Valerie Curtis, Why Disgust Matters

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Phil. Trans. R. Soc. B (2011) 366, 3478–3490


doi:10.1098/rstb.2011.0165

Review

Why disgust matters


Valerie Curtis*
Department of Infectious and Tropical Diseases, London School of Hygiene and Tropical Medicine,
Keppel Street, London WC1E 7HT, UK
The new synthesis about disgust is that it is a system that evolved to motivate infectious disease
avoidance. There are vital practical and intellectual reasons why we need to understand disgust
better. Practically, disgust can be harnessed to combat the behavioural causes of infectious and
chronic disease such as diarrhoeal disease, pandemic flu and smoking. Disgust is also a source of
much human suffering; it plays an underappreciated role in anxieties and phobias such as obsessive
compulsive disorder, social phobia and post-traumatic stress syndromes; it is a hidden cost of many
occupations such as caring for the sick and dealing with wastes, and self-directed disgust afflicts the
lives of many, such as the obese and fistula patients. Disgust is used and abused in society, being
both a force for social cohesion and a cause of prejudice and stigmatization of out-groups. This
paper argues that a better understanding of disgust, using the new synthesis, offers practical lessons
that can enhance human flourishing. Disgust also provides a model system for the study of emotion,
one of the most important issues facing the brain and behavioural sciences today.
Keywords: disgust; obsessive compulsive disorder; disease; behaviour; evolution

1. INTRODUCTION received scant scientific attention until recently [10].


The premise of the new synthesis about disgust is that This special issue demonstrates how disgust is now
it is an adaptive system that evolved to motivate dis- proving a fertile ground for study by psychologists,
ease-avoidance behaviour [1 – 7]. It arose in our zoologists and evolutionary biologists. Beyond the life
animal ancestors to facilitate the recognition of objects sciences, it also provides rich matter for the human-
and situations associated with risk of infection and to ities—in the social sciences, in history and classical
drive hygienic behaviour, thus reducing micro- and studies, in politics, jurisprudence and marketing, as
macro-parasite contact. Sometime in our evolution well as in the arts.
towards human ultrasociality, disgust took on an Clearly, the better we understand how and why dis-
extended role—providing a motive to punish antisocial gust evolved and the part that it plays in our natures
behaviour and to shun the breakers of social rules and in our societies, the better we will advance in all
[8,9]. Disgust is an adaptive system whereby individ- of these fields of intellectual endeavour. Such advances
ual responses vary according to an individual’s are important in themselves, but they also have prac-
personality and learning experience, as well as by tical repercussions. In this paper, I argue that there
local cultural effects such as norms about manners are three principal practical reasons why we need to
and the symbolism of pollution and purity [7]. This better understand the biology of this ‘dark side’ of
new synthesis replaces previous conceptions of disgust our nature.
as, for example, a Freudian means of repudiating First, as one of our principal defences against infec-
desired objects, such as the mother’s breast or faeces tion, disgust can be harnessed to efforts at improving
[10], a psychodynamic balancing mechanism to health. It can be employed in programmes to prevent
refuse reminders of our animal nature [6,11,12] or as diarrhoeal diseases, pandemic flu and to aid smoking
a social and cultural construction [13,14]. cessation, for example. Second, disgust has important
But why, in the end, does it matter that we under- implications for psychological welfare. It plays a role
stand how and why disgust evolved? Disgust impacts in obsessive compulsive and post-traumatic stress
on many aspects of our lives, from our individual, disorders (OCD and PTSD) and it is part of the
domestic, everyday hygiene habits, through our emotional cost of caring for the sick, elderly and
moral choices as members of society, to public policy infirm. Stigmatization and self-directed disgust cause
on issues such as health, justice, social exclusion and suffering in conditions such as obesity and fistula.
warfare. However, possibly because it is the part of Thirdly, disgust is a moral emotion that influences
our nature that deals with repulsion, disgust has social behaviours. Its role in religion, justice, techno-
logical progress, caste, class, xenophobia and the
politics of exclusion needs to be better understood if
* [email protected] we are to create healthier and more humane societies.
One contribution of 11 to a Theme Issue ‘Disease avoidance: from Here I tackle each of these issues in turn and
animals to culture’. then draw out some of the questions that remain to
3478 This journal is q 2011 The Royal Society
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Review. Why disgust matters V. Curtis 3479

