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PERSPECTIVES

SCIENCE AND SOCIETY

Complementary or alternative medicine


in cancer caremyths and realities
Gary Deng and Barrie Cassileth
Abstract | Complementary therapies are adjuncts to mainstream care, used primarily
for symptom control and to enhance physical and emotional strength during and after
mainstream cancer treatment. These therapies are rational, noninvasive and evidencebased that have been subjected to study to determine their value, document the
problems they aim to ameliorate and define the circumstances under which they are
beneficial. By contrast, alternative therapies are generally promoted as suchfor
use as actual antitumour treatments. Typically they lack biological plausibility and
scientific evidence of safety and efficacy, and many are outright fraudulent. Combining
the helpful complementary therapies with mainstream oncology care to address
patients physical, psychological and spiritual needs constitutes the practice of
integrative oncology. By providing patients nonpharmacological treatment modalities
that reduce symptom burden and improve quality of life, physicians enable patients
to have an active role in their care, which in turn improves the physicianpatient
relationship, the quality of cancer care and the well-being of patients and their families.
Deng, G. & Cassileth, B. Nat. Rev. Clin. Oncol. 10, 656664 (2013); published online 30 July 2013;
doi:10.1038/nrclinonc.2013.125

Introduction
Imagine this scene: the oncologist concludes
an outline of an adjuvant treatment plan to
a patient who has recently been diagnosed
with stage III breast cancer. The patient asks,
Should I be on an alkaline diet? Iheard
that alkalizing the body kills cancer cells.
Ive also heard that sugar feeds cancer.
Should I avoid sugar? How about graviola,
a herb from the Amazon that is supposed to
cure cancer? Can I get acupuncture during
chemotherapy to reduce side effects? This
not-uncommon scenario brings to mind
pressing questions. What are these therapies
and remedies that are not traditionally part
of Western mainstream medical care? How
do we, as oncologists, respond to questions
about nontraditional therapies?
Data on the use of adjunctive complementary therapies for symptom control is
often confused by the use of the convenient
acronym CAMcomplementary and
alternative medicinein publications that
fail to distinguish between alternative and
complementary modalities. The acronym
Competing interests
The authors declare no competing interests.

656 | NOVEMBER 2013 | VOLUME 10

is inherently imprecise. Some therapies,


such as vitamins, are part of mainstream
medical care when prescribed to patients
with vitamin deficiencies or taken in
appropriate amounts to maintain general
health. However, vitamins are alternatives
when used in megadoses as a treatment for
cancer, sometimes in lieu of mainstream
care. Similarly, prayer for health might be a
useful aid during mainstream cancer care in
some regions of the world for some patients,
but can be selected as a cancer treatment
in others. Thus, the terminology and its
varying interpretations interfere with
accurate reporting and hinder the accurate
understanding of survey data.
The interest in therapies outside of mainstream oncology care is not limited geographically or among particular segments
of the population. In countries in which
modern medicine predominates, 4050%
of patients with cancer use CAM therapies
outside the mainstream.16 Among cancer
survivors in the USA, up to 40% used complementary or alternative therapies during
the period following their treatment.7 The
2007 National Health Interview Survey
showed that four in 10 adults (38.3% of

adults; 83 million individuals) and one in


nine children <18years of age (11.8% of
children; 8.5 million individuals) in the
USA used dietary supplements and various
mindbody therapy techniques.8,9
Largely because the CAM terminology is an admixture of unrelatedoften
mutually contradictoryconcepts, the
term has become outdated and is no longer
in common use. As accurately stated in a
recent publication: the term integrative
medicine is fast replacing that of complementary and alternative medicine, or
CAM.10 Another publication sums up the
terminology problem well: this controversial term should be changed, since the
words complementary and alternative
have different meanings and should not
be connected by and.11 Complementary
therapies are those used to complement or
used alongside conventional methods of
therapy, whereas alternative methods refer
to those that are used instead of known conventional therapies. Accordingly, the term
integrative therapies accurately describes
the complementary treatments being used
in medical settings alongside conventional
practices. Centres for integrative medicine
are being established in many academic
medical centres.11 Indeed, the term CAM
is rarely applied in legitimate settings, and
virtually every National Cancer Institute
(NCI)-designated comprehensive cancer
centre in the USA has a programme or
department using the term integrative
medicine. In addition, the US Consortium
of Academic Health Centers for Integrative
Medicine has a membership of 55 esteemed
academic medical centres with medical
schools, all of which have integrative
medicineprogrammes.
In this article, we summarize the data
on helpful complementary therapies and
their appropriate incorporation into cancer
care (integrative oncology), discuss non
viable alternative therapies and examine
the patient interest in these therapies. We
also provide recommendations for how
oncology professionals can manage these
issues in an evidence-based, compassionate fashion that enhances trust and rapport,
strengthens the physicianpatient relationship and improves the quality of life for both
the patient and their caregivers.
www.nature.com/nrclinonc

