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

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This became a widespread biological assay for vita-

min D in foods.

0014 Rats were the principal animal used to discover

most of the vitamins, the essential trace elements,

and the essential amino acids. As a result, more is

known about the nutritional requirements of the

rat than about any other species. Dogs, chickens,

pigeons, mice, and guinea-pigs have also made valu-

able contributions to our knowledge of nutrition.

Animals as Models of Human Nutrition in

Research

0015 Factors considered when selecting an animal model

include anatomical, physiological, and biochemical

similarities to humans, similarities of disease pro-

cesses, susceptibility to etiological agents, availability,

cost, breeding lines available, behavior, size, genetic

characteristics, lifespan, resistance to infections, suit-

ability for experimental manipulation, and accumu-

lated pathobiological information. Considerations

particularly pertinent to nutrition research are as

follows.

Natural Diet in Habitat

0016 The omnivorous feeding patterns of the rat usually

make it a better model for human-nutrition questions

than a strict herbivore such as the rabbit. Although

nonhuman primates may be most genetically related

to humans, primates include insectivores, herbivores,

and omnivores. Researchers must evaluate each

primate species separately. Strict carnivores such as

cats have associated differences in nutrient metabol-

ism and requirements. For instance, the cat requires

arachidonic acid and preformed vitamin A from

animal foods, as it cannot synthesize these from the

respective plant food precursors, linoleic acid and

b-carotene.

Nutrient Requirements

0017 The requirement for vitamin C is a striking example

of qualitative differences between species; few species

require it in the diet. Humans share this uncommon

requirement with other primates, the guinea-pig, the

red-vented bulbul, and some Indian fruit-eating bats.

0018 Dietary fiber may provide a more subtle example

of species differences in nutrient requirements. Two

herbivores, the guinea-pig and the rabbit, require

dietary fiber, according to the US National Research

Council. Other laboratory animals are apparently not

as vulnerable to a fiber deficit. However, fiber is

routinely added to research diets for rodents, and

continued research may reveal reduced gastrointest-

inal diseases associated with fiber in the diets of

primates.

0019Quantitative comparisons of nutrient requirements

across species are difficult: limited research on some

species has yielded knowledge of adequate intakes

without determination of minimum requirements.

Vitamin requirements between species are influenced

by differences in production by intestinal flora. The

mineral requirements of most species are quite

similar.

Digestion and Absorption

0020The relative influence of gastrointestinal microorgan-

isms on metabolism of digesta varies widely between

species. Extensive fermentation in the pregastric

chambers of ruminants and the hindgut of the horse

makes these animals poor models for human nutri-

tion. Dogs and pigs are similar to humans in many

aspects of gastrointestinal morphology and physi-

ology, including the relative length of small and

large bowels, ingesta transit times, influence of diet-

ary factors on gastric emptying, glucose or xylose

absorption, fecal fat excretion, activities of intestinal

brush border and pancreatic enzymes at maturity, and

colonic volatile fatty acid concentration. However,

humans, dogs and pigs differ in the developmental

patterns and primary structure of some digestive

enzymes. The composition of bile and the structure

of bile acids differs substantially between humans

and pigs. Colonic volatile fatty acids may be an

important energy source for the pig, but not for the

dog; the importance of colonic fermentation for

humans probably falls between these two species.

Numerous strains of miniature pigs have been de-

veloped and used in experiments related to digestion

and absorption.

Body Composition, Nutrient Metabolism, and

Excretion

0021Species differences in chemical composition may

influence the suitability of animals as models for

human-nutrition problems. As an example, differ-

ences in relative skeletal mass may reduce the useful-

ness of animal models for bone health and related

nutrients. The skeleton constitutes about 16% of the

adult human body, as compared to 11% of the rat,

10% of the rabbit, and 7.7% of a 28-week-old pig.

This probably accounts for considerably higher

amounts of calcium and phosphorus per kilogram of

fat-free body tissue in humans than in pigs, cats,

rabbits, rats, or mice. Human cortical bones have

greater nitrogen and lower calcium:nitrogen ratios

than those of pigs, cats, rabbits, rats, and fowl. Dif-

ferences in nutrient excretion may complicate animal

modeling further. For example, the rat excretes less

than 1% of dietary calcium in the urine, which is

an important route for calcium excretion (and its

234 ANIMAL MODELS OF HUMAN NUTRITION

hormonal control) in humans. These examples may

help explain why there has not been a satisfactory

animal model for human osteoporosis.

0022 Coprophagy (the ingestion of feces) by rabbits and

rodents can confound dietary intake measurements in

nutrition studies. By increasing the total nutrient

intake, coprophagy can lower apparent requirements

and reduce signs of deficiency for many nutrients.

Particularly affected are those nutrients synthesized

or made more bioavailable through colonic microbial

flora, including the B-complex vitamins and essential

fatty acids. To study signs of deficiency for such

nutrients, steps must be taken to prevent coprophagy.

