Integrative oncology: Addressing the global challenges of cancer prevention and treatment
DISCLOSURES: Jun J. Mao and Memorial Sloan Kettering Cancer Center (MSK) staff are supported in part by an MSK National Institutes of Health/National Cancer Institute Cancer Center grant (P30 CA008748) and by the Herbal Education and Research in Oncology Program made possible by the Laurance S. Rockefeller Foundation. Jun J. Mao reports research funding provided to MSK from Tibet Cheezheng Tibetan Medicine Company, Ltd. Lorenzo Cohen receives royalties from the book, Anticancer Living: Transform Your Life and Health With the Mix of Six. All remaining authors report no conflicts of interest.
Where authors are identified as personnel of the International Agency for Research on Cancer/World Health Organization, the authors alone are responsible for the views expressed in this article, and they do not necessarily represent the decisions, policy, or views of the International Agency for Research on Cancer/World Health Organization.
We recognize the input and advice provided for this article by Dr. Jeffrey D. White, Director of the Office of Cancer Complementary and Alternative Medicine (OCCAM) at the National Cancer Institute/National Institutes of Health (NCI-NIH). We thank Dr. Satish Gopal, Director of NCI's Center for Global Health (CGH) and the staff from CGH for their contributions to the Trans–NCI-NIH International Conference on Integrative Oncology. Special thanks to Dr. Robert (Bob) Croyle and Ms. Stacey Vandor from NCI's Division of Cancer Control and Population Sciences (DCCPS) for their support and assistance with the coordination of the conference. We extend thanks to members of the Conference Planning Committee: Jeff White, OCCAM-Division of Cancer Treatment and Diagnosis (DCTD); Avraham Rasooly, OCCAM-DCTD; Miguel Ossandon, Cancer Diagnosis Program (CDP)-DCTD; Linda Zane, CDP-DCTD; Paige Green, DCCPS; Libin Jia, OCCAM-DCTD; Oluwadamilola Olaku, OCCAM-DCTD; Paul Jacobsen, DCPPS; Marya Levintova, NIH's Fogarty International Center; and Emmeline Edwards and Della White, NIH's Center for Complementary and Integrative Health.
We thank Jasmine Douglas for her assistance collecting the initial input from all authors. We also thank Colleen Smith, Krupali Desai, and Ingrid Haviland from the Integrative Medicine Service at Memorial Sloan Kettering Cancer Center for their editorial assistance and coordination of this article.
Abstract
The increase in cancer incidence and mortality is challenging current cancer care delivery globally, disproportionally affecting low- and middle-income countries (LMICs) when it comes to receiving evidence-based cancer prevention, treatment, and palliative and survivorship care. Patients in LMICs often rely on traditional, complementary, and integrative medicine (TCIM) that is more familiar, less costly, and widely available. However, spheres of influence and tensions between conventional medicine and TCIM can further disrupt efforts in evidence-based cancer care. Integrative oncology provides a framework to research and integrate safe, effective TCIM alongside conventional cancer treatment and can help bridge health care gaps in delivering evidence-informed, patient-centered care. This growing field uses lifestyle modifications, mind and body therapies (eg, acupuncture, massage, meditation, and yoga), and natural products to improve symptom management and quality of life among patients with cancer. On the basis of this review of the global challenges of cancer control and the current status of integrative oncology, the authors recommend: 1) educating and integrating TCIM providers into the cancer control workforce to promote risk reduction and culturally salient healthy life styles; 2) developing and testing TCIM interventions to address cancer symptoms or treatment-related adverse effects (eg, pain, insomnia, fatigue); and 3) disseminating and implementing evidence-based TCIM interventions as part of comprehensive palliative and survivorship care so patients from all cultures can live with or beyond cancer with respect, dignity, and vitality. With conventional medicine and TCIM united under a cohesive framework, integrative oncology may provide citizens of the world with access to safe, effective, evidence-informed, and culturally sensitive cancer care.
Introduction
Cancer is a global health challenge that knows no boundary. Over the next 2 decades, the number of new cancer cases is expected to rise approximately 50% worldwide.1 Many obstacles stand in the way of successful global cancer care, particularly in low- and middle-income countries (LMICs). In these regions, access to quality affordable care, including cancer screening facilities, trained medical professionals, availability of conventional treatment (such as surgery, chemotherapy, and radiation therapy), and supportive care services, can be extremely limited.2
Patients have been using culturally salient, lower cost traditional medicine practices, such as acupuncture, yoga, meditation, and herbal medicine, along their cancer journeys. Collectively, these modalities are classified as part of complementary and alternative medicine (CAM) in the West.3 Since 2002, the traditional medicine strategy of the World Health Organization (WHO) has encouraged and strengthened the insertion, recognition, and use of traditional, complementary, and integrative medicines (TCIMs) in national health systems at all levels: primary health care, specialized care, and hospital care.4 Therefore, we use the term TCIM in this article to refer to these practices.
Although TCIM is widely used among populations in high-income countries (HICs)5 as an adjunct to conventional medicine, TCIM may be considered primary health care in LMICs such as Chile, Brazil, and rural India.6-8 With economic development and international engagement, growing numbers of LMICs have initiated efforts to provide conventional cancer screening, treatment, and supportive care. Despite the increased use of both TCIM and conventional medicine globally, tension and conflicts between these approaches exist, and systematic integration remains extremely limited. It is precisely for this reason that the growing field of integrative oncology can contribute solutions for patients, families, and practitioners to navigate between the 2 health care paradigms. The Society for Integrative Oncology (SIO) defines this field as a patient-centered, evidence-informed approach to cancer care that uses lifestyle modifications, mind and body therapies, and natural products from different traditions in tandem with conventional cancer treatments.9 Integrative oncology offers both a bridge and path forward to help deliver culturally sensitive, high-quality care in LMICs.
In October 2020, over 700 participants virtually joined global leaders, researchers, and scholars to learn more about the opportunities and challenges of integrative oncology at the Trans–National Cancer Institute (NCI)-National Institutes of Health (NIH) Conference, International Perspectives on Integrative Medicine for Cancer Prevention and Cancer Patient Management. In this review, we have drawn upon the meeting procedures and summarized the key themes that emerged from the presentations and discussions on global integrative oncology, with a particular focus on LMICs. In addition, we performed a scoping review of current clinical guidelines that included integrative oncology treatments. Furthermore, selected conference presenters and moderators formulated recommendations based on the meeting summary. This review includes 6 sections: 1) a synthesis of the global cancer burden and cancer control challenges; 2) a review of the conceptual challenges between TCIM and conventional medicine in cancer care and examples in specific regions, eg, Latin America, Africa, and Asia (China and India); 3) the current evidence base for integrative oncology; 4) research challenges and opportunities in integrative oncology; 5) examples of global integrative oncology research collaborations to increase the evidence base; and 6) the formulation of policy, research, and practice recommendations to advance the global impact of integrative oncology.
