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FOOD ALLERGY
Methods of Detection and
Clinical Studies
FOOD ALLERGY
Methods of Detection and
Clinical Studies

Editor
Anas M. Abdel Rahman
Department of Genetics, Research Center
King Faisal Specialist Hospital and Research Center (KFSHRC)
and College of Medicine
Al-Faisal University
Riyadh
Saudi Arabia

p,
p,
A SCIENCE PUBLISHERS BOOK
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photo thethe
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Juan Fernandez Reproduced by kindby
seal: Reproduced courtesy of J.J. Alava
kind courtesy of L.P. Osman

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· Bottom-right photo of the Mediterranean monk seal: Reproduced by kind courtesy of A.A. Karamanlidis/MOm
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Preface

Bridging the gap between the clinicians and basic science researchers in
food allergy was the idea of writing this book. A few dozen of authors from
around the world were invited to share their bedside and bench top research
experience in the field of food allergy. We tried to cover all the clinical updates
in the first seven chapters starting from nomenclature to immunotherapy. The
other half of the book includes state of the art technology role in enhancing
the molecular knowledge in food allergy research and the updated experience
of the authors’ laboratories. The authors of these chapters introduced their
expertise in the novel technologies such as mass spectrometry and biosensors,
bioinformatics and databases, and the food labeling regulations. This book
will be a useful reading material for the young and expert scientists in food
allergy with the theme of introductory to the basic knowledge and literature
updates, respectively.
Contents

Preface v
1. Food Allergy Nomenclature 1
Sten Dreborg
2. Food Allergy in Children 14
Sophia Tsabouri, Gavriela Feketea and Nicolaos Nicolaou
3. Peanut Allergy: Clinical Relevance and Allergen Characterisation 35
Joana Costa, Caterina Villa, Telmo J.R. Fernandes, M. Beatriz P.P.
Oliveira and Isabel Mafra
4. The Pollen-Food Syndrome: An Update on Diagnostic and 58
Therapeutic Approaches
Sara Huber, Claudia Asam, Anargyros Roulias, Fatima Ferreira and
Lorenz Aglas
5. Advances in Seafood Allergy Research: Allergen Detection 80
and Allergen-Specific Immunotherapy
Nicki Y.H. Leung, Christine Y.Y. Wai, Ka Hou Chu and
Patrick S.C. Leung
6. Skin Prick/Puncture Testing in Food Allergy 106
Sten Dreborg
7. Immunotherapy for Food Allergy 131
Bright I. Nwaru and Aziz Sheikh
8. Allergenomics—A Strategy for Food Allergen Discovery 142
Anas M. Abdel Rahman
9. Proteomics in Food Allergy 160
Pasquale Ferranti, Anas M. Abdel Rhaman, Maria Adalgisa Nicolai
and Monica Gallo
10. Allergen Quantitation for Food Labeling 188
Martina Koeberl, Dean Clarke and Andreas L. Lopata
viii Food Allergy: Methods of Detection and Clinical Studies

11. Shellfish Allergy: Taking the Allergenomics Approach towards 205


Improved Allergen Detection and Diagnostics
Sandip D. Kamath and Andreas L. Lopata
12. Bioinformatics Approaches to Identifying the Cross-Reactive 225
Allergenic Risk of Novel Food Proteins
Ping Song, Rod A. Herman and Siva Kumpatla
13. The Pollen-Food Syndrome: A Molecular Perspective 246
Claudia Asam, Lorenz Aglas, Sara Huber, Fátima Ferreira and
Anargyros Roulias
14. Biotechnology: Methods for Assessing Potential Allergenicity 268
of Novel Proteins According to Global Regulations
Christal C. Bowman and Scott McClain
15. Advances in Biosensor Technologies for Food Allergen 289
Monitoring and Diagnosis
Shimaa Eissa, Raja Chinnappan and Mohammed Zourob
Index 311
CHAPTER 1

Food Allergy Nomenclature


Sten Dreborg

Introduction
Nomenclature is the basis for appropriate communication between scientists
and clinicians. Studies should be performed using defined methods, grouping
populations of patients with given characteristics, using words which describe
patients clearly enough to be understood by others. Results can be applied
to similar patients using the same methodology and patient characteristics
using established nomenclature. This makes nomenclature crucial to both
investigators as well as to clinicians to convey the message from research to
the clinic. Allergists as well as other scientists interested in allergy, and not
least lay persons and lay organizations must have a common language when
communicating.
The nomenclature of allergy and allergic diseases has varied from time
to time. However, within some areas confusing terms have been used such as
“non-atopic atopic dermatitis”, i.e., a dermatitis, clinically resembling that of
so called “atopic dermatitis” (with allergen specific IgE antibodies also called
eczema (Johansson et al., 2004)), but without allergen specific IgE antibodies.
That was, and still is, confusing. Accordingly, Gunnar O. Johansson formed a
task force within the European Academy of Allergy and Clinical Immunology,
EAACI, to write a position paper expressing the meaning of the Academy of
allergy nomenclature (Johansson et al., 2001). To make the message general he
later formed a group within the World Allergy Organization, WAO to discuss
the EAACI position paper (Johansson et al., 2001), adding views from other
continents and to agree on a common nomenclature for the worldwide allergy
community (Johansson et al., 2004). One of the main achievements was to start
using “eczema” instead of “atopic dermatitis”. However, as often happens,

Professor emeritus, Child and Adolescent Allergology, Women’s and Children’s Health Uppsala
University, Academic Hospital, SE-751 85 UPPSALA, Sweden.
Email: sten.dreborg@kbh.uu.se
2 Food Allergy: Methods of Detection and Clinical Studies

conservatives maintained atopic dermatitis as a parallel option to eczema,


why “non-atopic atopic dermatitis” could not be eradicated. Since then, many
people have tried to implement the new nomenclature. However, allergy and
thereby allergy nomenclature, concerns not only allergists, but even specialists
within adult and pediatric gastroenterology, dermatology, Ear, Nose and
Throat (ENT), and respiratory medicine, who therefore have an interest in
allergy nomenclature. All these related specialists and even lay persons and
lay organizations must be involved to implement the allergy nomenclature
to achieve global mutual understanding.
Recently, a Nomenclature Review Committee was set up by the WAO
Board of Directors (Rosenwasser et al., in prep.) for the purpose of updating
the present nomenclature (Johansson et al., 2004).
This chapter presents the existent nomenclature (Johansson et al., 2004)
discussing possible changes of the Food Allergy Nomenclature (Johansson et
al., 2001; Johansson et al., 2004).

General considerations

Hypersensitivity is the global term describing not tolerating an environmental


factor tolerated by the majority. Hypersensitivity can be mediated either by an
immunological mechanism, i.e., allergy, or by non-immunological mechanisms.
It does not include infection, autoimmunity or toxic reactions (Johansson et
al., 2004).

The WAO nomenclature 2004

The WAO nomenclature describes hypersensitivity as “objectively reproducible


symptoms or signs initiated by exposure to a defined stimulus at a dose
tolerated by normal persons”.
Hypersensitivity is either mediated by an immunological mechanism or
not, dividing hypersensitivity into immunologically mediated hypersensitivity
or allergy and non-immunologically mediated hypersensitivity, Fig. 1.1.

Immunologically mediated food hypersensitivity or allergy

Originally, allergy was defined by Clemens von Pirquet in 1906 as “changed


reactivity”, based on the old Greek words “allos” (different or changed) and
“ergos” (work or effect) (von Pirquet, 1906). The WAO nomenclature defines
allergy as “an immunologically mediated specific hypersensitivity” and this
definition is still accepted by the allergy community (Fig. 1.1) (Johansson et
al., 2004).
Immunologically mediated symptoms and diseases are named allergic.
The WAO definition is: “Allergy is a hypersensitivity reaction initiated by
specific immunologic mechanisms” (Johansson et al., 2004). Allergy includes
many mechanisms caused by environmental influences. “Allergy can be
Food Allergy Nomenclature 3

Fig. 1.1: Principles of Allergy nomenclature. Modified after (Johansson et al., 2001; Johansson et
al., 2004).

antibody-mediated or cell-mediated. In most patients with allergic symptoms


from mucosal membranes in the airways and gastrointestinal tract, the
antibody belongs to the IgE isotype, and these patients may be said to have
an IgE-mediated allergy or atopic allergy” (Johansson et al., 2004). Even
diseases/symptoms with obvious inflammatory components but without
known mechanism should be classified as allergic.
The WAO position paper classifies allergies mediated by IgE antibodies
as IgE-mediated allergy (previous paragraph). Atopic allergy is caused by low
dose of allergen exposure to mucosal membranes in genetically predisposed
individuals causing long standing sensitization. IgE-mediated allergy consists
of atopic allergy and high dose dependent IgE-mediated allergies. Doses are
discussed later.

Atopic allergy

Atopic allergy is due to an immunological response induced by very low


doses of seemingly harmless proteins (mainly) in the environment, stimulating
the immune system to respond with a humoral response of Th2 type with
production by B-cells of allergen specific IgE antibodies.