be answered about this powerful but, still poorly The final column of table 1 picks out items that
understood emotion. have been cited as disgusting in various studies [1,2].
There are a variety of disgust elicitors that relate to
almost every infectious condition. For the faecal –
2. DISGUST AND DISEASE CONTROL oral infections, these include faeces, dirty water and
The proper domain [15] of disgust is the avoidance contaminated foods; for the skin contact infections,
of infectious disease [1]. Despite major recent skin lesions; for sexually transmitted diseases, ulcer-
improvements in our understanding of the trans- ated genitals and individuals who may be at high risk
mission, prevention and treatment of infectious such as sex workers; for the respiratory infections,
disease, the problem is still with us. Table 1 presents respiratory secretions and contaminated materials.
the major current and recent infectious disease threats Sick people and bodily secretions/excretions occasion
to humans. Six conditions cause most deaths: diar- disgust as the source of multiple possible infections.
rhoeal diseases, acute respiratory tract infections, We have suggested elsewhere that most disgust elicit-
malaria, measles, HIV and tuberculosis. Parasitic ors can be incriminated in the transmission of
worms including schistosomes, hookworm, ascaris infection from source to host and that this explains
and the nematodes that cause lymphatic filariasis and why they are found to be disgusting [2]. Those with
oncocerciasis still infect one-third of the world’s popu- lower disgust sensitivity are known to suffer from
lation [16]. Leprosy, polio, smallpox, plague and more infectious disease [21], and selective partner
guinea worm were major causes of death and disability choice is an important, but underappreciated, factor
in previous centuries; they are now rare or eradicated, in the spread of sexually transmitted infections [22].
thanks to recent control efforts [17]. Measles, Of course, the diseases of recent centuries may not be
diphtheria and meningitis also cause far less mortality a perfect proxy for the diseases that shaped the disgust
owing to recent advances in vaccination. Newly response in our pre-human and human evolutionary
emerging or re-emerging infections such as Ebola, history. Diseases with their origins in the domestication
SARS, West Nile and Rift Valley fevers and pandemic of animals or in high-density urban settlement, for
influenza are a major cause for concern, as is the emer- example, are thought to be more prevalent now than
gence of resistance to antibiotics and antimalarials. in ancestral times [23]. Nevertheless, the table shows
Not included in the table are the infections that a general pattern whereby hygienic behaviour with
have also been shown to play a role in many chronic dis- respect to disgust elicitors plays an essential role in
eases, including cancer, stroke, multiple sclerosis and the prevention of infection. These behaviours are
cardiovascular disease [18]. ancient and ubiquitous, many of them are shared with
While medical effort and attention has focused on our animal ancestors [24] and are not contingent on
the pathology of disease, and the search for vaccines recent scientific knowledge about the behaviour of the
and cures, measures to prevent the acquisition of infec- agents of infectious disease. Indeed, the idea of contact-
tion in the first place have received less attention. Yet, as ing or consuming infectious substances such as saliva,
the table shows, avoidance behaviour is essential to pre- faeces or vomit, or of intimate contact with those
vent the spread of all of these conditions [17]. If hygiene known to be carrying infection is deeply uncomfortable
is defined as disease-avoidance behaviour [19], then to even contemplate. Self-limitation of such behaviour
hygienic measures help to defend all of the principal is so automatic and intuitive that it is often ignored as
portals of entry to the body. Safe excreta disposal, the front-line in our defence against disease.
hand, food and water hygiene prevent the faecal – oral Without disgust and the hygienic behaviours it eli-
transmission of the diarrhoeal diseases including cho- cits, then, infectious diseases would cause far more
lera, salmonelloses, as well as hepatitis A and E, polio morbidity and mortality in our own—and in all
and various worm infections. Avoiding sex with infected free-living animal—species. (There is one notable
others helps prevent the transmission of HIV, syphilis exception to this pattern. No disgust elicitor is involved
and hepatitis B and C. Diseases that use the respiratory in the insect-vectored infections such as malaria and
route such as tuberculosis, measles, influenza leprosy, oncocerciasis. Perhaps the adaptive response to a bite
diphtheria and respiratory tract infections are harder is not disgust, but to slap away the offending insect,
to prevent, but reducing proximity and contact with or, alternatively, perhaps ancestral conditions were
the sick hinders airborne transmission and the avoid- such that it was impossible to gain an adaptive
ance of contaminated fomites can help reduce advantage from insect bite-avoidance behaviour [1].)
infection risk [20]. Staphylococcal, streptococcal and Disgust therefore plays a major role in public
tetanus infections can be prevented through body sur- health. How can this knowledge be exploited in pro-
face hygiene, especially by avoiding fluid transfer from grammes to control disease? Where disgust reactions
and to skin lesions and from fomites. The body surface are appropriate to modern conditions they can be eli-
is also the route of injection of the infectious diseases cited. In cases where they are inappropriate, efforts
that are carried by insect vectors, including malaria, can be made at redirection. Further, disgust can also
onchocerciasis, leishmaniasis, typhus and yellow fever. be employed to help improve health beyond the
Here, disease prevention means avoiding insect bites. domain of infectious disease.
Other vector-borne infections including rabies and Take, for example, the diseases that are transmitted
toxoplasmosis can be prevented by avoiding contact via the faecal – oral route. Though the situation is
with bats, rats, dogs and cats. A number of these infec- improving, diarrhoeal diseases still kill an estimated
tions have multiple routes of infection, especially the 1.5 million children every year [25]. Human faeces are
diseases of crowding (measles and tuberculosis). the main source of infection [26]. Evidence suggests
Phil. Trans. R. Soc. B (2011)
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3480 V. Curtis Review. Why disgust matters

Table 1. Disgust, behaviour and the major causes of infectious disease.