Global Cancer Burden
Human and Societal Costs of Cancer
Over 19 million people around the world were diagnosed with cancer and almost 10 million died from cancer in 2020.10 By 2040, new case and death totals are expected to reach approximately 28 million and 16 million, respectively.11, 12 Cancer treatment alone costs the world approximately US$1.2 trillion annually—nearly 2% of the global gross domestic product in 2019.13 LMICs account for 80% of the global cancer burden; yet, with only 5% of the global spending to combat this disease, LMICs will continue to fall behind in efforts to provide quality cancer care to their citizens.14 Furthermore these countries will not remain aligned to achieve the WHO Sustainable Development Goal Target 3.414 for the year 2030, which aims to reduce by one-third premature mortality from noncommunicable diseases, including cancer, compared with rates from 2015.15 Countries with a low human development index (a summary measure of key dimensions affected by sustainability and equity) experience significantly higher premature mortality because of delayed diagnosis and access to therapeutic services as well as limited availability of quality treatment.16 Furthermore, a constellation of dynamics surrounding issues, such as lack of infrastructure, health policies, properly trained professionals to perform evidence-based screening and treatment, trust in providers, and continuity of care across services, underlies and exacerbates these global challenges in cancer care delivery (Fig. 1). For example, premature deaths from noncommunicable diseases that could be prevented through effective policies and public health interventions have increased nearly 50% over a few decades, from 23 million deaths in 1990 to over 34 million deaths in 2017, with one-third of those being cancer-related.17
Growing Inequality in Cancer Prevention
Suboptimal implementation of highly effective cancer prevention strategies, such as tobacco-control interventions and vaccination against hepatitis B virus (HBV) and human papillomavirus (HPV) in LMICs, has widened global cancer inequality. More than 80% of global smokers live in LMICs,18 and many of these countries have not satisfactorily enforced the 6 evidence-based measures identified by the WHO Framework Convention on Tobacco Control.19 Although the current prevalence of tobacco use is comparatively low in Africa, concerns have been expressed about the impact of lifestyle changes, weak tobacco-control measures, and intensified marketing by tobacco companies. A significant increase in smoking prevalence among men has already been documented in some African countries like Congo.20 Infection-related cancers constitute disproportionally high rates in LMICs where effective prevention and treatment strategies exist. Chronic HBV infection was responsible for 55% of the hepatocellular cancers occurring in 2018.21 Coverage of the birth dose of HBV vaccine is <40% globally, with huge disparities across countries.22 Only 40% of Asian countries and 31% of African countries have introduced HPV vaccination programs as of 2020, although the majority of the global cervical cancer burden is shared by these countries.23
Western Lifestyle Contributes to Growing Cancer Incidence
LMICs face additional challenges in responding to the rise of cancer incidence and premature death caused by undesirable lifestyle trends. Cancer incidence changes when people from Asia or Africa migrate to Western countries. Immigrants experience increased obesity and a spike in Western lifestyle-associated diseases, including cancer incidence rates higher than those observed in their home countries. Several epidemiological studies found that immigrant cancer rates can match those of their newfound home in as quickly as one generation for Africans and South Asians.24-26
In addition, cancer incidence trends in those LMICs that have experienced recent economic development are starting to mirror the trends in Western countries.27 Whereas breast cancer rates used to be low in China, India, and Brazil, metropolitan areas of these countries now have rates similar to the West because of changes in lifestyles as well as delays in pregnancy and changes in breast-feeding practices.28-30 Highly processed fast-food diets are common Western exports to LMICs, and obesity rates are increasing alongside Western diseases. In Brazil, for example, almost one-half of people who, in the recent past, were underweight and struggling to consume sufficient calories because of poverty are now overweight, which is linked to physical inactivity and an increased consumption of fast and processed foods that are low in nutrition.31
Limited Access to Cancer Treatment
It is well established that lack of resources and fragmented care contribute to global cancer treatment disparities. Despite the rapid development of novel cancer therapies like targeted treatment and immunotherapies in HICs, these treatments are not available to the majority of the population in LMICs. Furthermore, access to older and effective cancer treatment remains extremely limited in the majority of regions in Africa, rural Asia, and rural Latin America.32 The median density of radiotherapy machines per million population in 2020 was virtually nonexistent at only 0.0 (range, 0.0-0.4) in low-income countries compared with 5.1 (range, 0.4-11.6) in HICs.33
A recent Lancet Oncology article reported a 25-times difference between LMICs and HICs (3.5% vs 87%) in 5-year survival among women diagnosed with breast cancer. Those authors further estimated that, by implementing a conventional package of screening and treatment (imaging, surgery, radiation, and medical oncology), improving the quality of care delivery can improve survival from 3.5% to 55.3% in LMICs.34 Inadequate health care coverage systems can also lead to limitations in cancer treatment.35 Patients in LMICs often cannot afford conventional medicine options, and out-of-pocket payments dominate health care financing in many of these countries.36 This has led to elevated risks for adverse financial outcomes, such as medical impoverishment and death, especially in lower income households.37
In addition to cost, mistrust of conventional medicine further complicates cancer care in LMICs. More than one-half of patients with cancer in sub-Saharan African countries consulted a traditional healer because of access problems, high cost, stigma, and myths associated with Western cancer treatment.38 However, an overall lack of cancer education among TCIM practitioners may lead to delayed diagnosis and poor outcomes. For those who do have access to modern cancer advances, early detection and treatment contribute to increases in survival.
Lack of Survivorship and Palliative Care
Growth of the aging population also factors into the rise in cancer survivorship globally, with the WHO reporting that the number of people older than 60 years will increase approximately 2-fold by 2050.39 The intersection of aging and cancer survivorship can be particularly difficult to navigate for people affected by cancer. Despite progress in supportive care for survivors, gaps still exist in addressing complex symptoms such as anxiety, pain, fatigue, insomnia, neuropathy, and cognitive dysfunction.40, 41 Moreover, the physical, emotional, and social ramifications of cancer may linger years after treatment,42 further challenging the infrastructure and resources of health care systems.43
Early integration of palliative care, which is considered an essential component of universal health care by the WHO to improve quality of life,44 is also not easily accessible worldwide. For example, only 29% of patients with cancer in middle-income countries and 10% of those in low-income countries have access to oral morphine for pain relief.45 India and China do not have national policies or government funding that support palliative care,46, 47 and only 12 African countries reported having a stand-alone, nationwide palliative care policy.48 Therefore, culturally and socioeconomically sustainable solutions are especially needed to support patients and families with advanced disease in LMIC cancer populations.