High antigen dose IgE-mediated allergy

To this category belong, e.g., IgE mediated reactions to Hymenoptera venoms


and IgE reactions against helminths (Fig. 1.1).
4 Food Allergy: Methods of Detection and Clinical Studies

Comments

According to the WAO nomenclature (Johansson et al., 2001; Johansson et


al., 2004), there are two types of IgE-mediated allergy, low dose sensitization
(atopic) and reactivity and high dose sensitization and reactivity.
Low doses of allergen sensitizing via the mucous membranes is typical for
atopic sensitization. Atopy was introduced by Cooke and Coca in 1923 (Coca
and Cooke, 1923). Individuals with a predisposition to develop diseases like
asthma, rhino-conjunctivitis, eczema and urticaria, combined with a hereditary
predisposition to be sensitized to proteins that they were exposed to, were
classified as atopic. In 1975, Pepys defined atopy as a tendency to develop IgE
antibodies when exposed to low concentrations of environmental, normally
harmless, proteins called allergens (Pepys, 1975). The diseases caused by
sensitization were called atopic diseases. The WAO position paper (Johansson
et al., 2004) states: “The term atopy should be reserved to describe the genetic
predisposition to become IgE-sensitized to allergens commonly occurring in
the environment and to which everyone is exposed but to which the majority
do not produce a prolonged IgE antibody response. Thus, atopy is a clinical
definition of an IgE-antibody high-responder. The term atopy cannot be used
until an IgE sensitization has been documented by IgE antibodies in serum
or by a positive skin prick test”. And, “Allergic symptoms in a person of the
atopic constitution may be referred to as atopic, as in atopic rhinitis. A positive
skin test or the presence of IgE antibody to a less common allergen, especially
if the exposure is not low dose or does not occur via mucosal membranes, is
not a diagnostic criterion for atopy. Typical examples are Hymenoptera sting
allergy and most drug allergies. Such patients should be referred to as skin
test positive and IgE-sensitized, respectively” (Johansson et al., 2004). This is
confusing, since not all cases of atopic diseases are caused by IgE sensitization
and reactions involving allergens, allergen specific IgE and mast cells. In fact,
patients with long standing atopic eczema (atopic dermatitis) or asthma show
a neutrophil inflammation (Johansson et al., 2004). The use of the “atopic
diseases” concept has led to the term “atopic dermatitis” for infantile eczema,
even present in adults. However, since many patients with that disease do not
show any IgE-sensitization, i.e., are not atopic, the term “non-atopic atopic
dermatitis” was coined that is causing confusion. As mentioned, this was one of
the reasons for starting the nomenclature discussions that led to development
of the present WAO nomenclature (Johansson et al., 2001; Johansson et al., 2004).

Comments on doses

Inhalant allergies belong to the low allergen exposure group, reactions to


parasites to the high exposure group of IgE-mediated diseases. Insect venom
allergy and penicillin allergy and the like were considered to be high dose
allergy (Johansson et al., 2001). However, the oral dose of penicillin is at the
Food Allergy Nomenclature 5

milligram to gram level, a little higher than that of ordinary food allergens
(Eller et al., 2012). The injected dose of Hymenoptera venom is 100 mg of
venom, corresponding to 6–10 mg of major allergen.
This should be compared to the doses of food allergen that food allergic
patients are exposed to and are reacting to in double blind placebo controlled
food challenges, i.e., for hen’s egg, hazelnut and peanut with a 95% confidence
interval between 42 and 190 mg of fresh, solid food, for cow’s milk 1.5–5.4 ml
corresponding to 30–200 mg protein. It can also be compared with the amount
of inhalant allergen eliciting a reaction in the skin, conjunctiva or bronchi that
ranges from 0.001 to 1 mg of major allergen (Dreborg et al., 1987; Dreborg and
Einarsson, 1992).
The concentrations of inhalation allergens causing sensitization are
difficult to establish. However there are some data from the MAS study
(Wahn et al., 1997). During the first 3 years of life, children sensitized to mite
or cat were exposed to significantly higher house dust mite (median, 868 ng/
gm vs. 210 ng/mg; p = 0.001) and cat (median, 150 ng/gm vs. 64 ng/gm; p
= 0.011) allergen concentrations in domestic carpet dust compared with the
group without sensitization. Thus, lower concentrations in the environment
of children can be expected to sensitize than those causing asthma attacks, i.e.,
between 2 and 8 μg/g of carpet dust. However, the doses of airborne inhalant
allergens causing increase in bronchial hyperreactivity are much lower, less
than 1 ng/day (Dreborg and Einarsson, 1992; Ihre and Zetterstrom, 1993).
In conclusion, there is a floating dose level causing sensitization and
reactivity, between allergens and administration forms. The concentrations
causing sensitization are more difficult to define.

Non-IgE-mediated allergic diseases

Non-IgE-mediated allergic diseases are caused by other mechanisms than


allergen-IgE-mast cell interaction. Most non-IgE-mediated allergic diseases
are due to induction of allergen specific T-cells. Another mechanism is by
IgG-antibodies complement binding to dextran (Richter and Hedin, 1982),
etc., Fig. 1.1.

Comment

Since 2004 (Johansson et al., 2004), several diagnostic entities have been
recognized, Figs. 1.2 and 1.3.

Non-immunologically mediated mechanisms

The non-immunologically mediated diseases and symptoms were not given


any short name, are easy to understand and use.
6 Food Allergy: Methods of Detection and Clinical Studies

ure 3.
Fig. 1.2: The WAO nomenclature modified including recently defined diagnostic entities.

Allergy

IgE mediated IgG-mediated T-cell mediated Eosinophilic


Allergy Allergy Allergy GI Allergy

Alveolitis Aspergillosis Contact dermatitis Heiner syndrome / CM Eosinophilic Eosinophilic enteritis


pulmonary haemosiderosis esophagitis
Dextran-IgG- Aspergilloma Coeliac disease FPIES FPIAP FPE Eosinophilic Eosinophilic colitis
complement (+ IgE?) gastritis
anaphylaxis CM allergy–induced
iron deficiency anemia

Fig. 1.3: Proposed preliminary grouping of non-IgE-mediated allergies. The T-cell mediated
diseases can be partly further differentiated according to T-cell mechanism.

Comments

Recently, it has been proposed to use the word “Intolerance” to describe non-
immunological/non-allergic hypersensitivity conditions (Dreborg, 2015).
Intolerance has been used to describe the two most important groups of
diseases under this heading, i.e., not tolerating di-saccharides (lactose, sucrose,
fructose) (Durand, 1960; Holzel et al., 1962) due to enzyme deficiency in the
intestine and sometimes intolerance is used describing not tolerating aspirin,
e.g., aspirin induced asthma (Samter and Beers, 1967).

Auto-immune diseases

Auto-immune diseases are not included within allergy, since the causative
agents are not environmental but internal/of human origin. However, the limit
Food Allergy Nomenclature 7

between autoimmunity and allergy is floating, since, e.g., with time, asthma
and atopic eczema shift from an eosinophilic inflammation to an inflammation
dominated by neutrophils with not fully understood mechanisms.

Food allergy nomenclature modification

The general principles applied to food allergy are those of the general allergy
nomenclature, Fig. 1.1.

IgE-mediated food allergy

The contact with food allergens is mainly after oral intake, sometimes via the
skin.

Comments

After oral intake, symptoms can be induced in every organ system, mostly
gastrointestinal and skin symptoms, but even respiratory symptoms.
IgE-mediated food allergic symptoms appear within 2 hours of intake but
can appear immediately after intake of minute amounts of allergenic food.
Mostly, symptoms do not appear after intake of pg., ng or μg of allergenic
protein as is the case for inhaled allergens, even inhaled food proteins, but
rather after intake of mg to grams of whole food material (Eller et al., 2012).
Whether the difference in amount inducing a reaction is due to difference in
route of administration including digestion, difference in timing or difference
in mechanism, is not clear. See also above doses of food, injected, ingested or
inhaled allergen needed for induction of reactions.
Very seldom, allergic symptoms appear after inhalation of food protein. It
has been described in very sensitive food allergic patients and when handling
crops (Mason et al., 2015).
Contact via the skin of cold-buffet managers has caused a form of
IgE-mediated contact dermatitis, “IgE-associated allergic protein contact
dermatitis” (Cronin, 1987) that is a serious occupational allergy in cold-buffet
managers in restaurants.
A special form of food allergy is the local reaction in the oral mucosa,
sometimes spreading to the nose, eyes and larynx after ingestion of foods
containing allergens mostly cross-reacting with allergens in pollens (Juhlin-
Dannfelt, 1948), “para-allergies”, nowadays named Oral Allergy Syndrome,
OAS (Ortolani et al., 1988), Fig. 1.2. With the exception of laryngeal involvement
(Pastorello et al., 1999), these reactions are not life-threatening. The laryngeal
mucosa is as much part of the local oro-facial mucosa as the conjunctiva,
lips and the salpinges. If OAS symptoms escalate within minutes, involving
organs at distance, there is a high risk of severe anaphylaxis (Cox et al., 2010;
Dreborg, 2013).
8 Food Allergy: Methods of Detection and Clinical Studies

Non-IgE-mediated or non-atopic food allergy

Non-IgE-mediated food allergy is not discussed in detail in the WAO


nomenclature document (Johansson et al., 2004), stating: “If IgE is involved
in the reaction, the term IgE-mediated food allergy is appropriate. All other
reactions should be referred to as non-allergic food hypersensitivity”, thus
not mentioning, e.g., the non-IgE-mediated mechanisms involved in some,
probably T-cell mediated food induced gastrointestinal diseases. On this point,
the newly instituted “WAO Nomenclature Review Committee” will update
the present nomenclature.
Opposite to IgE-mediated allergic reactions, most reactions caused by non-
IgE-mediated mechanisms do not start until 2 hours after ingestion of the food.

Comments

Since non-IgE-mediated diseases were not clearly pointed at in the WAO


document (Johansson et al., 2004) this must be updated.
In addition to the diseases mentioned in the WAO and EAACI nomenclature
documents (Johansson et al., 2001; Johansson et al., 2004) a number of diseases
have been identified that are immunologically mediated without obvious IgE
involvement, although the mechanisms involved are not fully understood
(Nowak-Wegrzyn et al., 2015), Fig. 1.3. Furthermore, eosinophilic oesophagitis
(Furuta and Katzka, 2015), enterocolitis (Nowak-Wegrzyn et al., 2015) and
proctocolitis (Lake, 2000) can be IgE-mediated but even other mechanisms
have been proposed.
To this group also belongs Heiner syndrome, also known as pulmonary
haemosiderosis (Heiner et al., 1962).
Although not IgE-mediated, the mechanism causing gluten allergy
(formerly gluten intolerance or coeliac disease) is immunological. Therefore,
it should be considered allergic, i.e., belonging to the non-IgE-mediated,
mostly T-cell mediated, allergic diseases. It should not be confused with IgE
mediated wheat and gluten allergy. Furthermore, contact dermatitis belongs
to this group.