2013 Macmillan Publishers Limited. All rights reserved

PERSPECTIVES
Complementary approaches
Mindbody therapies
Mindbody modalities focus on inter
actions between the brain, mind, body and
behaviour with the intention of reducing
symptoms and promoting health. Some of
these therapies, such as meditation, relaxation techniques, hypnotherapy, yoga,
TaiChi, music therapy and qigong have
ancient roots; others, more recently developed, include the likes of guided imagery.12
The common goal of mindbody therapies is to reduce the effects of anxiety, fear,
phobia, anger, resentment, depression and
pain on the patient while promoting a sense
of emotional, physical and spiritual wellbeing. Mindbody therapies do not treat
cancerperse.
Numerous clinical trials of variable
quality have been conducted to assess the
benefits of these techniques. For example,
systematic reviews and meta-analyses have
consistently shown that mindbody techniques do reduce anxiety and stress, improve
sleep quality and overall quality of life,
especially when used with other treatments
(such as drugs).1317 Among such therapies,
mindfulness-based stress reduction is the
best studiedan approach that focuses on
developing the patients objective observer
role for emotions, feelings and perceptions
and creating a nonjudgmental mindful state
of conscious awareness. 18 Its meditative
components of body scan, sitting meditation and mindful movement are taught over
a period of weeks.18 By contrast, yoga, Tai
Chi and qigong, which originated in Asia,
are less well studied despite being commonly
used. They combine physical movement,
postures and breath control with meditation. A few small trials (2080patients)
have shown a reduction in anxiety, depression and distress as well as improved emotional well-being in patients with cancer
who practice these techniques, as measured
by standard validatedinstruments.1921
Although mindbody therapies are
generally safe, their effectiveness requires
instructors skilled in conveying appropriate
technique and regular practice by the patient.
These helpful complementary modalities
can be used as part of a multidisciplinary
approach to patient care. Major research
studies are underway to elucidate the
mechanisms by which mental activity exerts
control over physiologicalfunction.2224
Acupuncture
Acupuncture, an ancient technique with
great contemporary interest, involves the

Locating the point

Tapping the needle

Removing the guide tube

Manipulating the needle

Figure 1 | Acupuncture procedures. To insert an acupuncture needle, a | first locate the


acupoint, sterilize the skin and place the acupuncture guide tube (with needle inside) onto the
point, b | tap the needle into the skin, c | remove the guide tube and advance the needle to the
desired depth and d|manipulate the needle manually or by applying heat or electrical current.
Photographs Gary Deng, 2013. Reprintedwith permission.

placement of special needles at certain body


points (acupoints) a few millimetres to a few
centimetres into the skin (Figure1), which
can be followed by manual manipulation
or the application of heat or electric pulses
to the needles.25 Historically, acupuncture
was thought to exert its effect by regulating
the flow of energy (called chi or qi) along
meridians in the body when inserted into
these acupoints. 25 Although anatomical
studies have shown that acupoints tend to
be located over interstitial connective tissue
planes,26 current evidence does not conclusively support the claim that acupuncture
points or meridians are electrically distinguishable.27 However, substantial data
from neuroscientific research suggest that
the effects of acupuncture are mediated via
modulation of nervous system activity.2831
Regulated as medical devices in the USA,
acupuncture needles are sterile, single-use,
filiform, 3236 gauge and 3040mm in
length. A typical treatment session is provided by licensed or certified professionals
and lasts 2040minutes.
Acupuncture is used to treat a wide
variety of ailments, although its efficacy
has been evaluated with rigorous scientific research methodology only in the past
few decades. Clinical trials have shown
that the treatment is safe and effective for
several symptoms experienced by patients
with cancer.32 Indeed, a Cochrane review
of 11 randomized controlled trials (RCTs)
encompassing 1,247 patientsmost using
sham acupuncture as controlsconcluded
that acupuncture reduces chemotherapyinduced nausea and vomiting. 33 The
majority of acupuncture trials have been

NATURE REVIEWS | CLINICAL ONCOLOGY

conducted to determine the efficacy of acupuncture in reducing pain. Recent systematic reviews of RCTs support the analgesic
effects of acupuncture for certain types of
pain (for example, musculoskeletal pain,
osteoarthritis and chronic headache).34,35
Furthermore, acupuncture has shown
benefit in reducing radiation-induced xerostomia,36 but mixed results in reducing hot
flushes experienced by women with breast
cancer.3739 The technique is possibly effective in reducing lymphoedema in women
with breast cancer who had axillary dissection.40 Both a systematic review of 46 RCTs
and a Cochrane review showed that acupuncture seems effective in treating insomnia, although larger, rigorously designed
RCTs are warranted.41 Acupuncture has also
been shown to relieve anxiety in a diverse
patient population.4244
Acupuncture is generally safe when performed by qualified practitioners. After
760,000 treatments in 97,733 patients
receiving acupuncture in Germany, only six
cases of treatment-related serious adverse
events were reported.45 The most common
adverse effects (<5%) included minor bleeding or bruising and pain or unfamiliar sensations at the acupuncture sites. In patients
with cancer, acupuncture should not be
given to those with severe neutropenia or
thrombocytopenia due to their higher risk
of infection or bleeding, or at the site of
primary or metastatic neoplasm.
Acupuncture is not an optimum first-line
treatment for symptom relief. Rather, it can
be considered when standard treatment is
not satisfactory or not tolerated. In patients
with severe chemotherapy-induced nausea,
VOLUME 10 | NOVEMBER 2013 | 657

