Introduction

For more than two decades, oncology patients in the USA and around the world who are interested in complementary medicine have been increasingly referred by conventional healthcare professionals for integrative oncology consultation and treatment services. Integrative care approaches may include dietary/lifestyle interventions, herbal medicine, acupuncture, mind-body, manual or movement therapies, and other traditional therapies, which are offered by a range of integrative and complementary healthcare practitioners. Integrative oncology care is provided in an evidence-based manner, often within conventional oncology settings. Unlike “alternative” or “complementary” medicine, which are practiced outside or in parallel with conventional care, integrative oncology is an integral part of the multi-disciplinary and interprofessional oncology model of care that operates in conjunction with the work of oncologists, oncology nurses, psychosocial oncology practitioners, palliative care services, and other healthcare professionals. The concept of integrative oncology has been defined by Witt and colleagues as a patient-centered, evidence-informed field that “aims to optimize health, quality of life, and clinical outcomes across the cancer care continuum and to empower people to prevent cancer and to become active participants before, during, and beyond cancer treatment” [1].

In recent years, integrative oncology clinical practice has been supported by evidence arising from high-quality randomized controlled trials that indicate many integrative oncology modalities are both effective and safe for the management of issues that impinge on patients’ quality of life (QoL), such as cancer-related pain [2], chemotherapy-induced nausea and vomiting [3], cancer-related fatigue [4], and endocrine treatment-related hot flashes and night sweats [5]. The Society for Integrative Oncology (SIO), founded in 2003, has as its stated goal to advance evidence-based, comprehensive, integrative healthcare to improve the lives of people affected by cancer. The SIO is an international organization with published evidence-based guidelines for general cancer patients and for individuals living with lung and breast cancer [6, 7]. The latter guidelines were subsequently endorsed by the American Society of Clinical Oncology [8].

Integrative oncology centers have become more commonplace around the globe, with most offering therapies following a patient-centered approach. This approach involves co-designing a program of care with patients by an integrative physician or healthcare professional who is dually trained in integrative oncology and supportive cancer care [9]. The development of a patient-centered integrative oncology program requires knowledge about the effectiveness and safety of a wide range of modalities for the treatment of specific QoL-related indications. It also requires a non-judgmental approach that respects the patient’s health, beliefs and values, autonomy, and cultural background, as well as the patient’s willingness to undertake integrative oncology modalities, an important consideration for ensuring adherence to an integrative care program. In the integrative oncology setting, the physician and care team need to take into consideration the multi-modal, individualized, and dynamic nature of integrative medicine. This approach must be woven into an evidence-based, effective, safe, and feasible treatment plan that may change from visit to visit according to the patient’s evolving QoL-related concerns and the toxicities of the conventional oncology treatment.

The COVID-19 pandemic has presented a significant challenge to integrative oncology practitioners worldwide, severely limiting their ability to ensure continuity of integrative care. Several recently published commentaries discussing the impact of the COVID-19 pandemic, and associated physical distancing regulations, on cancer care provision have recommended delays in cancer treatment and a reduction in the number of in-person treatments and consultations [10,11,12]. Prioritization of cancer treatments by institutions during the pandemic has also meant that some treatments deemed non-essential by decision makers, include those falling under the rubric of supportive care and integrative oncology, have been made inaccessible [13]. This is particularly troubling in light of research that has shown cancer patients and survivors experiencing heightened levels of mental health issues during the pandemic exacerbated due to restricted access to timely and appropriate cancer care [14, 15]

While online consultation/treatment recommendations have been previously developed for lifestyle interventions for individuals living with cancer, they have not accounted for the challenges posed by a global pandemic [16]. More recently, clinical recommendations have been developed that have focused on the online delivery of exercise to cancer populations during the pandemic [17], and commentaries on the online provision of specific integrative oncology therapies, such as mindfulness and yoga, have emerged [18]. Pragmatic recommendations to guide integrative oncology care from a global perspective during the COVID-19 pandemic, including online patient consultation and treatment, however, are absent.