Challenges of Integrating TCIM Into Conventional Cancer Care
In many LMICs, TCIM practices are deeply rooted in societal cultures and traditions. When used appropriately, TCIM may offer some solutions to address global cancer challenges6; however, tensions exist between TCIM and conventional cancer care.
Key differences between conventional cancer care and TCIM perspectives hinder collaboration and integration. Conventional medicine uses a bottom-up, micro-to-macro approach to understand health and disease, examining how structure leads to function. Conversely, TCIM embraces a top-down, macro-to-micro approach, examining how function necessitates structure.49 Conventional medicine and TCIM have distinct philosophies and treatment approaches (Fig. 2). The conventional oncology paradigm focuses on treating cancer as a biologic disease with identifiable mutations and targets. Treatments have clear, basic science mechanisms and are evaluated through rigorous clinical trials with well defined end points. As a result, modern anticancer approaches such as surgery, chemotherapy, radiation, hormonal treatment, targeted therapy, and immunotherapy have increased survival for many types of cancer. TCIM, instead, often relies on ancient theory and wisdom as well as thousands of years of empirical practice with people of a particular culture and community. The treatment focuses on the person with the illness rather than the disease itself and embraces the holistic nature of health as the interplay among body, mind, and spirit. The therapeutic approaches, including herbs, acupuncture, touch therapies, and spiritual practices, achieve harmony in the patient regardless of disease status.
Examples of Progress and Challenges of Integrating TCIM and Conventional Medicine in LMICs
Recognizing the tension between TCIM and conventional medical practice, many LMICs are working to integrate their traditional healing practices with conventional cancer care. Below, we provide the examples of Latin America, Africa, and Asia (India and China) to highlight some unique approaches and challenges in health care delivery, research structures, and funding.
Latin America
TCIM is widely used by patients with cancer in Latin American countries.50-54 It is estimated that between 50% and 90% of adult or pediatric patients with cancer use TCIM.53, 55-62 Natural products and nutritional supplements are most frequently used, followed by spiritual practices. More recognized mind and body therapies, such as meditation, yoga, tai chi, acupuncture, massage, music therapy, dance therapy, mandalas, and horticultural therapy, are also used across Brazil, Argentina, and Chile.50, 53, 56, 58, 59, 61, 63
Although widespread use has led to more official recognition, implementation has been mixed. In Argentina, Garrahan Pediatric Hospital and FUNDALEU (Foundation to Fight Leukemia) are 2 examples of health centers that apply TCIM in the clinical setting with medical recommendation. In Chile, the Clinica Alemana, the Arturo Lopez Perez Foundation, the National Cancer Institute, and the Calvo Mackenna Hospital also offer TCIM services integrated with Western conventional therapies to patients with cancer.64, 65 Several Brazilian medical centers have established integrative oncology programs with an academic focus on clinical care, teaching, and research: Hospital Israelita Albert Einstein in Sao Paulo and the Brazilian NCI-Designated Cancer Centers (the National Cancer Institute in Rio de Janeiro and the university hospitals of Sao Paulo and Fortaleza).66-70 Brazil has a national policy that integrates TCIM within the United Health System, which now includes 29 practices.71-73 Despite recognition of its policy, these practices are not routinely provided for oncology patients in conventional health centers. In addition, health professionals do not often inquire whether patients are using TCIM; therefore, the extent of benefits or safety issues such as herb-drug interactions are unknown.59, 74, 75
Similarly, the current evidence on TCIM used in Latin America is nascent. Almost all research is preclinical investigation involving plants. Several native and exotic species of Annonaceae, Loranthaceae, and Lamiaceae have been extensively studied.76-81 Several early phase clinical trials have found preliminary efficacy that plants from the Amazon region, such as Uncaria tomentosa and guarana, may help manage adverse effects of cancer treatment (eg, neutropenia, anorexia, fatigue) and improve quality of life.82-86 The Ministry of Health in Brazil has charged the Brazilian Academic Consortium for Integrative Health, along with the Latin American and Caribbean Center on Health Sciences Information/Pan American Health Organization, with generating clinical guidelines based on systematic reviews that evaluate clinical evidence and treatment outcomes related to cancer symptoms such as fatigue, pain, nausea, and vomiting.67
Africa
For most people in Africa, contemporary cancer care is unavailable, inaccessible, or unviable. This is because of the shortage of skilled medical professionals in oncology and scarcity of the required infrastructure. These resources, when available, are concentrated around the few urban centers (mostly national capitals) of the respective countries. The insufficient infrastructure and supply of radiology, diagnostic pathology, therapeutic surgery, chemotherapy, and radiotherapy make conventional cancer care extremely expensive and unviable for the majority of the population. Therefore, TCIM providers are often the first line of health care providers when individuals present with symptoms of cancer, and, for a large segment of the population, they may be the only source of health care that is available and affordable to patients with cancer.87-90
African traditional medicine delivered to the community can be classified as divination, spiritualism, and herbalism. Often it is seen as a mixture of these 3 in different proportions, varying from one practitioner to another.91 In a recent systematic review and meta-analyses, the use of herbs by patients with cancer in Africa was reported to be approximately 40%, the highest of all continents.92 Because of limited conventional treatment options, many patients with cancer receive herbal medicine alone as monotherapy. Because of a lack of population-based screening and diagnostic capacity, cancer often presents at an advanced and incurable stage. For these patients, TCIM interventions provide symptom relief and solace until death. Therefore, in the context of Africa, we often find traditional medicine as the first line of treatment for cancer, which is accessible and is introduced as soon as the disease is identified.90 In urban settings where there are conventional cancer care resources, several hospital-based survey studies in Nigeria, Tunisia, and Morocco found that the use of TCIM treatments among patients receiving treatment was common, which raises the potential for drug-herb interactions.93-95 TCIM treatments can have side effects and can contribute to renal and hepatic toxicities, which can be a detriment to patients' health; despite common use, physicians rarely inquire about them.93, 94 Considering these drawbacks and the extensive exposure of the African population to TCIM for cancer management and care, it is essential that well defined and focused clinical and experimental investigations are conducted into the safety and effectiveness of these practices to determine their appropriate use in various stages of the cancer care continuum.87-89
India
The pluralistic health care system of India offers patients access to TCIM known in the country as AYUSH (Ayurveda, Yoga and Naturopathy, Unani, Siddha, Sowa Rigpa, and Homeopathy). Published estimates of TCIM use among patients who have cancer in India range from 24% to 39%,96-98 with Ayurveda being the most common.97 However, these estimates are based on small sample sizes and may not represent behavior of their larger population of patients with cancer. Underreporting raises the possibility of unnoticed harms and benefits and concerns about potential interactions with chemotherapeutic agents. The use of TCIM has been associated with delays in seeking help from oncologists,96 potentially contributing to delayed diagnosis and treatment and, thus, higher mortality rates. Conversely, benefits from the integration of TCIM therapies into cancer care go unnoticed and are underreported as well.