Reproduction

0023 Animal studies have demonstrated vital roles for

nutrition from estrus to parturition and lactation.

For example, animal studies have shown the essenti-

ality of zinc for normal estrus cycling and fertility,

development of preimplantation eggs, normal devel-

opment of organ systems (especially the skeletal and

central nervous systems), fetal growth, and normal

labor and delivery. Zinc deficiency during specific

stages of gestation causes postnatal abnormalities in

behavior and immune function.

0024 Special considerations when evaluating animals as

models of human reproduction include the number of

fetuses, the type of placentation, the tendency to

abort or resorb fetuses under teratological conditions,

the rate of development, and the maturity of the fetus

at delivery. Because members of a litter have a similar

genetic inheritance and intrauterine environment,

these similarities must be considered to plan experi-

ments with an appropriate number of animals and

distribution of experimental treatments. Maturity at

birth can determine the suitability of an animal model

for studies of late gestational development. For

example, epiphyseal calcification of the femur is

much greater in newborn piglets than in newborn

humans, and pigs walk soon after birth. This would

limit the usefulness of the pig in some studies of

prenatal bone development. Maturation at birth is

also a concern when selecting animals to study early

infant development. Another difficulty is that new-

born mammals often require maternal lactation,

limiting the investigator’s control of dietary variables

in early life.

Animal Models of Nutrient Evaluation

0025 Historically, animals were useful for food evaluation,

such as vitamin assays, because chemical techniques

were inadequate for direct analysis of foods. While

chemical-analysis difficulties have largely been over-

come, difficulties predicting nutrient bioavailability

have not.

0026Bioavailability is the fraction of a nutrient in food

that is absorbed and utilized. It is affected by chemical

form, interactions with other food components, and,

probably, physiological responses to food. For

example, the zinc bioavailability of foods fed to rats

depends on the amount of food fed, even though the

foods are compared in amounts providing similar

quantities of zinc. Important in vivo variables may

be pancreatic secretions in response to different

foods, competition between endogenous (pancreatic

carboxypeptidase) and dietary sources of zinc for

absorption, and coabsorption with ligands such as

histidine that have separate facilitated pathways of

absorption. In vitro estimates of zinc absorption are

limited by our incomplete understanding of the

dynamic gastrointestinal response to foods.

0027For investigating the bioavailability of some nutri-

ents, even animal models may not be sufficient. For

example, the heme form of iron present in foods of

animal origin is much better absorbed by humans

than ferrous iron; this is not true for rats.

0028The nutritional quality of dietary proteins has been

evaluated since as early as 1917 by measuring animal

growth or nitrogen retention. Despite attempts since

the mid-1940s to replace the biological assays with a

‘chemical score’ of amino acid composition, the

biological assays continue to be used extensively.

Although chemical scoring accounts for essential

amino acid composition and requirements, scoring

does not account for differences in amino acid bio-

availability, which can be reduced by chemical

changes during heating, or by inhibitors of proteolytic

digestion.

0029In vitro testing has progressed substantially and is

often preferred by scientists for efficient use of re-

sources. However, the complexity of living organisms

remains incompletely understood, and frequently, the

nutritional value of foods or diets is more accurately

evaluated by direct in vivo testing.

Genetically Altered Animal Models

0030Inheritance affects individual responses to nutritional

stress. Genetic factors may determine the absorption

and/or utilization of a given nutrient. Also, the

amount of the nutrient in the diet may influence

gene expression. Genetic engineering technology has

been used to study the effects of overexpression of a

specific gene on nutrient metabolism. More recently,

gene-ablation technology, commonly known as gene

knockout, has been used (primarily in mice) to

study the effects of inactivating a specific gene. Mice

with alterations to specific genes are produced by

targeting the specific gene in the embryonic stem

cells. Knockout mice provide an opportunity to

ANIMAL MODELS OF HUMAN NUTRITION 235

analyze the function and physiological effects of spe-

cific mammalian genes, to model a range of human

inherited disorders (e.g., low-density-lipoprotein re-

ceptor knockout mice for the study of familial hyper-

cholesterolemia and vitamin D-receptor knockout

mice for the study of dietary calcium and bone health)

and to explore potential intervention strategies for

disease treatment. Cross-breeding of knockout mice

to strains with other mutations can be useful in under-

standing biochemical controls and interactions. For

instance, a mutation in the HFE protein is associated

with hemochromatosis, a disorder of excessive iron

absorption and accumulation. Similar iron accumula-

tion occurs in HFE knockout mice, and this effect can

be exacerbated or reduced by cross-breeding these

mice with other knockout mice missing genes for

other proteins involved with iron absorption and me-

tabolism. Such mice can be further studied to assess

the interaction of the genetic mutation with different

forms and concentrations of dietary iron. Newer

methods can introduce more subtle gene alterations,

including specific point mutations. Animal research is

making an important contribution to improved

protocols for gene therapy, which should help in the

alleviation of many inherited human diseases.