disease infectious agent preventive behaviour disgust elicitor

AIDS human immunodeficiency safe sex, avoid needle sexual fluids, body fluids, sickly
virus sharing person
acute respiratory tract Streptococcus pneumoniae, hand hygiene, respiratory nasal mucous, spittle, droplets,
infections Haemophillus influenzae, hygiene, surface coughing, proximity and
Mycoplasma pneumoniae hygiene, proximity contact, contaminated fomites
avoidance
diarrhoeal diseases over 20 bacterial and viral avoid faecal –oral faeces, spoilt food, dirty water,
agents including: Vibrio transmission through vomitus, contaminated
cholerae, Shigella spp., hand hygiene, safe water fomites, contaminated food
Salmonella spp., consumption, safe
Campylobacter enteritis, disposal of faeces, safe
Cryptosporidium, food hygiene, surface
Escherichia coli hygiene, restrict animal
contact
diphtheria Corynebacterium diptheriae avoid contact, fabric sick person, soiled materials,
hygiene nasal discharges
lymphatic filariasis Wucheraria bancrofti, Brugia avoid being bitten by signs of deformity
malayi infected mosquitoes
hepatitis (viral) hepatitis A, E virus faecal–oral: see diarrhoeal faeces, dirty water, vomitus,
diseases contaminated food and fomites
hepatitis B, C virus safe sex, avoid close blood, saliva, body fluids
physical contact, avoid
shared needles
leishmaniasis Leishmania tropica, avoid sandfly bite, destroy rubbish heaps
Leishmania braziliensis, vector breeding sites
Leishmania spp.
leprosy Mycobacterium leprae contentious—avoid direct sick others, skin lesions,
contact and nasal deformity, nasal mucous
secretions
malaria Plasmodium falciparum, avoid being bitten by —
Plasmodium ovale, infected mosquitoes,
Plasmodium malariae and destroy breeding sites
Plasmodium spp.
measles measles virus isolation rash, sores, nasal and throat
secretions, and soiled items
meningitis Neisseria meningitides, avoid direct contact, nasal contact, nose and throat
Streptococcus pneumonia, secretions secretions
Haemophilus influenzae
type b (Hib)
onchocerciasis (river Oncocerca volvulus avoid bite of Simulium flies
blindness) blackfly, destroy
breeding sites
plague Yersinia pestis domestic hygiene, clothes pustules, sick people, exudates,
hygiene, avoid sick refuse, rats, fleas, sick animals
animals
poliomyelitis polio virus faecal–oral: see diarrhoeal faeces, throat secretions, soiled
disease articles
rabies rabies virus avoid bite or scratch from saliva, infected animal, dog, bat
infected animal
schistosomiasis Schistosoma mansoni, avoid wading into water, snails, stagnant water
Schistosoma haematobium, urinating in or
Schistosoma japonicum defaecating near water
smallpox variola virus case isolation, contact pustules, rash, blood, droplets
avoidance
staphylococcal skin Staphylococcus aureus skin hygiene, hand skin lesions, weeping sores, nasal
infections (impetigo, hygiene, clothes and discharges, soiled toilet articles
carbuncles, abscesses toilet items hygiene
etc.)
streptococcal infections Streptococcus pyogenes hand hygiene, food rash, fever, skin lesions,
(tonsillitis, scarlet fever, hygiene, avoid skin discharges, necrosis, vaginal
impetigo, septicaemia, contact, lesions secretions, respiratory droplets,
otitis, wound infections, skin contact, milk, meat
toxic shock, rheumatic
heart disease)
(Continued.)

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Review. Why disgust matters V. Curtis 3481

Table 1. (Continued.)

disease infectious agent preventive behaviour disgust elicitor

syphillis Treponema pallidum safe sex rash, skin lesions, chancre,


especially on genitals,
exudates, insanity, prostitution
taenia (tape worm) Taenia solium, avoid undercooked beef pig, cow, human faeces, worm
Taenia saginata and pork, sanitation, eggs in meat
handwashing
tetanus Clostridium tentani wound hygiene, safe soil, dust, human and animal
childbirth practice faeces
toxoplasmosis Toxoplasma gondii cook meat, wash cat faeces, soil,
vegetables, wash hands, dirt on food
avoid cat faeces
tuberculosis Mycobacterium tuberculosis respiratory hygiene, nasal mucous, spittle, droplets,
minimize close contact, stale air, homeless
ventilation

that handwashing with soap, were it practised globally, to a public toilet and found that disgust-based mess-
could save over a million lives a year, mainly from the ages such as ‘soap it off or eat it later’ were among
infectious enteric diseases [27]. It can also prevent the most effective in increasing soap use, especially
respiratory infections [28], including pandemic in men [34].
flu [20], infectious blinding trachoma [29], AIDS- Disgust featured in the UK Government response
associated infections [30] and potentially reduce to the threat of a pandemic of H1N1 influenza in
malnutrition [31]. Handwashing with soap is, however, 2009/2010. The cover image of an information leaflet
a rare practice. Direct observation showed that only 3 delivered to every household in the UK (see http://
per cent of mothers in Ghana, 4 per cent in Madagascar, www.dh.gov.uk/prod_consum_dh/groups/dh_digitalas
12– 14% in China, Tanzania and Uganda and 18 per sets/@dh/@en/documents/digitalasset/dh_098680.pdf;
cent in Kyrgyzstan [32] were washing their hands with [41]) to raise awareness of hand and respiratory hygiene
soap after using the toilet. In the UK, we found that explicitly depicts the aerosol spread of bodily secre-
only 43 per cent of mothers washed their hands with tions in a sneeze coming directly towards the viewer.
soap after changing a dirty nappy [33] and electronic Exposure to the campaign material was associated
sensors showed that only 32 per cent of men and 64 with increases in hygienic behaviour, such as the pur-
per cent of women washed their hands with soap after chase of antibacterial hand gel, though the specific
using a public toilet [34]. Formative research studies effect of the disgust component was not explicitly
into the reasons why people washed their hands found evaluated [29].
motives that included comfort, nurture, status and Mass media is, of course, not the only source of
attraction. However, disgust at the idea that faecal individual learning about disgust and hygiene. Chil-
material might be present on hands was consistently dren throughout the world are socialized into hygiene
reported as the most powerful motivator of handwash- rules at an early age by parents, family, school and
ing with soap after going to the toilet [32]. This the wider community [7,41]. Children learn to bathe
information was employed in the development of a and groom themselves, especially before social inter-
national handwashing campaign in Ghana. TV and action, to avoid sharing toilet articles, to avoid
radio commercials were designed to graphically high- wearing night clothes in public, where (and where
light the contamination of hands and to show how not) to defecate, to use a handkerchief and to eat
invisible matter could be transferred to foods that ‘politely’ without exchange of bodily fluids. Individ-
were being eaten by children [35]. The campaign uals who do not display continence with their own
improved nationally reported rates of handwashing emanations are regarded as having ‘bad manners’
with soap by 13 per cent after the toilet and by 41 per and are denied the benefits of social interaction [42].
cent before eating [36]. Similar improvements in hand Having well-mannered children is an important aspira-
hygiene were achieved in a social marketing campaign tion for mothers in most societies [32]. Though the
in Burkina Faso that used disgust-based messages, subject has been little investigated, it appears that
amongst others [37]. An image of a bacteria-ridden mothers recruit disgust to teach their children how to
hand used as a screen saver in a Los Angeles hospital behave, pulling disgust faces and making appropriate
reportedly improved staff handwashing practices ‘yuk’ noises as children ‘make messes’. The process
dramatically [38]. is aided by a predisposition or preparedness [43 – 45]
Disgust has been evoked to promote handwashing to learn disgust of bodily fluids. The fact that failing
in more controlled conditions. Porzig-Drummond to display continence with bodily fluids is socially
et al. showed that adding disgust-relevant images to unacceptable was exploited in a graphic television
educational films and posters improved handwashing commercial for the Florida Department of Health,
rates above the effect of education alone both in the where one character sneezes over food, surface,
laboratory and in the public washrooms [39]. Judah hands and workmates, causing colleagues to demon-
et al. displayed a variety of messages at the entrance strate their disgust at these lapses in respiratory
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3482 V. Curtis Review. Why disgust matters