In order to address this challenge, the SIO has established the Online Task Force to share creative healthcare initiatives among integrative oncology practitioners, particularly those offering online consultations and treatment. This paper presents the SIO Online Practice Recommendations with the goal of supporting integrative oncology practitioners, including those trained in conventional and/or complementary medicine, in addressing their patients’ supportive care, QoL, and symptom management needs by providing effective and safe online integrative oncology consultations and treatments during this time of pandemic risk, which can be applied moving forward to expand the accessibility and reach of integrative oncology care worldwide even post-pandemic. For the purposes of this paper, the term “integrative oncology practitioners” refers to the variety of conventional and complementary healthcare practitioners that collaborate in the provision of integrative oncology care, including but not limited to, physicians, nurses, dietitians, psychologists, rehabilitation specialists, massage therapists, acupuncturists, and arts-based therapists.

Methods

Establishment of the SIO Online Task Force

The SIO Online Task Force was established in March 2020 in response to the global COVID-19 pandemic that forced many integrative oncology programs to either close or significantly limit their clinical practice. In order to meet the challenges posed by the pandemic, a number of integrative oncology practices began to develop creative online solutions to enable them to continue treating their patients without compromising their safety. News of these local healthcare initiatives quickly spread via international videoconference meetings with SIO members from Israel, Italy, Germany, Switzerland, the USA, and Canada. In turn, they shared their strategies and offered practical suggestions for providing online integrative oncology consultations and practitioner-guided treatments to patients and their caregivers. These online initiatives were then presented to the SIO Executive Committee and Board of Trustees, who agreed to the creation of the SIO Online Task Force. The goal of this group was to develop recommendations to support integrative oncology practitioners in providing evidence-based integrative oncology care to patients, caregivers, and oncology staff through online programming and resources, in the comfort and safety of their homes. The SIO Online Task Force is comprised of seven researchers, clinicians (medical doctors including oncologists, registered nurses, massage therapists, and social workers), and administrators from four countries (USA, Canada, Israel, and Germany), representing a rich multi-disciplinary, interprofessional, and multi-cultural background.

Developing and implementing the questionnaire

Consensus methods that garner the perspectives and experiences of key stakeholders, including clinicians, administrators, and patients, have become commonplace and a standard process in the development of clinical guidelines [19]. Given the rapid evolving nature of the COVID-19 pandemic and the urgent need for recommendations that would help guide the online provision of integrative oncology consultations/treatment, an informal consensus process [20] was implemented that drew on the international expertise held within SIO and its membership. The SIO Online Practice Recommendations were developed using a four-phase consensus process led by the SIO Online Task Force. The first phase entailed a scoping review of the scientific literature conducted independently by two of the authors using PubMed, Medline, and Embase, with the goal of identifying clinical research published in the past 10 years (December 2011–December 2021) on both the efficacy and safety of online integrative oncology consultations and modalities. The following keywords were searched alone and then in combination:

  1. a.

    Oncology-related keywords (i.e., cancer, oncology, neoplasm, palliative, chemotherapy, radiation).

  2. b.

    Complementary and integrative medicine-related keywords (i.e., CAM, complementary/alternative/integrative medicine, integrative oncology, traditional medicine, herbs, herbal, mind-body, relaxation, meditation, guided imagery, hypnosis, homeopathy, acupuncture, nutritional/dietary supplements, naturopathy, energy therapy, manual therapy, massage, reflexology, yoga, qigong, Feldenkrais, anthroposophic medicine)

  3. c.

    Keywords related to online consultation/treatment during the COVID-19 pandemic (i.e., digital, online, online intervention, telehealth, telemedicine, virtual).

Further limits applied included articles published in English and limited to the following types of studies: clinical trials, comparative studies, meta-analyses, and systematic reviews. Practice guidelines were also included.