Animal Models of Disease States

0031 With the help of animal models, a major cause of

human disease – overt nutrient deficiency – was

largely solved as a scientific problem (it unfortunately

remains as a political and economic problem). Scien-

tific emphasis has turned to diet and chronic disease.

Perhaps because they are as yet unresolved, the prob-

lems of chronic disease seem more complex. Dietary

variables are likely to be slight deficiencies, excesses,

or imbalances in a lifelong interaction with other

genetic and environmental factors. Animal models

can provide the advantage of controlled environmen-

tal and dietary factors over a short lifetime. While

genetic differences can limit application to humans,

animal models of disease are improving through gen-

etic technology. The use of animals to study nutrition

and major chronic diseases is considered briefly

below.

Atherosclerotic Cardiovascular Disease

0032 The responsiveness of serum cholesterol and athero-

sclerosis to dietary cholesterol and saturated fatty

acids varies among animal species. Rabbits, guinea-

pigs, swine, and rhesus and cynomolgus monkeys are

more susceptible than humans. Rats and dogs are

more resistant. Baboons and vervet monkeys are in

the same moderate range of susceptibility as humans.

Genetic differences in lipid metabolism are confirmed

by the variation observed within and between species.

Hypertension

0033Hypertension in response to dietary salt is not

observed in all animal models but occurs in specific

animal strains without sufficient renal capacity to

excrete salt rapidly. The Dahl S and the Kyoto spon-

taneously hypertensive rat are susceptible to dietary

salt, and the addition of potassium to high-salt diets

reduces the incidence of stroke in these animals, and in

the Sprague–Dawley rat. Research on animal models

verifies an interaction between diet and genetic sus-

ceptibility to hypertension, and susceptible animals

may be useful in identifying dietary variables that

affect susceptible humans.

Obesity

0034Genetically obese strains of rodents – obese (ob/ob)

and diabetic (db/db) mice and obese (fa/fa) rats

(Figure 1) – confirm that inheritance can contribute

to obesity. The obese strains are either resistant to

leptin (db/db mice and fa/fa Zucker rats) or deficient

in leptin (ob/ob mice), a hormone produced by

adipocytes. This in turn results in overfeeding and

increased concentrations of Neuropeptide Y in

plasma and in the hypothalamus. Obesity in such

models has been associated with hyperinsulinemia,

abnormal glucose tolerance, and high body-fat com-

position even with normal diets. Rats without genetic

obesity increase their food intake and thermogenesis

in response to a ‘cafeteria’ diet of mixed human food.

The relationship between energy intake, physical ac-

tivity, thermogenesis, and body weight has been ex-

tensively studied in rodents. Results of these studies

generally support the biological maintenance of a

‘set-point’ for body weight; that varies only slightly

and controls energy balance.

Cancer

0035Approximately one-third of human cancer mortality

may be related to diet. Animal studies, mostly using

rats, have indicated that tumor development is en-

hanced in a variety of tissues by high-fat diets, espe-

cially diets rich in o-6 (but not o-3) polyunsaturated

fatty acids. This effect of high-fat diets has not been

completely differentiated from the effect of high

energy consumption. Animal models have shown

that selenium inhibits both the initiation and prolif-

erative phases of tumorigenesis. The effect of some

dietary components may depend on the specific site,

type, and stage of carcinogenesis as well as the

relative nutrient requirements of host and tumor.

For instance, zinc deficiency in animals increases

236 ANIMAL MODELS OF HUMAN NUTRITION

the incidence of esophageal carcinoma induced by

methylbenzylnitrosamine but decreases the incidence

of tumors induced by 3-methylcholanthrene and

4-nitroquinoline-N-oxide.

0036 Animal models are commonly used to test food

additives for carcinogenicity. Careful studies gener-

ally involve more than one species and exposure

over an extended portion of the lifespan. A US food

additive law, known as the Delaney Clause, which

prohibits the use of a food additive in any amount if

it has been shown to produce cancer in animal stud-

ies, has been controversial because it prohibits any

amount of a substance that may have been tested only

in high amounts. The evaluation of research results

must consider the average and peak human exposures

to the substance, and the potency of the substance to

determine whether dietary characteristics have been

experimentally exaggerated, and whether extrapola-

tion to humans is realistic.

Osteoporosis

0037 Diets low in calcium or high in phosphorus increase

bone reabsorption and decrease bone mass in rats,

mice, cats, dogs, and nonhuman primates. In contrast

with experimental animals, calcium balance in

humans is relatively insensitive to high dietary phos-

phorus. There are few animals that experience the

spontaneous ovarian failure in middle age that occurs

in humans. Researchers have not identified any ap-

propriate animal model of postmenopausal or age-

related osteoporosis (see the above section Body

Composition, Nutrient Metabolism, and Excretion).