manners [46]. In our public toilet study using unob- of children’s diets [57]. This helped to spur the UK
trusive sensors, we found that rates of handwashing government to improve the quality of school dinners.
decreased when there were few people in the facility, Variations on this idea, such as graphic displays of the
and the message that had the biggest positive effect fat and sugar content of common food items, could
was: ‘Is the person next to you washing hands with help to harness disgust to healthy eating campaigns.
soap?’ [34]. Manners are a subject about which One could imagine further uses of disgust targeted at
almost nothing has been written in the academic obesity or at unsafe sex, for example. However, disgust
press, yet understanding them better might prove has to be employed responsibly, as it can encourage
fruitful in the quest to prevent the person-to-person moralization and stigmatization, as we have seen.
spread of infection.
Whilst disgust of nasal emanations and of people who
spread them is probably an appropriate and adaptive 3. DISGUST AND PSYCHOLOGICAL WELFARE
reaction to the threat of pandemic influenza [47], Disgust is a strong and visceral emotion that can
disgust responses can sometimes be unhelpful to public arouse powerful affective and behavioural responses.
health. The disgust system operates by the precautionary While the emotion arose to defend against infectious
principle whereby it is better to miss one meal than to disease, it can also cause maladaptive behaviour, inter-
run the risk of contracting a life-threatening disease fering with the ability to lead a normal life. Some
[48,49]. Hence responses can be disproportionate to problems are associated with pathologies of the disgust
actual risk. The food industry is regularly affected by system. Others may be due to disgust’s ‘normal’ func-
contamination scares that can lead to huge, but tempor- tioning in the context of an abnormal or novel
ary shifts away from purchasing meat products, eggs or environment. Further, some professions require the
chocolate, for example [50]. The French public reduced suppression of disgust, which could be regarded as a
their consumption of beef in response to emotive stories psychological cost that has to be borne by those
in the press about what could happen if you ate ‘mad individuals—and by society as a whole.
cow’ [51]. A study of public reactions to a hypothetical Disgust sensitivity varies from one individual to
outbreak of pneumonic plague found that people were another along a continuum [58]. We might expect
likely to want to avoid health centres, when attending then that individuals at the very high, or very low ends
would have been beneficial to their health [52]. In of the spectrum might manifest behavioural problems
California, public protestations of disgust have derailed associated with being too easily or too little disgusted.
projects for converting wastewater into drinking Those who are too easily disgusted might be predicted
water [53]. to manifest phobias associated with potential disease
While disgust’s proper domain is that of infectious sources such as other people, body products, sexual
disease, it has also been employed in efforts to tackle organs and by-products, certain foodstuffs and dis-
other public health problems, most notably smoking. ease-related animals. Those who are, on the contrary,
Cessation campaigns have used disgust freely. For too little disgusted might find difficulty in being
example, the British Heart Foundation’s most success- accepted into society and in maintaining bodily and
ful media campaign entitled ‘Give up before you clog domestic hygiene, with implications for their own
up’ graphically depicted the impact of smoking on health and that of their dependants. Unfortunate
arteries by showing cigarettes apparently dripping disgust experiences might also leave unpleasant or
globs of fat [54]. The World Health Organization now debilitating sequelae including post traumatic stress
recommends the use of graphic images of diseased disorder (PTSD).
organs on cigarette packs. A Canadian study showed How far does the evidence bear out these predic-
that the greater the disgust reported at such pictures, tions? A number of studies suggest that some forms
the greater the likelihood that participants would have of obsessive compulsive disorder (OCD) can best be
attempted to, or succeeded in, quitting [55]. understood as disorders of the disgust system [59].
Disgust appears to have played a role in what Rozin Up to 50 per cent of OCD patients present with con-
calls the ‘moralization’ of smoking, which has become tamination fears [60]. They suffer from intrusive
disgusting because it has been linked to contamination thoughts of contamination and impurity and reduce
and disease. Individuals then display strong aversion to their distress by excessive sanitation and disinfection
even minimal contact with the offensive substance of the self and the environment [61]. These patients
(refusing smokers hotel rooms, for example). Rozin tend to rate contaminated objects as ‘disgusting’
notes, ‘when disgust becomes linked to an entity or rather than ‘frightening’ [62]. In one memorable
activity, rejection or avoidance of that activity becomes experiment, Tolin and colleagues created a chain of
highly motivated and internalized’. He found that contagion where a pencil was touched to a toilet
moral reactions to smoking depended more on how bowl and then wiped on another pencil, and that one
disgusting than on how unhealthy it was perceived to onto another in sequence. ‘Normal’ participants, and
be [56]. The modern practice of relegating smokers those with chronic anxiety, reported diminishing con-
to the outside of public buildings reinforces the tamination that had largely disappeared by the fourth
rejection of the disgusting practice and the stigmatization pencil. However, the OCD patients reported appreci-
of the individual as antisocial. able contamination even beyond the tenth pencil.
Food-related disgust can be employed to combat They described a world of spreading, looming vulner-
obesity. In a UK TV show, all of the snack and junk ability where they cannot control the threat of
food typically eaten by one school class was piled into contagion [62]. As OCD occurs along a continuum
one huge disgusting heap to highlight the poor quality of severity, it is likely that for every individual who
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Review. Why disgust matters V. Curtis 3483