2013 Macmillan Publishers Limited. All rights reserved

PERSPECTIVES
Complementary approaches
Mindbody therapies
Mindbody modalities focus on inter
actions between the brain, mind, body and
behaviour with the intention of reducing
symptoms and promoting health. Some of
these therapies, such as meditation, relaxation techniques, hypnotherapy, yoga,
TaiChi, music therapy and qigong have
ancient roots; others, more recently developed, include the likes of guided imagery.12
The common goal of mindbody therapies is to reduce the effects of anxiety, fear,
phobia, anger, resentment, depression and
pain on the patient while promoting a sense
of emotional, physical and spiritual wellbeing. Mindbody therapies do not treat
cancerperse.
Numerous clinical trials of variable
quality have been conducted to assess the
benefits of these techniques. For example,
systematic reviews and meta-analyses have
consistently shown that mindbody techniques do reduce anxiety and stress, improve
sleep quality and overall quality of life,
especially when used with other treatments
(such as drugs).1317 Among such therapies,
mindfulness-based stress reduction is the
best studiedan approach that focuses on
developing the patients objective observer
role for emotions, feelings and perceptions
and creating a nonjudgmental mindful state
of conscious awareness. 18 Its meditative
components of body scan, sitting meditation and mindful movement are taught over
a period of weeks.18 By contrast, yoga, Tai
Chi and qigong, which originated in Asia,
are less well studied despite being commonly
used. They combine physical movement,
postures and breath control with meditation. A few small trials (2080patients)
have shown a reduction in anxiety, depression and distress as well as improved emotional well-being in patients with cancer
who practice these techniques, as measured
by standard validatedinstruments.1921
Although mindbody therapies are
generally safe, their effectiveness requires
instructors skilled in conveying appropriate
technique and regular practice by the patient.
These helpful complementary modalities
can be used as part of a multidisciplinary
approach to patient care. Major research
studies are underway to elucidate the
mechanisms by which mental activity exerts
control over physiologicalfunction.2224
Acupuncture
Acupuncture, an ancient technique with
great contemporary interest, involves the

Locating the point

Tapping the needle

Removing the guide tube

Manipulating the needle

Figure 1 | Acupuncture procedures. To insert an acupuncture needle, a | first locate the


acupoint, sterilize the skin and place the acupuncture guide tube (with needle inside) onto the
point, b | tap the needle into the skin, c | remove the guide tube and advance the needle to the
desired depth and d|manipulate the needle manually or by applying heat or electrical current.
Photographs Gary Deng, 2013. Reprintedwith permission.

placement of special needles at certain body


points (acupoints) a few millimetres to a few
centimetres into the skin (Figure1), which
can be followed by manual manipulation
or the application of heat or electric pulses
to the needles.25 Historically, acupuncture
was thought to exert its effect by regulating
the flow of energy (called chi or qi) along
meridians in the body when inserted into
these acupoints. 25 Although anatomical
studies have shown that acupoints tend to
be located over interstitial connective tissue
planes,26 current evidence does not conclusively support the claim that acupuncture
points or meridians are electrically distinguishable.27 However, substantial data
from neuroscientific research suggest that
the effects of acupuncture are mediated via
modulation of nervous system activity.2831
Regulated as medical devices in the USA,
acupuncture needles are sterile, single-use,
filiform, 3236 gauge and 3040mm in
length. A typical treatment session is provided by licensed or certified professionals
and lasts 2040minutes.
Acupuncture is used to treat a wide
variety of ailments, although its efficacy
has been evaluated with rigorous scientific research methodology only in the past
few decades. Clinical trials have shown
that the treatment is safe and effective for
several symptoms experienced by patients
with cancer.32 Indeed, a Cochrane review
of 11 randomized controlled trials (RCTs)
encompassing 1,247 patientsmost using
sham acupuncture as controlsconcluded
that acupuncture reduces chemotherapyinduced nausea and vomiting. 33 The
majority of acupuncture trials have been

NATURE REVIEWS | CLINICAL ONCOLOGY

conducted to determine the efficacy of acupuncture in reducing pain. Recent systematic reviews of RCTs support the analgesic
effects of acupuncture for certain types of
pain (for example, musculoskeletal pain,
osteoarthritis and chronic headache).34,35
Furthermore, acupuncture has shown
benefit in reducing radiation-induced xerostomia,36 but mixed results in reducing hot
flushes experienced by women with breast
cancer.3739 The technique is possibly effective in reducing lymphoedema in women
with breast cancer who had axillary dissection.40 Both a systematic review of 46 RCTs
and a Cochrane review showed that acupuncture seems effective in treating insomnia, although larger, rigorously designed
RCTs are warranted.41 Acupuncture has also
been shown to relieve anxiety in a diverse
patient population.4244
Acupuncture is generally safe when performed by qualified practitioners. After
760,000 treatments in 97,733 patients
receiving acupuncture in Germany, only six
cases of treatment-related serious adverse
events were reported.45 The most common
adverse effects (<5%) included minor bleeding or bruising and pain or unfamiliar sensations at the acupuncture sites. In patients
with cancer, acupuncture should not be
given to those with severe neutropenia or
thrombocytopenia due to their higher risk
of infection or bleeding, or at the site of
primary or metastatic neoplasm.
Acupuncture is not an optimum first-line
treatment for symptom relief. Rather, it can
be considered when standard treatment is
not satisfactory or not tolerated. In patients
with severe chemotherapy-induced nausea,
VOLUME 10 | NOVEMBER 2013 | 657

2013 Macmillan Publishers Limited. All rights reserved

PERSPECTIVES
Box1 | Factors contributing to patients interests in alternative therapies
Poor prognosis and lack of effective treatmentwillingness to try anything
Patient activismwishing to search for nonmainstream treatments perceived as unknown
byoncologists
Patient empowermentfeeling like an active participant in self care
Cultural values and belief systemsbelieving that anything natural is good and synthetic
chemicals are bad
Tradition of using indigenous medical systemsincluding traditional Chinese, Ayurvedic
andLatin American folk medicine
Conspiracy theoriesbelieving that pharmaceutical companies suppress curative natural
products out of profit motive
The internet and search engine technologyproviding quick access to a vast amount of
information and misinformation
Direct-to-patient marketingpromotions by product manufacturers that include attractive
packaging and specious scientific jargon
Viral messagesmedical myths, health tips and cancer cure secrets propagated by friends,
relatives and others; a patients willingness to comply

vomiting, pain, xerostomia or hot flushes


in spite of optimal medical management,
acupuncture can be included as part of a
multimodal management plan. Although
some insurance companies do cover acupuncture treatment provided by qualified
therapists for certain indications, the costeffectiveness of acupuncture remains to
bedetermined.

