Review and Special Articles
Beyond Toxicity
Human Health and the Natural Environment
Howard Frumkin, MD, DrPH, FACP, FACOEM
Abstract: Research and teaching in environmental health have centered on the hazardous effects of
various environmental exposures, such as toxic chemicals, radiation, and biological and
physical agents. However, some kinds of environmental exposures may have positive health
effects. According to E.O. Wilson’s “biophilia” hypothesis, humans are innately attracted to
other living organisms. Later authors have expanded this concept to suggest that humans
have an innate bond with nature more generally. This implies that certain kinds of contact
with the natural world may benefit health. Evidence supporting this hypothesis is presented
from four aspects of the natural world: animals, plants, landscapes, and wilderness. Finally,
the implications of this hypothesis for a broader agenda for environmental health,
encompassing not only toxic outcomes but also salutary ones, are discussed. This agenda
implies research on a range of potentially healthful environmental exposures, collaboration
among professionals in a range of disciplines from public health to landscape
architecture to city planning, and interventions based on research outcomes.
Medical Subject Headings (MeSH): animals, ecology, environmental health, nature, plants,
trees (Am J Prev Med 2001;20(3):234–240) © 2001 American Journal of Preventive Medicine
A
dvances in the field of environmental health
have taught us much about human health
hazards. We know that air pollution can cause
respiratory disease,1
that heavy metals can cause neu-
rotoxicity,2
and that global climate change is likely to
fuel some infectious diseases.3
Clearly, environmental
exposures can threaten health.
But the natural environment, broadly conceived, can
also enhance health. A well-recognized example is the
many pharmaceuticals that derive from plants and
animals—a compelling argument for preserving biodi-
versity.4–6
But another example is even more intuitive,
both to clinicians and to laypeople. Contact with the
natural world may be directly beneficial to health. If so,
then the field of environmental health needs to extend
beyond toxicity to consider possible health benefits.
This article reviews the evidence for health benefits of
the natural environment, and suggests some of the
research and interventions that such a broader paradigm
of environmental health might imply.
Links Between Health and Environment
Fifty years ago the World Health Organization defined
health as “a state of complete physical, mental, and
social well-being and not merely the absence of disease
or infirmity.” Does contact with the natural environment
contribute to our “complete physical, mental, and
social well-being”?
Many people appreciate a walk in the park, or the
sound of a bird’s song, or the sight of ocean waves
lapping at the seashore. Even if these were only aesthetic
preferences, they would be of interest, since they
are so common as to seem nearly universal. As one
environmental psychologist has written,7
“Nature matters
to people. Big trees and small trees, glistening
water, chirping birds, budding bushes, colorful flowers—these
are important ingredients in a good life.”
But perhaps these are more than aesthetic preferences.
Perhaps we as a species find tranquility in certain
natural environments—a soothing, restorative, and
even a healing sense. If so, contact with nature might be
an important component of well-being.
From an evolutionary perspective, a deep-seated connection
with the natural world would be no surprise.
Primate evolution began at least 65 million years ago,
and the first hominids appeared as much as 5 million
years ago. Homo habilis probably appeared 2 or 3 million
years ago, and our immediate predecessor, Homo erectus,
appeared about 1.5 million years ago. Human history as
we now know it began during the neolithic period just
10,000 or 15,000 years ago, when the last great ice age
From the Department of Environmental and Occupational Health,
Rollins School of Public Health, Emory University, Atlanta, Georgia
Address correspondence and reprint requests to: Howard
Frumkin, MD, Department of Environmental and Occupational
Health, Rollins School of Public Health of Emory University, 1518
Clifton Road, Atlanta, GA 30322. E-mail: medhf@sph.emory.edu.
The full text of this article is available via AJPM Online at
www.elsevier.com/locate/ajpmonline.
