Good practice recommendations to better coordinate the management of oncological pain: a Delphi survey

Treatment of oncological pain is complex and requires a multidisciplinary management approach between oncology services and pain units. Although significant improvements have been achieved in the treatment and overall survival of cancer patients, the management of oncological pain has not followed the same directions. Many patients are not referred to pain units even though they could benefit from it. The purpose of this Delphi survey was to map the current situation in the management of cancer pain, identify barriers and propose recommendations to improve its management by emphasizing the importance of collaboration and coordination between oncology services and pain units. A survey among members with recognized experience in the management of oncology patients and oncological pain was held based on the Delphi method principles. The experts were asked to vote preselected statements on cancer pain management in two rounds and conclusions and recommendations were formulated based on the consensus reached for each statement. Barriers and areas for improvement were identified: need of multidisciplinary management approach, effective communication between oncology services and pain units, timely referral of cancer patients to pain units, training of health care professionals dealing with cancer aspects and identification of those patients that could benefit from a multidisciplinary management of their oncological disease. The experts issued recommendations targeting the identified barriers and areas for improvement by defining the service requirements of hospital and units treating cancer pain patients, establishing referral pathways necessities and adopted measures to improve the care of cancer patients.

1. Identifying the necessary resources that an institution or clinical service should be equipped with to effectively manage cancer pain patients. 2. Proposing referral pathways and coordination/communication processes between the country's pain units and oncology services for an effective treatment and follow up of cancer pain patients. 3. Introducing training opportunities for the health care professionals handling cancer pain cases to improve therapeutic outcomes and consequently life quality of affected patients.

Expert panel selection. The Spanish Medical Oncology Society (SEOM) and the Spanish Society of Pain
(SED) promoted the initiative and designated 3 representatives from each one to appoint a lead scientific committee. This committee was composed of experts with recognized experience in clinical oncology and oncological pain management. The scientific committee generated statements/items, focusing on patients, healthcare providers and healthcare system perspectives, addressing current issues and identifying barriers in the various management stages of cancer pain. These statements were sent for assessment to an expert panel consisting of 35 members, who were selected by the scientific committee and all were SEOM and SED members. They were chosen taking into account their recognized experience, professional prestige and publications in their reference field respectively. Study design. A Delphi method was used, whose aim is to transform individual opinions into an expert group consensus 13 . After an exhaustive literature review and discussion, the scientific committee generated 79 debatable items distributed in three content blocks: general considerations on the cancer pain management, referral criteria to a pain unit, and barriers and opportunities for the improvement for cancer pain management improvement.
The items were sent to the panelists for an online evaluation and validation by voting in two rounds. Panelists assessed the items using a single 9-point Likert-type ordinal scale, according to the model developed by the UCLA-RAND Corporation for the comparative assessment and prioritization between different health options (minimum 1 = full disagreement; and maximum 9 = full agreement) 13 .
To analyze the group's opinion and the consensus degree reached on each question, the median and the interquartile range of the scores obtained for each item were used.
Those items that did not reach consensus (in favor or against) in the first round were reformulated and included again in the second round questionnaire. In this second round the panelists received the first survey results so that they could contrast their personal opinions with those of their fellow panelists and, if necessary, reconsider their initial opinion.
Results are shown in tables as median and IQR of the panelists' responses and degree of agreement. Taking into account the consensus statements, the scientific committee developed a table of conclusions and recommendations on the management of cancer pain patients.

