finished product. As with all wine processing,

small amounts of potassium ferrocyanide may be

necessary to reduce the trace metals. Due to losses

from the base wines during the transfer and blending,

small amounts of sulfur dioxide may be added to

maintain the antiseptic and antioxidant effects of

the latter. After a suitable contact time (up to several

days), the blend is decanted and filtered.

0033Although alcohol is generally added at a later

stage of the process, the base wines of some ver-

mouths (particularly in France) may be fortified

by the addition of this ingredient at an earlier

stage. They are then subjected to a physical aging in

wood (sometimes up to a year), as well as a form of

biological aging similar to the flor sherry process

used in Spain, to enrich the organoleptic qualities of

the wines.

Botanical Extracts

0034The botanicals are usually incorporated into the ver-

mouth in the form of an extract (strictly speaking, a

tincture) produced by macerating them in aqueous

alcohol or a distillate obtained by distilling them in

the presence of aqueous alcohol (an alcoholate).

0035Maceration is the most commonly used process.

The botanicals are placed in a tank, covered with a

mixture of aqueous alcohol, and are agitated period-

ically so that they remain constantly covered by the

liquid. The operation is frequently performed in ro-

tating tanks and may last for several weeks. At the

end of this time, the extract is drawn off and the

botanicals are pressed.

0036Distillation is used when it is desired to make par-

ticular use of the volatile substances contained in the

botanicals (e.g., fruits, St John’s wort), and to exclude

higher-molecular-weight compounds which could

have negative physical or organoleptic effects. The

botanicals are distilled in the presence of a mixture

of alcohol and water, with or without an initial period

of maceration. The actual strength of the aqueous

alcohol used, and the complete or partial recovery

5982 VERMOUTH

of the distillate, together form part of the traditional

recipe that characterizes a particular vermouth.

0037 In some cases, in particular in the production of a

well-known French dry vermouth, the botanicals are

macerated directly in the wine, which has already

been fortified by alcohol.

Blending the Ingredients

0038 The sugar required in the product is generally incorp-

orated into the base-wine blend, which is then mixed

with alcohol, water, and the botanical extracts, to-

gether with caramel if required, in blending tanks,

which often have a capacity of up to 200 000 l. After

careful homogenization of the liquid, the vermouth is

then allowed to mature for up to several weeks, in

order to achieve a proper harmony and balance of its

ingredients.

Stabilization

0039 At the end of this maturation time, the vermouth

undergoes cold stabilization treatment. It is refriger-

ated, and is held for several days at around 8



close to its freezing point. This precipitates substances

(mainly potassium bitartrate) which may form a

natural deposit later if the vermouth is subjected to

low temperatures during storage and transport, or to

contact with ice when served. The precipitate is re-

moved by a low-temperature filtration, guaranteeing

the physical stability of the product under all condi-

tions.

0040Finally, to insure perfect clarity and brilliance, and

also biological stability in the case of products with

an alcohol strength of less than 16% vol, the ver-

mouth is generally subjected to a very fine sterilizing

filtration immediately prior to bottling. The latter is

carried out using the modern techniques common to

other sectors of the beverage industry.

0043An example of an overall production process is

shown in Figure 1.

Analysis

0041Most of the routine analyses of vermouth are of ne-

cessity those used for the analysis of wines, since

wines form the basis of all vermouths. In addition,

modern techniques of gas and liquid chromatography

are used to analyze for the volatile and nonvolatile

compounds which are derived from the botanicals

used, and which contribute to the specific aroma

and taste of vermouth. In both cases, these chromato-

graphic techniques often need to be coupled to mass

Wines Botanicals Water Sugars Caramel

Maceration

Clarification

Distillation

Extract

Distillate

Filtration

Clarification

Refrigeration

Filtration

Vermouth

Bottling

Alcohol

Bulk blend

fig0001 Figure 1 Typical overall production process for vermouth.

VERMOUTH 5983

spectrometry in order to identify and monitor the low

levels of these compounds (typically a total of the

order of less than a few tens of mg l

1

0042 In common with the rest of the food industry, great

care is also taken today to monitor and limit any low

levels of contaminants, using these same techniques,

which may potentially be introduced by contact with

processing or transport equipment, or packaging

materials.