Initially, 562 articles were identified; screening of titles and abstracts resulted in 524 articles being deemed ineligible (see Fig. 1). Of the remaining 38 articles, a review of the full text resulted in 9 articles being selected as relevant for the scoping review. Two were systematic reviews [21, 22], six were clinical trials [23,24,25,26,27,28], and one was an observational study [29]. While these articles concluded that integrative oncology therapies, such as mind-body and behavioral therapies [22, 23, 25,26,27,28], yoga [24], and exercise [21], could be feasibly offered in a virtual format and positively affect physical and psychosocial well-being, symptom management, and overall quality of life, limited pragmatic recommendations were provided regarding how to address the unique challenges of online integrative consultations/treatment. The studies examining the feasibility of online interventions provided the most useful suggestions, including the need to maintain the confidentiality of online group sessions, provide initial and on-going technical support, and address slow Internet access and limited technological knowledge [25,26,27,28]. While the online format was perceived by some patients as increasing access to care and decreasing burden [28, 29], others preferred face-to-face interactions for a more social and guided experience [22].

Fig. 1
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Scoping review protocol

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The findings of the scoping review, along with the clinical experience and insights of the integrative oncology teams in Israel and Europe, were presented to the SIO Online Task Force, which discussed and identified a number of core issues surrounding the provision of online integrative oncology care that required elucidation. Task Force members also identified several relevant clinical trials that assessed self-administered modalities, including self-acupressure [30], self-acupuncture [31], and self-hypnosis [32], which provided insight regarding the feasibility of self-management in the context of integrative oncology.

During the second phase of the process, the Task Force developed a questionnaire to further delineate the core issues related to providing online integrative oncology consultation and treatment modalities. A draft questionnaire was prepared and reviewed by the SIO Executive Committee and a group of leading SIO members and clinicians (physicians, nurses, psychologists, and other integrative oncology practitioners) who were actively providing online integrative oncology consultations. The final version of the questionnaire addressed three domains: (1) general challenges to providing online integrative oncology treatments, with practical suggestions for ways to overcome these challenges (25 open-ended items identified as core issues); (2) integrative oncology modalities available in integrative oncology centers before the COVID-19 pandemic, and whether they were moved online during the pandemic (16 integrative oncology modalities, provided as a checklist); and (3) specific challenges and practical suggestions associated with the provision of integrative oncology therapies via an online format (7 open-ended items that captured the main types of integrative oncology modalities). A final open-ended item was provided for respondents to share any additional insights regarding online integrative oncology consultation/treatment (see Supplementary Material for a copy of the questionnaire).

In the third phase, the final version of the questionnaire was distributed via email to 78 integrative oncology leaders from integrative oncology programs situated within leading oncology centers around the world. Some of those leaders were identified through the SIO member directory and others through snowball sampling. All were asked to share their clinical insights, with the ultimate goal of developing the SIO Online Practice Recommendation for integrative oncology care provided online. Survey replies were obtained from 54 integrative oncology experts from 19 countries (Argentina, Australia, Brazil, Canada, Chile, China, France, Germany, India, Israel, Italy, Japan, Lithuania, Netherland, Spain, Switzerland, Turkey, United Kingdom, USA) (see Table 1).

Table 1 Demographics of questionnaire respondents
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In the concluding fourth phase, the Task Force created the SIO Online Practice Recommendations after a brief thematic analysis of the open-ended survey data. This analysis was independently performed by four authors (EBA, NS, NA, LGB), who grouped the responses into a preliminary list of 10 challenges that had been identified by respondents as being associated with online integrative oncology consultations and treatments. For each of these challenges, key principles of online care were identified and specific recommendations for practical implementation were developed. This list of challenges and recommendations were thoroughly discussed by members of the SIO Online Task Force and then reviewed by the SIO Executive Committee for final confirmation. The SIO Executive Committee is an interdisciplinary group of integrative oncology key stakeholders, including oncology health professionals (i.e., physicians, nurse, psychologist), integrative oncology researchers, patient advocates, and clinical administrators. The final SIO Online Practice Recommendations presented in this article is, thus, the cumulation of a rigorous consensus process that engaged international leaders and clinicians in integrative oncology.