Non-immunologically mediated food hypersensitivity

The main alimentary disease among diseases/symptoms that are not caused by
an immunological hypersensitivity/allergy is lactose intolerance, i.e., primary
or secondary enteric lactase deficiency (Durand, 1960; Sicherer and Sampson,
2014), leading to bacterial fermentation of lactose in the gut. Lactose in dairy
products not digested in the intestine are fermented in the gut leading to
acid loose stools. Similarly, inherited lack of enzyme for digestion of sucrose
(Weijers et al., 1961) and fructose (Cox, 1990) leads to similar symptoms. The
other major cause of non-allergic food hypersensitivity is aspirin intolerance
(Samter and Beers, 1967).
Food Allergy Nomenclature 9

Comments

It is proposed to use the term intolerance to describe the non-immunologically


mediated hypersensitivities.

Non-acceptable entities and terms

Among laypersons, gastrointestinal symptoms of different kinds are named


allergy or intolerance.
The basis for classification should be according to mechanism, i.e.,
according to the WAO nomenclature. As mentioned non-atopic atopic
dermatitis is still used by some dermatologists, but should, in my opinion,
be avoided.
Some gastroenterologists are using terms that cannot be accepted from an
allergological point of view such as cow’s milk protein allergy/intolerance,
CMPA/I and “cow’s milk related symptoms”.

Comments

For some years, Yves Vandenplas and colleagues used the term cow’s milk
protein allergy/intolerance, CMPA/I (Vandenplas et al., 2011; Vandenplas
et al., 2013). The same group of mainly pediatric gastoenterologists (Vandenplas
et al., 2015; Vandenplas et al., 2016a) launched a series of non-proven stepwise
hypotheses, supporting the use of the non-defined diagnosis “cow’s milk
related symptoms”. The 10 steps are:
1. Double Blind Placebo Controlled Food Challenges, DBPCFC, are the
gold standard for diagnosis of food allergy. However, this is expensive
and not possible to perform in primary care. Therefore, elimination
and reintroduction should be the standard diagnostic procedure when
diagnosing CMPA in primary care.
2. The next step is claiming simple gastrointestinal symptoms like infantile
colic, regurgitation and constipation may be due to CMPA (Vandenplas,
2015; Vandenplas et al., 2011; Vandenplas et al., 2016a), based on the fact
infantile colic, regurgitation and constipation sometimes are present in
infants with CMPA.
3. Since these symptoms sometimes are seen in children with CMPA, children
with such symptoms may have CMPA.
4. Thus, CMPA should be diagnosed in these children. Primarily they
proposed an elimination diet, followed by reintroduction at home in those
improving after some months.
5. To “easily” diagnose CMPA in infants, they worked out a non-validated
scoring system mainly based on the common symptoms, infantile colic,
regurgitation and obstipation (Vandenplas et al., 2015).
10 Food Allergy: Methods of Detection and Clinical Studies

6. Those improving on an elimination diet and not relapsing when normal


formula is re-introduced are said to have “cow’s milk related symptoms”
(Vandenplas et al., 2016a).
7. The treatment recommended is an elimination diet, in this age group a
hypoallergenic formula.
8. Since, in infants, the common symptoms mentioned are self-limited, the
therapeutic success will be marked.
9. The parents will be stigmatized and the “diagnosis” of “CMPA/I” (or
CMPA) will follow the child.
10. Furthermore, parents without economic resources will suffer from
economic loss to the benefit of formula companies.
The terms CMPA/I and “cow’s milk related symptoms” may not be used,
especially since the concept is not evidence based and has been developed
in cooperation with formula industry (Vandenplas et al., 2014). It should be
regarded a marketing concept.
The GI Committee of the European Society on Paediatric Gastroenterology,
Hepatology and Nutrition, ESPGHAN, does not mention CMPA/I or “cow’s
milk related symptoms” in their practical guidelines on the management of
CMPA in infants and children (Koletzko et al., 2012). Recently, a committee
within ESPGHAN has banned the widespread use of partially hydrolyzed
formulas among non-diseased children (Vandenplas et al., 2016b).

Future Perspectives
I reviewed (Dreborg, 2016) the paper by the group of gastroenterologists led
by Yves Vandenplas (Vandenplas et al., 2015). At the same time, I wrote the con
paper on “Intolerance does not exist” (Dreborg, 2016) for the WAO Journal.
Simultaneously Vandenplas wrote the “pro intolerance” paper (Vandenplas,
2016) in a series of pro-con debates in the WAO J. I found the reasoning of the
gastroenterologists to be threatening the present nomenclature. Therefore, I
asked the World Allergy Organization, WAO Board of Directors to initiate an
update of the old nomenclature document (Johansson et al., 2004) that resulted
in the formation of a “WAO Nomenclature Review Committee” that has started
its work. It can be foreseen that the new version of the allergy nomenclature
will mainly follow the design of the old nomenclature document and this
summary, but if possible be more detailed (Rosenwasser et al.).
Furthermore, reactivity is not limited to the organ that gets sensitized.
Patients react to the sensitizing allergen in other organs than that causing
most symptoms, e.g., a majority of patients with asthma also report rhinitis
(conjunctivitis) (Passalacqua et al., 2006). Furthermore, in asthmatics, the skin,
conjunctiva and bronchi (Dreborg et al., 1986) react, in rhinitis patients the
nose or conjunctiva and skin (Dreborg et al., 2016; Østerballe, 1982) and in
food allergic patients the skin, gut and conjunctiva (Kvenshagen et al., 2010).
Food Allergy Nomenclature 11

These references were chosen since they exemplify documentation of the fact
allergic inflammation is universal, i.e., is not limited to the organ showing
most symptoms.
Like IgE-mediated diseases non-IgE-mediated allergic diseases should
be split up according to their partly understood mechanisms as illustrated
in Fig. 1.3.
To assure well defined diseases are continuously evaluated, a permanent
committee on allergy nomenclature should be set up. The group should govern
allergen nomenclature with the responsibility to evaluate and register new
syndromes-diseases when their mechanisms have been elucidated.

Summary
The allergy nomenclature is based on mechanisms. Most important is to differ
between allergy, i.e., immunological hypersensitivity and hypersensitivity
due to other mechanisms. Furthermore, it will be of importance to reveal
immunological mechanism involved in different types of allergic diseases,
phenotypes and genotypes. To assure new terms are in accordance with the
new WAO system it is proposed to register of accepted disease entities with
proposed mechanisms within the area of allergy.
Keywords: Hyperreactivity, Allergy, IgE, non-IgE, Immunological
hypersensitivity, Non-immunological hypersensitivity, non-IgE-mediated
allergy, Intolerance

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CHAPTER 2

Food Allergy in Children


Sophia Tsabouri,1,* Gavriela Feketea2 and
Nicolaos Nicolaou3,4

Introduction
Food Allergy (FA) refers to an immune response directed toward food (Chafen
et al., 2010). As defined in the 2010 US National Institutes of Allergy and
Infectious Diseases (NIAID)–sponsored guidelines, FA is ‘‘an adverse health
effect arising from a specific immune response that occurs reproducibly on
exposure to a given food’’ (Boyce et al., 2010a). This definition encompasses
immune responses that are IgE-mediated, non-IgE-mediated or a combination
of both and is in agreement with other international guidelines (Fiocchi et
al., 2010; Sackeyfio et al., 2011; Urisu et al., 2011). Allergic sensitization occurs
when food-specific IgE (sIgE) antibodies are produced by plasma cells that
have differentiated from allergen-specific B lymphocytes. The sIgE antibodies
bind to the surface of tissue mast cells and blood basophils, and on re-exposure
to the food, antigenic proteins in the food bind to and cross-link these cell
surface–bound sIgE antibodies, which triggers the release of symptom-causing
mediators, such as histamine and leukotrienes. Subjects can have allergic
sensitization (production of sIgE) to food allergens without having clinical
symptoms of an allergic reaction on exposure. Thus, sensitization alone is not
sufficient to define food allergy. IgE-mediated food allergy requires both the

1
Professor of Paediatrics-Paediatric Allergy, Child Health Department, University of Ioannina,
Greece.
2
Consultant in Paediatrics and Paediatric Allergy Paediatric Department, General Hospital of
Ilias, Amaliada Hospital Unit.
Email: gabychri@otenet.gr
3
The University of Manchester, Institute of Inflammation and Repair, University Hospital of
South Manchester NHS Foundation Trust, Manchester, UK.
4
The University of Nicosia Medical School, Nicosia, Cyprus.
Email: nic.nicolaou@gmail.com, nicolas@allergycy.com
* Corresponding author: stsabouri@gmail.com, tsabouri@cc.uoi.gr
Food Allergy in Children 15

presence of sensitization and the development of specific signs and symptoms


on exposure to that food (Boyce et al., 2010a).
There are numerous adverse reactions to foods that do not involve an
immune response and therefore are not considered as a result of FA (Boyce
et al., 2010b). These include metabolic disorders, such as lactose and alcohol
intolerance, response to pharmacologically active foods components (e.g.,
caffeine) or illness in response to toxins from microbial contamination (Sicherer
and Sampson, 2014). Certain psychological or neurological responses (food
aversion or rhinorrhea caused by spicy foods) can also mimic FA but are not
considered allergic disorders (Fig. 2.1).

Epidemiology
In the United States, prevalence estimates range from 1 to 10%, and most are
derived from self-report or parent report of FA (Sicherer and Sampson, 2014).
A recent United State of America (USA) nationally representative population-
based study (the National Health and Nutrition Examination Survey
[NHANES]) found the prevalence of self-reported FA in children from 2007
to 2010 to be 6.53% (McGowan and Keet, 2013). The most common childhood
FA reported were to milk (1.94%), peanut (1.16%) and shellfish (0.87%). A
slightly higher estimate of childhood FA prevalence (8%) was reported in
another USA population-based study (Gupta et al., 2011). In other developed

Ig-E-mediated

Non-IgE-mediated

Food allergy
(Immune
mediated)
Mixed IgE and non-IgE-
mediated

Adverse Food Reaction


(Food hypersensitivity)

Metabolic (lactose and


alcohol intolerance)

Food Intolerance
(Non-Immune
mediated) Pharmacologic (caffeine)

Toxic (scromboid fish toxin)

Other/idiopathic (sulfites)

Fig. 2.1: Classification of food reactions [modified from (Sampson et al., 2014)].
16 Food Allergy: Methods of Detection and Clinical Studies

countries, the overall prevalence estimates are in line with USA reports. A
recent meta-analysis of European FA prevalence from 2000 to 2012 found an
overall prevalence of self-reported FA of 5.9%. Although many of the primary
studies had at least moderate potential for bias (Nwaru et al., 2014). Estimates
relying on self-reports are of course limited in part by the subjective nature
of the data. Other, more objective methods include measuring sensitization
using food allergen sIgE. Using NHANES data, prevalence estimates for
sensitization were 7.6% to peanut, 5.9% to shrimp, 4.8% to milk and 3.4% to
egg in the overall population aged 6 and over, and 6.8% to peanut, 21.8% to
milk and 14.2% to egg in children aged 1 to 5 years old in the USA. These are
certainly an overestimation of true clinical FA prevalence but are valuable
because they provide some objectivity (Salo et al., 2014).