See also: Alcohol: Properties and Determination;

Caramel: Properties and Analysis; Grapes; Herbs: Herbs

Used in Alcoholic Drinks; Spices and Flavoring

(Flavouring) Crops: Use of Spices in the Food Industry;

Wines: Types of Table Wine

Further Reading

Amerine MA (1973) A multi-language dictionary of ver-

mouth ingredients. Rivista Italiana EPPOS 15: 504–516.

Anonymous (1974) From the wine of Hippocrates to

vermouth. Revue Vinicole Internationale 1–2: 33–36.

Council Directive 88/388/EEC of 22 June 1988 on the

approximation of the laws of the Member States

relating to flavourings for use in foodstuffs and to source

materials for their production. Official Journal of

the Europeon Communities L 184, 15/07/1988, pp.

61–66.

Council Regulation (EEC) No 1601/91 of 10 June 1991

laying down general rules on the definition, description

and presentation of aromatized wines, aromatized wine-

based drinks and aromatized wine-product cocktails.

Official Journal of the Europeon Communities L 149,

14/06/1991, pp. 1–9.

Commission Regulation (EC) N. 122/94 of 25 January

1994 laying down certain detailed rules for the applica-

tion of Council Regulation (EEC) N. 1601/91 on the

definition, description and presentation of aromatized

wines, aromatized wine-based drinks, and aromatized

wine-product cocktails. Official Journal of the Euro-

pean Communities L 21, 26/01/1994, p. 7.

VIBRIOS

Contents

Vibrio cholerae

Vibrio parahaemolyticus

Vibrio vulnificus

Vibrio cholerae

J G Morris, Jr, University of Maryland School of

Medicine, Baltimore, MD, USA

Introduction

0001 Vibrio cholerae is a curved, Gram-negative bacilli.

The organism is widely distributed in aquatic envir-

onments, where it is a natural, free-living organism.

A subset of V. cholerae strains, carrying the genes

for cholera toxin (CT) and the Vibrio pathogenicity

island (VPI), cause cholera, a disease characterized

by severe, dehydrating diarrhea; virtually all of

these latter ‘epidemic strains’ are within either O

group 1 or O group 139. Cholera remains a persistent

cause of morbidity and mortality in Asia and Africa.

In 1998, the World Health Organization (WHO) re-

ceived reports of 293 121 cholera cases and 10 586

deaths from 74 countries, with the actual number of

cases (including unreported cases) probably greatly

exceeding this figure. Cholera can also move explo-

sively through populations that have been free of the

disease for generations, as demonstrated by the occur-

rence of over 100 000 cases in Peru in 1991 and the

subsequent rapid spread of cholera to other South

American countries.

0002V. cholerae strains which lack the virulence factors

necessary to cause epidemic cholera (‘nonepidemic

strains’) have in the past been referred to as non-O1

V. cholerae, nonagglutinable (NAG) Vibrio,or

noncholera Vibrio. While the majority of these envir-

onmental, nonepidemic strains appear to be non-

pathogenic for humans, some have been linked with

human disease.

Cholera

0003Cholera has been endemic in the delta of the Ganges

and Brahmaputra rivers since the beginning of recorded

history. Seven pandemics of cholera have occurred

since 1817. The seventh pandemic began in Indonesia

in 1961, with subsequent spread through Asia, Africa,

5984 VIBRIOS/

Vibrio cholerae

parts of Europe, and, beginning in 1991, South Amer-

ica. Transmission during an epidemic is thought to

occur primarily through contamination of potable

water. However, foodborne transmission is well recog-

nized, and may play an important role in the introduc-

tion of the organism to a new area or transmission in

areas of low endemicity, such as the USA.

0004 Illness in cholera is due primarily to the action of

CT, a protein enterotoxin that stimulates profuse,

watery diarrhea, leading to dehydration and death.

V. cholerae strains may be classified by O group,

and prior to 1992, it was assumed that epidemic

cholera could only be caused by strains in O group 1

(V. cholerae O1). In 1992, cholera caused by a new

serogroup, subsequently designated as O group 139

(V. cholerae O139), appeared in epidemic form in

India and Bangladesh. Genetic studies have demon-

strated that O139 strains are virtually identical to O1

strains, except for the replacement of a 22-kb DNA

fragment responsible for O1 antigen biosynthesis

with a 35-kb capsular polysaccharide biosynthesis

region. With this change in surface antigens,

V. cholerae O139 strains were able to cause cholera

in persons with prior immunity to V. cholerae O1.