Diabetes Mellitus

0038 Experimental diabetes can be induced in animals by

pancreatectomy or injection of b-cell toxins such as

streptozotocin or alloxan. There is a genetically obese

strain of diabetic (db/db) mice. The Psammomys

obesus (sand rat) strain of rat remains lean and

nondiabetic in the wild but becomes obese and dia-

betic under laboratory feeding conditions. In normal

strains of animals, a greatly increased food intake for

an extended time leads to adiposity and an increased

incidence of insulin resistance, which is reversible

with weight reduction. It has not been possible with

animal research to show that a high energy consump-

tion causes diabetes.

Interpretation and Extrapolation of Data

0039Animal studies are most appropriately applied to

humans when they complement, and are consistent

with, human studies. Relevance of animal research to

humans is more likely if the results are confirmed in

several animal species.

0040The highly uniform experimental conditions char-

acteristic of animal models can provide disadvantages

as well as advantages. For example, energy restriction

reproducibly increases longevity in rodents. However,

such studies are usually conducted under laboratory

conditions in which the rodents spend their entire

lives in a small space, have no social relationships,

do not reproduce, have low exposure to hazardous

biological or chemical substances, and have little

need for physical activity or development of self-

preservation skills. Scientists must evaluate whether

the food-restricted animals would have an improved

quality, or even quantity, of life if tested under more

realistic living conditions.

0041The control of experimental diets in animal nutri-

tion studies can present similar problems in extrapo-

lation to humans. To enhance experimental control

fig0001 Figure 1 Control and fa/fa Zucker rat, a genetic strain used to investigate obesity. From Judith S. Stern, Sc.D., Professor, University

of California at Davis, USA with permission.

ANIMAL MODELS OF HUMAN NUTRITION 237

and comparability between studies, animal diets for

nutrition research are often standardized, purified,

and fed ad libitum. Purified diets composed of a

small number of refined ingredients, such as refined

proteins, carbohydrates, and fat, with added vitamin

and mineral mixtures, reproducibly control specific

nutritional variables but also limit the context of the

experiment. Unlike many animal research diets,

human diets contain thousands of compounds and

are usually scheduled in meals. As nutrition research

moves from single nutrient deficiencies to more com-

plex dietary interactions that affect health, laboratory

diets and other conditions may need to become more

like human conditions to facilitate comparability to

humans. An example is the ‘cafeteria’ diet of mixed

human food used to attain overeating in rodents.

Limitations of Animal Models in Nutrition

Research

0042 Nutritional knowledge has rapidly expanded in the

nineteenth and twentieth centuries. During this time,

an increasing share of biomedical advances depended

on animal research. Two-thirds to three-quarters of

major biomedical advances in the 1900s required the

use of animals. This trend was accompanied by an

antivivisectionist movement in Victorian England in

the late 1800s, which may be a predecessor of the

current ‘animal rights/liberation’ movement. High-

quality animal care improves experimental reliability

and engenders public trust. Scientists have an ethical

obligation to ensure animal well-being and minimize

pain and suffering. Scientists must be involved in

public policy influencing legal regulations that benefit

humans through science while treating animals

humanely and without inefficient bureaucracy.

0043 Scientists should consider alternative methods,

including the use of more socially acceptable species,

such as the experimental use of rodents rather than

dogs, cats, or monkeys, and the possible use of non-

mammalian vertebrates, invertebrates, and micro-

organisms. However, depending on the research

problem, such alternatives may be unacceptable in

answering questions applicable to humans. Nutrition

knowledge may also be gained by using cell and tissue

cultures, human tissues removed at surgery or at

autopsy, and in vitro systems and mathematical

models. Such methods can be more efficient, con-

trolled, and economical than research with living

animals. But again, researchers must be cautious not

to extrapolate to human nutrition without adequate

validation of the simpler model.

0044A straightforward alternative to using animals is

to study humans directly. Although the technology to

study humans safely continues to improve, many

nutrition research topics require animal models.

Such topics include the effects of nutrition on repro-

duction, growth and development, longevity, and be-

havior. Animal experiments can verify observations in

humans that often cannot be controlled sufficiently to

be conclusive. The use of animals for initial experi-

ments in nutrition research improves efficiency and

progress. Animal studies facilitate the investigation

of physiological and molecular mechanisms. Animal

research has been instrumental in identifying required

nutrients and developing the science of nutrition.

Animal research continues to answer questions

about nutrition and health that can be learned only

from living organisms.

See also: Atherosclerosis; Cancer: Epidemiology;

Coronary Heart Disease: Etiology and Risk Factor;

Diabetes Mellitus: Etiology; Hypertension: Physiology;

Obesity: Etiology and Diagnosis; Osteoporosis; Zinc:

Properties and Determination; Physiology

Further Reading

Hui DY (1998) Utility and importance of gene knockout

animals for nutritional and metabolic research. Journal

of Nutrition 128: 2052–2057.

