Managing Pain in People with Cancer—a Systematic Review of the Attitudes and Knowledge of Professionals, Patients, Caregivers and Public

Cancer pain is a common symptom experienced by patients, caused either by the disease or its treatment. Morphine remains the most effective and recommended treatment for cancer pain. However, cancer patients still do not receive appropriate management for their pain, and under-treatment is common. Lack of knowledge and negative attitudes towards cancer pain and analgesia among professionals, patients and family caregivers are reported as one of the most common barriers to effective cancer pain management (CPM). To systematically review research on the nature and impact of attitudes and knowledge towards CPM, a systematic literature search of 6 databases (the Cochrane library, MEDLINE, PsycINFO, CINAHL, Web of Science and EMBASE) was undertaken in July 2018. Additionally, hand-searching of Google, Google Scholar and reference lists was conducted. The inclusion criteria were adult (18–65 years of age), studies which included attitudes and knowledge towards CPM, studies written in English, published literature only and cross-sectional design. Included studies were critically appraised by two researchers independently using the Joanna Briggs Institute Analytical Cross Sectional Studies Assessment (JBI-ACSSA). A total of 36 studies met the inclusion criteria. The main finding was that among professionals, patients, caregivers and the public there were similar attitudinal barriers to effective CPM. The most commonly cited barriers were fear of drug addiction, tolerance of medication and side effects of opioids. We also found differences between professional groups (physicians versus nurses) and between different countries based on their potential exposure to palliative care training and services. There are still barriers to effective CPM, which might result in unrelieved cancer pain. Therefore, more educational programmes and training for professionals on CPM are needed. Furthermore, patients, caregivers, and the public need more general awareness and adequate level of knowledge about CPM. Electronic supplementary material The online version of this article (10.1007/s13187-019-01548-9) contains supplementary material, which is available to authorized users.


Introduction
Cancer has become the most common cause of death worldwide [7,86]. It has been estimated that by 2030, there will be about 21.4 million new cancer cases annually, and approximately 13.3 million cancer patients expected to be die from the disease [31]. Pain related to cancer is a common problem that can occur among patients who are having active cancer treatment [47].This can be a result of some complications following treatment of cancer, which can be physical or psychological symptoms [21,73]. The prevalence of cancer pain can be associated with the stage of disease and the location of cancer [36,41]. According to a recent meta-analysis, pain was reported by more than 50% of cancer patients who received anti-cancer treatment and about 66% of patients with advanced and metastatic cancer [26]. Several attempts have been made to establish effective CPM. One of the most important attempts is the Banalgesic ladder,^established by the World Health Organisation (WHO), to manage cancer pain in adult patients [91]. Morphine remains the most effective and recommended treatment for CPM [99,103]. Despite the improving quality of pharmacological options for pain management, several studies have revealed that patients at different stages of their disease still do not receive appropriate CPM [3,18,25,37,52,92]. Lack of knowledge and negative attitudes towards Electronic supplementary material The online version of this article (https://doi.org/10.1007/s13187-019-01548-9) contains supplementary material, which is available to authorized users. CPM among professionals [1,18,80,82,93], cancer patients [61] and family caregivers [79] were reported by recent reviews and studies as one of the most common barriers to effective CPM.
Numerous studies conducted worldwide have assessed independently either professionals', patients', caregivers', or the publics' attitudes and knowledge towards CPM. However, synthesis of these results has not yet been undertaken. Conducting such a review is important as it is now well established from a variety of studies that many common barriers delay the delivery of effective CPM to patients; this could be caused by professionals [9,11,18,24,46,80,83,84], cancer patients [57], caregivers [95] and the general public [51], which is likely to result in inadequate CPM. Thus, the aim of this systematic review is to determine the nature and impact of attitudes and knowledge towards CPM.

Protocol and Registration
The preferred reporting items for systematic reviews and meta-analysis (PRISMA) statement has been used as a guideline for reporting the findings in this systematic review [53,63,85]. The protocol for this review was registered with PROSPERO; the registration number is CRD42018117625.

Adapting PICO into PCO for This Current Systematic Review
The types of studies, participants and interventions, as well as the types of outcome measures (PICO) will be modified to PCO (population, context and outcome) as there are no interventions or comparisons needed. [78,89]. For more details, see Table 1.