seeks help, there will be many more borderline indi- system to affect sexual function. Though the problem
viduals who suffer from some form of debilitating has been little studied, several authors report that dis-
contamination anxiety. gust is implicated in undermining sexual arousal and
It might be expected that contamination anxiety desire [77,78]. De Jong et al. [77] present case studies
would become more severe when disease reminders of women who had turned disgust on themselves;
become more prevalent, for example, during epi- associating dirt, disease, fistula and defaecation prob-
demics [63]. Indeed, contamination fears and lems with their vagina which led to an inability to
washing rituals were exacerbated in OCD patients face intercourse.
during the recent H1N1 swine flu pandemic [64]. Disgust may also play a role in the decision to
Planners need to bear in mind the possible social remain celibate. The problem is described by one
costs of pandemic awareness campaigns and consider ex-celibate, the UK broadcaster Stephen Fry:
the need for additional support services.
As ultrasocial beings, humans depend on others ‘I would be greatly in the debt of the man who could tell
for survival, yet others are also the main source of me what would ever be appealing about those damp,
dark, foul-smelling and revoltingly tufted areas of the
infectious disease. Overactive disgust responses may
body that constitute the main dishes in the banquet of
play a role in some forms of social phobia. Though
love. . . . . .Once under the influence of the drugs sup-
most goes unreported, at any one time 4.5 per cent of plied by one’s own body, there is no limit to the
Americans may be suffering from social phobias and indignities, indecencies, and bestialities to which the
2.3 per cent from agoraphobia [65]. Symptoms of both most usually rational and graceful of us will sink’ [79].
include an abnormal unwillingness to venture into
crowds and to contact other people. The evidence is If the psychological problems we have discussed
equivocal as to whether disgust plays a role—while agora- above are pathologies of the disgust system, then
phobics have heightened disgust sensitivity [66] and comorbidities are also to be expected. Monteiro et al.
agoraphobia is twice as common in women than it is in [80] found that 24 per cent of patients with untreated
men (consistent with female disgust sensitivity being OCD were virgins and another 9 per cent had not been
higher on average than it is for men [2]), one study sexually active for years. Of their 25 patients, seven
found no heightened disgust sensitivity in social phobia who reported sexual problems also suffered from
(possibly because an instrument measuring only extreme shyness, suggesting possible social phobia
food-related disgust was employed) [66]. comorbidity with OCD.
A variety of other debilitating specific phobias are If sexual, social, contamination, blood injury and
also candidates for pathologies of the disgust system. food-related phobias may, at least partly, be explained
Blood-injection-injury phobia is characterized by as maladaptive disorders of an evolved disease-avoidance
extreme aversion to the sight of blood, injuries, or sur- system, another class of disgust-related psychological
gical procedures including injections. Sufferers have disorders can be classed as adaptive responses to a hostile
higher disgust sensitivity, rate disgusting images as environment. In particular, it seems that one class of
more disgusting than controls and display stronger PTSD may result from extreme experiences associated
facial expressions of disgust [67]. A variety of small with disgust. Olatunji et al. [81] showed that rape victims
animal and insect phobias are also potentially disgust- with PTSD suffer from feelings of dirtiness associated
related. Animals that have connections with disease with mental pollution. Victims of childhood sexual
and dirt are much more likely candidates for phobias abuse and survivors of torture may suffer in similar
and childhood fears than those that do not (e.g. spiders, ways. Dalgleish and Power provide case histories where
rats, worms, maggots, cockroaches and teeming insects extremely disgusting events such as encounters with
[68]). Recent research also suggests that disgust is a decomposed corpses in war or at work, or biological
stronger predictor than anxiety of spider avoidance contaminants in food lead to intrusive thoughts, flash-
[69]. Trichotillomania may also be disgust-related; backs, recurrent nausea, feelings of dirtiness that
pulling out skin hairs may be an exaggerated response cannot be removed by washing and other manifestations
to the possible presence of ectoparasites in skin— that can leave patients unable to lead a normal life [82].
a hypothesis that has some support in the literature [70]. If the clinical and subclinical conditions that I have
Clinical observation suggests that disgust is a pri- described are indeed disgust system disorders, then
mary feature of eating disorders such as anorexia and practical implications follow. First of all, accurate diagno-
bulimia [10]. While some studies have shown correl- sis is required, and seeing such problems as potentially
ations between measures of disgust sensitivity and of disgust-related can help to hone the instruments of
eating disorders [71,72]), others have failed to find diagnosis. Secondly, many of these conditions occur on
such associations [66,73]. Disgust with the shape of a sliding scale in the population, and many are associated
one’s own body is often a feature of eating disorders, with shame and an extreme reluctance to disclose or
and indeed obesity does tend to be seen as disgusting present to health services; hence much suffering goes
[74,75]. Meat is one of the most likely sources of patho- undiagnosed and unaided. Health workers need to be
gens in food and is also a particular focus of food-related well-briefed to detect hints of these conditions and to
disgust. It is therefore unsurprising that most cultures look for comorbidities, for example, for sexual dysfunc-
have taboos about what meats are suitable to eat and tion in those presenting with OCD. Internet-based
many cultures and sub-cultures such as Hindus and support for such conditions may be more acceptable to
vegetarians/vegans reject it entirely [76]. many than face-to-face interaction [77].
As sexual acts, body parts and products are a focus Thirdly, there are many approaches to treatment both
of disgust, one might expect pathologies of the disgust through behavioural and drug therapies. A systematic
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3484 V. Curtis Review. Why disgust matters