Lusk G (1933) Nutrition. New York: Paul B Hoeber.

National Research Council, Committee on Diet and Health

(1989) Diet and Health. Implications for Reducing

Chronic Disease Risk. Washington, DC: National

Academy Press.

National Research Council, Committee to Revise the Guide

for Care and Use of Laboratory Animals (1996) Guide

for the Care and Use of Laboratory Animals. Washing-

ton, DC: National Academy Press.

Phillips RW (ed.) (1984) Animal Models for Nutrition Re-

search. Report of the Fifth Ross Conference on Medical

Research, Ross Laboratories, Columbus, Ohio.

Widdowson EM (1986) Animals in the service of human

nutrition. Nutrition Reviews 44: 221–227.

238 ANIMAL MODELS OF HUMAN NUTRITION

ANNONACEOUS FRUITS

A P George and R J Nissen, Maroochy Horticultural

Research Station, Nambour, Queensland, Australia

This article is reproduced from Encyclopaedia of Food Science,

Introduction

0001 The main commercial species of Annona grown

throughout the world are the cherimoya (A. cheri-

mola), the atemoya (A. hybrids), and the sugar

apple (A. squamosa). Expansion of production of

these three species in many subtropical countries is

limited by several factors, including low yields of

better-quality cultivars, unattractive external appear-

ance of the fruit, a high susceptibility of the fruit to

blemishing, poor and unreliable internal fruit quality,

and a very short postharvest shelf- and storage life. In

the short term, fruit quality can be improved by field

management practices. In the longer term, selection

and breeding of new varieties will be necessary.

Classification

0002 The family, Annonaceae, comprises 50 genera. Three

genera (Annona, Rollinia, and Asimina) produce

edible fruit, but only two genera are of com-

mercial importance – Annona, comprising approxi-

mately 100 species, and Rollinia, comprising

approximately 50 species. The four most commer-

cially important species are the cherimoya, the sugar

apple, the atemoya, and the soursop (A. muricata).

The cherimoya is native to the subtropical highlands

of Peru and Ecuador, and is grown commercially in

Chile, Spain, California, and New Zealand. The

atemoyas, most of which are hybrids between A.

cherimola and A. squamosa, are grown commer-

cially in Florida and Australia. Both the sugar apple

and the soursop are widely distributed throughout

the tropical regions of South-east Asia and Central

America, where they are found growing wild. The

rollinia (Rollinia mucosa) and biriba (R. deliciosa)

are native to the jungles of South America. A list of

the edible species of Annona and Rollinia grown

throughout the world is presented in Table 1.It

should be noted that common names, such as custard

apple, have been used with reference to many differ-

ent species.

Climate

0003 Most Annona species are tropical or subtropical in

their growth requirements. Both the atemoya and the

cherimoya are best grown in frost-free locations as

the young trees are killed at 1



C and mature trees at

3



C. The cherimoya is more cold-tolerant than the

atemoya and is able to stand a longer duration of cold

at 3



C. The sugar apple and the soursop, on the

other hand, are very frost-sensitive. Most cherimoya

and atemoya cultivars are semideciduous and enter

either a true rest or environmentally induced dor-

mancy in the late winter or spring. This dormancy

or rest period allows the plant to avoid the effects of

late-winter frost and drought.

0004Different species exhibit varying climatic require-

ments for fruit development and maturation. Exces-

sively low temperature during the fruit maturation

period may retard the process, while excessively

high temperatures during this period may cause pre-

mature ripening and fermentation of the fruit whilst

still on the tree. For example, atemoya cultivars

grown in cool subtropical regions of California or

New Zealand may fail to mature properly. In these

regions the main commercial species grown is the

cherimoya. In contrast, cherimoya fruit grown in

tropical climates often fails to develop full flavor,

and postharvest shelf-life is short.

0005Besides the influence of temperature on fruit

maturation, physiological disorders such as skin rus-

setting are more prevalent under cool night tempera-

tures, particularly when ambient temperatures fall

below about 13



Fruit Morphology

0006The cherimoya, atemoya, and sugar apple fruits are

syncarpiums, made up of many individual carpels

which are fused together with the receptacle to

form a fleshy mass. Each carpel, if pollinated, con-

tains an oval seed. Depending on species and culti-

var the number of seeds per 100 g of flesh can vary

from five to 15. The fruit ranges in shape from con-

ical, through globular to ovoid, and the skin type

may be smooth, finger-imprinted, or bumpy. The

skin is relatively thick and contains numerous

stomata. The mesocarp consists mainly of paren-

chyma, cholenchyma, and sclerenchyma cells, the

latter often being highly lignified, similar to those

found in pears.

Varietal Selection and Breeding

0007The atemoya and the cherimoya produce fruit super-

ior in quality to other Annona species. The fruit

of some species, such as the bullock’s hearts (A.