Manipulative and body-basedpractices


Massage therapy and other manual
te chniquessuch as Swedish massage,
shiatsu, tui na, reflexology, Thai massage,
Ayurvedic massage, lymphatic drainage
and myofascial releaseare provided by
massage therapists, physical therapists and
occupational therapists.46 These practices,
which evolved from various cultures, focus
primarily on the musculoskeletal system and
connective tissues. For example, Swedish
massage, the most commonly practiced
massage therapy in the West, uses five styles
of long, flowing strokeseffleurage (gliding),
petrissage (kneading), tapotement (rhythmic
tapping), friction and vibration/shakingto
manipulate soft tissues.
Most cancer-related clinical trials of
massage therapy focus on Swedish massage
and reflexology (foot massage using specified parts of the sole thought to relate to
bodily organs or locations). Results have
been summarized in two systematic reviews
that incorporate 14 RCTs and 12 RCTs,
respectively, with some overlap. 47,48 The
control interventions used in these trials
include standard of care, attention (where
patients received interpersonal interactions
but not massage therapy) or low-intensity
bodywork, such as light touch. Although
the reviewers indicate that the research
methodology of most trials included in
658 | NOVEMBER 2013 | VOLUME 10

both reviews was poorfor example, small


sample sizes or the lack of any attempt to
control for nonspecific effectsthe data
do support massage therapy as an effective
adjunct in cancer supportive care to reduce
anxiety and pain.47,48
Massage therapy in patients with cancer
must be provided by certified massage
therapists who are also trained in working
with patients with cancer to minimize
risk of injury. For example, only lighttouch massage should be provided to frail
patients. Strong pressure should be avoided
in areas harbouring tumours or metastases,
or to patients with bleeding tendencies.
Cases of serious adverse eventsincluding
cerebrovascular accidents, ureteral stent
displacement, haematoma, nerve damage
and posterior interosseous syndrome
have been reported, usually as a result of
exotic types of massage (such as application of very strong pressure not appropriate for the anatomical location) or massage
delivered by laypeople.49,50 When delivered
appropriately, massage therapy is a valuable,
soothing complementary therapy that aids
symptom control in patients with cancer
and on which many patients rely.

Alternative therapies
Patients might seek alternative therapies for
a variety of reasons (Box1), including frustration with a lack of improvement using
mainstream treatments. In the past, cancer
was considered a dire disease with few effective treatments; accordingly, patients sought
more-effective, gentler treatmentsreal
orimaginary.51
Today, the primary danger of alternative
therapies is that patients delay or forego
altogether effective cancer treatment. For
example, instead of undergoing surgical

resection of an early stage breast cancer, a


patient might opt for an alternative natural
therapy. By the time it becomes apparent to the patient that the therapy has
not controlled the growth of her cancer,
it has metastasized, rendering it incurable. Another risk to patients is that most
alternative therapies are very costly. And,
as these are rarely covered by insurance
schemes, patients must pay out of pocket
for them, often depleting their resources
with the false hope that they are receiving
effective therapy. The subsequent financial havoc creates tremendous distress for
the patient and family. Athird risk is that
these therapies make false promises to
desperate patientsresults that cannot be
delivered, representing an act of deception
and betrayal. As clinicians, we have a moral
obligation to dissuade patients from these
useless therapies.

Miraculous cancer cures


Proponents of alternative therapies claim to
produce amazing results in patients with
cancer who have not responded to conventional therapy. The treatment can be as
simple as a single product from an exotic
source or derived from a breakthrough
discovery decades ago yet suppressed
by mainstream medicine thereafter. For
example, amygdalin (also known as laetrile) is an extract from bitter apricot seeds
that is notdespite its other moniker of
vitaminB17a vitamin. Although clinical
studies have shown a lack of efficacy 52,53 and
a risk of cyanide toxicity,54 some patients
continue to seek and use it. In our own
recent experience, one patient proudly displayed her vitaminB17 pill bottle during a
consultation and claimed that someone told
her it cured his cancer after he had been
toldhe had only months to live. We are
certain other oncologists have been faced
with similar situations.
Another touted miracle cure iscaesium
therapy, in which patients ingest caes
ium chloride (CsCl) to alkalinize the
body. Proponents claim CsCl will kill the
cancer cells because cancer cells perish
in an alkaline, high pH, environment. 55
Unfortunately, ingestion of CsCl can lead
to torsade de pointes, a potentially lethal
cardiac arrhythmia. 56,57 This alternative
treatment can also include an elaborate
regimen of special diets, detoxification techniques and large doses of natural products.
Furthermore, these therapies rely heavily
on testimonials of purported users of the
products; the promotional materials are
www.nature.com/nrclinonc

2013 Macmillan Publishers Limited. All rights reserved

PERSPECTIVES
often laden with specious scientific jargon
that can appeal to laypersons, but their misleading nature is obvious to anyone versed
in cancer biology. Other examples include
oxygen therapy (ingestion or injection of
substance containing hydrogen peroxide
or ozone) and variations of bioelectro
magnetism (subjecting the body to electromagnetic field generated by a device), as are
various energy therapies.58
The parties that stand to profit from these
products use various tactics to circumvent
laws and regulations. They often use carefully
worded statements or testimonials to create
the impression that the products can cure
cancer without literally saying so. Or, they
disassociate themselves from the promoters by engaging in multilevel marketing or
guerrilla marketing schemes. Although the
FDA has investigated numerous unsubstantiated claims and the Federal Communications
Commission (FCC) investigates such false
advertisements, the resources required to
gather evidence and initiate legal actions are
such that they can only prosecute a small
number of violators. Physicians should
educate their patients about why these
therapies should beavoided.