234 Am J Prev Med 2001;20(3) 0749-3797/01/$–see front matter
© 2001 American Journal of Preventive Medicine • Published by Elsevier Science Inc. PII S0749-3797(00)00317-2
ended, and global climate and ecology came to resemble
those we know. Our Homo sapiens ancestors began to
form settlements, cultivate crops, domesticate animals,
dig mines, and even make art. If the last 2 million years
of our species’ history were scaled to a single human
lifetime of 70 years, then the first humans would not
have begun settling into villages until 8 months after
the 69th birthday. Some people—aboriginal groups in
Australia, South America, the Pacific Islands, and elsewhere—would
remain hunter-gatherers until a day or
two before the 70th birthday. We have broken with
long-established patterns of living rather late in our life
as a species.
For the great majority of human existence, human
biology has been embedded in the natural environment.
Those who could smell the water, find the plants,
follow the animals, and recognize the safe havens, must
have enjoyed survival advantages. According to biologist
E.O. Wilson,8
“It would...be quite extraordinary to
find that all learning rules related to that world have
been erased in a few thousand years, even in the tiny
minority of peoples who have existed for more than
one or two generations in wholly urban environments.”
Wilson9
hypothesized the existence of biophilia, “the
innately emotional affiliation of human beings to other
living organisms.” Building on this theory, others have
postulated an affinity for nature that goes beyond living
things, to include streams, ocean waves, and wind.10
The human relationship with nature, and
the idea that this might be a component of
good health, have a long history in philosophy,
art, and popular culture, from ancient
Greece to the New England transcendentalists
(e.g., Nash,11
McLuhan,12
Mazel,13
and
Murphy14
). A century ago, the early American
conservationist John Muir15
observed,
“Thousands of tired, nerve-shaken, over-civilized
people are beginning to find out that going to the
mountains is going home; that wilderness is a necessity;
and that mountain parks and reservations are useful
not only as fountains of timber and irrigating rivers, but
as fountains of life.” Is there any evidence to support
this view, and to suggest that contact with nature can
function to enhance health? Evidence is available from
four aspects of the natural world—animals, plants,
landscapes, and wilderness experience.
Domains of Nature Contact
Animals
Animals have always played a prominent part in human
life.16
Today, more people go to zoos each year than to
all professional sporting events.8
A total of 56% of U.S.
households own pets.17
Animals comprise more than
90% of the characters used in language acquisition and
counting in children’s preschool books.18
Numerous
studies establish that household animals are considered
family members; we talk to them as if they were human,
we carry their photographs, we share our bedrooms
with them.19
An estimated 50% of adults and 70% of
adolescents confide in their animals.17
A wide body of evidence links animals with human
health. In a study in a Melbourne cardiovascular disease
risk clinic,20
nearly 6000 patients were divided into
those who owned pets and those who did not. Among
men, the pet owners had statistically significantly lower
systolic blood pressure, cholesterol, and triglycerides
than the non–pet owners. Among women, a similar
trend was observed. These findings did not appear to
be due to differences in exercise levels (say, from dog
walking), diet, social class, or other confounders. In a
1995 study,21
369 survivors of myocardial infarction
were followed for 1 year. Of these, 112 owned pets and
257 did not. The dog owners had a 1-year survival six
times higher than that of the non–dog owners, and this
benefit was not due to physiological differences. (Cat
owners showed no such advantage.)
Investigators in Cambridge, England22
followed 71
adults who had just acquired pets, and compared them
with 26 petless controls, over a 10-month period.
Within a month of acquiring the pet, the pet owners
showed a statistically significant decrease in minor
health problems. In the dog owners (but not the cat
owners) this improvement was sustained for the entire
10 months of observation. In another study,
this one in the United States,23
938 Medicare
enrollees were divided into pet owners and
non–pet owners. The pet owners, especially
the dog owners, had fewer physician visits
than non–pet owners. Moreover, stressful life
events were associated with more doctor visits
among the non–pet owners, but not among
the pet owners, suggesting that owning a pet
helped mediate stress.
The role of animals in helping people handle stress
has been tested specifically. In one study,24
patients
about to undergo oral surgery were randomly assigned
to one of five conditions: a half-hour looking at an
aquarium, with or without hypnosis; a half-hour looking
at a picture of a waterfall, with or without hypnosis; and
a half-hour of sitting quietly. The patients’ comfort and
relaxation during surgery were graded independently
by the oral surgeon, the investigator, and the patients
themselves. The most relaxed patients were those who
looked at the aquarium, irrespective of whether they
had been hypnotized. The patients who looked at the
waterfall picture were almost as relaxed, but only if they
had been hypnotized first. Otherwise, they had low
relaxation scores, as low as those of the control patients.