Eligibility Criteria: Population, Context and Outcome
The inclusion and exclusion criteria are listed in Table 2 Search Strategy for Identification of Studies In this systematic review, we searched 6 electronic databases (the Cochrane library, MEDLINE, PsycINFO, CINAHL, Web of Science and EMBASE) in July 2018. Additionally, handsearching of Google, Google Scholar and reference lists was conducted. The search terms were based on population, contexts (context pain, context opioids and context cancer) and outcome [16]. To identify publications for inclusion in the present systematic review, the keywords employed were as shown in Table 3. For more information regarding search strategy, see Appendix 5.

Data Extraction
The data extraction form was developed and piloted independently by two reviewers (SM & SP). A third reviewer (MB) was involved to reconcile any disagreements. Using data extraction forms can potentially reduce bias and improve validity and reliability [17]. In this review, the data extraction form was adapted from Centre for Reviews and Dissemination, University of York [17] (see Appendix 1). The extraction of data from the included studies was based on the names of authors, year, country of publication, design of study, the aim of study, sample size, the setting of study, mean age, sex ratio, type of measurements, type of sample, type of cancer, main findings and the quality of study as outlined in Table 4.

Quality Assessment of the Included Studies
The reason for using a critical appraisal process for the included studies was that studies can be published with variable levels of methodological rigour and therefore their results could be unreliable [15]. It has been strongly recommended that the assessment of quality should be done separately by at least two reviewers [56,64,72,90]. Accordingly, all 36 included studies have been critically apprised by two researchers (SM & SP) independently using the Joanna Briggs Institute Analytical Cross Sectional Studies Assessment (JBI-ACSSA) (see Appendix 2). To reconcile any differences, a third reviewer (MB) was involved. The JBI-ACSSA tool was chosen as it is appropriate for the study design of included quantitative studies [64,90]. The assigning score for the quality of the data was performed as 1 point for each applicable item with a score of 7 as the maximum score [74]. An overall score was calculated for each included study and the rating of quality was judged as good (6/7 and 7/7), fair (3/7 to 5/7) or poor (< 3/7) [35] (see Appendix 3). No score was below 3/7, so no study was excluded based on the quality assessment only.

Information Sources and Study Selection
The total number of studies identified by 6 electronic databases (the Cochrane library, MEDLINE, PsycINFO, CINAHL, Web of Science and EMBASE) was 6830 articles (see Appendix 5). In addition, 17 studies were identified by hand-searching (including Google, Google Scholar and checking the reference lists). Among these 6847 studies, 5650 articles were included after the duplicate studies were removed. Among the 5650 included studies, 5523 studies were excluded after the title and abstract of each study were carefully reviewed. The total number of full-text articles assessed for eligibility was 133. A further 97 studies were excluded and all full references of these excluded articles and the reasons for exclusion are listed in Appendix 4. Consequently, a total number of 36 studies were included in this review as illustrated in Fig. 1.

Characteristics of Included Studies
The 36 studies included in this review used a cross-sectional design, employing various questionnaires, to assess knowledge of and attitudes towards CPM. The studies were based in 18 countries. The characteristics of included studies are illustrated in Table 4.  [2]. Another example [20] is that more than 50% of Turkish patients refused to receive strong opioids, such as morphine, and 36.8% of them preferred another (nonopioid) medication for managing their cancer pain.

Professionals' Knowledge and Attitudes Towards CPM
Several studies showed that physicians had better knowledge and attitudes towards CPM compared with nurses [22,32,44,45]. For instance, it has been reported that physicians who work at oncology units had higher understanding and knowledge about CPM than nurses. The mean scores on the KAS (range 0-39) for physicians was 24.3 (62.3%) compared with 20.08 (51.5%) for nurses (p < 0.001) [22]. The outcomes also showed that oncologists recorded higher knowledge of CPM than surgeons (p < 0.001) [33]. An interesting finding, which was reported by McCaffery and Ferrell [59], is that Canadian Not include adults (n= 5).
Same data were used in another study (n=2).