Anticancer diets
A near universal patient question concerns
diet. Often patients are not satisfied with the
usual dietary advice offered by dieticians,
and seek anticancer dietsan approach
that has spawned its own category of
selfhelp books.
Alkaline diets
One example that is frequently cited in this
category is the so-called alkaline or pH diet.
This diet is similar to the concept behind
caesium therapy, that acidity promotes
cancer and cancer cells cannot survive
in an alkaline environment. By drinking
alkaline water, distributed from an expensive device hooked up to a faucet, and eating
alkaline foods, which happen to be mainly
fresh vegetables, fruits, legumes and nuts,
one can ward off cancer, arthritis, obesity
and other diseases. These claims disregard
the fact that the body maintains a tight pH
range and eliminates excess acid or alkaline
to preserve pH balance. Treated water has
little buffering capacity, therefore, drinking
so-called alkaline water will not signifi
cantly affect blood pH levels. Similarly,
glorifying alkaline foods simply translates
to eating food that is healthy, which provides essential nutrients and not an alkaline
environment toxic to cancer cells.

Other anticancer diets


Many other anticancer diets with little
scientific basis circulate among patients,
including the Budwig diet, the Gerson diet,
the raw food diet and many more.58 In addition, detox or mono diets (such as those
relying mainly on vegetable and fruit juice)
can restrict or preclude important food categories that are necessary for a full range
ofnutrition.
A high-fat, low-carbohydrate ketogenic
diet is another popular subject of inquiry.
Animal studies suggest that ketogenic diets
induce excessive oxidative stress and might
enhance the therapeutic effects of radiotherapy.59 Clinical trials are underway to
evaluate their benefits andrisks.6062
When responding to diet-related inquiries, oncologists might find it helpful to
point to the kernels of truth in the market
ing materials for these programmes. The
basic requirements for optimal health are
to consume a variety of wholesome fresh
foods and to reduce the intake of processed
food. None of the radical anticancer diets
that employ restrictive regimens have been
shown to significantly improve survival. As
such, patients adhering to these schemes
run the risk of malnutrition. Optimal
caloric and nutrient intake is very important for patients to be able to withstand
their cancer therapies. Counselling patients
who ask about these diets also provides a
good opportunity to put dietary advice in
the context of an overall healthy lifestyle,
which also includes regular exercise.63 The
potential for physical activity to improve
outcomes,64,65 including benefits to patients
receiving palliative care, 66,67 should be
noted. Many leading cancer facilities have
exercise programmes tailored to the needs
of patients with cancer, with experienced
fitness instructors who routinely work with
patients across a broad range of abilities
anddisabilities.
Sugar and cancer
The notion that sugar feeds cancer is
frequently cited by concerned patients.
Although not entirely without merit
glucose metabolism is an active area of
research in anticancer drug development 68
it is often exaggerated in public perception.
Some patients become paranoid about all
sugar-containing food, regardless of the
amount. Such anxiety by itself is detrimental to the quality of life of patients and
should be avoided. Instead, patients should
be advised to keep things in perspective:
no definitive data have shown that sugar

NATURE REVIEWS | CLINICAL ONCOLOGY

promotes cancer growth. However, excessive intake of refined sugar is unhealthy


for many reasons, especially for its associ
ation with metabolic syndrome, and
should accordingly be minimized. A small
amount of refined sugar is not harmful. To
meet caloric requirements, patients should
consume complex, unrefined carbohydrates
and unsaturated fat (unless they have a
digestive tract condition that precludes
those foods) and avoid large amounts of
foods with added sugar.69

Natural product dietary supplements


The use of supplements is among the most
frequently questioned subjects by patients.
Over-the-counter dietary supplements
available to patients with cancer include
vitamins and trace-element formulations that have well-defined constituents.
Additionally, botanical extracts and herbal
products that often contain complex compositions of many compounds, some of
which are unidentified, are also available. Indeed, botanicals, fungi and marine
organisms (such as sea sponges) are a rich
source of therapeutic compounds that are
used in cancer therapy; chemotherapeutic
agents derived from natural sources
so-called natural products in chemical
jargoninclude the taxanes (paclitaxel is
isolated from the Pacific Yew tree), campto
thecin (isolated from of C.acuminata, the
Chinese happy tree) and its analogues,
vinca alkaloids (isolated from the peri
winkle C.roseus) and numerous microbial
compounds.70 However, decades of research
are needed to ascertain the clinical safety
and efficacy of compounds derived from
natural sources in clinical studies. Natural
products available as dietary supplements are not viable cancer treatments
until their efficacy has been established in
suchstudies.
Patients with cancer often ask about
natural products that have been shown
to have activity against cancer in animal
or invitro studies, but unconfirmed in
clinical trials. Many are readily available as
dietary supplements, and patients can use
them on their own, often without informing their physicians. In addition, patients
might pursue the use of natural products
marketed with buzzwords such as anti
oxidant, immune booster or detox. Acomprehensive list of such supplements has been
reported.71 Patients view these products as
helpful during cancer treatment because of
claims that the products protect good cells
from damage, restore suppressed immune
VOLUME 10 | NOVEMBER 2013 | 659

2013 Macmillan Publishers Limited. All rights reserved

PERSPECTIVES
Table 1 | Commonly asked questions by patients with cancer and example responses
Question, belief or statement

Possible responses

Examples

XYZ was reported to kill cancer


cells in a laboratory
experiment. Should I take it?