Results

Table 2 presents, in detail, the SIO Online Practice Recommendations. The recommendations focus on ten challenges that need to be addressed during the online integrative oncology consultation and treatment process. Each of the ten challenges is accompanied by a list of recommendations for addressing each challenge and specific suggestions for their practical implementation. The following challenges to online integrative oncology consultations and treatments are addressed in the Online Practice Recommendations:

  1. 1.

    Identify any skepticism about, or antagonism toward, the feasibility and effectiveness of an online integrative oncology treatment program. Acknowledge that resistance to online consultation/treatment may not be a concern only for the patient and/or caregiver, but also for the integrative oncology practitioner.

  2. 2.

    Be aware of ethical and medical-legal issues regarding the patient’s privacy and data security, selection bias by healthcare practitioners related to which patients are offered online consultations and the treatment modalities deemed appropriate for the online format, and the potential for specific online-associated risks (e.g., breaches in patients’ privacy).

  3. 3.

    Assess and proactively respond to technical challenges associated with the virtual environment before and during an online session.

  4. 4.

    Prepare the online setting to ensure a quiet, safe, and private environment in which the therapeutic nature of the interaction can be maintained. This includes scheduling the session ahead of time; co-organizing the home setting with the patient and/or caregiver; and addressing the setting from which the integrative oncology practitioner will be conducting the online session, whether at the clinic or from home.

  5. 5.

    Address potential care challenges at the beginning of the online session, including discussing the patient’s expectations and co-defining treatment goals, while continuously monitoring the patient’s attentiveness and fatigue, especially in light of the potential for distractions due to the online remote setting.

  6. 6.

    Ensure effective communication during the online session, avoiding the use of technical and unidirectional instructions and establishing a space for patients to discuss their emotions, while emphasizing the clinical therapeutic goal, just as a practitioner would if the session were taking place in-person at a clinic.

  7. 7.

    Strive to promote specific treatment effects, such as the relief of at least one of the patient’s leading concerns (e.g., pain, fatigue, insomnia, nausea), while at the same time maximizing general and non-specific effects of the treatment (e.g., expressing compassion with regards to the patient’s sense of isolation during the pandemic).

  8. 8.

    Consider including the caregiver in the therapeutic process, based on the patient’s consent and ethical-therapeutic considerations. Clarify whether the caregiver is only there to assist the patient, or is also in need of support and treatment as well, especially in the context of therapies that are amenable to group participation, including mind-body and movement modalities (e.g., Yoga, Qi Gong, Feldenkrais method).

  9. 9.

    Proactively plan how to conclude the online integrative oncology session while ensuring a sense of containment and encouragement by scheduling a follow-up session.

  10. 10.

    Ensure continuity of care by discussing the need to schedule and coordinate the next consultation and treatment sessions, and to communicate with other integrative and conventional oncology practitioners involved in the patient’s treatment and care.

Table 2 Top 10 SIO Online Practice Recommendations
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Discussion

The SIO Online Practice Recommendations for online treatment and care were created in response to the COVID-19 pandemic and are based on the insights and experience of an international group of experts dedicated to ensuring continuity of integrative oncology care despite the challenges posed by this global threat. Earlier guidance on the use of online consultation/treatment can be seen in the World Health Organization (WHO) 2019 Guideline recommendations on digital interventions for health system strengthening and the 2018 WHO Guideline on the integration of palliative care in response to humanitarian emergencies and crises [33, 34]. The 2018 WHO Guidelines recommend the use of telemedicine “under the condition that it complements, rather than replaces, face-to-face delivery of health services; and in settings where patient safety, privacy, traceability, accountability and security can be monitored.” (p. 20). The emphasis on a complementary rather than alternative role of online consultation/treatment is important and addresses the recommendation that it be implemented after careful consideration of “what can and cannot be done in the remote consultation.” (p. 21). Fortunately, many of the therapies utilized in integrative oncology are amenable to virtual presentation.