Results
The questionnaire consisted of 79 items addressing the current coordination status between pain units and medical oncology services in Spain regarding cancer pain patients treatments, and proposed measures to improve patient flow and collaboration between pain units and medical oncology services for better therapeutic outcomes and life quality of the affected patients (Tables 1, 2, 3).
The questionnaire was submitted to the experts' panel. Of the 35 panelists to which the items were sent, 30 responded to both evaluation rounds. Consensus was reached on 46 out of the 79 items evaluated in the first round. Additional 5 items reached consensus after the second evaluation round making a total of 51 out of the 79 proposed items (64.6%). Of them, 55 reached consensus on agreement and 6 on disagreement. The results of the items that reached maximal consensus are shown in Table 4. Table 5 summarizes the main statements agreed by the panelists and shows recommendations on the monitoring of the disease.
Regarding cancer pain management (Table 1) the panelists agreed that there are many cancer patients not referred to pain units, and thus they do not receive relevant beneficial treatments. They recommended ( Table 5) that in hospitals managing cancer patients at least a type II pain unit (unit with one or more healthcare providers with different professional training) must be available together with a pain commission and/or tumor committee where oncologists and pain specialists can discuss the management of cancer pain clinical cases. High quality communication and coordination regarding cancer pain management must exist between oncology services www.nature.com/scientificreports/ and pain units. In the case that such pain unit is not available, referral processes to a suitable unit in a different hospital must be in place. Medical oncologist should be familiar with the services available in the referral pain units and both should organize training courses for their healthcare professional and trainees and issue regular updates regarding advances in their fields of practice aiming to keep healthcare professionals well informed and familiar with oncological and cancer pain treatments.
Regarding the referral criteria (Table 2), it appears that there are not clear-cut referral guidelines, as most of the assessed items did not reach consensus. The panelists agreed and advocated ( Table 5) that cancer pain patients should be referred rather early to pain units and, most importantly, those with significant co-morbidities or difficult to manage analgesic treatments. Waiting times for urgent, preferential or routine referrals should be kept short. Moreover, referrals to pain units should be prioritized individually and they should be less than 48 h for urgent patients and less than 7 days for preferential patients. Oncologist and pain specialist should both follow up patients in a consensual manner by establishing appropriate circuits.
The panelists identified various barriers to an adequate management of cancer pain patients and also indicated improvement opportunities ( Table 3). Lack of effective communication amongst healthcare professionals and with patients and their families, insufficient training, experience and skills in cancer and/or pain and their treatments and ignorance of the service portfolio of the pain unit were some of the deficiencies with a negative impact on the management of cancer pain patients.
In order to improve cancer pain care, they prioritized communication and coordination between oncology services and pain units, consultation waiting times reduction, infrastructure improvements and staff expansion www.nature.com/scientificreports/ of the pain units and interdisciplinary committees creation together with establishment of care quality evaluation systems for cancer pain (Table 5).