What works in the test tube often does not work in


humans because the concentration used in the
laboratory is so high that you could never achieve that
level in the tumour tissue by ingesting the herb.
Many things kill cancer cells in the test tube, but what
kills the cancer cells might also hurt the healthy cells.

Paclitaxel is a drug derived from the yew tree. To get the


equivalent of one dose, you would need to ingest >100lbs of tree
bark. Taking a few capsules of the tree bark will not do anything.
If you add bleach to cancer cells, they will die. However, noone
would drink bleach to treat cancer.

Chemotherapeutic drugs
aretoxins. I want to detoxify
mybody.

Some detox therapies increase the activity of the


enzymes in the liver to remove toxins. These enzymes
can also remove chemotherapy drugs faster, meaning
you are not getting the correct dose needed.

St Johns wort seems to reduce the adverse effects of


chemotherapy, but was later found to also lower the level of the
active metabolite of irinotecan in the blood.77

I have so many adverse effects


from my cancer treatment.
CanI take XYZ to give me more
energy or boost my
immunesystem?

Be carefulsome herbs have their own adverse effects


or can fight against other medications you are taking.

Some energy boosting herbs can raise your heart rate and
blood pressure. Others can make your blood thinner if you are
taking anticoagulants. Some might contain oestrogen-like
substances, which might reduce your hot flushes, but can reduce
the effect of the hormonal therapy you are on. Some herbs
elevate your liver enzymes.

I heard that antioxidants have


anticancer properties. Should I
takethem?

Antioxidants can protect DNA from damage by harmful


elements in the environment, but they will not revert
already-mutated genes back to normal. Antioxidants
might have a role in cancer prevention, but they will
not treat cancer; their effects in cancer prevention
have not been confirmed. A healthy diet is more
important than taking individual supplements.

Initial small studies suggested that vitamin E and selenium might


prevent prostate cancer. Later, a randomized controlled study
with tens of thousands of people showed no cancer preventive
effects and even aharmful effect.78,79

Antioxidants protect the body


from damage caused by
chemotherapy and radiotherapy.

For antioxidants to protect from chemotherapy and


radiotherapy the antioxidants would need to
distinguish between normal cells and cancer cells,
otherwise they would protect the cancer cells as well.

High-dose antioxidants given during radiotherapy have been


shown to reduce adverse effects during treatment, but also might
have made the cancer more likely to recur.104

function or remove toxins left behind by


cancer treatment. Some of these agents
might hold promise in cancer prevention or treatment; for example, early phase
clinic al trials of polyphenols extracted
from green tea have demonstrated benefit
in the treatment of chronic lymphocytic
leukaemia (CLL) 72 and in the chemo
prevention of breast cancer.73 Similarly,
docosahexanoic acid (DHA, an 3-fatty
acid) has demonstrated positive results in
breast cancer prevention74 and treatment,75
as has curcumin in slowing progression
from monoclonal gammopathy of undeter
mined significance (MGUS) to multiple
myeloma.76 Nonetheless, the majority of
the available supplements has not shown a
reasonable possibility of meaningful clinical benefits when ingested orally. Many also
carry the risk of interacting with prescription medicines or have their own detri
mental effects. 7780 For example, several
herbs possess oestrogen-like activity, the
intake of which is not advisable for women
with oestrogen-receptor-positive cancers.81
Other supplements can alter drug metabolism, such as St Johns wort, leading to serum
drug levels higher or lower than intended.82
Misconceptions held by patients after
reading news reports or marketing materials
need to be invalidated in a language patients
can understand(Table1).
660 | NOVEMBER 2013 | VOLUME 10

Patient characteristics
Surveys indicate that patients with cancer
who use complementary or alternative
approaches tend to be female as well as
younger, better educated and more affluent than those who do not, representing a
health-conscious segment of the population
that is proactive in its health care, that seeks
health information and that has the means
to pay for services not typically covered by
insurance or public health schemes.16 Given
the increased sophistication of patients and
physicians in recent years, patients and their
oncologists increasingly pursue discussions
of integrative oncology, alert to the fact that
incorporating complementary (adjunctive)
therapies into mainstream cancer treatment
can decrease symptoms and improve overall
quality of life. Furthermore, such discussions facilitate patients in having an active
role in theircare.83
Patients acquire information about
complementary approaches primarily from
friends (65%), family (48%) and the media
(21%),1,84 with additional informationas
well as misinformationbeing delivered
via the internet and social networks.85 The
general interest in complementary modalities has increased in recent decades because
of increasing supportive data on the value of
complementary therapies, as well as growing
professional and patient acceptance of the

modalities used. Additionally, the emphasis


on wellness and survivorship, which incorporates managing long-term adverse effects
from cancer treatment and reducing risk of
cancer recurrence, has enhanced general
interest in complementary modalities.