In another study,25
45 women were exposed to a
stressful stimulus alone, in the presence of a human
friend, and in the presence of their dog. Their autonomic
nervous system responses to stress, such as heart
See
related
Commentary
on pages 241
and 243.
Am J Prev Med 2001;20(3) 235
rate, were measured. The stress response was marked
when subjects were alone, and even more marked when
a friend was present. But having a dog present significantly
reduced the stress response. Animal facilitated
therapy in the treatment of psychiatric conditions is
now well established.26
Evidence such as this supports the conclusion of
animal researchers Alan Beck and N. Marshall Mey-
ers17
: “Preserving the bond between people and their
animals, like encouraging good nutrition and exercise,
appears to be in the best interests of those concerned
with public health.”
Plants
People feel good around plants. In the 1989 National
Gardening Survey of more than 2000 randomly selected
households,27
50.1% of respondents agreed with
the statement, “The flowers and plants at theme parks,
historic sites, golf courses, and restaurants are important
to my enjoyment of visiting there,” and 40.0%
agreed with the statement, “Being around plants makes
me feel calmer and more relaxed.” Among residents of
retirement communities,28
99% indicate that “living
within pleasant landscaped grounds” is either essential
or important, and 95% indicate that windows facing
green, landscaped grounds are either essential or important.
Office employees report that plants make
them feel calmer and more relaxed, and that an office
with plants is a more desirable place to work.29
In urban
settings, gardens and gardening have been linked to
social benefits ranging from improved property values
to greater conviviality (e.g., Patel30
). Psychologist Michael
Perlman31
has written of the psychological power
of trees, as evidenced by mythology, dreams, and selfreported
emotional responses.
Indeed, the concept that plants have a role in mental
health is well established. Horticultural therapy evolved
as a form of mental health treatment, based on the
therapeutic effects of gardening.32
It is also used today
in community-based programs, geriatrics programs,
prisons, developmental disabilities programs, and special
education.33
In prisons, although rigorous evidence
is not available, observers have noted that gardening
has a “strangely soothing effect,” making
“pacifists of potential battlers,”34
and seeming to decrease
the numbers of assaults among prisoners.35
Could contact with plants also contribute to healing
from physical ailments?36
There is a memorable passage
in Oliver Sacks’ 1984 account37
of his recovery
from a serious leg injury. After more than 2 weeks in a
small hospital room with no outside view, and a third
week on a dreary surgical ward, he was finally taken out
to the hospital garden:
This was a great joy—to be out in the air—for I
had not been outside in almost a month. A pure
and intense joy, a blessing, to feel the sun on my
face and the wind in my hair, to hear birds, to see,
touch, and fondle the living plants. Some essential
connection and communion with nature was
re-established after the horrible isolation and
alienation I had known. Some part of me came
alive, when I was taken to the garden, which had
been starved, and died, perhaps without my knowing
it.
Sacks37
credited his garden contact with an important
role in his recovery, and mused that perhaps more
hospitals should have gardens, or even be set in the
countryside or near woods.
Swee-Lian Yi38
was aged 29 when she suffered a
severe stroke, and was hospitalized in New York’s Rusk
Institute for rehabilitation. Like Sacks, she found her
first visit to the hospital greenhouse a turning point. “It
was when I walked through that building, perfectly
quiet, filled with green and growing plants and the
sweet smell of healthy soil that my anxiety began to ebb
away. In its place came a tranquility I had not experienced
since the day of my stroke.”38
In fact, hospitals
have traditionally had gardens as an adjunct to recuperation
and healing, and despite the depredations of
managed care, notable examples survive in many parts
of the country.39
Perhaps this time-honored practice
reflects an ancient recognition that proximity to plants,
like proximity to animals, may in some circumstances
enhance health.