ANNONACEOUS FRUITS 239

reticulata) and ilama (A. diversifolia), are barely

edible. The fruit of the sugar apple are highly seeded

and are not grown commercially in regions where

cherimoya or atemoya can be grown. The fruits

of rollinia and biriba, although edible, deteriorate

rapidly within a few days after harvesting, thus

limiting their commercial acceptability for local

markets only.

0008 The University of Puerto Rico’s Agricultural Ex-

periment Station at one time cataloged 14 different

types of soursop. In El Salvador, two types of soursop

are grown: guanaba azucaro

n (sweet), eaten raw and

used for drinks, and guanaba acida (very sour), used

only for drinks. A yellow, fiberless form of soursop

has been selected in Cuba.

0009The most important commercially grown cultivars

are as follows: of cherimoya, Bronceada (Chile), Fino

de Jete (Spain), and Bays (California); of atemoya,

African pride (Australia) and Gefner (Israel, Florida

and Hawaii); of soursop, Cuban fiberless. Wide

genetic variability exists between different species of

cherimoya and atemoya. Selection of varieties with

round, symmetrical shape, smooth skin, high ratios of

flesh to seed, and long postharvest storage life is

highly desirable. Intensive varietal selection programs

for cherimoya are currently being undertaken in

Spain, New Zealand, and Chile. A small breeding

program, currently in progress in Queensland, Aus-

tralia, has produced promising new interspecific and

intraspecific hybrids.

tbl0001 Table 1 Important species of the genera Annona and Rollinia

Speciesnames Common names Chromosome

number (2n)

Gene center Potential uses

Annona hybrids Atemoya 16 Various Fresh fruit

Cherimorinones Rootstock

Custard apple Processing with dairy products

A. cherimola Mill Cherimuyu

Cherimoya

Cherimola

16 Andean valleys of

Peru and Ecuador

Fresh fruit

Rootstock

Processing with dairy products

Custard apple

A. squamosa L. Sugar apple 16 West Indies Fresh fruit

Sweetsop Rootstock

Sitaphal Processing with dairy products

Ata

Custard apple

A. reticulata L. Bullock’s hearts 16 West Indies, Mexico Fresh fruit

Ramphala Rootstock

Custard apple (often

considered the true

custard apple)

A. muricata L. Soursop 16 West Indies, Mexico Fresh fruit

Guanabana Drinks and pure

Corossol Processing with dairy products

Graviola

A. glabra L. Pond apple 28 Florida (USA) Rootstock

Alligator apple

A. senegalensis Wild Transvaal apple South Africa Pollinator species

Rootstock

A. diversifolia Safford Ilama Mexico, Guatemala,

El Salvador

Fresh fruit

Cherimoyer of the lowlands

A. montana Macf. Mountain soursop 16 Cuba, West Indies Fresh fruit

Rootstock

A. purpurea Moc. and Sesse Soncoya Mexico Fresh fruit

Manirote Rootstock

A. longiflora Wild cherimoya Mexico Rootstock

A. scleroderma Safford Posh te Mexico, Guatemala Fresh fruit

Rollinia deliciosa Safford Biriba 48 Brazil Fresh fruit

Rootstock

R. emarginata Schlecht Brazil, Paraguay Fresh fruit

Rootstock

R. mucosa Rollinia Brazil, Paraguay Fresh fruit

Rootstock

240 ANNONACEOUS FRUITS

Maturity and Quality

0010 No reliable quantitative maturity indices for when to

harvest Annona fruit have been developed. Individual

trees are normally harvested up to 10 times, and fruits

are judged to be mature when the skin changes from a

darker to a lighter green and becomes smoother. In

some regions, fruits which develop during the colder

winter months may fail to mature properly. Total

soluble solids contents at full maturity can vary

from 18% to 28%.

Physiological Disorders

Fruit Splitting

0011 Fruit splitting may occur while fruits are still on the

tree or after harvest. Splitting appears to be related to

sudden changes in fruit moisture content or tempera-

ture. Some cultivars appear to be less susceptible than

others.

Russetting

0012 Superficial russetting of skin seems to be caused by

low night temperatures (less than 13



C), accompan-

ied by low humidity. Near-mature fruit appear to be

particularly susceptible. Cherimoya cultivars are

apparently less susceptible than atemoya cultivars.

Crocodile Skin

0013 The extremely wavy and pointed carpels that are

symptomatic of this disorder are particularly severe

on highly vigorous trees, which may indicate some

harmful effect of tree vigor on pollination processes.

Based on fruit and leaf analyses, nutrition does not

appear to be implicated.

Hard Seed Casing and Brown Lumps

0014 Possible causes are boron deficiency or sudden

changes in fruit water content.