Key cholera virulence factors can be transferred

among V. cholerae strains by phage, and it is likely

that other serotypes (such as O37), when carrying an

appropriate complement of virulence genes, can also

cause cholera.

Occurrence in the Environment

0005 As previously noted, V. cholerae is a free-living or-

ganism in the aquatic environment. Growth is influ-

enced by salinity (isolation generally occurs in water

with a salinity of 2–20 parts per thousand) and water

temperature (optimally > 17



C). V. cholerae produces

a chitinase, and may bind to and colonize plankton

and other aquatic organisms. The bacterium can shift

to a ‘rugose’ morphologic form, in which it produces

an amorphous exopolysaccharide that contributes to

the formation of biofilms. Strains in the environment

may also assume a ‘viable but nonculturable’ form.

Studies in Peru demonstrate that seasonal cholera

epidemics are often preceded by increases of V. cho-

lerae in the environment, with subsequent ‘spill-over’

of the bacterium into human populations. As humans

become infected, V. cholerae present in their feces can

contaminate food and water sources and further

increase environmental V. cholerae levels, resulting

in amplification of the organism and initiation of

the epidemic cycle.

Entry to Food Chain

0006 Entry of V. cholerae into the food chain is most

clearly described in association with shellfish. In

areas of low endemicity, such as the USA, the occur-

rence of illness has been linked with the consumption

of raw or undercooked shellfish (crabs, oysters) har-

vested from areas in which the organism is known

to be present. Outbreaks of illness have also been

reported in association with consumption of raw or

undercooked mussels, cockles, and fish. Environmen-

tal and/or fecally derived organisms may contaminate

other foods as a result of irrigation or when water is

used for cleaning or washing of fruits and vegetables

or other foods eaten without cooking. Direct fecal

contamination of cooked foods within a household

can also serve as a route of transmission, particularly

if foods are left at ambient temperature for a period of

hours after contamination.

Fate on Processing/Storage

0007There is an extensive body of literature on the sur-

vival of V. cholerae in food, beginning with the obser-

vation of Babes in 1885 that cholera Vibrio remained

alive up to 48 h on fresh nonacid vegetables, potatoes,

and cheese, but not longer than 24 h on sour fruit and

vegetables. In general, cooked foods appear to be a

more favorable milieu than raw foods as cooking

destroys many competing bacteria. Growth is in-

hibited by low pH and enhanced by neutral or alka-

line pH. Recent studies suggest that cooked rice is a

particularly good growth medium.

0008Survival on shellfish has been reported for 15–45

days, depending on the holding temperature. V. cho-

lerae are readily killed by high temperatures (5 min at



C, ‘seconds’ at 80–100



C). However, studies con-

ducted by the US Centers for Disease Control during

the Louisiana cholera outbreaks in the late 1970s

demonstrated that, after experimental inoculation of

the organism, V. cholerae O1 could be cultured from

crabs that were boiled up to 8 min or steamed for up

to 30 min; crabs boiled for 8 min or steamed for

25 min were red, and the meat was firm and appeared

well-cooked. In recent studies with cockles, mild heat

treatment for up to 25 s was inadequate to eliminate

V. cholerae O139; the persistence of V. cholerae O1 in

frozen shrimp, with shell, has been reported for over a

month.

0009With the rapid means of transportation now avail-

able, any raw or undercooked food (particularly raw

or undercooked seafood) imported from an area with

epidemic or endemic disease has the potential for

carrying the organism. This was dramatically illus-

trated with the 1991 South American epidemics,

where transmission of the disease across national

borders (and across continents) was associated with

importation of food items such as ceviche (raw,

marinated fish) and crab meat. The risk of such trans-

mission is dependent on the level of sanitation in the

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Vibrio cholerae

5985

country of origin, the extent of the disease within the

country (i.e., products from a country with low levels

of endemic disease constitute a much smaller risk

than products from a country in the midst of a

major epidemic), and the handling of the product

during shipment. In this context, it should be noted

that WHO feels that the risk of cholera transmission

associated with trade in food products is ‘very small,’

and considers restrictions on food and beverage

importations to be ‘inappropriate cholera control

measures.’

Detection in Food, Water, and Physiological

Samples

0010 Isolation of the organism from environmental

samples generally requires an enrichment procedure.