Despite pluralistic health care systems in India, policies to facilitate cooperation and integration between TCIM and conventional medicine do not exist. Practitioners of these different systems work independently, and integration is challenging because of fundamental distrust in the other.99 For this reason, integrative oncology is not well developed in India. There have been many scattered and isolated attempts to integrate AYUSH treatments for cancer care in public and private hospitals. For example, several conventional oncology hospitals have established adjunct Ayurveda/AYUSH clinics to integrate relevant treatments with the goals of improving quality of life among patients with cancer. In addition, an Ayurvedic cancer care hospital in Pune, India integrates Ayurvedic drugs in coordination with modern oncology treatments such as chemotherapy, with some reported preliminary benefit.100
Research of AYUSH and cancer is predominantly preclinical and focuses on anticancer properties of herbs and formulations, with Curcuma longa and Withania somnifera being the most studied.101, 102 Some Ayurvedic formulations appear to have chemopreventive, antimetastatic, antiproliferative, chemosensitizing, and radiosensitizing activities.103-107 To translate any of these findings into effective clinical interventions at the point of care, well designed and rigorous clinical trials are needed. One study of 36 patients with cancer who were undergoing chemotherapy and radiation showed that the Ayurvedic formulation Rasayana Avaleha could reduce adverse events such as vomiting, mucositis, alopecia, and ageusia when used as an adjuvant.108 Limited funding opportunities, lack of research training, and ethical issues are just some of the challenges faced by researchers in India studying the role of TCIM in cancer management.
China
Traditional Chinese medicine (TCM) is deeply rooted in Chinese culture and everyday life is and held as a symbol of the nation.109 Approximately 75% to 80% of patients in China use TCM after a cancer diagnosis, with Chinese herbal medicine (55%-75%) used most often and tai chi/qi gong (7%) and acupuncture (1%-5%) used less frequently.110-112 TCM is widely integrated in oncology departments within China's hospitals in conjunction with conventional cancer treatment.113 Furthermore, conventional oncology diagnosis (eg, pathology, imaging) and treatment (eg, surgery, chemotherapy, radiation, and hormonal treatment) are available in elite TCM hospital oncology departments in addition to TCM approaches. One medical insurance analysis of oncology inpatients in China showed that 42% used TCM herbs and 25% combined herbs with conventional cancer drugs.114 In addition, traditional herbal formulas and TCM cancer drugs are listed in China's National Basic Medical Insurance Drug Catalog.
In Hong Kong in 2014, the hospital authority of the Special Administrative Region launched the Integrated Chinese-Western Medicine Pilot Program in 3 public hospitals, which included the integration of acupuncture and Chinese herbal medicine for inpatients with late-stage cancer.115 The results showed that the practices were safe and feasible, and the program was expanded to 8 hospitals in 2017. Clinical trials conducted in Hong Kong also demonstrated acupuncture benefits in cancer care, including reduced need for postoperative analgesics and improvements in cancer-related cognitive impairment and chemotherapy-induced peripheral neuropathy.116-118
In mainland China, with rapid economic growth, government and industry have invested in basic, clinical, and outcomes research of TCM in oncology.119 For example, in a prospective cohort study, the use of a physician-prescribed TCM formula was associated with improved survival in patients with stage II or III colorectal cancer.120 In a phase 2 clinical trial, the TCM formula Renshen Yangrong Tang reduced cancer-related fatigue.121 A systematic review and meta-analysis found that acupuncture was associated with moderate evidence for reducing pain in patients with cancer.122 Despite progress, TCM often involves complex herbal formulas or individualized prescriptions based on a patient's presentation; therefore, there is a need to increase the quality of TCM clinical trials by developing standardized diagnostic criteria, treatment approaches, and outcome measures according to defining TCM characteristics.123
Despite extensive TCM use in China and its surrounding regions, challenges in delivering comprehensive and equitable services exist. One survey of patients that identified barriers to care cited TCM treatment concerns (42%), such as side effects, its hindrance of conventional treatments, and lack of scientific evidence for its use, along with logistical difficulties (42%), including herb decoction, locating a good TCM physician, concerns over treatment cost, and adherence to longer treatments.124 Furthermore, patients aged 60 years or younger with localized disease had more concerns, and those actively employed reported more logistical difficulties.124 These findings highlight the need for more basic, clinical, and health services research on TCM treatments, better evidence-based education, and more patient-centered and convenient TCM treatment approaches for patients with cancer.124
Current State and Evidence of Integrative Oncology
As shown by the examples above, despite numerous challenges, the practices of conventional medicine and TCIM do not need to be mutually exclusive. By appropriately incorporating specific, evidence-informed TCIM therapies alongside conventional medicine, the field of integrative oncology can overcome tensions and create an inclusive environment in which both philosophies and treatment approaches effectively coexist to produce better patient outcomes. With this goal in mind, it is useful to review the current state of integrative oncology and how it might be used to advance solutions to persistent global challenges in cancer prevention and patient management. Over 20 years ago, leading North American academic cancer institutions, including Memorial Sloan Kettering Cancer Center, Dana-Farber Cancer Institute, and The University of Texas MD Anderson Cancer Center, developed clinical, educational, and research integrative oncology programs in response to the growing demand from patients with cancer to incorporate TCIM into conventional cancer treatment and survivorship care. The NCI also established the Office of Cancer Complementary and Alternative Medicine (OCCAM) to coordinate and enhance activities in TCIM research as it relates to the prevention, diagnosis, and treatment of cancer, cancer-related symptoms, and side effects of conventional cancer treatment.125 By 2016, the majority of 45 US NCI-designated cancer centers provided integrative medicine information to patients on their websites, including acupuncture/massage (73% each), meditation/yoga (69% each), nutrition consultations (91%), dietary supplements (84%), and herbs (67%), and most also offered these services.126 Building on 20 years of clinical research, including data from high-quality randomized controlled trials (RCTs), both the SIO and the American Society of Clinical Oncology (ASCO), a leading oncology organization, recommend integrative medicine for supportive care of various disease-related and treatment-related symptoms.127-129 Furthermore, guidelines from the National Comprehensive Cancer Network (NCCN) include acupuncture, massage, meditation, yoga, music therapy, exercise, and nutrition among their recommendations for alleviating common symptoms, such as fatigue, pain, nausea, hot flashes, and sleep disorders (Table 1).130-136 A brief summary of the evidence of selected integrative medicine approaches follows.