Impediments to communication
Optimal cancer care demands dealing with
issues that are important to patients, including those that are likely to be detrimental if
left unaddressed. Proper dialogue about the
use and application of therapies is important.
The majority of patients want to discuss the
topic with their oncologists given the opportunity, yet nondisclosure remains a problem,
in part because the opportunity fails to
arise. 86 Additionally, patients have also
reported being fearful of physician disappro
val or disinterest in what they do outside of
conventional treatment, or assume that such
information is not important or relevant to
their cancer treatment.87,88 By contrast, physi
cians believe that patient nondisclosure is
attributable to patient fears of physician
disapproval or lack of understanding.89 As
the prevalence of complementary therapy
use is high, initiating a discussion provides
an excellent opportunity for the physician
to demonstrate compassion, understanding and humanity, in addition to providing
highquality care based on scientific data.
www.nature.com/nrclinonc

2013 Macmillan Publishers Limited. All rights reserved

PERSPECTIVES
Dilemmas for clinicians
Although most patients use natural products
(supplements) hoping to reduce the adverse
effects of conventional treatment, support
the body through cancer treatment or
prevent cancer recurrence, other patients
with few or no effective treatment options
might want to try anything. This desperation can lead the patient to use natural
products that have shown some possible
anticancer activity in early preliminary
studies. Although the chances of efficacy
might be extremely remote, these patients
might come to the clinic with information
about the benefits of various elaborate,
socalled anticancer regimens.
One example is the Bill Peeples cocktail,
which is often asked about by patients with
advanced-stage sarcoma.90 This product
contains more than a dozen dietary sup
plemental ingredients that the manufacturer
claims have antiangiogenic or antioxidant
properties based on laboratory studies,
plus a few prescription medicines used offlabel. Such a scenario presents a dilemma
for the oncologist faced with a patient for
whom there is no effective treatment or an
appropriate clinical trial. How do we provide
compassionate care while safeguarding our
patients best interests?
We believe that the answer lies in meeting
patients where they are. We can affirm their
perseverance not to give up, and tolerate
their use of agents that are generally safe
and have shown some preliminary evidence
of anticancer activity. At the same time, we
also need to help the patient work towards
accepting whatever outcome he or she will
eventually face, despite their best efforts
and those of the treating physicians and
caregivers. Palliative care often begins too
late in clinical practice.91 Instead, patients
options, goals and preferences should be
assessed early in the course of cancer treatment. Personalized care of patients with
advanced-stage cancer should be tailored
to the diverse physical, psychological,
social and spiritual consequences of cancer
for the individual.92 Using complementary
or alternative therapies might help patients
feel content that they have explored every
possible option, help them to accept the
futility of further treatment and facilitate
closure. Accordingly, the treating oncologist must take a compassionate approach
in accepting these decisions by the patient.
Similarly, an effort must be made to minimize the physical, emotional and financial burdens experienced by the patient,
discuss and closely monitor adverse

re actions and prepare the patient and


family for endoflife issues.

Open the conversation by acknowledging


the patients interest in complementary
or alternative therapies

Integrative oncology programmes


Combining helpful complementary therapies with mainstream cancer care to reduce
symptoms and improve quality of life constitutes the practice of integrative oncology.
Many, if not most, cancer centres have established integrative oncology departments or
programmes to provide complementary
therapies and to counsel patients about
potentially problematic dietary supplements
and alternative therapies. Counselling by
trained and experienced physicians should
include guiding patients away from potentially harmful therapies and addressing
their underlying psychosocial or cultural
needs. 93,94 Referring patients to qualified specialists, therapists, counsellors or
instructors connects these individuals to
appropriate sources of facts and sound
advice. These qualified personnel can serve
as valuable resources for future questions, to
provide support for patients efforts, and to
divert energy away from useless and potentially harmful or expensive approaches.
Furthermore, as patients gain information about additional symptom management techniques, they experience positive
interactions with their physicians, improve
self-care skills and enhance their physical,
emotional and overall well-being.95,96
A structured approach to discussing the
use of complementary or alternative medicine with patients in general was described
in 1997 and updated in 2002.97,98 Although
written for use in the primary care or internal medicine settings, this approach might
be helpful in the oncology setting as well.
Asimilar report focused on discussing complementary or alternative medicine with
patients in the oncology care setting.93 In
2010, a set of comprehensive communication guidelines was proposed on the basis of
a systematic literature review of methods for
the discussion of complementary modalities for oncologists.94 Together, these works
provided a framework for counselling
patients with cancer on complementary or
alternative therapies.
At Memorial SloanKettering Cancer
Center, each new patient receives an information packet that reminds them to discuss
any self-prescribed supplements or medications with their physicians. All patients are
asked at each visit to disclose any herbs
and other dietary supplements they are
taking. Patients who raise questions about
complementary or alternative therapies

NATURE REVIEWS | CLINICAL ONCOLOGY

State the physicians role of working together


with the patient to achieve the best outcome

Provide ample opportunity for patients


to voice any questions or concerns

Explore the underlying reasons for the


questions and concerns, including
the psychosocial and cultural context
Analyse the patients questions and concerns,
and present evaluations in a fashion most
effective for that particular patient

Explain why some therapies are either


without scientific merit or are potentially harmful
Introduce the broader concept of integrative
medicinean approach to health that
promotes well-being of the body, mind and spirit
Offer a comprehensive life-style assessment
and recommend changes

Discuss specific therapies, both mainstream


and complementary, that are appropriate for the
patients clinical concerns, taking into
consideration that patients situation and needs

Summarize the key points of the conversation

Confirm the patients understanding and that


all questions have been answered satisfactorily

Document the encounter and make the


documentation available to the patients
primary physician
Arrange follow-up visits to monitor adverse
reactions and response to treatment

Adjust the treatment plan as required

Figure 2 | Steps in advising patients who are


interested in complementary and alternative
therapies.

that require discussionand those who are


on supplements at risk of interacting with
prescription medicinesare referred to the
Integrative Medicine Service for comprehensive counselling. During the counselling
(Figure2), physicians well versed in both
oncology and integrative medicine make a
comprehensive assessment of the patients
needs and address the issues from both
the overall cancer care perspective and the
patient-specific perspective.
VOLUME 10 | NOVEMBER 2013 | 661