Enrichment broths rely on the ability of Vibrio species

to grow at alkaline pH in the presence of bile salts, or

upon the ability of Vibrio to use gelatin as the only

available carbon and nitrogen source: commonly

used enrichment broths include alkaline peptone

water and gelatin phosphate saline broth. The enrich-

ment broth should be streaked within 6–8 h after

inoculation on to a selective media such as thiosulfate

citrate bile salts sucrose (TCBS) agar. Isolation of the

organism from stool samples also requires the use of a

selective medium such as TCBS, and may be facili-

tated by an enrichment step in alkaline peptone water.

0011 Identification of typical colonies from TCBS plates

is based on standard biochemical characteristics.

Epidemic strains can be tentatively identified by ser-

otyping with O1 and O139 specific antisera. V. cho-

lerae of O group 1 can be further divided into two

serovars, Ogawa and Inaba, and a rare third type,

Hikojima, as well as two biotypes, classical and El

Tor. Confirmation that an isolate is capable of caus-

ing epidemic disease requires demonstration that the

strain has the ability to produce cholera toxin. DNA

probes are now available for identification of strains

carrying the genes for cholera toxin, VPI, and other

critical virulence factors. These probes have proven to

be extremely useful in epidemiologic studies and in

the screening of environmental isolates.

Symptoms and Characteristics

0012 Despite the dread inspired by the term ‘cholera’, the

majority of persons infected with epidemic V. cho-

lerae strains do not have severe illness: 75% of per-

sons infected with strains of the classical biotype have

inapparent or mild disease, while 93% of infections

with biotype El Tor strains (which are responsible for

the most recent pandemic) have illnesses that are

inapparent or mild. The infectious dose is dependent

to a large degree on gastric acidity and the associated

buffering capacity of the vehicle carrying the organ-

ism. When normal, healthy, adult North American

volunteers ingested 10

V. cholerae O1 organisms in

water, neither illness nor infection resulted. However,

volunteers consistently became infected after ingesting

organisms with 2 g of sodium bicarbonate or with

food; 10

organisms caused illness in four of six vol-

unteers when administered with sodium bicarbonate.

0013The incubation period for cholera varies from

several hours to 7 days. Although there may be pre-

monitory symptoms such as anorexia and abdominal

pain, in most cases onset is sudden, with profuse

diarrhea. Initially the stool is brown with fecal matter,

but soon the evacuations assume a pale gray color;

mucus in the stool imparts the characteristic rice-

water appearance. Tenesmus is absent; instead, there

is a feeling of relief as enormous amounts of fluid

are passed effortlessly. Vomiting may be present, oc-

curring within a few hours of the onset of diarrhea.

Temperature is usually normal or subnormal. Peak

stool losses occur within 24 h of the onset of diarrhea

and in cholera gravis (the most severe form of chol-

era) may exceed 1 l of fluid per hour, resulting in

profound dehydration and circulatory collapse.

0014In epidemic settings there is no other disease that

can consistently cause severe, life-threatening diar-

rhea and dehydration in adults. In individual cases,

diarrhea approaching the severity of cholera can be

caused by other diarrheal pathogens, including

enterotoxigenic Escherichia coli and strains of non-

O1 V. cholerae. Among children, rotavirus can also

be a cause of severe, dehydrating diarrhea.

Treatment, Prevention

0015Treatment of cholera is based on replacement of

fluids lost through diarrhea: this can almost always

be accomplished by oral rehydration, although in the

most severe cases intravenous rehydration may be

necessary. Antibiotics such as tetracycline can shorten

the duration of diarrhea and reduce the period of

carriage. However, antibiotics should always be

regarded as ancillary therapy to vigorous rehydration.

0016Prevention is based on the maintenance of good

sanitation, provision of safe potable water, and avoid-

ance of raw or undercooked foods in or from highly

endemic or epidemic areas. Currently available par-

enteral vaccines are of low efficacy, and their use is

not recommended. Several oral vaccines are under

active development; their role in disease prevention

remains to be determined.

‘Nonepidemic’

Vibrio cholerae

0017Strains of V. cholerae that do not carry virulence

factors necessary to cause cholera have been

implicated as a cause of diarrheal disease and, in

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Vibrio cholerae

susceptible hosts, may cause septicemia. Epidemiolo-

gic studies, and studies with volunteers, have linked

the occurrence of diarrheal illness with the produc-

tion of a heat-stable enterotoxin (NAG-ST) similar to

that produced by enterotoxigenic E. coli; diarrheal

illness has also been linked with the production of

cholera toxin or a cholera toxin-like toxin, and with

the ability of a strain to colonize the intestine.