SYMPTOMS | ACUPUNCTURE | MASSAGE | MEDITATION/MBSR | YOGA | MUSIC THERAPY | EXERCISE | NUTRITION |
---|---|---|---|---|---|---|---|
Adult cancer pain | X | X | X | X | X | ||
Cancer-related fatigue | X | X | X | X | X | X | |
Sleep disorders | X | X | |||||
Distress (anxiety/depression) | X | X | X | X | X | ||
Cancer-associated cognitive dysfunction | X | X | |||||
Hot flashes/night sweats | X | X | X | ||||
Sexual dysfunction | X | X | |||||
Nausea/vomiting | X | X | X | ||||
Anorexia | X | X |
Lifestyle Management
Promotion of healthy lifestyles is a key component of integrative oncology and a critical component of cancer prevention. Smoking cessation has been a crucial strategy for cancer prevention on a population level.137-139 Studies that have examined poor diet, insufficient physical activity, and being overweight or obese have been largely observational. However, consistent associations have been demonstrated over time, and it is now well accepted that up to 50% of cancers could be prevented by modifying common lifestyle factors.140 Reducing alcohol consumption will lower the risk of more than 12 different cancers because alcohol has long been known as a carcinogen.141 Strategies such as safe sex and vaccinations can decrease the risk of virally mediated cancers caused by HPV, and healthy sun protection practices can reduce the risk of melanoma or other skin cancers.142
The same lifestyle risk factors of poor diet, insufficient physical activity, and excess weight are also associated with disease recurrence and mortality after cancer diagnosis for several cancer types.143 Overweight and obesity are associated with more than 12 types of cancer and account for approximately 5% to 8% of cancer cases.144-148 Furthermore, they are linked to an increased mortality risk for several common forms of cancer, such as breast, colorectal, and prostate cancers.149-151 One disturbing observation in LMICs is that the modulation of key biologic pathways associated with metabolic syndrome, such as developing diabetes, and with other cancer risk factors in overweight groups is happening at much lower body weights than in the West.152, 153 Obesity also interferes with physical activity goals and makes people less likely to exercise.
Importantly, however, being overweight, being sedentary, having a poor diet, and other high-risk behaviors are modifiable conditions. In the Look AHEAD Study (ClinicalTrials.gov identifier NCT03952728), which evaluated the impact of a weight loss intervention on cardiovascular events in individuals with type II diabetes, participants who were randomized to the weight loss intervention had a 20% reduction in obesity-related cancers compared with those who were randomized to the control group.154 Other research has demonstrated that people who eat a plant-centered, high-fiber diet have a lower risk of many cancers and that those with cancer who eat such a diet may respond better to treatment and tend to live longer.140 In addition, recent studies show that replacing 30 minutes of sedentary time with light or moderate physical activity is associated with an 8% and 31% lower risk of cancer mortality, respectively.155 Large-scale randomized trials are currently ongoing to evaluate the impact of weight loss, increased physical activity, and dietary modification on disease outcomes in individuals with early stage cancers.156-160
The global cancer epidemic cannot be overcome with treatment alone. Although billions of dollars each year are invested in precision-based treatments and early detection, cancer prevention through lifestyle modifications remains the cheapest and most effective method to reduce the incidence of cancer.
Mind and Body Interventions
Mind and body interventions, such as acupuncture, meditation, massage therapy, and yoga, have an increased evidence base for improving symptom management during treatment and survivorship.
Acupuncture
Studies indicate that acupuncture, a TCM practice that stimulates specific points on the body with needles, helps control pain in patients who have cancer.161-163 A systematic review and meta-analysis found moderate evidence that patients with cancer who received acupuncture and/or acupressure also had a decrease in analgesic use and pain.122 Specifically for breast cancer survivors receiving aromatase inhibitors, one phase 3 RCT demonstrated that acupuncture was associated with reduced joint pain compared with both sham acupuncture and usual care. For example, approximately 60% of those who received acupuncture had a clinically meaningful reduction in pain compared with 30% response rates in sham or usual care groups.164 More recently, a large RCT (N = 360) among diverse groups of cancer survivors with chronic musculoskeletal pain also showed that both electroacupuncture and auricular acupuncture reduced pain severity (by 1.9 and 1.6 points on the Brief Pain Inventory, respectively), reduced analgesic use, and improved quality of life compared with usual care.165 Several clinical trials in breast cancer survivors suggest that acupuncture produces lasting benefits for managing hot flashes with fewer adverse events than gabapentin and vanlafaxine.166-168 Furthermore, SIO, ASCO, and NCCN clinical practice guidelines have recommended acupuncture among options for the treatment of chemotherapy-induced nausea/vomiting and pain management.128-130, 132, 134
Massage therapy
The application of touch therapy to muscles and connective tissue, known as massage therapy, has been studied in chemoinfusion settings, where it has been shown to reduce fatigue, pain, nausea, and anxiety in patients, with demonstrated safety during active treatment.169, 170 It has also been widely used for depression, insomnia, and pain in patients with various cancer types.171-177 A randomized clinical trial in patients with advanced cancer experiencing moderate to severe pain (N = 380) found that massage was more effective than simple touch for improving pain and mood immediately (mean difference, 0.90 and 0.61 points, respectively; P < .001); however, there was no difference over time.178 In addition, an early phase, randomized study conducted in breast cancer survivors (N = 66) found that 6 weeks of Swedish massage therapy resulted in a clinically meaningful reduction in cancer-related fatigue (−16.50 points on the Multidimensional Fatigue Inventory, which was the primary outcome) compared with an active control (light touch, −8.06 points) and a wait-list control (+5.88 points).179 A systematic review and meta-analysis that included 12 high-quality and 4 low-quality RCTs of massage therapy for pain management in cancer populations demonstrated that massage therapy was effective for treating pain compared with no-treatment (standardized mean difference [SMD], −0.20) and active (SMD, −0.55) comparators. Compared with active comparators, massage therapy was also identified as beneficial for treating fatigue (SMD, −1.06) and anxiety (SMD, −1.24).180 In patients with breast cancer, a specialized treatment known as manual lymphatic drainage massage reduced lymphedema181 and prevented secondary lymphedema.182, 183 ASCO has endorsed SIO massage guidelines for managing depression and mood disorders, and the NCCN includes massage as a treatment option for pain and fatigue.128-130, 132, 133
Meditation
Mindfulness-based interventions like meditation focus on awareness of sensations and feelings in the present moment without judgment or interruption. Meditation can involve breathing techniques and guided imagery, which encourage a deep state of relaxation of the body and mind. Randomized trials have shown that meditation is effective for reducing anxiety, depression, fear of recurrence, and fatigue in patients who have breast cancer.184, 185 It also improves sleep, quality of life, and psychosocial adjustment in this population.184, 186, 187 Mindfulness-based stress reduction—a program developed to bring active awareness into daily activities, relationships, and communications—also demonstrated large effect sizes in stress, depression, and anxiety in a meta-analysis of 9 studies of patients with breast cancer.188 In addition, in a large RCT among breast cancer survivors (N = 322), mindfulness-based stress reduction improved symptoms of anxiety, reduced fear of recurrence, and improved fatigue; however, the effect sizes were generally small to moderate.185 In another RCT among 271 breast cancer survivors, compared with supportive-expressive group therapy and a one-day stress management control group, the mindfulness-based cancer recovery group significantly reduced stress symptoms and improved quality of life and social support.189 Recently, an RCT among 247 young breast cancer survivors (aged 50 years and younger) found that both mindful awareness practices and survivorship education significantly improved depressive symptoms from preintervention to postintervention relative to wait-list controls; however, the improvement was persistent only for mindful awareness practices, and not for survivorship education, at the 6-month follow-up. Furthermore, mindful awareness practices, but not survivorship education, improved fatigue, insomnia, and vasomotor symptoms.190 Given the growing evidence, both the SIO and ASCO suggest meditation for improving quality of life and reducing anxiety, stress, and depression during and after treatment; and the NCCN lists meditation for pain, fatigue, and distress management.127-130, 132, 133, 135