Included
Records screened based on title and abstract (n= 5650)                and American nurses were more likely to use morphine for CPM than nurses in Japan or Spain. For example, 71.5% of Canadian nurses and 66.3% of nurses from America reported using morphine for managing cancer pain, compared with 61.6% of Japanese nurses and 51.2% of nurses from Spain [59]. The results also revealed that there was a degree of misunderstanding regarding opioid addiction by nurses between countries. For instance, the majority of nurses who answered the relevant questions correctly were from Canada and the USA (51.3% and 43.4%), respectively, whereas, only 14% of Spanish nurses and 17.2% of Japanese nurses responded correctly [59]. Another interesting observation to emerge from the results was that there were geographical variations within countries, for example, the nurses who worked in the central region of Italy had lowest score of pain knowledge (

Family Caregivers' Knowledge and Attitudes Towards CPM
A study revealed that caregivers' attitudes towards CPM and the patients' pain knowledge explained 23.2% of the total variance in the patients' average scores for their attitudes towards CPM when entered into a regression equation [57]. This indicates that patients' attitudes towards CPM were influenced by their caregivers' attitudes and the patient's pain knowledge [57]. The results from a study conducted in Taiwan indicated that family caregivers held some moderate to strong concerns towards CPM. These concerns were shown through the Barriers Questionnaire-Taiwan (BQT) survey (ranged 0-5) as follows: disease progression (3.82), side effects (3.29), given as needed (p.r.n) (3.01), tolerance (2.96) and addiction (2.67) [55].
The results also showed some family caregivers reporting their hesitation to administer opioids and to report pain to their patients during the preceding month, because caregivers believed that opioids would cause constipation and harm to patients' kidneys [55]. Surprisingly, there were also similar concerns towards CPM by caregivers in China, where these concerns were shown as higher or lower in some dimensions; tolerance (3.74), given as needed (p.r.n) (3.51), addiction (3.43), disease progression (3.27) and side effects (3.22) [57]. However, these concerns were lower in the USA, indicating that caregivers in the USA might have a good level of knowledge and positive attitudes towards CPM compared with caregivers in Taiwan and China. For example, the areas of concern for caregivers in the USA were about opioid-related side effects (2.41), fears of addiction (2.35), disease progression (2.28) and tolerance (1.37) [95].

General Public's Knowledge and Attitudes Towards CPM
The results from 472 general public respondents in the USA who had not been diagnosed with cancer showed that 18% indicated they would avoid seeking care because of concerns about pain associated with cancer treatment. Fifteen percent of the sample agreed or strongly agreed if they had cancer their fear of the disease would make them seek medical care, whereas 9% of them agreed or strongly agreed their concern about cancer pain would lead to avoidance of medical care [51]. The most common key concern among the general public in the USA that would affect them if they had cancer was the Bpotential for upset to their family^, followed by concern about the Bpossibility of dying of cancer^. Nearly 50% reported a significant concern about pain resulting from both the cancer and the process of its management [51]. The study also reported that 62% of the general public believed that pain is usually associated with disease progression, 57% thought that cancer patients usually die with a painful death and 50% had significant concerns about opioid side effects including confusion or disorientation, tolerance and opioid addiction [51].