Food Allergens
Food allergens, which are usually proteins but sometimes chemical haptens, are
recognized by allergen-specific immune cells and elicit specific immunologic
reactions, resulting in characteristic symptoms (Boyce et al., 2010a). Most food
allergens can cause reactions when ingested either in the raw form or after
being cooked, and occasionally after inhalation. Cross-reactivity can occur
when a food allergen has structural or sequence similarity with a different food
allergen or aeroallergen. The likelihood of having clinical allergic reactions to
cross-reactive allergens is highly variable and depends on the type of food. For
example, clinical cross-reactivity among legumes is generally uncommon (e.g.,
most patients with peanut allergy tolerate beans and peas), whereas clinical
cross-reactivity among different types of crustacean shellfish is common
(Tsabouri et al., 2012). Although any food can potentially trigger an allergic
response a minority of foods cause the majority of allergic reactions, namely
peanut, tree nuts, egg, milk, fish, crustacean shellfish, wheat and soy (Boyce
et al., 2010a). Celery, mustard, sesame, lupine and molluscan shellfish have
been identified as significant allergens in European countries, and in Japan
buckwheat is also a common allergen (Akiyama et al., 2011). Protein-containing
food additives and colouring agents, such as annatto, carmine and gelatine,
can induce allergic reactions. Chemical additives, such as artificial flavours
(e.g., tartrazine) and preservatives (e.g., glutamates and sulphites), might
cause adverse reactions, but an immune mechanism has not been identified,
and such reactions are classified as intolerances.

Clinical manifestations of food allergy

Based on the underlining pathophysiological mechanism, FA can be classified as


IgE-mediated, non-IgE-mediated and mixed IgE/non-IgE-mediated reactions.
According to the time pattern of food-induced allergic reactions, these may
be: (i) immediate (occurring within minutes to a few hours of exposure to
Food Allergy in Children 17

the offending food and typically involve IgE-mediated mechanisms), or (ii)


delayed (occurring within several hours to a few days, usually involving
cellular mechanisms) (Boyce et al., 2010a). Clinical manifestations (Table 2.1)
vary depending on the systems that are affected. IgE-mediated reactions may
present with symptoms affecting the skin, gastrointestinal tract, respiratory
system and circulatory system, while non-IgE-mediated and mixed IgE- and
non-IgE-mediated reactions present predominantly with gastrointestinal
symptoms (vomiting, diarrhoea, abdominal pain, bloody stools) (Burks et
al., 2012).
Furthermore, a wide range of disorders is recognized to be secondary to
FA (Table 2.2) (Sampson, 2014). The table does not include disorders that are
not clinically specific to syndromes associated with FA. Thus infantile colic,
constipation and gastrointestinal reflux disease are not listed.

Table 2.1: Symptoms and signs of food-induced allergic reactions [modified from (Boyce et al.,
2010b)].

Target system Systemic, Skin Respiratory Gastrointestinal


circulatory
anaphylaxis urticaria nasal congestion nausea
hypotension angioedema rhinorrhea vomiting
arrhythmia erythema hoarseness colic-like ab-
dominal pain
drowsiness itching laryngeal oedema
IgE-mediated
syncope stridor
cough
chest tightness
dyspnoea
wheezing

loss of appetite nasal congestion nausea


food aversion rhinorrhea vomiting
failure to thrive cough abdominal pain
Non-IgE-
mediated wheezing gastroesophageal
reflux (GER)
haemoptysis hematochezia
bloody stools

exacerbation of nausea
atopic dermatitis
vomiting-regur-
Mixed IgE gitation
and non-IgE-
abdominal pain
mediated
gastroesophageal
reflux
heartburn
18 Food Allergy: Methods of Detection and Clinical Studies

Table 2.2: Clinical manifestations secondary to FA [modified from (Sicherer and Sampson, 2014)
(Worm et al., 2015)].

Affected system Generalized Skin Respiratory Gastrointestinal


Anaphylaxis Urticaria Rhinitis Oral allergy
syndrome (Pollen
IgE-mediated associated food al-
(immediate lergy syndrome)
onset -30 min up Food-depended Angioedema Asthma Immediate gastro-
to 2 hours) exercise-in- intestinal hyper-
duced anaphy- sensitivity
laxis (FDEIA)

Contact derma- Food-induced Food protein-in-


titis pulmonary duced enterocolitis
hemosidero- syndrome (FPIES)
Non-IgE-medi- sis (Heiner’s
ated (delayed syndrome)
onset - few
Dermatitis Food protein-in-
hours to days)
herpetiformis duced enteropathy
Food protein-in-
duced proctocolitis

Mixed IgE and Atopic derma- Eosinophilic


non-IgE-medi- titis esophagitis
ated (delayed Eosinophilic gas-
onset) troenteritis

IgE-mediated reactions

In IgE-mediated reactions, symptoms may present from almost any system


(Table 2.1). Skin, oral, gastrointestinal and respiratory symptoms are usually
the most frequently observed (Lack, 2008). Food allergic reactions range from
mild and often spontaneously resolving events to life-threatening anaphylaxis
which unfortunately sometimes becomes fatal (Bock et al., 2007). The clinical
course of the Oral Allergy Syndrome (OAS) commonly described in older
children and adults allergic to pollens is usually mild; symptoms are limited to
the oropharynx and resolve within an hour in the majority of cases (Hofmann
and Burks, 2008). Patients with OAS, who are allergic to pollens, cross-react to
homologous food proteins (Table 2.3) Anaphylaxis is a severe systemic reaction
involving significant respiratory and/or cardiovascular compromise (Muraro
et al., 2007). Food-induced anaphylaxis is the leading cause of anaphylactic
reactions presented to the Accident and Emergency hospital departments in
both children and adults (de Silva et al., 2008; Ross et al., 2008). Peanut and tree
nuts are amongst the most common food allergens related to fatal anaphylaxis
(Pumphrey, 2000). Food-allergic individuals with asthma (particularly those
with uncontrolled asthma) are at higher risk of developing anaphylaxis (Bock
et al., 2007).
Food Allergy in Children 19

Table 2.3: Cross-reactivity between pollens and fruits and vegetables in OAS.

Pollens Fruits and vegetables


Birch pollen apples, carrots, celery, hazelnuts, almond, nuts, peaches,
pears, nectarine, plum, kiwi, raw potatoes
Ragweed pollen bananas, melons, cucumber, courgette
Grasses melons, oranges, peanuts, tomatoes, white potato
Mugwort pollen apples, bell peppers, carrots, celery, garlic, onion, some
spices (coriander, anise seeds, fennel seeds)

Food-Dependent Exercise-Induced Anaphylaxis (FDEIA) is a special condition


occurring where exercise following allergen ingestion triggers anaphylaxis,
although exercise and allergen exposure are independently tolerated (Kleiman
and Ben-Shoshan, 2014).

Non-IgE-mediated reactions

Food Protein-Induced Allergic Proctocolitis (FPIAP) is the most common non-


IgE mediated FA in the first months of life, characterized by blood-streaked
stools in otherwise healthy, thriving infants. Food Protein-Induced Enterocolitis
Syndrome (FPIES) is an increasingly recognized disorder affecting young
infants. It is typically presents with profuse vomiting and diarrhoea 2 to 4
hours after ingestion of the incriminating food. If untreated, it may lead to life-
threatening hypovolemic shock (Caubet et al., 2014). It is often caused by cow’s
milk, soy and rice. The development of FPIES into secondary IgE-mediated
allergy has been described. Food Protein-induced Enteropathy (FPE) manifests
with diarrhoea, failure to thrive, vomiting and abdominal distension (Feuille
and Nowak-Wegrzyn, 2015). Heiner syndrome (pulmonary hemosiderosis)
is a rare food hypersensitivity pulmonary disease mostly caused by cow’s
milk. It affects infants primarily and is characterized by unexplained chronic
pulmonary infiltrates (Moissidis et al., 2005).

IgE and non-IgE-mediated (mixed) reactions

Atopic Dermatitis (AD) is a chronic inflammatory skin disease characterized


by intense itching and recurrent eczematous lesions. One in three children
with moderate to severe AD has food allergy, where egg and milk being the
most common allergens involved (Burks, 2003).
Eosinophilic esophagitis is the most common among the eosinophilic
gastrointestinal disorders and represents a chronic, immune/antigen-mediated
disease. It is clinically characterized by symptoms related to esophageal
dysfunction and histologically by eosinophil-predominant inflammation
(Liacouras et al., 2011). It is clinically characterized by dysphagia, regurgitation,
abdominal and/or chest pain, poor appetite and failure to thrive (Sampson
et al., 2014).
20 Food Allergy: Methods of Detection and Clinical Studies

Diagnostic workup in food allergy

Although there is evidence to suggest that the prevalence of FA is increasing,


recent studies have demonstrated that many “self-reported” FA cases are not
confirmed when objectively assessed, and unnecessary over-restricted diets are
often followed (Nwaru et al., 2014). Given the impact of FA on patients, families
and healthcare systems, accurate diagnosis is critically important (Bollinger
et al., 2006). The diagnosis of suspected FA is generally based on detailed
clinical history and physical examination, determination of sensitization (to
the food/s in question) by skin tests and/or the measurement of specific IgE
(sIgE) antibodies in serum, elimination diets, and the outcome of Oral Food
Challenge (OFC) (Boyce et al., 2010a). Endoscopy and biopsy may be required
to establish the diagnosis in the case of some non-IgE- or mixed IgE/non-IgE-
mediated food-related disorders, e.g. (eosinophilic esophagitis). However,
any in vivo and/or in vitro testing performed in the diagnostic work-up of
FA should be guided and interpreted according to the clinical history and
the suspected underlying immunologic mechanism. A number of unproved
or non-standardized procedures and tests, including allergen-specific
IgG measurement, cytotoxicity assays, applied kinesiology, provocation
neutralization and hair analysis are not considered useful in the evaluation
of food allergy (Sampson et al., 2014).