Yoga
An ancient Indian practice, yoga involves the incorporation of postures, meditation, and breathing exercises to achieve greater physical and emotional health. Studies show that this modality helps promote stress reduction, a sense of well-being, restful sleep, and better quality of life in patients with recently diagnosed cancer as well as survivors.191-199 It also improves social functioning and psychological symptoms and reduces stress and fatigue.189, 200-202 In an RCT among 200 breast cancer survivors, compared with usual care, those assigned to 12 weeks of twice-weekly yoga classes experienced a reduction in fatigue (5.4 vs 12.4 on the Multidimensional Fatigue Symptom Inventory–Short Form) and increased vitality (58.1 vs 51.6 on the energy/fatigue [vitality] scale from the Medical Outcomes Study 36-item Short-Form Health Survey) at the 3-month posttreatment visit.203 In another large, multicenter RCT involving 410 cancer survivors, participants in the yoga group reported overall better sleep quality than those in the usual care group.197 The effect size in the yoga group for improving sleep quality was large and clinically meaningful. In addition, the yoga group reduced sleep medication use by 21% per week during the intervention period.197 SIO and ASCO guidelines indicate that yoga may be considered to manage depression, anxiety, and mood disturbances and to decrease stress and enhance overall quality of life.128, 129 According to NCCN guidelines, yoga may be considered for improving some survivorship issues, such as distress, cognitive functioning, menopausal symptoms, and pain.131 Yoga is also listed in the NCCN guidelines for addressing cancer-related fatigue and anticipatory nausea/vomiting.133, 134
Natural Products
Herbal medicines are deeply rooted in many cultures and traditions. Interest is also high among patients with cancer, who take herbal supplements more frequently than the general population, with one-third of cancer survivors reporting the use of herbs.204-206 However, the quality of herbal products and the lack of robust clinical evidence currently hinders their integration into cancer care practices. The herbal industry faces challenges in consistently formulating products that deliver the promised physiologic effects.207 Studies show that the content of standardized marker compounds thought to be responsible for medicinal benefits can range from high to nonexistent, even within different batches of the same product.208 The accessibility of marker compounds or reference standards is another critical issue that hinders the proper biologic and chemical assessment of herbs.209 Furthermore, the classification of herbal products as dietary supplements in some HICs (for example, in the United States under the Dietary Supplement Health and Education Act) has facilitated their haphazard use and does not help address questions on efficacy and safety. Finally, lack of patent protection does not provide any financial incentives for industry to conduct clinical trials. Therefore, despite strong patient interest,210 conducting high-quality and adequately powered clinical trials of herbal products with limited resources remains difficult, if not impossible.
Research has shown potential herb-drug interactions with chemotherapy, immunosuppressant agents, anticoagulants, and hormonal therapies, all of which are used in cancer care.211 To educate both physicians and patients on the benefits and risks of supplements, the Integrative Medicine Service at Memorial Sloan Kettering Cancer Center developed and maintains About Herbs (aboutherbs.com).212 This comprehensive database provides reliable, evidence-based information on herbs, vitamins, minerals, and other dietary supplements, including uses, adverse effects, and herb-drug interactions.212
Drug development based on compounds derived from natural products has yielded 4 classes of agents available on the market: vinca alkaloids (vinblastine, vincristine, and vindesine), epipodophyllotoxins (etoposide and teniposide), taxanes (paclitaxel and docetaxel), and camptothecin derivatives (camptotecin and irinotecan).213 However, rigorous research investigating herbal medicine as part of a whole system, as it is used in TCIM for specific cancer outcomes, remains very limited.123 On the basis of reviewing the available evidence for women undergoing treatment for breast cancer, SIO clinical guidelines consider American ginseng for fatigue, ginger for nausea, and mistletoe for quality of life while recommending against guarana for fatigue, glutamine for nausea/vomiting, and acetyle-L-carnitine for chemotherapy-induced peripheral neuropathy because of lack of efficacy.127
Challenges and Opportunities in Research
To guide evidence-informed and patient-centered care, more research on the potential safety, effectiveness, and appropriate integration of TCIM interventions is needed. The design and implementation of integrative oncology studies present several challenges, including the standardization of interventions and the selection of appropriate control conditions. Contrary to clinical trials of pharmaceuticals, it is difficult to blind patients to group assignment when testing the impact of an integrative therapy. This is especially critical in symptom-intervention research, when the outcomes of interest are subjective and prone to the placebo effect. Acupuncture is an example of an integrative therapy intervention with a well established control condition; however, no consensus exists about which sham method is most appropriate for research.214, 215 For integrative interventions with no existing sham, such as yoga or meditation, the selection of a control condition can be more complex. Study strategies range from a comparison of the intervention versus usual care or the development of attention or active control for contact-time and group effect as well as blinding participants to the intent of the trial (comparing 2 behavioral programs when the intent is to test the benefit of yoga, per se).
Intervention standardization is also a challenge for integrative oncology research. By definition, integrative therapies are personalized to the individual. However, research typically involves a standardized intervention that can be tested across a diverse population so that the findings can be easily replicated, generalized to large patient groups, and ultimately implemented in a standardized manner.123 However, such issues do not just affect the field of integrative oncology. For example, in the field of psychology, cognitive-behavioral interventions follow a specific manual that allows for structured delivery of particular intervention components based on responses of the individual. Careful development and pilot testing of treatments are needed before launching clinical trials to refine intervention components, optimize dose, frequency of delivery, and factors for individualization. Novel research methodologies and whole systems approaches are needed to explore individualization of TCIM interventions. In addition, careful training of interventionists and frequent fidelity testing are needed to ensure treatment fidelity.
Because many TCIM practices exist in the culture and health systems of LMICs, real-world research using surveys, electronic medical records, and qualitative and mixed-methods research can help uncover disparities in utilization, expectations and motivations of patients with cancer, and barriers related to both TCIM and conventional medicine use, all of which can help design more cohesive and integrated care approaches. Systemic documentation and evaluation of existing TCIM integration models with conventional medicine in specific cultural contexts can further identify barriers and facilitators that can contribute to sustainable and effective clinical programs.