Landscapes
Natural landscapes may have a similar effect. Returning
to an evolutionary perspective, human history probably
began on the African savanna, a region of open grasslands
punctuated by scattered copses of trees and
denser woods near rivers and lakes. If this sounds like
the choicest real estate in most cities and towns, that
may not be a coincidence. As E.O. Wilson9
points out,
“certain key features of the ancient physical habitat
match the choices made by modern human beings
when they have a say in the matter”—a pattern that
repeats in parks, cemeteries, golf courses, and lawns. “It
seems that whenever people are given a free choice,
they move to open tree-studded land on prominences
overlooking water.”
Could evolution have selected for certain landscape
preferences? Perhaps. According to Wilson,10
“A crucial
step in the lives of most organisms, including
humans, is selection of a habitat. If a creature gets into
the right place, everything else is likely to be easier.
Habitat selection depends on the recognition of objects,
sounds, and odors to which the organism responds
as if it understood their significance for future
behavior and success.” For example, many birds use
patterns of tree density and vertical arrangement of
branches as primary settling cues; presumably these
cues are correlated with such crucial information as
236 American Journal of Preventive Medicine, Volume 20, Number 3
food availability, concealment from predators, and
other benefits. For early humans, a place with an open
view would have offered better opportunities to identify
food and shelter and to avoid predators, than a spatially
restricted setting. But not too open a view: Clumps of
trees would offer hiding places in a pinch, and, like
streams and lakes, might also signal the presence of
prey for the hunter.40
Going further, perhaps the
ability to identify relaxing, restorative settings, and the
capacity to recover from fatigue and stress, could also
have been adaptive.40,41
If you can run away from a
saber-toothed tiger, your survival is enhanced. But if,
having run away, you can get to a peaceful place, relax,
and gather your strength, that may further enhance
your survival. Perhaps individuals who chose such settings
gained a survival advantage.40
There is considerable evidence that people’s aesthetic
preferences conform to this scenario. When
offered a variety of landscapes, people react most
positively to savanna-like settings, with moderate to
high depth or openness, relatively smooth or uniformlength
grassy vegetation or ground surfaces, scattered
trees or small groupings of trees, and water.42,43
Notably,
these findings emerge cross-culturally, in studies of
North Americans, Europeans, Asians, and Africans
(e.g., Hull and Revell,44
Purcell et al.,45
and Korpela
and Hartig46
).
This effect may extend beyond aesthetics, to restoration
or stress recovery. Research on recreational activities
has shown that savanna-like settings are associated
with self-reported feelings of “peacefulness,” “tranquility,”
or “relaxation.”40
Viewing such settings leads to
decreased fear and anger, and enhanced positive affect
on the Zuckerman Inventory of Personal Reactions.47
Moreover, viewing nature scenes is associated with
enhanced mental alertness, attention, and cognitive
performance, as measured by tasks such as proofreading
and by formal psychological testing.48–50
The same results emerge from studies that directly
consider conventional health endpoints. In 1981,
Ernest Moore, a University of Michigan architect, took
advantage of a natural experiment at the State Prison of
Southern Michigan, a massive depression-era struc-
ture.51
Half the prisoners occupied cells along the
outside wall, with a window view of rolling farmland
and trees, while the other half occupied cells that faced
the prison courtyard. Assignment to one or the other
kind of cell was random. The prisoners in the inside
cells had a 24% higher frequency of sick-call visits,
compared to those in exterior cells. Moore could not
identify any design feature to explain this difference,
and concluded that the outside view “may provide some
stress reduction.” Like prisoners, employees with views
of nature at work report fewer headaches (as well as less
job pressure and greater job satisfaction) than those
without such a view.52
Similar observations have come from health care
settings. A short 1984 paper in Science 53
bore the
provocative title, “View through a window may influence
recovery from surgery.” Like the Michigan prison
study, this study also took advantage of an inadvertent
architectural experiment. On the surgical floors of a
200-bed suburban Pennsylvania hospital, some rooms
faced a stand of deciduous trees, while others faced a
brown brick wall. Postoperative patients were assigned
essentially randomly to one or the other kind of room.