History and physical examination

As for any other medical condition a detailed history and thorough clinical
examination are of paramount importance in the diagnostic process. History
taking in suspected FA is complex detective work and requires fastidious
attention to detail from the physician as there is considerable overlap of
symptoms in the clinical spectrum of adverse reactions to foods (Fig. 2.1).
It can provide clues suggestive of the immunologic mechanisms involved
and the likely causative food allergens (Burks et al., 2012). Clinicians should
consider that culprit food allergens may differ depending on the different
epidemiology aspects related to the affected individuals (e.g., age, origin and
dietary habits). For example, egg and milk in early life vs. fruits, nuts and
seafood in older children and adults, and peach in the Mediterranean area
vs. apple in central/northern Europe.
Amongst others, the medical history should capture information on the
nature of the suspected allergenic food, the timing of exposure to the initiation
of the reaction, the type, duration and severity of symptoms, the treatment
received and the patient’s response, as well as the presence of allergic and
other diseases. Important questions to be precisely answered when obtaining
the history from food-allergic individuals, particularly when suspecting IgE-
mediated food allergy are summarized in Table 2.4.
Although the physical examination alone cannot be considered diagnostic
of FA, it may reveal indicative findings. Signs of anaphylaxis (e.g., generalized
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insulted her and is expected to pay damages. If a man meets his
mother-in-law coming along the road and does not recognise her,
she will fall down on the ground as a sign, when he will run away. In
the same way a father-in-law will signal to his daughter-in-law; the
whole idea being that they are unworthy to be noticed till they have
proved that they can beget children.”79.2 However, if a wife should
prove barren for three years, the rules of avoidance between the
young couple and their parents-in-law cease to be observed.79.3
Hence the custom of avoidance among these people is associated in
some way with the wife’s fertility. So among the Awemba, a Bantu
tribe of Northern Rhodesia, “if a young man sees his mother-in-law
coming along the path, he must retreat into the bush and make way
for her, or if she suddenly comes upon him he must keep his eyes
fixed on the ground, and only after a child is born may they converse
together.”79.4 Among the Angoni, another Bantu tribe of British
Central Africa, it would be a gross breach of etiquette if a man were
to enter his son-in-law’s house; he may come within ten paces of the
door, but no nearer. A woman may not even approach her son-in-
law’s house, and she is never allowed to speak to him. Should they
meet accidentally on a path, the son-in-law gives way and makes a
circuit to avoid encountering his mother-in-law face to face.79.5 Here
then we see that a man avoids his son-in-law as well as his mother-
in-law, though not so strictly.
Among the Thonga, a Bantu tribe about
The custom of Delagoa Bay, when a man meets his mother-in-
avoiding mother-in-
law and wife of law or her sister on the road, he steps out of the
wife’s brother road into the forest on the right hand side and sits
among the Thonga down. She does the same. Then they salute each
of Delagoa Bay.
other in the usual way by clapping their hands.
After that they may talk to each other. When a man is in a hut, his
mother-in-law dare not enter it, but must sit down outside without
seeing him. So seated she may salute him, “Good morning, son of
So-and-so.” But she would not dare to pronounce his name.
However, when a man has been married many years, his mother-in-
law has less fear of him, and will even enter the hut where he is and
speak to him. But among the Thonga the woman whom a man is
bound by custom to avoid most rigidly is not his wife’s mother, but
the wife of his wife’s brother. If the two meet on a path, they carefully
avoid each other; he will step out of the way and she will hurry on,
while her companions, if she has any, will stop and chat with him.
She will not enter the same boat with him, if she can help it, to cross
a river. She will not eat out of the same dish. If he speaks to her, it is
with constraint and embarrassment. He will not enter her hut, but will
crouch at the door and address her in a voice trembling with
emotion. Should there be no one else to bring him food, she will do it
reluctantly, watching his hut and putting the food inside the door
when he is absent. It is not that they dislike each other, but that they
feel a mutual, a mysterious fear.80.1 However, among the Thonga,
the rules of avoidance between connexions by marriage decrease in
severity as time passes. The strained relations between a man and
his wife’s mother in particular become easier. He begins to call her
“Mother” and she calls him “Son.” This change even goes so far that
in some cases the man may go and dwell in the village of his wife’s
parents, especially if he has children and the children are grown
up.80.2 Again, among the Ovambo, a Bantu people of German South-
West Africa, a man may not look at his future mother-in-law while he
talks with her, but is bound to keep his eyes steadily fixed on the
ground. In some cases the avoidance is even more stringent; if the
two meet unexpectedly, they separate at once. But after the
marriage has been celebrated, the social intercourse between
mother-in-law and son-in-law becomes easier on both sides.81.1
Thus far our examples of ceremonial avoidance
The custom of between mother-in-law and son-in-law have been
avoiding the
mother-in-law drawn from Bantu tribes. But in Africa the custom,
among other than though apparently most prevalent and most
the Bantu tribes of strongly marked among peoples of the great Bantu
Africa.
stock, is not confined to them. Among the Masai of
British East Africa, “mothers-in-law and their sons-in-law must avoid
one another as much as possible; and if a son-in-law enters his
mother-in-law’s hut she must retire into the inner compartment and
sit on the bed, whilst he remains in the outer compartment; they may
then talk. Own brothers-in-law and sisters-in-law must also avoid one
another, though this rule does not apply to half-brothers-in-law and
sisters-in-law.”81.2 So, too, among the Bogos, a tribe on the outskirts
of Abyssinia, a man never sees the face of his mother-in-law and
never pronounces her name; the two take care not to meet.81.3
Among the Donaglas a husband after marriage “lives in his wife’s
house for a year, without being allowed to see his mother-in-law, with
whom he enters into relations only on the birth of his first son.”81.4 In
Darfur, when a youth has been betrothed to a girl, however intimate
he may have been with her parents before, he ceases to see them
until the ceremony has taken place, and even avoids them in the
street. They, on their part, hide their faces, if they happen to meet
him unexpectedly.81.5
To pass now from Africa to other parts of the
The custom of world, among the Looboos, a primitive tribe in the
avoiding relations
by marriage in tropical forests of Sumatra, custom forbids a
Sumatra and New woman to be in her father-in-law’s company and a
Guinea. man to be in his mother-in-law’s society. For
example, if a man meets his daughter-in-law, he
should cross over to the other side of the road to let her pass as far
as possible from him; but if the way is too narrow, he takes care in
time to get out of it. But no such reserve is prescribed between a
father-in-law and his son-in-law, or between a mother-in-law and her
daughter-in-law.82.1 Among the Bukaua, a Melanesian tribe of
German New Guinea, the rules of avoidance between persons
connected by marriage are very stringent; they may not touch each
other or mention each other’s names. But contrary to the usual
practice the avoidance seems to be quite as strict between persons
of the same sex as between males and females. At least the writer
who reports the custom illustrates it chiefly by the etiquette which is
observed between a man and his daughter’s husband. When a man
eats in presence of his son-in-law, he veils his face; but if
nevertheless his son-in-law should see his open mouth, the father-in-
law is so ashamed that he runs away into the wood. If he gives his
son-in-law anything, such as betel or tobacco, he will never put it in
his hand, but pours it on a leaf, and the son-in-law fetches it away. If
father-in-law and son-in-law both take part in a wild boar hunt, the
son-in-law will abstain from seizing or binding the boar, lest he
should chance to touch his father-in-law. If, however, through any
accident their hands or backs should come into contact, the father-
in-law is extremely horrified, and a dog must be at once killed, which
he gives to his son-in-law for the purpose of wiping out the stain on
his honour. If the two should ever fall out about anything, the son-in-
law will leave the village and his wife, and will stay away in some
other place till his father-in-law, for his daughter’s sake, calls him
back. A man in like manner will never touch his sister-in-law.82.2
Among the low savages of the Californian
The custom of peninsula a man was not allowed for some time to
avoiding relations
by marriage among look into the face of his mother-in-law or of his
the Indian tribes of wife’s other near relations; when these women
America. were present he had to step aside or hide
himself.83.1 Among the Indians of the Isla del
Malhado in Florida a father-in-law and mother-in-law might not enter
the house of their son-in-law, and he on his side might not appear
before his father-in-law and his relations. If they met by accident they
had to go apart to the distance of a bowshot, holding their heads
down and their eyes turned to the earth. But a woman was free to
converse with the father and mother of her husband.83.2 Among the
Indians of Yucatan, if a betrothed man saw his future father-in-law or
mother-in-law at a distance, he turned away as quickly as possible,
believing that a meeting with them would prevent him from begetting
children.83.3 Among the Arawaks of British Guiana a man may never
see the face of his wife’s mother. If she is in the house with him, they
must be separated by a screen or partition-wall; if she travels with
him in a canoe, she steps in first, in order that she may turn her back
to him.83.4 Among the Caribs “the women never quit their father’s
house, and in that they have an advantage over their husbands in as
much as they may talk to all sorts of people, whereas the husband
dare not converse with his wife’s relations, unless he is dispensed
from this observance either by their tender age or by their
intoxication. They shun meeting them and make great circuits for
that purpose. If they are surprised in a place where they cannot help
meeting, the person addressed turns his face another way so as not
to be obliged to see the person, whose voice he is compelled to
hear.”83.5 Among the Araucanian Indians of Chili a man’s mother-in-
law refuses to speak to or even to look at him during the marriage
festivity, and “the point of honour is, in some instances, carried so
far, that for years after the marriage the mother never addresses her
son-in-law face to face; though with her back turned, or with the
interposition of a fence or a partition, she will converse with him
freely.”84.1
It would be easy to multiply examples of similar
The custom of customs of avoidance between persons closely
avoiding relations
by marriage cannot connected by marriage, but the foregoing may
be separated from serve as specimens. Now in order to determine
the similar custom the meaning of such customs it is very important
of avoiding relations
by blood; both are to observe that similar customs of avoidance are
probably practised in some tribes not merely between
precautions to
prevent improper
persons connected with each other by marriage,
relations between but also between the nearest blood relations of
the sexes. different sexes, namely, between parents and
children and between brothers and sisters;84.2 and
the customs are so alike that it seems difficult or impossible to