In addition, appropriate retrospective and prospective cohort studies incorporating validated patient-reported outcomes and relevant clinical outcomes can inform how these treatments impact populations in real-world settings and potentially generate more specific testable hypotheses that can then be confirmed in clinical trials.216 Consistent with patient-centered outcomes research, engaging patients and relevant clinical and policy stakeholders in defining research questions and facilitating dissemination efforts are key to generating evidence that actually matters to patients in their specific cultural and societal settings.217, 218
Global Integrative Oncology Partnerships to Increase the Evidence Base
A global commitment to research is critical to advance evidence-informed integrative oncology programs.219 Utilization of TCIM in cancer care is highly prevalent in LMICs, but those countries struggle to conduct research in this area.220 Collaboration and professional associations are key to advancing research, but most have been concentrated in HICs.220, 221 National-level alliances, and bilateral and multinational collaborative endeavors seek to increase research collaborations and training to increase the evidence base of TCIM for cancer prevention, treatment, and symptom management.
National Cancer Institute
The NCI's OCCAM leads initiatives focused on LMICs, facilitating training opportunities, conferences, technical support, and funding for developing and testing novel therapies and applications. OCCAM has focused on medicinal herbs and interventions of traditional Chinese and Indian systems of medicine.222, 223 Partnerships with various Chinese institutions have enabled the investigation of herbal formulations, their components, applications, and effects as part of cancer care. Mechanisms of action are being explored individually or combined with conventional cancer treatments. OCCAM and the Cancer Institute of the China Academy of Chinese Medical Sciences also joined together to hold 2 international conferences in Beijing, China, on cancer research and Chinese medicine. Thereafter, a development committee for the International Consortium for Chinese Medicine and Cancer was established to promote and advance Chinese medicine and cancer research, clinical trials, and symptom management.223 OCCAM recently signed a Letter of Intent with the Central Council for Research in Ayurvedic Sciences (Ministry of AYUSH, Government of India) aimed to enhance cancer research, research training, and scientific exchanges on the Ayurvedic sciences between US and Indian scientists. The partnership will explore ways of enhancing dialogue and cooperation between scientists and practitioners from both countries.
International Collaborations With Other US-Based Organizations
Large cancer centers around the United States are also collaborating with international partners to advance the field of integrative oncology. Memorial Sloan Kettering Cancer Center's Herbal Education and Research in Oncology program focuses on synthesizing the evidence base of TCM herbs to inform clinical research, education, and practice.123 The initiative promotes bidirectional learning with Chinese experts to share their knowledge and experience in incorporating TCM approaches in cancer care while the US team trains Chinese physician-scientists on literature review, data analysis, protocol design, and scientific writing in China.224-228 The University of Texas MD Anderson Cancer Center and its sister institutions have facilitated the documentation of TCIM use in patients with cancer in South America.62 The MD Anderson team also has collaborations with herbal companies in China and research teams in India. Moreover, these partnerships, along with other mechanisms for promoting research collaborations and training (such as the Brazilian Academic Consortium for Integrative Health229 or the TCIM Americas Network230), could catalyze the expansion of integrative oncology research in LMICs. To highlight the ongoing challenges and opportunities within the field, the SIO led an effort to publish a special Journal of National Cancer Institute Monograph titled Advancing the global impact of integrative oncology.231 The SIO also established a global task force to attract and engage international members, expanding to over 600 members representing more than 40 countries across 5 continents.
Specific Recommendations for Advancing the Global Impact of Integrative Oncology
The Trans–NCI-NIH Conference on International Perspectives on Integrative Medicine for Cancer Prevention and Cancer Patient Management stimulated rich dialogue about how best to promote the integration of TCIM into conventional cancer care and related research. We identified 3 thematic priorities (Fig. 3): 1) educating and integrating TCIM providers into the cancer control work force to promote risk reduction (ie, reducing initiation of tobacco use and increasing access to tobacco cessation interventions, prevention/treatment of infections such as HIV and HPV) and to promote culturally salient, healthy life styles (diet, physical activities, and overweight/obesity prevention); 2) developing and testing TCIM interventions to address cancer symptoms or treatment-related adverse effects (eg, pain, insomnia, fatigue, psychological distress); and 3) disseminating and implementing evidence-based TCIM interventions as part of comprehensive palliative and survivorship care so patients from all cultures can live with or beyond cancer with respect, dignity, and vitality. The long-term goal of integrative oncology is to empower each individual to become an active participant in their health, from prevention and treatment to survivorship and end of life, using high-quality, safe, and effective therapies from both TCIM and conventional medicine in a cohesive and coordinated manner. A concerted global effort as well as changes in perspective and ways of working are needed in the areas of policy, research, clinical practice, and education to achieve these outcomes. Specific recommendations are listed in Table 2.7
FOLLOWING THE 2020 TRANS–NATIONAL CANCER INSTITUTE–NATIONAL INSTITUTES OF HEALTH CONFERENCE ON INTERNATIONAL PERSPECTIVES ON INTEGRATIVE MEDICINE FOR CANCER PREVENTION AND CANCER PATIENT MANAGEMENT, WE RECOMMEND: |
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- Abbreviations: LMICs, low- and middle-income countries; TCIM, traditional, complementary, and integrative medicine; WHO, World Health Organization.
Policy
Integrative oncology can make a significant contribution to the goal of universal health care by being included in the provision of essential health services. Programs must have support from local institutional leadership and health professionals and must be culturally sensitive to meet the unique needs of their patient population. The WHO is committed to strengthening the contribution of TCIM to universal health care worldwide. Countries integrating TCIM with conventional medicine need to examine not only the differences between the 2 systems but also areas in which they converge to help tackle unique 21st century health challenges. Those with pluralistic health systems, such as South Korea, India, and China, have a natural advantage because they offer a range of health care options.232, 233 Specific societal context has a major influence on the way each system addresses the needs of patients with cancer along the care continuum. Critically evaluating the strengths and weaknesses of each system in specific contexts will allow for more effective collaborations and efficient utilization of resources.
Health Care Disparities
Growing cancer burden and health disparities in cancer care in LMICs require effective and sustainable solutions. Challenges include geographic barriers to receiving care, lack of trained medical professionals, late-stage cancer diagnosis, disease stigma, and treatment affordability.2 In these countries or regions, TCIM practitioners are often more accessible and affordable than allopathic services, they are often the first point of contact, are more likely to speak the same language, and are trusted by patients, providing an imperative for integration of the 2 approaches.6 Such integration, facilitated by the WHO's global frameworks, can help address existing health disparities in cancer care in low-resource regions and ensure that treatments are evidence-informed and safe.