look at what has worked in each of these conditions contaminate by association, it is used to marginalize
through the lens of disgust might reveal effective outsiders to groups (stigmatization) and is employed
therapies. For example, we know that cognitive reapprais- in ritual and religion to demarcate what is pure and
al is possible. Just as rotting milk can be relabelled as what is polluted. There is some evidence that disgust
yoghurt and so becomes palatable, de Jong suggests plays a role in morality, as much anti-social behaviour,
that exercises aimed at reconstructing sexual organs, as a form of social parasitism, is met with disgust. The
not as smelly and dirty, but as examples of exquisite workings of disgust as an adaptive system for disease
design could be effective in reducing sexual phobias avoidance in social groups have been discussed at
[83]. Work is needed to determine whether behavioural length in a recent paper [7]. Here, I am concerned
therapies such as Exposure with Response Prevention with the practical implications.
and microbiological experiments demonstrating the There is much evidence that humans tend to shun
lack of organisms on objects perceived to be contamin- other individuals that display signs of disease, as do
ated [62] are effective. Cognitive behavioural therapy ants, fish [90,91], bullfrogs [92], mice [93], lobsters
involving habituation to disgust objects and extinction [94] and chimps [95]. Human faces made up to look
along with the formation of new and positive associations sick are found to be more disgusting than healthy
could be used across these phobias, possibly with the counterparts [2]. Individuals perceived to have disabilities
addition of cortisol, which has been shown to enhance or disfigurements automatically activate disease-relevant
the consolidation of newly learnt memories [77]. Drug cognitions, even when perceivers are explicitly aware
therapies might also focus on the possible implication that these individuals do not harbour contagious diseases
of serotonin pathways in disgust [84]. [96,97]. A hypervigilant disgust may be triggered
Finally, research suggests that the disgust system is implicitly by a range of conditions that may, or may
made up of a series of components that relate to not, be associated with risk of infection, such as epilepsy,
different types of disease threat (sexual, hygiene, blood- mental illness, mental retardation, obesity, skin con-
and-guts, food, sick people, animals/insects, etc.; [85]). ditions such as psoriasis, cancer and HIV [98]. People
It seems likely that each type of threat has its own type who are more concerned with disease are less likely to
of phobia. The disgust scales in current use [86–88] have friends with disabilities [99], to dislike obese individ-
are based on psychodynamic conceptions of disgust uals more [75] and to display implicit ageism [100].
that predate the new evolutionary synthesis [89] or do Having a psychology that is hypervigilant to cues as to
not distinguish between types of organic disgust [6]. who might be carrying an infectious illness means that
We are currently preparing a new scale based on the dis- we are particularly sensitive to socially acquired infor-
crete disease-avoidance tasks of disgust which should mation about who is sick. Power-seeking individuals
have more power to help in distinguishing the discrete can exploit this fact. A common tactic for the playground
pathologies of disgust subsystems. bully, for example, is to label another child as infected or
as having ‘cooties’; the victim then suffers shunning by
their peer group.
4. THE SOCIAL USES AND ABUSES OF DISGUST Damaging as this can be to the individuals who are the
While disgust is the primary means by which individ- subject of suspicion, stigmatization extends the problem
ual humans detect and avoid infectious pathogens, of the labelling of individuals as diseased to whole groups.
the problem is not just an individual one. Parasites Out-groups, already a subject of suspicion because they
tend to specialize in exploiting the particular bio- could be carrying novel infections to which the in-group
chemical and morphological features of their hosts, has not previously been exposed [1], can be especially
making parasite transmission most likely between bio- easily labelled as disease carriers. A body of work has
logically similar organisms. Social animals thus face a recently emerged that links parasite stress to assortative
conundrum; sociality brings fitness benefits, but at sociality (reviewed by Fincher & Thornhill [101]). Cul-
the same time it carries an elevated risk of infectious tural groups that have historically faced high rates of
disease. For an ultrasocial species, such as humans, parasite stress tend to be more xenophobic, have stronger
the problem is more acute, as parasites adapt to take family ties, and have more languages, ethnic groups
advantage of sustained social proximity and inter- and religions. There are a number of possible explan-
action. Individuals have to protect themselves and ations for why this may be the case and confounding
their kin from parasites that have evolved to take factors cannot be ruled out. However, it is clear that,
every transmission opportunity. Appropriate disease- throughout history, in-groups have been able to bolster
avoidance strategies thus include preferring to mix groupishness by labelling members of out-groups as
with insiders (ethnocentrism), avoiding outsiders polluting, dirty, unhygienic, disease-carriers, so justify-
(xenophobia), excluding any individuals that show ing caste and class divisions, cruelty, exploitation,
signs of infection (shunning) or punishing those that pogroms, ethnic cleansing, genocide and war [102].
behave in ways that may threaten others with disease, Such problems persist globally because the old tricks
by displaying poor hygiene, for example. So as not to still work. The powerful continue to exploit our inherent
be punished or excluded, individuals self-police their tendencies to cleave to the in-group in the face of a
own hygiene and social contact behaviour, sometimes disease threat from the outside. Intercommunal violence
turning disgust on themselves (shame). Group norms and discussion of immigration hence peak at election
of hygiene behaviour (manners) may emerge and times [103,104].
groups may agree to cooperate on activities that pro- Because access to social life is so fundamental to our
tect the group as a whole (public health). Because species, we are predisposed to learn not to inflict our
disgust is ‘strong magic’ that recognizes an ability to own infectious emanations on others. We learn ‘good
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Review. Why disgust matters V. Curtis 3485