Another organization that has raised awareness regarding the use of online consultation/treatment during the COVID-19 pandemic is the European Society of Medical Oncology (ESMO). The ESMO recommendations for patients with lung cancer suggest that all non-priority out-patient appointments be converted to a telemedicine platform, acknowledging this option as a valuable tool while at the same time emphasizing that it should not completely replace standard practice [35]. Suggestions on how to optimize the use of online consultation/treatment in the oncology setting have also been published by various international researchers in the field of palliative care [10, 36, 37]. Recently, Israeli researchers reported on a qualitative study summarizing practical suggestions on how to perform online treatments in the integrative oncology setting during the COVID-19 pandemic [38].

The SIO Online Practice Recommendations for online consultations/treatment address challenges associated with telemedicine that may be different from those faced in the conventional medical setting. In the integrative oncology setting, the therapeutic relationship is reliant on verbal and non-verbal communication, and often involves hands-on treatments with the integrative oncology practitioner guiding the patient on the self-application of a therapy, such as self-acupuncture/acupressure, manual/movement modalities, and mind-body therapies. It is with these factors in mind that the SIO Online Practice Recommendations were established, with the goals of providing integrative oncology practitioners with the knowledge and skills to: (1) overcome the challenges faced in the online setting; (2) properly plan and schedule the current intervention and plan subsequent interactions; (3) monitor safety-related issues; (4) ensure ethical and open communication with patients and/or caregivers; and (5) document the online integrative oncology intervention and its outcomes.

The SIO Online Practice Recommendations and the process through which they were created have been limited by a number of factors. As with other guidelines and recommendations published during the COVID-19 pandemic, the SIO Online Practice Recommendations were created in a short period of time and in response to an unexpected worldwide crisis faced by nearly all fields of healthcare, including oncology. However, the provision of integrative oncology presented additional challenges, especially when many integrative oncology services were either closed or operating with significantly restricted activity, including the cancellation of all group-based therapies due to physical distancing restrictions. The Online Practice Recommendations were also based on expert opinions of a select group of global leaders of integrative oncology services, and require confirmatory research. As such, the present SIO Online Practice Recommendations should be seen as a preliminary step, to be followed by mixed method research that explores the feasibility, effectiveness, and safety of the Recommendations across individual and group interventions, as well as among complementary healthcare practitioners and professional associations. A revised version of the Recommendations would then be developed and could be subsequently updated, as required, and subject to a formal critical appraisal process, such as the application of the AGREE II tool [39]. The final version of the Recommendations would then be shared within the international integrative oncology community through SIO as well as with conventional oncology healthcare professionals.

From an equity, diversity and inclusion perspective, online integrative oncology care may improve access to some individuals who are unable to attend sessions in person due to a variety of economic and social reasons. However, the lack of recognition within the present SIO Online Practice Recommendations regarding the unique challenges posed by online care for those living with accessibility issues, such as hearing and visual impairment, is a limitation that requires attention. Future version of the Recommendations would benefit from the insights from other established telemedicine guidelines that have offered suggestions regarding appropriate accommodations and modifications for those living with accessibility needs [40,41,42].

It is of utmost importance that the SIO Online Practice Recommendations not be seen only as a local and specific initiative in response to the COVID-19 pandemic. The use of online consultation/treatment is increasingly becoming a part of conventional medical practice, and those involved in the provision of integrative oncology care should not let themselves be left behind. The guidelines are, and will continue to be, relevant to other situations, including maintaining continuity of oncology care for patients with limited accessibility to the treatment center due to factors such as geographical distance or economic constraints; patients with reduced mobility, especially during active oncology treatment or with progression of disease; and patients whose caregivers are unable to facilitate and/or support their access to the integrative oncology care setting. At the same time, it is important to emphasize that online treatments should not become a substitute for face-to-face interactions. The integration of in-person and online interactions will provide patients with a richer repertoire of integrative oncology services access, and allow for tailoring treatments to patients’ needs, expectations, and health beliefs.