Discussion
We aimed to systematically review research on the nature and impact of attitudes and knowledge towards CPM. Overall, the results of this review show that a majority of included studies indicated similar attitudinal barriers to effective CPM shared across patients, caregivers, professionals and the public. The barriers most commonly cited by professionals [11,22,28,44,48,59,98,100], patients and their caregivers [20,55,57,95] and the general public [51] were the fear of poor tolerance, side effects of opioids and drug addiction. However, the most common barriers cited by professionals were contrary to other similar studies, which have suggested that the most important barriers were poor assessment of pain and its management, patient reluctance to take opioids and inadequate staff knowledge of CPM [14,22,27,32,34,44,45,104]. Furthermore, a previous systematic review by Jacobsen et al. [42] showed that physicians from countries, such as some states in the USA, Australia and Denmark were more often prescribing strong opioids in efficient doses, as they were less concerned about opioid addiction [42]. Nonetheless, their general findings were that physicians consistently reported being concerned about high doses of opioid and the fear of side effects, and these fears were common reasons for reluctance to prescribe adequate amounts of opioids for managing cancer pain [42]. It can thus be suggested that people from different countries have different attitudes and knowledge towards CPM. One interesting finding was that the results from the majority of studies with cancer patients showed low mean scores on patient's knowledge and attitudes towards CPM [19,20,57,77]. This result may be explained by the fact that many patients could be reluctant to report their pain to professionals because they have a mistaken belief regarding opioid medication [68]. This finding was also reported by a systematic exploratory review by Jacobsen et al. [43]. Another important finding was that negative attitudes towards morphine were shown by Turkish patients as they continued rejecting morphine for their cancer pain after sessions about opioids were given. The reasons for that were due to fear of addiction, religious reasons and cultural prohibitions [20,58]. Silbermann and Hassan [88] stated that patients' response to cancer can differ based on the patients' beliefs and culture. It has been argued that many patients and their family caregivers viewed opioid medications as a path to death; accordingly, opioid analgesics became their last choice [87]. Despite pain being considered an individual experience, many patients are influenced by their culture, mainly when they are interpreting their pain or accepting the medication of CPM [5,23,65]. Therefore, understanding patients' culture and beliefs can provide the professional with a consideration into how cancer is viewed by the patient [88]. However, professionals can also be influenced by their culture, as it has been reported that cultural beliefs among professionals were one of the most obviously identified barriers towards CPM [80].
Another interesting outcome was that several studies showed physicians had a better level of attitudes and knowledge towards CPM than nurses [22,32,44,45]. There was also a difference between oncologists and surgeons regarding their level of knowledge about cancer pain and its management [33]. It seems possible that these results are due to work experience and training in CPM, as many studies have shown that working with cancer patients' care and receiving training in CPM can improve professionals' knowledge and attitudes towards CPM [29,38,40,44,50,67,94,100].
Most notably, there was a variation between nurses from different countries regarding the level of knowledge and attitudes towards CPM [59]. As could be expected, the variation in knowledge about CPM among those nurses could indicate that morphine is under-prescribed. This view was supported by a systematic review by Oldenmenger et al. [68] who reported that the rates of adherence to opioids for CPM varied from 20 to 95%, with the majority of cancer patients taking their treatments only as needed.
The results also showed that some oncology nurses had an incorrect self-evaluation about their knowledge in CPM [11,102]. This finding is consistent with that of Omran et al. [70] who also found that Jordanian oncology and non-oncology nurses have a low level of knowledge about CPM. In contrast to earlier findings, several studies indicated that the oncology nurses and doctors achieved higher scores on the knowledge and attitudes surveys (KAS) compared with general nurses and physicians [33,44,50,84,94]. These positive results could be due to the work experience of professionals in cancer pain settings, as this was reported by McCaffery and Ferrell [59] who stated that nursing staff from countries such as Canada and the USA, which have the longest experience of palliative care units, showed a better level of attitudes and knowledge about CPM than nurses from countries (Japan and Spain) that had palliative care services more recently.
However, it seems that direct experience in oncology units without education and training is not enough to increase professionals' knowledge about CPM. This view was supported by Bernardi et al. [11] who reported that the years of experience of cancer nurses were not related to pain knowledge scores (p = 0.2). It is possible therefore that education in CPM is the key issue for improving the professionals' level of knowledge and attitudes towards CPM. A number of authors have considered the effects of educational interventions on professionals' attitudes and knowledge towards CPM [4,6,9,12,49,70,71]. According to previous systematic reviews of educational interventions aimed to improve CPM in different settings, a significant effect was shown on pain scores, however, the quality of opioid prescription and interference from pain in daily activities was not affected by the majority of interventions [4,6,8,69].
As could be expected, lack of professional education and training in CPM could be one of the most important key barriers for physicians and nurses [34,39]. Furthermore, this was reported as the highest physician barrier to morphine usage in clinical practice [100]. Another argument was that professionals with cancer patients' care need professional teaching regarding CPM, which could aid patients in reporting pain and in effectively using the opioids that are prescribed to them [39,97]. It is also well documented that there is less than optimal pain management for patients with cancer as a result of a lack of professional healthcare education about CPM [18,60]. Numerous studies have showed that professionals who had experience in palliative care units, receiving training and high level of education in CPM obtained higher scores on the knowledge of cancer pain and its management [45,49,70,71,94,100].
Several studies have shown that caregivers had low level of knowledge and attitudes towards CPM [55,57,95]. These negative attitudes and inadequate knowledge by caregivers towards opioids could result in attitudinal barriers towards effective CPM [30,54,55]. Therefore, it has been argued that it is important to increase caregivers' ability to participate in CPM and enable them to assess pain and to help their patients take adequate doses of opioids [101]. The correlation between caregivers' attitudes and their patients' pain knowledge towards CPM is interesting because patients' attitudes towards CPM were influenced by their caregivers' attitudes and the patient's pain knowledge [57]. Therefore, caregivers should have general awareness and adequate level of knowledge about CPM. It has been argued that caregivers with higher pain management knowledge had significantly fewer barriers to CPM [95].
Results from a study on the general public showed that many people were concern about disease progression and believed that pain was usually associated with this concern. However, some of the public had significant concerns about opioids side effects, tolerance and addiction [51]. Surprisingly, only two studies were found on the general public's attitudes and knowledge towards CPM and both of articles were published before 2000, consequently updated studies about this area are needed.
Overall, the results of this review have found some evidence that there are negative attitudes and lack of knowledge towards CPM among the four groups included in this review. These findings are consistent with those of recent studies and systematic reviews [12,13,20,26,37,79,80,96]. Thus, it can be argued that due to these negative attitudes and lack of knowledge towards CPM, the management of cancer pain remains a major problem worldwide, especially in countries within Europe, Africa and Asia [13,26,52,75,76,81,92]. These could be due to lack of education and training about CPM among professionals and lack of general awareness and adequate level of knowledge about CPM among patients, caregivers and the public, as these were stated in all of the included studies. Therefore, healthcare professionals expressed a desire for additional education and training on CPM. A recent systematic review indicated that educational programmes on CPM, including CPM topics in nursing curricula, and training programmes on CPM are the most important factors for enhancing nurses' knowledge and attitudes towards CPM [12]. It has also been argued that nurses who had received educational programmes on CPM reported significantly higher mean of scores on knowledge about CPM than those who did not have pain education (M = 22 versus M = 20; p = 0.02) [11].
Furthermore, patients, caregivers and the public need general awareness and adequate level of knowledge about CPM. A systematic review reported that providing educational sessions on CPM can improve caregivers' knowledge and reduce their attitudinal barriers towards CPM [62]. Regarding the general public's views, it is expected and inevitable that the general public will know very little about CPM unless they have cancer or someone close to them does. Thus, general awareness and adequate level of knowledge about CPM are needed.