2013 Macmillan Publishers Limited. All rights reserved

PERSPECTIVES
Box2 | Reputable resources on complementary medicine
American Cancer Society. Guidelines for Using Complementary and Alternative Methods
(http://www.cancer.org/Treatment/TreatmentsandSideEffects/Complementary
andAlternativeMedicine/guidelines-for-using-complementary-and-alternative-methods)
Medline Plus. Herbs and Supplements (http://www.nlm.nih.gov/medlineplus/druginfo/
herb_All.html)
Memorial SloanKettering Cancer Center. About Herbs, Botanicals & Other Products (http://
www.mskcc.org/aboutherbs)
Memorial SloanKettering Cancer Center. Integrative Medicine (http://www.MSKCC.org/
IntegrativeMedicine)
National Cancer Institute. Topics in Complementary and Alternative Therapies (PDQ;http://
www.cancer.gov/cancertopics/pdq/cam/topics-in-cam/healthprofessional)
National Center for Complementary and Alternative Medicine (NCCAM). Cancer and
Complementary Health Practices (http://nccam.nih.gov/health/cancer/camcancer.htm)
NCCAM. Time to Talk: Ask Your Patients About Their Use of Complementary Health Practices
(http://nccam.nih.gov/timetotalk/forphysicians.htm)
NIH Office of Dietary Supplements. Dietary Supplement Fact Sheets (http://ods.od.nih.gov)
Society for Integrative Oncology (http://www.integrativeonc.org)
US Pharmacopeial Convention. USP Dietary Supplement Standards (http://www.usp.org/
dietary-supplements/overview)
Abrams, D. & Weil, A. Integrative Oncology (Weil Integrative Medicine Library, Oxford University
Press 2009)
Cassileth, B.R. The Complete Guide to Complementary Therapies in Cancer Care: Essential
Information for Patients, Survivors and Health Professionals (World Scientific Publishing, 2011)
Ernst, E., Pittler, M. H. & Wider, B. (eds) The Desktop Guide to Complementary and
Alternative Medicine: An Evidence-Based Approach, 2e (Mosby, 2006)

Practice models of integrative oncology


vary according to the patient demographics
and the societal environment of the medical
facility. The integration is not always easy
and can be hampered by a lack of awareness or perceived importance by oncologists, a lack of properly trained physicians
knowledgeable in both cancer medicine
and complementary therapies, a lack of
trust between physicians and complementary therapies practitioners who are
not medical doctors or insufficient funds.
An investigation of six integrative onco
logy programmes across four continents
identified several essential elements for
a successful programme: location within
the oncology department area, oncologist
referral to consultation with integrative
oncologist, sufficient time for integrative
oncologistoncologist communic ation,
integrative practice that is evidence based,
professional complementary medicine practitioners and coverage of the cost for the
integrative oncology service.99
For busy oncologists, staying abreast of
new complementary medicine research
results and of the ever-expanding world
of alternatives to mainstream cancer treatment is difficult. However, many excellent continuing education materials are
available from reputable sources (Box2).
In addition, the knowledge and expertise
available from integrative oncology colleagues can be extremely helpful, especially
662 | NOVEMBER 2013 | VOLUME 10

those dual-trained in mainstream onco


logy and integrative medicine. Nationallevel and international-level efforts can
provide helpful information to practi
cing oncologists. A multidisciplinary
nonprofit organizationthe Society for
Integrative Oncologywas formed by
clinicians, researchers and patient advocates to provide a platform for the advancement of evidence-based, comprehensive,
integrative healthcare to improve the lives
of people affected by cancer.100 Using the
standard methodology for development
of a practice guideline, which consists of
systematic review of current literature and
multiple rounds of peer reviews the group
evaluated the strength of the evidence
for common complementary therapies,
as well as any potential risks or burdens.
The resulting recomm endations were
graded, peer-reviewed and adapted by the
American College of Chest Physicians101,102
and the Society for Integrative Oncology.103
These guidelines represent an initial effort
in giving clinicians who might not be
familiar with complementary therapies
evidence-based assessments of the therapies, and when and how to incorporate
them into the care of patients with cancer.
With time, these national and international
efforts in raising the awareness of integrative oncology and its application in clinical care would improve the overall care of
cancerpatients.

Conclusions
Complementary or alternative medicine are
topics that patients with cancer are highly
interested in and also find quite confusing. Safe and beneficial complementary
therapies should be integrated into regular
cancer care to improve patient quality of life
and outcome. However, patients should be
steered away from alternative cancer thera
pies that are risky and do not have clinical value. Integrative oncology combines
complementary therapies with mainstream
care, trying to optimize the patients physical, psychological and spiritual well-being,
taking into consideration the individuals
values and priorities in life. A robust integrative oncology programme should be part of
any high-quality cancer care institution, as
is the case for virtually all NCI-designated
comprehensive cancer centres. By understanding and addressing issues our patients
feel are important, compassionate care can
be tailored to each patient, and oncology will
reach the noble goal of treating each patient
as a person with cancer, rather than treating
only the cancer in a patient.
Integrative Medicine Service, Memorial
SloanKettering Cancer Center, 1429 First
Avenue, New York, NY 10021, USA (G. Deng,
B.Cassileth).
Correspondence to: G. Deng
dengg@mskcc.org
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Acknowledgements
The authors would like to thank Ingrid Haviland for
her valuable expert editorial assistance in the
preparation of this manuscript.
Author contributions
Both authors researched the data for the article,
contributed to the discussion of its content, wrote
the manuscript and edited it before submission.

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