Occurrence in the Environment

0018 As previously noted, nonepidemic strains of V. cho-

lerae are ubiquitous in the estuarine environment:

these organisms have been isolated from surface

water at multiple sites in North America, Europe,

Asia, and Australia, and it is likely that they are

present in coastal and estuarine areas throughout

the world. Nonepidemic strains have also been isol-

ated from a variety of wild and domestic animals,

including 6% of seagulls sampled in England; 14%

of dogs in Calcutta, India; cows, goats, dogs, and

chickens in India; ducks in Denmark; and horses,

lambs, and bison in Colorado.

Entry to Food Chain

0019 Nonepidemic V. cholerae can be isolated from a

high percentage of oysters and other filter-feeding

shellfish, particularly during warm summer months

when counts of the organism are the highest in estu-

arine waters. Isolation is not associated with the

presence of fecal coliforms. Results of a US Food

and Drug Administration study of random oyster

lots are shown in Table 1: overall, nonepidemic

(non-O1) V. cholerae strains were isolated from

14% of 790 oyster lots tested, ranging from a high

of 38.5% in July to a low of 0% in December and

March. Not unexpectedly, epidemiologic studies in

the USA have shown a significant association be-

tween non-O1/non-O139 V. cholerae diarrhea and

eating raw oysters.

0020Outbreaks of non-O1/O139 V. cholerae-associated

diarrhea have also been associated with other foods,

including chopped egg (on an airplane flight to Aus-

tralia), and preprepared gelatin (Mexico). In a study

in the Ban Vinai refugee camp in Thailand, nonepi-

demic strains were isolated from a number of food

items, including 4% of vegetables and 39% of meat

samples. Routes by which the organism entered the

food chain in these instances are unclear.

Fate on Processing

0021Characteristics of nonepidemic V. cholerae strains

during processing have not been extensively investi-

gated; preliminary studies suggest that they are

similar to those described for epidemic strains.

Detection in Food, Water, and Physiological

Samples

0022Isolation and identification techniques are identical

for epidemic and nonepidemic strains. Strains shown

by DNA probes or other genetic techniques to carry

genes for CT or NAG-ST would appear to have the

highest risk of causing illness. However, given our

current state of knowledge, it is not possible to differ-

entiate clearly nonepidemic V. cholerae which are

potentially pathogenic from those which are non-

pathogenic.

0023As noted below, nonepidemic V. cholerae can also

cause wound infections and septicemia. Isolation is

readily made from blood agar or other standard media

used in culturing wounds; the organism grows well on

standard blood culture media. Isolates from patients

with septicemia tend to be more heavily encapsulated

than general environmental isolates.

Symptoms and Characteristics

0024The most common manifestation of nonepidemic

V. cholerae infection is diarrhea. Based on outbreak

reports and volunteer studies, the incubation period

appears to be short (< 24 h). Abdominal cramps

may be prominent; bloody diarrhea is occasionally

reported. Illness is usually mild and self-limited, al-

though a diarrheal stool volume of 5.3 l was seen in

one volunteer receiving 10

CFU of one nonepidemic

strain.

0025Nonepidemic V. cholerae strains have also been

isolated from persons with septicemia. Mortality

rates in these cases exceed 50%. Illness appears to

be confined to persons with underlying liver disease

tbl0001 Table 1 Frequency distribution of oyster samples positive for

Vibrio cholerae by month of harvest

Month of

harvest

No. of samples No of samples

with V. cholerae

O1 Non-O1

January 73 0 (0) 1 (1.4)

February 68 0 (0) 3 (4.4)

March 68 0 (0) 0 (0)

April 64 0 (0) 5 (7.8)

May 53 1 (1.9) 7 (13.2)

June 62 2 (3.2) 22 (35.5)

July 104 3 (3.2) 40 (38.5)

August 85 1 (1.2) 20 (23.5)

September 93 0 (0) 11 (11.8)

October 53 0 (0) 1 (1.9)

November 40 0 (0) 1 (2.8)

December 27 0 (0) 0 (0)

Percentages are given within parentheses.

From Twedt RM, Madden JM, Hunt JM et al. (1981) Characterization of

Vibrio cholerae isolated from oysters. Applied Environmental Microbiology

41: 1475–1478.

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