Postharvest Handling and Physiology

0015 The skin of most Annona fruits, in particular those

cultivars which produce fruit with protruding carpels,

is easily damaged by rough handling. Fruits are usu-

ally size-graded by hand because of their irregular

shape, and are packed into single-layer trays before

shipment. The cherimoya and atemoya are classified

as climacteric fruits which show two peaks in carbon

dioxide production. The fruit softens, develops pleas-

ant aroma and flavor, and is considered ripe at the

beginning of the second respiratory rise. Compared

with other fruits, the cherimoya and atemoya have

high rates of ethylene production and respiration.

With the exception of a few cultivars, postharvest

shelf-life is short (between 7 and 10 days). (See

Ripening of Fruit.)

Storage

0016The optimum storage temperatures for atemoya and

cherimoya fruit are between 13



C and 16



C. At

these temperatures most atemoya and cherimoya cul-

tivars can be stored for up to a maximum of 2 weeks

with minimum loss of quality. One cultivar of cher-

imoya, Bronceada, has a reported cool storage life of

3 weeks. Storage at temperatures below 13



C for

more than 1 week can cause severe chilling injury.

Chilled fruit develops blackened skin, discoloration

of the core, and watery patches in the fruit flesh; after

removal from storage the fruit fails to ripen properly.

However, fruit used for processing can be stored for

1 week at between 5



C and 10



C without loss of

internal fruit quality. For short-distance transport

precooling of fruit at 10



C for up to 18 h prior to

shipment at ambient temperatures has been shown to

be beneficial in extending shelf-life by 3–4 days. Be-

cause of the presence of numerous stomata on the

surface of the fruit, one of the main problems during

storage is rapid water loss. Maintenance of relatively

high humidity during storage should improve the

appearance of fruit after the removal from storage.

The main postharvest disease is anthracnose, caused

by a range of disease organisms (Colletotrichum spp.,

Phomopsis spp., Rhizopus spp.). Postharvest fungi-

cidal dips have successfully controlled fruit rots, pro-

vided that recommended dipping temperatures and

concentrations are adhered to. Only limited studies

have been conducted on controlled-atmosphere stor-

age of Annona species. Further studies are needed to

evaluate the benefits of packaging fruit in polyethyl-

ene bags, which may help to prevent water loss and

blackening of fruit during storage. (See Controlled-

atmosphere Storage: Applications for Bulk Storage of

Foodstuffs; Fungicides; Storage Stability: Mechan-

isms of Degradation.)

Fresh Food Uses

0017The flesh of most Annona species is most commonly

eaten out of hand. Because seeds of the fruit are

interspersed throughout the flesh, cultivars contain-

ing few seeds are the most desirable. Eating quality of

atemoya and sugar apple fruit, which are particularly

sweet, may be enhanced by adding a few drops of

lime juice to the flesh. Soursops of least acid flavor

and least fiber are the only ones suitable for eating

fresh. The best eating quality is obtained from fruit

that has been ripened at 17–20



C and then placed in

the refrigerator to cool just before eating. In terms of

ANNONACEOUS FRUITS 241

appearance, color, flavor, and texture, the most

acceptable pulp for both eating and processing is to

be found 1 day after the first detectable softening.

Softened fruit can be stored in the refrigerator (4



for about a week with a minimal loss in flavor, but

some skin blackening will result. Segments of the pulp

can be added to fruit salads, or used for making

sherbets or icecream.

Processed Products

0018 Atemoya, cherimoya, and soursop pulp has potential

for mixing with dairy products such as icecream and

yogurt, and sweetened soursop juice can be made into

a canned beverage. Because of its higher acidity, sour-

sop pulp is the most suitable of all the Annona species

for processing. Cultivars with a low level of grit or

fiber in the flesh have been found to be more suitable

for processing than others. Passing the flesh through

fine screens (20 000–10 000 mm), and homogeniza-

tion, as used for guava pulp, should eliminate this

problem. The pulp can also be used to make semi-

dried fruit ‘leathers,’ and jams and jellies of fair flavor

and quality. In Central America, sweet soursop pulp

is sieved and squeezed, diluted with either milk or

water, and sweetened, before canning to make a

refreshing drink. When mixed with a little cream or

icecream, the frozen soursop concentrate makes a

delicious dessert.

0019Some species of Annona have been used in

the production of soaps, domestic cooking oils,

essential oils, herbal medicines, alcohol, fertility

drugs, and insecticides. However, the commercial

potential of these products at the present time appears

limited.

Pulp Extraction

0020The production of pulp on a commercial scale does

not appear to be easy because the skin of Annona

fruits, at full ripeness, is soft and disintegrates easily

if conventional processing techniques are used for

skin removal. Other processed fruits, such as

mango, passion fruit, and guavas, have leathery

skins which are brushed clean of pulp before being

discarded. Annona fruit disintegrates and is brushed

through the screens and mixed in with the pulp. The

skins of most Annona fruits are high in polyphenols.