Cancer Care Delivery
Important areas for the use of TCIM services in LMICs are primary prevention, early detection and screening, public education and outreach, improved accessibility, and promotion of societal acceptance of evidence-based screening, prevention, and conventional cancer treatment and follow-up. Because many TCIM treatments have a rich cultural basis and address the physical, psychological, and spiritual well-being of the individual, they can potentially play a major role in improving cancer-related symptom management, quality of life, mental health, and palliative and survivorship care. Despite extensive historical use, many TCIM interventions have poorly understood mechanisms and lack biologic plausibility as tumor-directed treatments. Therefore, we should guide against the use of TCIM for tumor-directed indications unless they are supported by evidence. The use of TCIM in cancer care must be supported with appropriate synthesis and implementation of policies and must be part of public health programs rolled out by health care systems. It requires concentrated global efforts and partnerships, knowledge sharing, and advocacy to overcome worldview-based biases.
Therefore, it is also critical to re-examine the health financing systems in LMICs. The Declaration of Astana, adopted at the Global Conference on Primary Health Care in October 2018, made clear that the success of primary health care will be driven by applying scientific as well as traditional knowledge and extending access to a range of health care services, which include TCIM.
Research
Rigorous research cannot be performed without an adequate workforce, funding support, and coordinated procedures. The NCI and NIH currently have several funding opportunities that can be applicable to research training or international collaborations in the area of TCIM in LMICs (see Table 3). Despite economic challenges, other countries and regions should also invest in research training and high-quality research and should incentivize collaboration between TCIM practitioners and conventional medical researchers. Agreement on approaches to mapping integrative oncology services provisions at cancer centers and patient-reported outcome measures, as well as a robust approach to recognizing intervention safety and potential interactions, are needed to move forward.221, 234 Standardized platforms for patient-reported outcome assessment selection, delivery, and data collection and interpretation across centers can help facilitate cross-cultural and cross-institutional research efforts.216 International collaborations for sustained research training and mentoring are important to increase the capacity for conducting high-quality global integrative oncology research.
FUNDING OPPORTUNITIES | |
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https://grants.nih.gov/grants/guide/rfa-files/RFA-CA-20-031.html |
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https://www.cancer.gov/about-nci/organization/cgh/research-training#current-funding-opportunities |
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https://www.cancer.gov/about-nci/organization/cgh/research-training/stsep |
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https://www.crdfglobal.org/funding-opportunities/ncis-cancer-research-training-travel-awards-lmic-investigators |
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https://www.fic.nih.gov/Programs/Pages/scholars-fellows-global-health.aspx |
https://grants.nih.gov/grants/guide/rfa-files/rfa-tw-21-004.html |
PROFESSIONAL EDUCATION FOR LMIC CLINICIANS AND RESEARCHERS | |
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https://training.iarc.fr/cards_page/postdoctoral-fellowships/ |
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https://integrativeonc.org/ |
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#integrativeonc21 |
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https://www.asco.org/about-asco/about-asco-association |
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https://www.asco.org/international-programs |
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#ASCO21 |
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2021 Annual Meeting abstracts |
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https://www.nccn.org/global/what-we-do/harmonized-guidelines |
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https://www.nccn.org/global/what-we-do/international-adaptations-and-translations |
https://www.nccn.org/global/opportunities | |
https://www.nccn.org/global/global-events |
- Abbreviations: IARC, International Agency for Research on Cancer; NCI, National Cancer Institute; NIH, National Institutes of Health.
Education
Addressing gaps in professional training will help support the goal of safe and effective delivery of integrative oncology care. Conventional medical practitioners need to receive more robust education on TCIM and must draw from growing evidence-informed research so they can safely and effectively incorporate these practices into clinical settings to improve cancer outcomes. Similarly, TCIM practitioners can be educated and integrated into routine cancer care settings to more effectively collaborate with the conventional cancer care workforce.6 It is essential that they receive training in areas such as basic cancer prevention and oncology knowledge, which, in turn, can help them prevent delayed diagnoses, administer some treatments, and work together with conventional medical practitioners. Similar to the HIV/AIDS programs in Africa, TCIM practitioners could help maintain the quality of health care programs and adherence to care.235 Another example is that, in China, specialized TCM physicians receive additional training in medical oncology or radiation oncology; therefore, they can provide conventional anticancer treatment for those populations that seek out TCM treatment options because of trust, stigma, and preference. Interprofessional organizations like the SIO can play a key role in increasing international representation and engagement of TCIM researchers and practitioners from LMICs.
Clinical Practice Guidelines
To ensure that patients with cancer from around the globe have access to high-quality cancer care, the unique resource limitations and challenges faced by LMICs must be acknowledged. Defining evidence-informed, culturally sensitive, and resource-aware clinical guidelines that help inform careful integration of TCIM into conventional cancer care is key. For example, the SIO and ASCO have established clinical guidelines for integrative oncology.129 Building on this work, the addition of appropriate cultural context can help LMICs adopt and use these guidelines. Furthermore, in countries with specific TCIM disciplines, such as Ayurveda in India and TCM in China, collaboration between TCIM and conventional medicine societies to establish joint guidelines may help standardize practices and increase the quality of care delivery.
Potential Obstacles and Setbacks
It important to acknowledge that the framework of integrative oncology to systematically bring together TCIM and conventional cancer control and treatment effort can feel aspirational, with challenges and obstacles. Political, economic, cultural, and social norms and beliefs can create obstacles for TCIM and conventional health care providers to collaborate. Some TCIM providers may inaccurately claim adherence to integrative oncology principles as a marketing strategy to promote nonevidence-informed alternative cancer treatment for economic gain. The process of generating research evidence is both expensive and long, which LMICs with limited resources may not be able to support. Finally, each country or region has a unique political, economic, cultural, and social infrastructure, and it is unlikely that one size can fit all; therefore, the process of integration will likely be specific to its local context and iterative based on progress in both TCIM and conventional oncology approaches.
Conclusion
To address the global challenge of continued increases in cancer incidence, particularly in LMICs, a timely and unified effort is required. Patients with cancer in LMICs face challenges because of limited access to primary prevention strategies, delayed diagnosis because of poor access to screening and gaps in timely referral of symptomatic patients for conventional diagnostic testing, limited treatment options, and very underdeveloped or nonexistent palliative or survivorship care. Many patients with cancer turn to TCIM to address myriad unmet physical, emotional, and spiritual needs. Integrative oncology provides a clear definition and systematic approach to bring TCIM and conventional cancer care together and presents the opportunity to make care more affordable, accessible, and equitable for patients with cancer worldwide, and particularly in LMICs. By developing rigorous research, robust education and research training, high-quality clinical care, and inclusive policies, integrative oncology can be part of the solution to address the current and future global challenges of cancer.