The records of all cholecystectomy patients over a
10-year interval, restricted to the summer months when
the trees were in foliage, were reviewed. Endpoints
were the length of hospitalization, the need for pain
and anxiety medications, the occurrence of minor
medical complications, and nurses’ notes. Patients with
tree views had statistically significantly shorter hospitalizations
(7.96 days compared to 8.70 days), less need for
pain medications, and fewer negative comments in the
nurses’ notes, compared to patients with brick-wall
views.
Other evidence is available from therapeutic settings.
In a study of dental patients,54
researchers placed a
large mural of an open natural scene on the wall of a
dental waiting room during some days, and removed it
on others. On the days when the mural was visible,
dental patients had lower blood pressure and less
self-reported anxiety than on the days when it was taken
down. In a study of psychiatric in-patients,40
patients
were exposed to two kinds of wall art: nature scenes
such as landscapes, or abstract or symbolic art. Interviews
suggested more positive responses to the nature
scenes. Moreover, in 15 years of records on patient
attacks on the wall art, every attack was on abstract art,
none on a nature scene. (No information was provided
on how many of the psychiatric patients were artists or
art critics.) Viewing landscapes and related nature
scenes, whether genuine or in pictures, seems to have a
salutary effect.
Wilderness Experience
Wilderness experiences—entering the landscape
rather than viewing it—may also be therapeutic. David
Cumes55,56
has described “wilderness rapture,” including
self-awareness; feelings of awe, wonder, and humility;
a sense of comfort in and connection to nature;
increased appreciation of others; and a feeling of
renewal and vigor. These outcomes are often cited in
favorable accounts of so-called wilderness therapy for
psychiatric patients57–60
; emotionally disturbed children
and adolescents61–63
; bereaved people64,65
; rape
and incest survivors66
; and patients with cancer,67
endstage
renal disease,68
post-traumatic distress syndrome
(PTSD),69
addiction disorders,70,71
and other
ailments.72
Most documented examples relate to mental health
endpoints. A group of emotionally disturbed boys aged
Am J Prev Med 2001;20(3) 237
5.5 to 11.5 years attending an outdoor day camp was
compared to a group of similar boys not attending the
camp.73
The campers’ self-ratings and teachers’ ratings
of their emotional adjustment were significantly better
than those of the controls, although neither parents’
ratings nor scores on formal psychological testing
showed an improvement. A group of adolescents being
treated for depression, substance abuse, or adjustment
reactions improved on measures of cooperation and
trust following a wilderness experience, while controls
did not.58
Psychiatric in-patients showed improvements
in coping ability and locus of control following a
wilderness adventure program.59
In-patients at the Oregon
State Mental Hospital showed improved function
and greater probability of discharge following wilderness
adventure programs.57
In a convenience sample of
more than 700 people who had participated in 2- to
4-week wilderness excursions, 90% described “an increased
sense of aliveness, well-being, and energy,” and
90% reported that the experience had helped them
break an addiction (defined broadly, from nicotine to
chocolate).74
While this literature is more extensive than the
literature on plants and animals,75
several limitations
make it difficult to interpret.76,77
Much of the published
research comes from proponents with a personal
or commercial interest in wilderness experiences, such
as companies that market adventures. Much of the
research refers to structured trips or summer camp
programs rather than to the more general phenomenon
of contact with wilderness. To the extent that such
research seems to show benefits, this may be due to the
vacation quality of the experience, to the psychological
value of setting and achieving difficult goals, and/or to
the group bonding that occurs on some such trips,
rather than (or in addition to) a direct effect of
wilderness contact. Few studies have been randomized,
and selection bias can rarely be excluded. Blinding of
subjects has been impossible, and blinding of investigators
has not been attempted.
Despite these limitations, many published accounts
do suggest some benefit from wilderness experiences.
Mental health has been more studied than somatic
conditions, and short-term benefit has been demonstrated
more than long-term benefit.
There is evidence, then, that contact with the natural
world—with animals, plants, landscapes, and wilderness—may
offer health benefits. Perhaps this reflects
ancient learning habits, preferences, and tastes, which
may be echoes of our origins as creatures of the wild.