Discussion
Approximately 10 million individuals are diagnosed with cancer yearly. Almost 70% of them will succumb to their disease or its complications and 60% will suffer from severe pain 14,15 . Epidemiological studies in Spain have also indicated that almost 55% of cancer patients experience pain 16 , frequently neuropathic in origin (20-33%) 17 and 41% of cancer pain sufferers experience breakthrough pain 18 .
Since the introduction of the WHO´s analgesic ladder together with the American Pain Society recommendations on the assessment and quality indicators development for effective cancer pain management, an immense progress in oncological pain control has been achieved 19 . Remarkable efforts to improve pain management quality have been made; however, many cancer patients worldwide have their cancer-related pain inadequately managed 20 , causing poor life quality, anxiety and distress, depression and poor functional status 21 . www.nature.com/scientificreports/ Traditionally, individual healthcare professionals, most often an oncologist, have managed cancer pain. However, cancer pain is complex and dynamic and therefore it requires a more thorough approach to assimilate the knowledge, experiences and skills of all those involved in its treatment via a multidisciplinary process with a shared philosophy, mission, and objectives 22 , preferably in specially created facilities, which allow for flexible collaborative pathways and movements among health care professionals. The International Association for the Study of Pain (IASP) proposed a four types (I-IV) classification of pain units depending on characteristics such as healthcare professionals participation, treatment options available, focus on pain types and education and research provisions 22,23 The panelists agreed ( Table 5) that all hospitals managing cancer patients must have at least one type II pain unit, a service of several unidisciplinary specialists for the treatment of pain and highlighted the importance of being able to refer patient from a unit with less facilities to a better one, where pain can be managed more adequately.
The importance of a multidisciplinary approach to the care of cancer pain has been emphasized by a recent Spanish quality recommendations publication on oncological pain management (Norma ACDON), which besides a shared philosophy, mission and objectives, is characterized by several other aspects: interdependence among team members, mutual respect, open communications, cooperation and diverse viewpoints being some of the most important ones 24 . It is necessary that all teams and disciplines involved collaborate and coordinate their activities and combine their skills and experience effectively towards a common goal. Importantly, a delivery system must be in place, which promotes and facilitates execution 22 .
Both patient-centered care and continuity of care are fundamental for coherent and consistent interventions directed to cancer patients´ medical and personal needs 25 . Constant communication, not only among the team members but also with the patients and their families by encouraging active participation, is a central element for coordinated care and clinical and mental status improvement of the patient by focusing on specific issues furthering common aims and managing pain and possible side effects in a holistic and multidisciplinary way.
Critical for effective communication and collaboration among all those involved in this cancer pain multidisciplinary care is accurate and detailed care documentation, through which, progression towards shared short and long-term management targets can be established. This, together with a proper follow-up schedule is a useful tool to substantiate effectiveness of treatment, detect therapeutic issues and prevent and manage complications and relapses 22 . Shared clinical sessions for cancer pain cases discussion, shared cancer pain management protocols, common referral pathways arrangements and extensive and constant contact possibilities via telecommunication Table 3. Block III results. Barriers and opportunities for cancer pain management improvement. *IQR interquartile rang. www.nature.com/scientificreports/ facilities for case consultation are essential requirements for a high quality care of cancer pain patients and they have been strongly recommended by the panelists ( Table 5). The panelists also identified those patients that may benefit the most by this multidisciplinary approach when treating oncological pain: patients with high doses of opioids, or with hyperalgesia, those that require or may benefit from interventional techniques, those with co-morbidities or important side effects from analgesic treatments and with advanced disease and major pain.

A frequent cause for not referring a patient to the pain unit when there is an indication for it, is
Another area of attention highlighted by our experts was training and education of oncologist and pain healthcare professionals and research ( Table 5). Lack of knowledge regarding cancer treatments and cancer pain management amongst the members of the multidisciplinary team has been reported as a cancer pain poor management factor in clinical practice 8 . Interestingly, often healthcare professionals do not recognize their cancer management knowledge deficits 4 . There is a need for continuing education and training in: pain management techniques (both, pharmacological and interventional), psychological support, pain topics such as controlled analgesia methods, pain evaluation scales, questionnaires for practicing physicians, trainees of medical oncology units and similarly cancer therapeutic modalities and communication skills with cancer patients and their families for the pain services providers, multidisciplinary cancer and cancer pain rounds where cases can be discussed and most importantly familiarity of the involved parties with portfolios of the available services. There are many cancer pain patients who are not referred to pain units even though they could benefit from it Agreement All hospitals that manage cancer patients must have 1. A pain unit of any kind, or failing that, a referral unit in another hospital center, where patients for pain treatment can be referred to Agreement

A hospital oncological pain commission, where members of the oncology services and pain units can participate Agreement
The medical oncology service and the pain unit of a hospital center must have The recommended waiting time for oncology patients between an urgent request from the service of origin and their assessment by the pain unit should be < 48 h Agreement

Shared protocols for cancer pain management
Pain management is never urgent Disagreement The recommended waiting time for a cancer patient between the request for consultation from the service of origin on a preferential basis and its assessment by the pain unit should be < 1 week Agreement The pain follow-up of an oncology patient who is cared for in the pain unit should be carried out by both, the doctor who sends the patient and the pain unit in consensual manner Agreement In such cases that patients with cancer pain need a technique not available in their center they should be referred directly from the pain unit to a unit where this technique is available Agreement www.nature.com/scientificreports/ Deciding who, how and when to refer cancer pain patients to pain units can be quite complex and factors such as resources availability, involved teams capacities, disease characteristics, levels of care provided and health care policies may play an important role 26 . The complexity of this process is also displayed in our panelists' answers, where 41% of the items regarding referral criteria to pain units did not reach consensus.