separate them and to offer one explanation of the avoidance of
connexions by marriage and another different explanation of the
avoidance of blood relations. Yet this is what is done by some who
attempt to explain the customs of avoidance; or rather they confine
their attention wholly to connexions by marriage, or even to mothers-
in-law alone, while they completely ignore blood relations, although
in point of fact it is the avoidance of blood relations which seems to
furnish the key to the problem of such avoidances in general. The
true explanation of all such customs of avoidance appears to be, as I
have already indicated, that they are precautions designed to
remove the temptation to sexual intercourse between persons whose
marriage union is for any reason repugnant to the moral sense of the
community. This explanation, while it has been rejected by theorists
at home, has been adopted by some of the best observers of savage
life, whose opinion is entitled to carry the greatest weight.85.1
That a fear of improper intimacy even between
Mutual avoidance of the nearest blood relations is not baseless among
mother and son, of
father and daughter, races of a lower culture seems proved by the
and of brother and testimony of a Dutch missionary in regard to the
Battas or Bataks of Sumatra, a people who have
sister among the attained to a fairly high degree of barbaric
Battas.
civilization. The Battas “observe certain rules of
avoidance in regard to near relations by blood or marriage; and we
are informed that such avoidance springs not from the strictness but
from the looseness of their moral practice. A Batta, it is said,
assumes that a solitary meeting of a man with a woman leads to an
improper intimacy between them. But at the same time he believes
that incest or the sexual intercourse of near relations excites the
anger of the gods and entails calamities of all sorts. Hence near
relations are obliged to avoid each other lest they should succumb to
temptation. A Batta, for example, would think it shocking were a
brother to escort his sister to an evening party. Even in the presence
of others a Batta brother and sister feel embarrassed. If one of them
comes into the house, the other will go away. Further, a man may
never be alone in the house with his daughter, nor a mother with her
son. A man may never speak to his mother-in-law nor a woman to
her father-in-law. The Dutch missionary who reports these customs
adds that he is sorry to say that from what he knows of the Battas he
believes the maintenance of most of these rules to be very
necessary. For the same reason, he tells us, as soon as Batta lads
have reached the age of puberty they are no longer allowed to sleep
in the family house but are sent away to pass the night in a separate
building (djambon); and similarly as soon as a man loses his wife by
death he is excluded from the house.”85.2
In like manner among the Melanesians of the
Mutual avoidance of Banks’ Islands and the New Hebrides a man must
mother and son and
of brother and sister not only avoid his mother-in-law; from the time
among the when he reaches or approaches puberty and has
Melanesians. begun to wear clothes instead of running about
naked, he must avoid his mother and sisters, and
he may no longer live in the same house with them; he takes up his
quarters in the clubhouse of the unmarried males, where he now
regularly eats and sleeps. He may go to his father’s house to ask for
food, but if his sister is within he must go away before he eats; if she
is not there, he may sit down near the door and eat. If by chance
brother and sister meet in the path, she runs away or hides. If a boy,
walking on the sands, perceives footprints which he knows to be
those of his sister, he will not follow them, nor will she follow his. This
mutual avoidance lasts through life. Not only must he avoid the
persons of his sisters, but he may not pronounce their names or
even use a common word which happens to form part of any one of
their names. In like manner his sisters eschew the use of his name
and of all words which form part of it. Strict, too, is a boy’s reserve
towards his mother from the time when he begins to wear clothes,
and the reserve increases as he grows to manhood. It is greater on
her side than on his. He may go to the house and ask for food and
his mother may bring it out for him, but she will not give it to him; she
puts it down for him to take. If she calls to him to come, she speaks
to him in the plural, in a more distant manner; “Come ye,” she says,
not “Come thou.” If they talk together she sits at a little distance and
turns away, for she is shy of her grown-up son. “The meaning of all
this,” as Dr. Codrington observes, “is obvious.”86.1
Mutual avoidance of
a man and his
When a Melanesian man of the Banks’ Islands
mother-in-law marries, he is bound in like manner to avoid his
among the mother-in-law. “The rules of avoidance are very
Melanesians.
strict and minute. As regards the avoidance of the
person, a man will not come near his wife’s mother; the avoidance is
mutual; if the two chance to meet in a path, the woman will step out
of it and stand with her back turned till he has gone by, or perhaps if
it be more convenient he will move out of the way. At Vanua Lava, in
Port Patteson, a man would not follow his mother-in-law along the
beach, nor she him, until the tide had washed out the footsteps of
the first traveller from the sand. At the same time a man and his
mother-in-law will talk at a distance.”87.1
It seems obvious that these Melanesian
It is significant that customs of avoidance are the same, and must be
mutual avoidance
between blood explained in the same way whether the woman
relations of opposite whom a man shuns is his wife’s mother or his own
sexes begins at or mother or his sister. Now it is highly significant that
near puberty.
just as among the Akamba of East Africa the
mutual avoidance of father and daughter only begins when the girl
has reached puberty, so among the Melanesians the mutual
avoidance of a boy on the one side and of his mother and sisters on
the other only begins when the boy has reached or approached
puberty. Thus in both peoples the avoidance between the nearest
blood relations only commences at the dangerous age when sexual
connexion on both sides begins to be possible. It seems difficult,
therefore, to evade the conclusion that the mutual avoidance is
adopted for no other reason than to diminish as far as possible the
chances of sexual unions which public opinion condemns as
incestuous. But if that is the reason why a young Melanesian boy, on
the verge of puberty, avoids his own mother and sisters, it is natural
and almost necessary to infer that it is the same reason which leads
him, as a full-grown and married man, to eschew the company of his
wife’s mother.
Similar customs of avoidance between mothers
Mutual avoidance of and sons, between fathers and daughters, and
mother and son, of
father and daughter, between brothers and sisters are observed by the
and of brother and natives of the Caroline Islands, and the writer who
sister in the records them assigns the fear of incest as the
Caroline Islands.
motive for their observance. “The prohibition of
marriage,” he says, “and of sexual intercourse between kinsfolk of
the same tribe is regarded by the Central Caroline natives as a
divine ordinance; its breach is therefore, in their opinion, punished by
the higher powers with sickness or death. The law influences in a
characteristic way the whole social life of the islanders, for efforts are
made to keep members of families of different sexes apart from each
other even in their youth. Unmarried men and boys, from the time
when they begin to speak, may therefore not remain by night in the
huts, but must sleep in the fel, the assembly-house. In the evening
their meal (âkot) is brought thither to them by their mothers or
sisters. Only when a son is sick may his mother receive him in the
hut and tend him there. On the other hand entrance to the assembly-
house (fel) is forbidden to women and girls except on the occasion of
the pwarik festival; whereas female members of other tribes are free
to visit it, although, so far as I could observe, they seldom make use
of the permission. Unmarried girls sleep in the huts with their
parents.
“These restrictions, which custom and tradition have instituted
within the family, find expression also in the behaviour of the
members of families toward each other. The following persons,
namely, have to be treated with respect—the daughters by their
father, the sons by their mother, the brothers by their sisters. In
presence of such relations, as in the presence of a chief, you may
not stand, but must sit down; if you are obliged on narrow paths to
pass by one of them you must first obtain permission and then do it
in a stooping or creeping posture. You allow them everywhere to go
in front; you also avoid to drink out of the vessel which they have just
used; you do not touch them, but keep always at a certain distance
from them; the head especially is deemed sacred.”88.1
In all these cases the custom of mutual
Mutual avoidance of avoidance is observed by persons of opposite sex
male and female
cousins in some who, though physically capable of sexual union,
tribes. are forbidden by tradition and public opinion to
have any such commerce with each other. Thus
far the blood relations whom a man is forbidden to marry and
compelled to avoid, are his own mother, his own daughter, and his
own sisters. But to this list some people add a man’s female cousins
or at least certain of them; for many races draw a sharp line of
distinction between cousins according as they are children of two
brothers or of two sisters or of a brother and a sister, and while they
permit or even prefer marriage with certain cousins, they absolutely
forbid marriage with certain others. Now, it is highly significant that
some tribes which forbid a man to marry certain of his cousins also
compel him to adopt towards them the same attitude of social
reserve which in the same or other tribes a man is obliged to
observe towards his wife’s mother, his own mother, and his own
sisters, all of whom in like manner he is forbidden to marry. Thus
among the tribes in the central part of New Ireland
Mutual avoidance of (New Mecklenburg) a male and a female cousin,
male and female
cousins in New the children of a brother and a sister respectively,
Ireland. are most strictly forbidden by custom to marry
each other; indeed this prohibition is described as
the most stringent of all; the usual saying in regard to such relations
is, “The cousin is holy” (i tábu ra kókup). Now, in these tribes a man
is not merely forbidden to marry his female cousin, the daughter of
his father’s sister or of his mother’s brother; he must also avoid her
socially, just as in other tribes a man must avoid his wife’s mother,
his own mother, his own daughter, and his own sisters. The cousins
may not approach each other, they may not shake hands or even
touch each other, they may not give each other presents, they may
not mention each other’s names; but they are allowed to speak to
each other at a distance of some paces. These rules of avoidance,
these social barriers erected between cousins, the children of a
brother and a sister respectively, are interpreted most naturally and
simply as precautions intended to obviate the danger of a criminal
intercourse between persons whose sexual union would be regarded
by public opinion with deep displeasure. Indeed the Catholic
missionary, to whom we are indebted for the information, assumes
this interpretation of the rules as if it were too obvious to call for
serious discussion. He says that all the customs of avoidance “are
observed as outward symbols of this prohibition of marriage”; and he
adds that “were the outward sign of the prohibition of marriage, to
which the natives cleave with genuine obstinacy, abolished or even
weakened, there would be an immediate danger of the natives
contracting such marriages.”90.1 It seems difficult for a rational man
to draw any other inference. If any confirmation were needed, it
would be furnished by the fact that among these tribes of New
Ireland brothers and sisters are obliged to observe precisely the