manners’ early; covering our mouths when we cough disgust reactions from others, facing disdain, sus-
and respecting designated defaecation locations, for picion and sometimes exclusion. Unscrupulous
example [7]. Failures in this department lead to a feeling individuals make political capital from blaming
of shame. Shame also leads those with conditions that and stigmatizing victims and the groups to which
they perceive as possibly infecting and hence repulsive they belong, and the victims often turn blame and
to others to sequester themselves. Acne can cause disgust on themselves.
shame and poor self image [105], and fistula can lead What can be done to prevent or reverse this unhappy
sufferers to remove themselves from the society for cycle? The recent story of the response to the HIV pan-
fear of causing offence [106]. Incontinence sufferers demic holds lessons that give some cause for optimism.
feel humiliated, as one doctor recounted from his own First, irrational fears of contamination were, in early
experience: days, recognized as a factor in the social response to
the disease and the public was educated that victims
To lay in bed, and against all physical rules, and I may were not contagious and did not pose a threat to the gen-
say psychological rules as well, and do what you nor- eral population [113]. Groups that were particularly
mally do at the toilet was a humiliating experience of
affected, such as homosexuals and sex workers, recog-
the helplessness patients feel when help with basic
nized that a process of stigmatization was underway
functions is needed. Why did I never question this
part of caring when I worked as a doctor? For us,
and organized attempts to combat it. They refused
defaecation was only an abstract category in the collective stigma by declaring their individuality, for
patient’s medical record [107]. example through artistic productions such as plays,
films, literature and events [114]. They supported
A common fear among terminally ill people is that of one another to publicly refuse to accept shame and
losing control over their physical functions. Isaksen self-blame. Political activists, patients, academics and
[108] suggests that this fear is based on becoming health professionals worked together to change public
‘dirty’ and hence ‘untouchable’ because of the fears opinion about HIVand AIDS [115]. While the problem
that bodily fluids evoke in others. While the old, the has not been fully solved—those living with HIV
frail, the sick and the disabled, who have to hand still suffer from stigma, exclusion and sometimes vio-
their body care to others, fear the disgust that they lence—the public debate and the political response
may occasion, overcoming revulsion of body products did much to reduce the suffering of the affected and,
is one of the issues faced by carers. When the carer is a beyond this, to raise general awareness of the social
partner, this can put an extreme stress on the relation- effects of infectious disease.
ship [109] and is part of the, often unrecognized,
emotional cost of caring [110].
Like the sick, carers face a double whammy, in 5. MORAL DISGUST
having not just to deal with the products of sickness There are a number of lines of argument that link
but with social stigmatization. Individuals whose disgust to our implicit sense of morality. Antisocial
work involves contact with body products, hair, feet, acts and individuals are often labelled as disgusting
sewage, used clothes, wastes and dead bodies tend to [1], similar physiological and brain activation has been
be poorly rewarded and suffer low status, perhaps observed in moral and biological disgust [9,116] and a
because the nature of the work is perceived to contamin- number of studies have suggested that physiological dis-
ate the individual. Though common throughout the gust can affect moral judgement [117 – 119], though
world, it is in the Hindu caste system where such occu- doubt has been cast on some of these findings [120].
pational pollution is most visible—and damaging— While the link between disgust and morality needs
despite recurrent efforts at reform [111]. Those that further exploration, disgust clearly plays a major and
campaign against abortion, homosexuality and genetic- visceral role in our response to wrongdoing, exploitation
ally modified foods exploit the imagery and language of and injustice. We asked teenagers at one UK school to
disgust and its ability to contaminate; they employ pic- list what they found to be morally disgusting; of several
tures of aborted foetuses, talk of ‘dirty’ sexual practices hundred examples the most common were rape, racism,
and raise the spectre of ‘Frankenfoods’. By labelling the killing, murder, torture, bullying, paedophilia, discrimin-
outsider as dirty and diseased, racists and nationalists ation, necrophilia, genocide, exploitation, incest, theft,
find that they can also, to some extent, recruit morality bestiality and cannibalism. Several authors have made a
to their side [112]. The best defence against such start on unpicking the nature of the relationship
manipulative tactics is first, to understand what is hap- [1,6,121]—is it an exaptation of an ancient system
pening, and second, to expose such strategies to the designed to distance ourselves from parasites, turned to
light of public revulsion. the function of ostracizing social parasites? Is it purely
Although disgust plays a key role in protecting us metaphorical? Or is disgust elicited because many of
from disease, it is also responsible for much human these offences involve bodily fluids? Whatever the expla-
suffering. Our evolved psychological defences against nation, there is no doubt that the emotion of disgust plays
parasites are a double-edged sword. On the one hand, a major role in our decision-making about what is right
they provide the first line of defence against infection and wrong. Nussbaum, for example, describes how the
in social interaction. But at the same time they pre- rhetoric of disgust influences judgement in the legal
vent social interaction, often at a time when it is system. She argues that we should distrust our disgust
most needed. Individuals who are sick or who have responses, because they can lead to prejudice and dis-
become contaminated by association, real or im- crimination [122]. While this may indeed be the case,
agined, find themselves the subject of involuntary Nussbaum fails to acknowledge that disgust also plays a
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3486 V. Curtis Review. Why disgust matters