A frequent cause for not referring a patient to the pain unit when there is an indication for it, is
Referrals to pain units can be either oncologist-driven or automatic. Oncologist-driven referrals require identification of patients with specific symptomatology and care necessities, and are subject to varying thresholds the referring physicians might have depending on their knowledge, experience and skills 27 . Often this referral pattern leads to treatment delays.
In the automatic referral process pre-established criteria act as consultations triggers with pain units depending on patients clinical needs. It appears that this referral pattern has the potential to streamline cancer pain management and, in general, palliative care 28 . The items that reached consensus could be used as the triggering criteria to structure this referral pattern.
As it has been mentioned already, 33% of cancer pain patients are not controlled effectively 2 . Recent studies have identified various barriers to their adequate treatment, such as insufficient understanding and experience with the available therapeutic options and approaches to the evaluation and management of cancer pain, lack of coordination and cooperation amongst the various disciplines involved in the management of these patients, often inadequate pain management resources in cancer units, inefficient communication flows and referral patterns between oncology and pain control units, anxiety for opioid use side effects and patients misconceptions regarding analgesic usage 29 .
Furthermore, barriers in cancer pain management may be related to healthcare professionals, patients themselves or the existing healthcare system (limited access to specialist's services). The most frequently mentioned barrier related to the clinicians is inadequate pain evaluation. Pain assessment can be very subjective and only a small percentage of physicians use the available pain assessment tools (like the visual analog scale VAS) routinely for an accurate evaluation 30 . Clinicians are often reluctant to start opioid treatments and tend to use them only in terminal cancer or intractable pain cases 10 . Finally, lack of specific knowledge concerning medications for chronic cancer pain, pain pathogenesis, dose titration, breakthrough pain, addiction and tolerance appears to be another barrier in the effective treatment of these patients 31 .
Patients´ perspective barriers can be of cognitive or affective nature or related to non-adherence to analgesics. Under cognitive barriers we see situations where painkillers concern and misconceptions lead to pain underreporting, inadequate communication with clinicians and side effects fear, addiction and tolerance 32 . Depression, stress and anxiety are affective barriers that alter pain perception and predict treatment responses 33 . Finally, adherence to pain medication is positively related with better pain control 34 .
A series of interventions have been proposed to overcome all these barriers between oncology and pain management units with the aim to facilitate patient flow, minimize waiting times and achieve adequate cancer pain control: effective pain assessment by using appropriate validating tools and multidimensional evaluations; pain management according to the published guidelines, by using the indicated medications, monitoring outcomes and side effects in a multidisciplinary approach; educating health care professionals and trainees through continuing medical education, lectures and interdisciplinary pain management rounds; educating patients and their families by informing them regarding their disease and appropriate medication use and providing psychosocial  www.nature.com/scientificreports/ support and finally, healthcare system-based issues can be better controlled by increasing pain and palliative services 4 . Our experts have also highlighted the importance of the above interventions during their assessment in order to improve the management of cancer pain and consequently the patients' wellbeing (Table 5).
There are some limitations of our work that ought to be mentioned. The consensus methodology prevents in depth discussions and some matters may be overlooked. In addition, subjectivity linked to personal evaluations may be a problem, and there is a potential bias in the selection of the expert panel. However, panelists were selected taking into account their contrasted clinical experience and expertise in cancer field, and in our opinion their point of view could be helpful for the rest of the health providers. Further studies may be carried out to identify impediments and approaches to overcome these barriers from the point of view of other healthcare professionals such as nurses specialized in cancer or primary care physicians.

Conclusions
In summary, the results of this survey identified patterns of effective collaboration between oncology and pain units, referral criteria regulating cancer pain flow among the involved services in a multidisciplinary way, and the main barriers to optimal cancer pain management. Also practical recommendations to overcome these barriers were proposed. This consensus may be useful for clinicians and health managers to implement measures aimed to improve cancer patients' pain management.