Introduction

Cancer is a devastating diagnosis equally for patients and their families1. Cancer diagnosis is almost always synonymous with pain, which affects life quality of patients, their family and caregivers2. Pain can be present even in early disease stages and its frequency and intensity increase progressively affecting almost 90% of patients during its late stages3,4. Effective pain treatment is essential in the overall management of cancer patients and the importance of controlling cancer pain effectively cannot be overemphasized5. Aggressive and meticulous pain control prolongs cancer patients’ survival6.

Many patients still suffer from significant amount of pain, as analgesic treatments might be inadequate7. Interestingly, this lack of adequate pain control either due to cancer or its complications or its association with surgical procedures did not improve significantly over the years8. Ineffective cancer pain control is a multifaceted issue and its adequate evaluation depends on a collaborative interaction between patients and healthcare professionals.

Pain is subjective and, often, patients do not emphasize it adequately believing that their doctors will divert their attention to the symptom rather than focusing on main disease treatments9. Also health care professionals have often limited knowledge and skills when using opioids, a cornerstone in the pharmacotherapy of cancer pain, which together with local opioid accessibility problems, contributes importantly to the under management of the symptoms.

Recent surveys have identified a need for education regarding pain practices amongst the various professionals involved in cancer pain treatments10. A review published by Kwon regarding barriers in cancer pain management highlighted important topics like opioid rotation and appropriate breakthrough pain handling as suitable educational targets to improve outcomes4.

Cancer pain management can be quite complex because pain is often accompanied by emotional problems and a variety of other symptoms. Therefore, a multidisciplinary approach is required to assess and manage patients suffering from it11. An extensive collaboration and coordination amongst providers and optimal use of available therapeutic options are necessary, together with accurate technical information exchange and frequent communication flow amongst not only the health care professionals involved in the management of cancer pain but the patients as well12.

Our aim was to outline current trends in oncological pain management, recognize barriers and recommend measures to improve the situation by:

  1. 1.

    Identifying the necessary resources that an institution or clinical service should be equipped with to effectively manage cancer pain patients.

  2. 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. 3.

    Introducing training opportunities for the health care professionals handling cancer pain cases to improve therapeutic outcomes and consequently life quality of affected patients.

Methods

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 consensus13. 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).

Table 1 Block I results.
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Table 2 Block II results.
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Table 3 Block III results.
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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 4 Results with maximal consensus.
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Table 5 summarizes the main statements agreed by the panelists and shows recommendations on the monitoring of the disease.

Table 5 Recommendations.
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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 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 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 pain14,15. Epidemiological studies in Spain have also indicated that almost 55% of cancer patients experience pain16, frequently neuropathic in origin (20–33%)17 and 41% of cancer pain sufferers experience breakthrough pain18.

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 achieved19. Remarkable efforts to improve pain management quality have been made; however, many cancer patients worldwide have their cancer-related pain inadequately managed20, causing poor life quality, anxiety and distress, depression and poor functional status21.

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 objectives22, 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 provisions22,23 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 ones24. 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 execution22.

Both patient-centered care and continuity of care are fundamental for coherent and consistent interventions directed to cancer patients´ medical and personal needs25. 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 relapses22. 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 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.

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 practice8. Interestingly, often healthcare professionals do not recognize their cancer management knowledge deficits4. 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.

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 role26. 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.

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 skills27. 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 care28. 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 effectively2. 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 usage29.

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 evaluation30. Clinicians are often reluctant to start opioid treatments and tend to use them only in terminal cancer or intractable pain cases10. 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 patients31.

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 tolerance32. Depression, stress and anxiety are affective barriers that alter pain perception and predict treatment responses33. Finally, adherence to pain medication is positively related with better pain control34.

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 support and finally, healthcare system-based issues can be better controlled by increasing pain and palliative services4. 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.