major part in our ability to distinguish right and disgust is an adaptive system for infectious disease
wrong—an ability which underpins our ability to func- control has yet to be fully taken on board in the
tion in ultrasocial groups. To outlaw disgust in moral brain and behavioural sciences. Evolutionary theory
judgement would be akin to throwing the baby out offers a new means of integration of studies of brain
with the bathwater. As Leon Kass [123] has argued, architecture, neurochemistry and pathology, and of
there is ‘wisdom in repugnance’. Moral disgust is individual, social and cultural behaviour. The theory
one of the major positive forces that builds, maintains base for such work is vital—it provides both concep-
and polices the cooperative societies in which we have tual unity for prediction and a means for interpreting
to live to thrive. Understanding disgust’s part in the results. Theory should also inform the tools of
morality puzzle remains a major task for social scien- such work—if psychological constructs are incorrectly
tists—one that could offer important cues for the conceived of, then the tools that are used to try to
ways in which we make social policy. measure them will fail, giving false or misleading
results. A key priority is the development of
better measures of disgust. An early task for such
6. CONCLUSIONS tools is to use them to explore the relationship between
Disgust is a powerful emotion that plays an under- subtypes of disgust and pathological phobias and
appreciated part in all of our lives, not just in our anxieties.
everyday hygiene habits and in our manners, but in our Further work is needed to elucidate the developmental
response to disease, to social hierarchy, to those who pathways of disgust and to explore how predispositions
are different from ourselves and to immorality. Disgust interact with social norms to create manners, the first
is a double-edged sword that is both the first line of line of defence against interpersonal infection and a
defence against disease, but also a cause of much possible evolutionary precursor of morality. The origins
human suffering. Throughout this paper, I have argued of the human ability to live in ultrasocial groups is one
that it is vital that we shine a spotlight into this less- of the hottest topics in evolutionary biology today
explored darker recess of our psychology. Doing so [127–129]. Disgust provides a key thread that may help
allows us to enhance our abilities at disease prevention, us to unravel this problem.
to deal with many of our commonest anxieties and pho- Disgust studies, however, face the same problem of
bias better and to combat the many prejudices that repulsion that they confront. Olatunji searched the
plague human social relations. It may even help us to published literature and found 10 – 20 times more
understand how to build more cooperative societies. papers per year on anger and fear than on disgust
Understanding disgust matters, both in itself, and for [67], perhaps owing to its lack of attractiveness when
the practical consequences that stem from understand- compared with other emotions. A similar problem
ing. Understanding the function of the brain is possibly afflicts public health. Though diarrhoeal diseases are
the most important intellectual challenge faced by the number two killer of children in the world today,
scientists today. Emotions remain a contested subject they still attract only a fraction of the research funds
in psychology with little agreement as to what they that go to malaria or HIV, for example [16,130].
are, how they should be characterized, how they Lack of sanitation and hygiene are among the biggest
should be studied, even as to how many there are culprits, yet it is hard to attract students to carry out
[124 – 126]. If disgust is an example of an emotion, studies of the faecal –oral transmission of infection,
then the new synthesis suggests that other emotions or on how to meet 40 per cent of the planet’s urgent
should have similar features. They should all have an need for sanitation. A recent review found that men-
adaptive purpose, an ancestral animal history, a set of strual hygiene had been comprehensively ignored in
cues that engage emotive processes and a set of typical health research. Our group is devoting efforts to find-
behaviours, which may or may not be adaptive in the ing ways of making sanitation sexy, setting-up events
current environment [124]. Though they may have such as the ‘Golden Poo Awards’ for example. Artistic
associated feelings, this is not definitive of an emotion. exploration of the disgusting such as the Wellcome
Disgust provides a rich test bed and a prototype for Trust’s season on ‘Dirt’ and the ‘Grossology’ exhibi-
emotion studies. tions that tour the world, help to attract interest and
On the practical side, we have seen that understand- expose disgust to the light of day. Such efforts are
ing disgust has many benefits. Understanding disgust beginning to pay off in terms of increased research
as a disease-avoidance mechanism can help us to funding.
change the behaviours that cause infection and chronic Disgust is a voice in our heads, it is the voice of our
disease. Understanding how disgust tends to err on the ancestors telling us to avoid infectious disease and
‘safe side’ helps to explain why exclusion of the sick, social parasites. The voice of emotion is there for a
the old, the lower caste and the different is still so reason, it guides us to behave in ways that are good
common and shows us that social movements can for our genes, or more precisely, to behave in ways
refuse such prejudice—even labelling it disgusting— that were good for the genes of our ancestors. But
as witnessed by the fact that the kids of today now we no longer live in the environments in which we
find racism and homophobia disgusting. Understand- evolved, and emotion is not the only voice in our
ing how individuals exploit disgust’s ability to heads. We have also evolved an executive brain which
contaminate and spoil in their own quest for power can listen to reasoned argument, weigh outcomes,
can help us to expose such strategies. learn from experience in new environments, and
If understanding is the key to action, then yet more from science, and which can override emotional
understanding is needed. The new synthesis that responses when the long-term benefits may outweigh
Phil. Trans. R. Soc. B (2011)
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Review. Why disgust matters V. Curtis 3487

the short-term gain [124]. Disgust is a vital force in 17 Heymann, D. 2008 Control of communicable diseases
our lives, we need to listen to it, to act on it and some- manual, 19th edn. Washington, DC: American Public
times we need to over-ride it. Above all we need to Health Association.
understand it. 18 Cochran, G. M., Ewald, P. W. & Cochran, K. D. 2000
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Thanks to Mı́cheál de Barra and Robert Aunger for spective. Perspect. Biol. Med. 43, 406–448.
comments on a first draft of this paper and to Josh Tybur 19 Curtis, V. 2007 Dirt, disgust and disease: a natural
and Dick Stevenson for comments on the second draft. history of hygiene. J. Epidemiol. Commun. Health 61,
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