This causes two problems when the skin is mixed

with the flesh – a rapid browning of the pulp and a

strong off-flavor. The Food Industry Development

Centre of the University of New South Wales, Austra-

lia, has evaluated two methods for removing custard

apple pulp – a screen pressing process and a reaming

process. Although the reaming process offers yield

advantages, it requires the use of skilled labor, and

this would reduce its potential economic advant-

ages. A prototype screen press extractor has been

tbl0002 Table 2 Chemical and nutritional composition (per 100 g of ripe fruit) of the more important Annona spp. fruits

Parameter Cherimoya Atemoya Sugar apple Soursop

Water (g) 74.6–82.8 71.5–78.7 72.5–79.0 77.9–84.0

Fiber (g) 1.5–4.3 0.05–2.5 1.0–1.6 0.8–1.2

Starch (g) NA 1.1 NA NA

Sugar (g) 12.0–15.0 18.1 14.6 10.4–12.5

Ash (g) 0.6–1.0 0.4–0.75 0.4–1.4 0.6–0.9

Fat (g) 0.1–0.4 0.4–0.6 0.4–0.6 0.6–1.0

Protein (g) 1.0–2.4 1.1–1.4 1.3–2.4 0.7–1.7

Total acidity (citric acid equivalent) 0.17–0.50 0.2–0.6 NA 0.9–1.3

pH 3.9–4.8 4.4–5.1 3.9–4.8 3.6–4.8

Total energy (kJ) NA 310–394 368–398 267–297

Ascorbic acid (mg) 4.3–16.8 50 10–51 13–32

Carotene (mg) 0.0–0.02 0.0–0.02 0.01 0.0–0.01

Thiamin (mg) 0.06–0.13 0.05 0.11–0.17 0.05–0.11

Riboflavin (mg) 0.11–0.15 0.07 0.08–0.16 0.03–0.05

Nicotinic acid (mg) 0.73–2.03 0.80 0.7–1.0 0.57–1.28

Calcium (mg) 8.0–32.0 17 19.4–44.7 8–26

Magnesium (mg) 27 32 NA NA

Phosphorus (mg) 30.2–47.0 NA 23.6–55.3 27–29

Potassium (mg) 298–370 250 NA 179–265

Sodium (mg) 4–6 4.5 NA 9.0–14.0

Zinc (mg) NA 0.2 NA NA

Iron (mg) 0.8 0.3 0.28–0.36 0.5–0.8

NA, no data available.

Major sources: Morton JF (1987) Fruits of Warm Climates, pp. 65–91. Greenboro, Carolina: Media Incorporated; Duckworth RB (1966) The Composition of

Fruits and Vegetables, London: Pergamon Press; Nagy S and Shaw PE (1998) Tropical and Sub-tropical Fruits. Long Boat Key, Florida, FL: Florida Sc. Source

Inc.

242 ANNONACEOUS FRUITS

developed but this unit has yet to be tested commer-

cially. (See Phenolic Compounds.)

Pulp Storage

0021 Heating or pasteurization impairs pulp flavor consid-

erably, and often results in the development of a bitter

character. However, unblanched frozen pulps treated

with either ascorbic acid (1500–2000 mg kg

1

)or

potassium metabisulfite (500 mg kg

1

) can be stored

for up to 120 days with minimal loss of flavor. Upon

thawing, pulp treated with ascorbic acid may develop

a pinkish discoloration, whereas pulp treated with

potassium metabisulfite retains a bright, fresh color.

(See Ascorbic Acid: Properties and Determination.)

Nutritional Value

0022 The fruit is rich in starch when firm but increases

markedly in sugar as it softens. The main sugars are

glucose and fructose (80–90%). There is some phen-

olic content associated with an increase in the activity

of peroxidase, which causes oxidation of the pulp.

The volatile fraction consists of alcohol, esters, car-

bonyls, and hydrocarbons. The nutritional properties

of the more important Annona species are presented

in Table 2. Compared with other fruits, the Annona

fruits contain significant quantities of vitamin C, thia-

min, potassium, magnesium, and dietary fiber con-

tent. The calorific value of the flesh is high (300 kJ per

100 g) and is almost double that of peach, orange, and

apple. Refer to individual nutrients.

Marketing Characteristics

0023 Both the cherimoya and the atemoya are best eaten

as fresh fruits. Both fruits are currently virtually

unknown on world markets, and Chile is the only

country which exports significant quantities. The

major problem facing expansion of cherimoya and

atemoya production throughout the world is the

high perishability of the product. The transportation

of atemoya and cherimoya to distant export markets,

given current cultivars and postharvest technology, is

difficult. The processing potential of soursop and

other Annona fruits is yet to be fully exploited. (See

Fruits of Tropical Climates: Commercial and Dietary

Importance.)

See also: Ascorbic Acid: Properties and Determination;

Controlled-atmosphere Storage: Applications for Bulk

Storage of Foodstuffs; Fruits of Tropical Climates:

Commercial and Dietary Importance; Fungicides;

Phenolic Compounds; Ripening of Fruit; Storage

Stability: Mechanisms of Degradation