Satisfying these preferences—taking seriously our affiliation
with the natural world—may be an effective way
to enhance health, not to mention cheaper and freer of
side effects than medications. If so, then medicine and
the other health professions will need to articulate a
broad vision of environmental health, one that
stretches from urban planning to landscape architecture,
from interior design to forestry, from botany to
veterinary medicine.
The Greening of Environmental Health
A paradigm of environmental health that includes
health as well as illness, has implications in at least three
arenas: research, collaboration, and intervention.
Research
Clinical and epidemiologic research in environmental
health addresses many variants of the same question: Is
there an association between exposure and outcome?
We need a research agenda directed not only at exposures
we suspect to be unhealthy, but also at those we
suspect to be healthy, and at outcomes that reflect not
only impaired health, but also enhanced health. If
people have regular contact with flowers or trees, do
they report greater well-being, better sleep, fewer headaches,
reduced joint pain? Do inner city children who
attend a rural summer camp have better health during
the next semester of school than their friends who
spent the summer in the city? Do patients with cancer
or AIDS survive longer, or have fewer infections, or less
pain, or higher T-cell counts, if they have pets? Do
gardens in hospitals speed postoperative recovery? Can
psychotherapy that utilizes contact with nature—
known as ecopsychology78
—have an empirical basis? If
any of these therapeutic approaches shows promise,
which patients will benefit and what kinds of contact
with nature have the greatest efficacy and cost
effectiveness?
Research questions like these pose challenges of
defining and operationalizing unfamiliar variables.
Landscape architects, horticulturists, and environmental
psychologists work with the exposure variables, but
physicians and clinical investigators do not. Similarly,
the outcome variables that reflect health instead of
disease are less familiar, and need to be developed and
validated. These challenges offer broad opportunities
for methods development and hypothesis testing.
Collaboration
Environmental health specialists, from researchers to
clinicians, have long recognized the need to collaborate
with other professionals. We work with mechanical
engineers to build exposure chambers, with chemists to
measure exposures, and with software engineers to
apply geographic information systems to health data. If
we turn our attention to aspects of the environment
that may enhance health, we need to open collaborations
with a broad range of professionals, such as
landscape architects to help identify the salient features
of outdoor “exposures,” interior designers to do the
same in micro-environments, veterinarians and ethologists
to help us understand more about human rela-
238 American Journal of Preventive Medicine, Volume 20, Number 3
tionships with animals, and urban and regional planners
to help link environmental health principles with
large-scale environmental design.
Intervention
Finally, as we learn more about the health benefits of
particular environments, we need to act on these
findings. On the clinical level, this may have implications
for patient care. Perhaps we will advise patients to
take a few days in the country, to spend time gardening,
or to adopt a pet, if clinical evidence offers support for
such measures. Perhaps we will build hospitals in scenic
locations, or plant gardens in rehabilitation centers.
Perhaps the employers and managed care organizations
that pay for health care will come to fund such
interventions, especially if they prove to rival pharmaceuticals
in cost and efficacy.
On the public health level, environmental health has
a long history of providing data, and advocating action
based on these data to achieve control of environmental
hazards, such as more protective air pollution regulations,
lower automobile emissions, safer pesticide
practices, and cleaner rivers and streams. In the same
way, we need to act on emerging evidence of environmental
health benefits. Environmental health could be
a factor in zoning decisions, transportation planning,
and regional development strategies. Environmental
health could appear in the curricula of schools of
architecture and civil engineering. We take for granted
that health experts play a prominent role in the Food
and Drug Administration and the Environmental Protection
Agency, but how about the National Park Service
or the local zoo? As we learn more about the health
benefits of contact with the natural world, we need to
apply this knowledge in ways that directly enhance the
health of the public.
This article was adapted from an Emory University Great
Teachers Lecture delivered on 15 October 1998, and from a
talk given at the Institute of Medicine Roundtable on Environmental
Health Sciences, Research, and Medicine, on 20
June 2000. Partial support came from NIEHS Environmental/Occupational
Medicine Academic Award ES00257.
Thanks to Beryl Cowan, Bill Harlan, Howard Hu, Dick
Jackson, and Melissa Walker for valuable comments.
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