Limitations
As only studies published in English were considered within the inclusion criteria, as well as just published studies, it is possible that there are studies that have been published in other languages, also unpublished articles that could have been included in this review. Other limitations could be that even though all included studies used the same design (cross-sectional design), the questionnaires that were used to conduct surveys in this particular area were different and some studies did not state which questionnaire was used or failed to provide information regarding the validity of the tools. Therefore, it was difficult to directly compare studies and the reliability of these included studies in this review could be compromised [74,90]. In the quality analysis, 15 of the 36 included studies were judged to be only fair quality (see Appendix 3). The reason for a fair quality score instead of a good quality score is that these articles had some methodological limitations. However, almost two-thirds of the included studies, 25 out of the 36 (69.44%), were rated as of good quality. Included studies were from high and low income countries and thus different healthcare systems and cultural beliefs across people form these countries could have affected their attitudes and knowledge towards CPM. Moreover, the possibility of bias could have happened during the reporting of outcomes.

Implications for Clinical Practice
Healthcare professionals should follow specific guidelines for CPM, which have been established by WHO [91] and NICE [10,66]. Moreover, knowledge and attitudes of professionals need to be improved by intensive training on opioids and educational interventions about cancer pain and its management in order to have effective CPM. Likewise, patients, caregivers and the public will need different approaches to improve general awareness and obtain an adequate level of knowledge about CPM.

Implications for Research
All studies included in this review were quantitative studies. More in-depth understanding of the conceptions and attitudes towards CPM can be provided by qualitative studies [93]. Additionally, qualitative methods could help to identify the factors which can influence the professionals, cancer patients, caregivers and the general public's attitudes and knowledge towards CPM [93]. Furthermore, more updated studies within CPM are needed to generate more contemporary data in this area.

Conclusions
This systematic review confirms that there are still barriers to effective CPM by professionals, patients, caregivers and the general publics' lack of knowledge and/or poor attitudes towards CPM, which might result in unalleviated cancer pain. More detailed understanding of how these attitudes arise within different contexts and tailoring educational initiatives to address these are likely to have most impact on improving CPM.