same rules of mutual avoidance, and that incest between brother
and sister is a crime which is punished with hanging; they may not
come near each other, they may not shake hands, they may not
touch each other, they may not give each other presents; but they
are allowed to speak to each other at a distance of some paces. And
the penalty for incest with a daughter is also death by hanging.90.2
Amongst the Baganda of Central Africa in like
Mutual avoidance of manner a man was forbidden under pain of death
certain male and
female cousins to marry or have sexual intercourse with his
among the cousin, the daughter either of his father’s sister or
Baganda; marriage of his mother’s brother; and such cousins might
or sexual
intercourse not approach each other, nor hand each other
forbidden between anything, nor enter the same house, nor eat out of
these cousins under
pain of death.
the same dish. Were cousins to break these rules
of social avoidance, in other words, if they were to
approach each other or hand each other anything, it was believed
that they would fall ill, that their hands would tremble, and that they
would be unfit for any work.90.3 Here, again, the prohibition of social
intercourse was in all probability merely a precaution against sexual
intercourse, for which the penalty was death. And the same may be
said of the similar custom of avoidance which among these same
Baganda a man had to observe towards his wife’s mother. “No man
might see his mother-in-law, or speak face to face with her; she
covered her face, if she passed her son-in-law, and he gave her the
path and made a detour, if he saw her coming. If she was in the
house, he might not enter, but he was allowed to speak to her from a
distance. This was said to be because he had seen her daughter’s
nakedness. If a son-in-law accidentally saw his mother-in-law’s
breasts, he sent her a barkcloth in compensation, to cover herself,
lest some illness, such as tremor, should come upon him. The
punishment for incest was death; no member of a clan would shield
a person guilty thereof; the offender was disowned by the clan, tried
by the chief of the district, and put to death.”91.1
The prohibition of marriage with certain cousins
Marriage between appears to be widespread among African peoples
certain cousins
forbidden among of the Bantu stock. Thus in regard to the Bantus of
some South African South Africa we read that “every man of a coast
tribes but allowed tribe regarded himself as the protector of those
among others.
females whom we would call his cousins, second
cousins, third cousins, and so forth, on the father’s side, while some
had a similar feeling towards the same relatives on the mother’s side
as well, and classified them all as sisters. Immorality with one of
them would have been considered incestuous, something horrible,
something unutterably disgraceful. Of old it was punished by the
death of the male, and even now a heavy fine is inflicted upon him,
while the guilt of the female must be atoned by a sacrifice performed
with due ceremony by the tribal priest, or it is believed a curse will
rest upon her and her issue.… In contrast to this prohibition the
native of the interior almost as a rule married the daughter of his
father’s brother, in order, as he said, to keep property from being lost
to his family. This custom more than anything else created a disgust
and contempt for them by the people of the coast, who term such
intermarriages the union of dogs, and attribute to them the insanity
and idiocy which in recent times has become prevalent among the
inland tribes.”91.2
Among the Thonga, a Bantu tribe about
Marriage between Delagoa Bay, marriages between cousins are as a
cousins allowed in
some African tribes rule prohibited, and it is believed that such unions
on condition that an are unfruitful. However, custom permits cousins to
expiatory sacrifice marry each other on condition that they perform an
is offered.
expiatory ceremony which is supposed to avert the
curse of barrenness from the wife. A goat is sacrificed, and the
couple are anointed with the green liquid extracted from the half-
digested grass in the animal’s stomach. Then a hole is cut in the
goat’s skin and through this hole the heads of the cousins are
inserted. The goat’s liver is then handed to them, quite raw, through
the hole in the skin, and they must tear it out with their teeth without
using a knife. Having torn it out, they eat it. The word for liver
(shibindji) also means “patience,” “determination.” So they say to the
couple, “You have acted with strong determination. Eat the liver now!
Eat it in the full light of the day, not in the dark! It will be an offering to
the gods.” Then the family priest prays, saying: “You, our gods, So-
and-so, look! We have done it in the daylight. It has not been done
by stealth. Bless them, give them children!” When he has done
praying, the assistants take all the half-digested grass from the
goat’s stomach and place it on the wife’s head, saying, “Go and bear
children!”92.1 Among the Wagogo of German East Africa marriage is
forbidden between cousins who are the children of two brothers or of
two sisters, but is permitted between cousins who are the children of
a brother and sister respectively. However, in this case it is usual for
the wife’s father to kill a sheep and put on a leather armlet, made
presumably from the sheep’s skin; otherwise it is supposed that the
marriage would be unfruitful.92.2 Thus the Wagogo, like the Thonga,
imagine that the marriage of cousins is doomed to infertility unless
an expiatory sacrifice is offered and a peculiar use made of the
victim’s skin. Again, the Akikuyu of British East Africa forbid the
marriage of cousins and second cousins, the children and
grandchildren of brothers and sisters. If such persons married, they
would commit a grave sin, and all their children would surely die; for
the curse or ceremonial pollution (thahu) incurred by such a crime
cannot be purged away. Nevertheless it sometimes happens that a
man unwittingly marries a first or second cousin; for instance, if a
part of the family moves away to another district, it may come about
that a man makes the acquaintance of a girl and marries her before
he discovers the relationship. In such a case, where the sin has
been committed unknowingly, the curse can be averted by the
performance of an expiatory rite. The elders take a sheep and place
it on the woman’s shoulders; there it is killed and the intestines taken
out. Then the elders solemnly sever the intestines with a sharp
splinter of wood taken from a bush of a certain sort (mukeo), “and
they announce that they are cutting the clan kutinyarurira, by which
they mean that they are severing the bond of relationship which
exists between the pair. A medicine man then comes and purifies the
couple.”93.1 In all these cases we may assume with a fair degree of
probability that the old prohibition of marriage between cousins is
breaking down, and that the expiatory sacrifice offered when such a
marriage does take place is merely a salve to the uneasy conscience
of those who commit or connive at a breach of the ancient taboo.
Thus the prohibition of marriage between
The mutual cousins, and the rules of ceremonial avoidance
avoidance of male
and female cousins observed in some tribes between persons who
is probably a stand in that relationship to each other, appear
precaution against both to spring from a belief, right or wrong, in the
a criminal intimacy
between them. injurious effects of such unions and from a desire
to avoid them. The mutual avoidance of the
cousins is merely a precaution to prevent a closer and more criminal
intimacy between them. If that is so, it furnishes a confirmation of the
view that all the customs of ceremonial avoidance between blood
relations or connexions by marriage of opposite sexes are based
simply on a fear of incest.
The theory is perhaps confirmed by the
The mutual observation that in some tribes the avoidance
avoidance between
a man and his between a man and his wife’s mother lasts only
wife’s relations until he has had a child by his wife;94.1 while in
seems to be partly
grounded on a fear others, though avoidance continues longer, it
of rendering the gradually wears away with time as the man and
wife infertile.
woman advance in years,94.2 and in others, again,
it is observed only between a man and his future mother-in-law, and
comes to an end with his marriage.94.3 These customs suggest that
in the minds of the people who practise them there is a close
connexion between the avoidance of the wife’s relations and the
dread of an infertile marriage. The Indians of Yucatan, as we saw,
believe that if a betrothed man were to meet his future mother-in-law
or father-in-law, he would thereby lose the power of begetting
children. Such a fear seems to be only an extension by false analogy
of that belief in the disastrous consequences of illicit sexual relations
which we dealt with in an earlier part of this chapter,94.4 and of which
we shall have more to say presently.94.5 From thinking, rightly or
wrongly, that sexual intercourse between certain persons is fraught
with serious dangers, the savage jumped to the conclusion that
social intercourse between them may be also perilous by virtue of a
sort of physical infection acting through simple contact or even at a
distance; or if, in many cases, he did not go so far as to suppose that
for a man merely to see or touch his mother-in-law sufficed to blast
the fertility of his wife’s womb, yet he may have thought, with much
better reason, that intimate social converse between him and her
might easily lead to something worse, and that to guard against such
a possibility it was best to raise a strong barrier of etiquette between
them. It is not, of course, to be supposed that these rules of
avoidance were the result of deliberate legislation; rather they were
the spontaneous and gradual growth of feelings and thoughts of
which the savages themselves perhaps had no clear consciousness.
In what precedes I have merely attempted to sum up in language
intelligible to civilized man the outcome of a long course of moral and
social evolution.
These considerations perhaps obviate to some extent the only
serious difficulty which lies in the way of the theory here advocated.
If the custom of avoidance was adopted in order to
The mutual guard against the danger of incest, how comes it
avoidance between
persons of the that the custom is often observed towards persons
same sex was of the same sex, for example, by a man towards
probably an his father-in-law as well as towards his mother-in-
extension by false
analogy of the law? The difficulty is undoubtedly serious: the only
mutual avoidance way of meeting it that I can suggest is the one I
between persons of
different sexes.
have already indicated. We may suppose that the
deeply rooted beliefs of the savage in the fatal
effects of marriage between certain classes of persons, whether
relations by blood or connexions by marriage, gradually spread in his
mind so as to embrace the relations between men and men as well
as between men and women; till he had worked himself into the
conviction that to see or touch his father-in-law, for example, was
nearly or quite as dangerous as to touch or have improper relations
with his mother-in-law. It is no doubt easy for us to detect the flaw in
this process of reasoning; but we should beware of casting stones at
the illogical savage, for it is possible or even probable that many of
our own cherished convictions are no better founded.
Viewed from this standpoint the customs of
The custom of ceremonial avoidance among savages assume a
mutual avoidance
between near serious aspect very different from the appearance
relations has of arbitrariness and absurdity which they are apt to
probably had the present to the civilized observer who does not look
effect of checking
the practice of below the surface of savage society. So far as
inbreeding. these customs have helped, as they probably
have done, to suppress the tendency to
inbreeding, that is, to the marriage of near relations, we must
conclude that their effect has been salutary, if, as many eminent
biologists hold, long-continued inbreeding is injurious to the stock,
whether animal or vegetable, by rendering it in the end infertile.95.1
However, men of science are as yet by no means agreed as to the
results of consanguineous marriages, and a living authority on the
subject has recently closed a review of the evidence as follows:
“When we take into account such evidence as there is from animals
and plants, and such studies as those of Huth,95.2 and the instances
and counter-instances of communities with a high degree of
consanguinity, we are led to the conclusion that the prejudices and
laws of many peoples against the marriage of near kin rest on a
basis not so much biological as social.”96.1 Whatever may be the
ultimate verdict of science on this disputed question, it will not affect
the result of the present enquiry, which merely affirms the deep and
far-reaching influence which in the long course of human history
superstition has exercised on morality. Whether the influence has on
the whole been for good or evil does not concern us. It suffices for
our purpose to shew that superstition has been a crutch to morality,
whether to support it in the fair way of virtue or to precipitate it into
the miry pit of vice. To return to the point from which we wandered
into this digression, we must leave in suspense the question whether
the Australian savages were wise or foolish who forbade a man
under pain of death to speak to his mother-in-law.
I will conclude this part of my subject with a few
Other examples of more instances of the extreme severity with which
the severe
punishment of certain races have visited what they deemed
sexual crime. improper connexions between the sexes.
Among the Indians who inhabited the coast of
The Indians of Brazil near Rio de Janeiro about the middle of the
Brazil. sixteenth century, a married woman who gave
birth to an illegitimate child was either killed or
abandoned to the caprice of the young men who could not afford to
keep a wife. Her child was buried alive; for they said that were he to
grow up he would only serve to perpetuate his mother’s disgrace; he
would not be allowed to go to war with the rest for fear of the
misfortunes and disasters he might draw down upon them, and no
one would eat any food, whether venison, fish, or what not, which
the miserable outcast had touched.96.2 In Ruanda,
The natives of
Ruanda.
a district of Central Africa, down to recent years
any unmarried woman who was got with child
used to be put to death with her baby, whether born or unborn. A
spot at the mouth of the Akanyaru river was the place of execution,
where the guilty women and their innocent offspring were hurled into
the water. As usual, this Puritanical strictness of morality has been
relaxed under European influence; illegitimate children are still killed,
but their mothers escape with the fine of a cow.97.1
The Saxons.
Among the Saxons down to the days of St.
Boniface the adulteress or the maiden who had dishonoured her
father’s house was compelled to hang herself, was burned, and her
paramour hung over the blazing pile; or she was scourged or cut to
pieces with knives by all the women of the village till she was
dead.97.2 Among the Slav peoples of the Balkan
The Southern
Slavs.
peninsula women convicted of immoral conduct
used to be stoned to death. About the year 1770 a
young betrothed couple were thus executed near Cattaro in
Dalmatia, because the girl was found to be with child. The youth
offered to marry her, and the priest begged that the sentence of
death might be commuted to perpetual banishment; but the people
declared that they would not have a bastard born among them; and
the two fathers of the luckless couple threw the first stones at them.
When Miss M. Edith Durham related this case to some Montenegrin
peasantry, they all said that in the old days stoning was the proper
punishment for unchaste women; the male paramours were shot by
the relations of the girls whom they had seduced. When “that
modern Messalina,” Queen Draga of Servia, was murdered, a
decent peasant woman remarked that “she ought to be under the
cursed stone heap” (pod prokletu gomilu). The country-folk of
Montenegro, who heard the news of the murder from Miss Durham,
“looked on it as a cleansing—a casting out of abominations—and
genuinely believed that Europe would commend the deed, and that
the removal of this sinful woman would bring prosperity to the
land.”97.3 Even down to the second half of the nineteenth century in
cases of seduction among the Southern Slavs the people proposed
to stone both the culprits to death.98.1 This happened, for example, in
Herzegovina in the year 1859, when a young man named Milutin
seduced or (to be more exact) was seduced by three unmarried girls
and got them all with child. The people sat in judgment upon the
sinners, and, though an elder proposed to stone them all, the court
passed a milder sentence. The young man was to marry one of the
girls, to rear the infants of the other two as his legitimate children,
and next time there was a fight with the Turks he was to prove his
manhood by rushing unarmed upon the enemy and wresting their
weapons from them, alive or dead. The sentence was fulfilled to the
letter, though many years passed before the culprit could carry out
the last part of it. However, his time came in 1875, when
Herzegovina revolted against the Turks. Then Milutin ran unarmed
upon a regiment of the enemy and found among the Turkish
bayonets a hero’s death.98.2 Even now the Old Catholics among the
South Slavs believe that a village in which a seducer is not
compelled to marry his victim will be punished with hail and
excessive rain. For this article of faith, however, they are ridiculed by
their enlightened Catholic neighbours, who hold the far more
probable view that thunder and lightning are caused by the village
priest to revenge himself for unreasonable delays in the payment of
his salary. A heavy hail-storm has been known to prove almost fatal
to the local incumbent, who was beaten within an inch of his life by
his enraged parishioners.98.3
It is difficult to believe that in these and similar
Inference from the cases the community would inflict such severe
severe punishments
inflicted for sexual punishment for sexual offences if it did not believe
offences. that its own safety, and not merely the interest of a
few individuals, was imperilled thereby.
If now we ask why illicit relations between the
Why should illicit sexes should be supposed to disturb the balance
relations between
the sexes be of nature and particularly to blast the fruits of the
thought to disturb earth, a partial answer may be conjecturally
the balance of suggested. It is not enough to say that such
nature?
relations are displeasing to the gods, who punish
indiscriminately the whole community for the sins of a few. For we
must always bear in mind that the gods are creations of man’s fancy;
he fashions them in human likeness, and endows them with tastes
and opinions which are merely vast cloudy projections of his own. To
affirm, therefore, that something is a sin because the gods will it so,
is only to push the enquiry one stage farther back and to raise the
further question, Why are the gods supposed to dislike and punish
these particular acts? In the case with which we
The reason why the are here concerned, the reason why so many
gods of savages
are supposed to savage gods prohibit adultery, fornication, and
punish sexual incest under pain of their severe displeasure may
crimes so severely
may perhaps be perhaps be found in the analogy which many
found in a mistaken savage men trace between the reproduction of the
belief that human species and the reproduction of animals
irregularities of the
human sexes and plants. The analogy is not purely fanciful, on
prevent the the contrary it is real and vital; but primitive
reproduction of peoples have given it a false extension in a vain
edible animals and
plants and thereby attempt to apply it practically to increasing the food
supply. They have imagined, in fact, that by
strike a fatal blow at
the food supply. performing or abstaining from certain sexual acts
they thereby directly promoted the reproduction of
animals and the multiplication of plants.99.1 All such acts and
abstinences, it is obvious, are purely superstitious and wholly fail to
effect the desired result. They are not religious but magical; that is,
they compass their end, not by an appeal to the gods, but by
manipulating natural forces in accordance with certain false ideas of
physical causation. In the present case the principle on which
savages seek to propagate animals and plants is that of magical
sympathy or imitation: they fancy that they assist the reproductive
process in nature by mimicking or performing it among themselves.
Now in the evolution of society such efforts to control the course of
nature directly by means of magical rites appear to have preceded
the efforts to control it indirectly by appealing to the vanity and
cupidity, the good-nature and pity of the gods; in short, magic seems
to be older than religion.100.1 In most races, it is true, the epoch of
unadulterated magic, of magic untinged by religion, belongs to such
a remote past that its existence, like that of our ape-like ancestors,
can be a matter of inference only; almost everywhere in history and
the world we find magic and religion side by side, at one time allies,
at another enemies, now playing into each other’s hands, now
cursing, objurgating, and vainly attempting to exterminate one
another. On the whole the lower intelligences cling closely, though
secretly, to magic, while the higher intelligences have discerned the
vanity of its pretensions and turned to religion instead. The result has
been that beliefs and rites which were purely magical in origin often
contract in course of time a religious character; they are modified in
accordance with the advance of thought, they are translated into
terms of gods and spirits, whether good and beneficent, or evil and
malignant. We may surmise, though we cannot prove, that a change
of this sort has come over the minds of many races with regard to
sexual morality. At some former time, perhaps, straining a real
analogy too far, they believed that those relations of the human
sexes which for any reason they regarded as right and natural had a
tendency to promote sympathetically the propagation of animals and
plants and thereby to ensure a supply of food for the community;
while on the contrary they may have imagined that those relations of
the human sexes which for any reason they deemed wrong and
unnatural had a tendency to thwart and impede the propagation of
animals and plants and thereby to diminish the common supply of
food.
Such a belief, it is obvious, would furnish a
Such a belief would sufficient motive for the strict prohibition of what
account both for the
horror with which were deemed improper relations between men
many savages and women; and it would explain the deep horror
regard such crimes, and detestation with which sexual irregularities are
and for the severity
with which they viewed by many, though certainly not by all,
punish them. savage tribes. For if improper relations between
the human sexes prevent animals and plants from
multiplying, they strike a fatal blow at the existence of the tribe by
cutting off its supply of food at the roots. No wonder, therefore, that
wherever such superstitions have prevailed the whole community,
believing its very existence to be put in jeopardy by sexual
immorality, should turn savagely on the culprits, and beat, burn,
drown or otherwise exterminate them in order to rid itself of so
dangerous a pollution. And when with the advance of knowledge
men began to perceive the mistake they had made in imagining that
the commerce of the human sexes could affect the propagation of
animals and plants, they would still through long habit be so inured
to the idea of the wickedness of certain sexual relations that they
could not dismiss it from their minds, even when they discerned the
fallacious nature of the reasoning by which they had arrived at it. The
old practice would therefore stand, though the old theory had fallen:
the old rules of sexual morality would continue to be observed, but if
they were to retain the respect of the community, it was necessary to

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