ORIGINAL RESEARCH published: 20 November 2020 doi: 10.3389/fneur.2020.592366 Pain in Older Adults With Dementia: A Survey in Spain Lydia Giménez-Llort 1,2*, Maria Luisa Bernal 3,4 , Rachael Docking 5 , Aida Muntsant-Soria 1,2 , Virginia Torres-Lista 1,2 , Antoni Bulbena 1 and Patricia A. Schofield 5,6 1 Department of Psychiatry and Forensic Medicine, Universitat Autònoma de Barcelona, Cerdanyola del Vallès, Spain, 2 Institut de Neurociències, Universitat Autònoma de Barcelona, Cerdanyola del Vallès, Spain, 3 Department of Pharmacology and Physiology, University of Zaragoza, Zaragoza, Spain, 4 Instituto de Investigación Sanitaria de Aragón, Zaragoza, Spain, 5 Abertay University, Dundee, United Kingdom, 6 Sheffield Hallam University, Sheffield, United Kingdom The risk of suffering pain increases significantly throughout life, reaching the highest levels in its latest years. Prevalence of pain in nursing homes is estimated to range from 40 to 80% of residents, most of them old adults affected with dementia. It is already known that pain is under-diagnosed and under-treated in patients with severe cognitive impairment and poor/absent verbal communication, resulting in a serious impact on their quality of life, psychosocial, and physical functioning. Under-treated pain is commonly the cause of behavioral symptoms, which can lead to misuse of antipsychotic treatments. Here, we present two Regional and National Surveys in Spain (2015–2017) on the current practices, use of observational tools for pain assessment, guidelines, and policies. Edited by: Maria Tiziana Corasaniti, Results, discussed as compared to the survey across central/north Europe, confirm University of Catanzaro, Italy the professional concerns on pain in severe dementia, due to poor standardization and Reviewed by: lack of guidelines/recommendations. In Spain, observational tools are scarcely used Elisabetta Farina, because of their difficulty and low reliability in severe dementia, since the poor/absent Fondazione Don Carlo Gnocchi Onlus (IRCCS), Italy verbal communication and comprehension are considered limiting factors. Behavioral Carlo Caltagirone, observation tools should be used while attending the patients, in a situation including Santa Lucia Foundation (IRCCS), Italy rest and movement, should be short (3–5 min) and scored using a numeric scale. *Correspondence: Lydia Giménez-Llort Among the pain items to score, “Facial expression” and “Verbalization” were considered lidia.gimenez@uab.cat essential and very useful, respectively. This was in contrast to “Body movements” and “Vocalizations,” respectively, according to the survey in central/north Europe. Specialty section: Scarce time availability for pain assessment and monitoring, together with low feasible This article was submitted to Neurorehabilitation, and time-consuming tools, can make pain assessment a challenge. The presence of a section of the journal confounding factors, the low awareness and poor knowledge/education of specific Frontiers in Neurology tools for this population are worrisome. These complaints draw future directions to Received: 11 August 2020 Accepted: 19 October 2020 improve pain assessment. More time available, awareness, and involvement of the Published: 20 November 2020 teams would also benefit pain assessment and management in cognitive impairment. Citation: The experiences and opinions recorded in these surveys in Spain and other E.U. Giménez-Llort L, Bernal ML, countries were considered sources of knowledge for designing the “PAIC-15 scale,” a Docking R, Muntsant-Soria A, Torres-Lista V, Bulbena A and new internationally agreed-on meta-tool for Pain Assessment in Impaired Cognition and Schofield PA (2020) Pain in Older the “Observational pain assessment” in older persons with dementia. Adults With Dementia: A Survey in Spain. Front. Neurol. 11:592366. Keywords: pain, dementia, elderly, pain assessment, pain management, International “IR” framework, guidelines, doi: 10.3389/fneur.2020.592366 impaired cognition Frontiers in Neurology | www.frontiersin.org 1 November 2020 | Volume 11 | Article 592366 Giménez-Llort et al. Pain Assessment in Dementia INTRODUCTION throughout the disease until they are completely absent in the more advanced stages. In this scenario, it is important to note Pain is, in all cases, a threat to human dignity, and when that agitation, shouting, aggression, and increased irritability are it comes to avoidable pain in those who cannot properly common ways for patients with dementia to express discomfort think or speak for themselves, we find ourselves faced with an and pain. If the latter is the case, the use of antipsychotics imperative to join efforts to improve the situation. The risk of to manage the expression of these neuropsychiatric (NPS) or suffering pain increases significantly throughout life, reaching behavioral (BPSD) symptoms could be inappropriate. Atypical the highest levels in its latest years. It is estimated that pain antipsychotics are associated with a significantly greater mortality exists in 50% of community-dwelling older adults, while the risk than placebo (15). Increased mortality risk has also been prevalence in nursing homes is estimated to range from 40 to described in cerebrovascular adverse events in elderly users of 80% of residents (1). These rates indicate a serious impact on antipsychotics (16). Therefore, improvement in pain assessment the quality of life and psychosocial and physical functioning. in the elderly demented patients is important for the proper Although pain is a frequent complaint in residents at nursing pharmacological pain management in this population (17, 18). homes, 25% do not regularly receive pain-relieving drugs (2). Currently, the use of antipsychotics and opioids and in elderly The administration and prescription of pain treatment occur with dementia to treat BPSD is an important topic in the below the experts’ recommendations (3). In the older population, pharmacological management of Alzheimer’s disease (19). factors of pain management that can explain this situation In this regard, a series of specialized tools have been developed are five. First, less self-report of pain. Second, pain is often since the early 1990s to assess pain in community and nursing present along with multiple problems and comorbidities that homes, particularly in patients with communication difficulties complicate evaluation and treatment. Third, increased incidence especially dementia (20). The pros and cons of these scales are of side effects. Fourth, a greater potential for adverse effects and already well known in the forums on this topic. However, due complications secondary to treatment procedures. Finally, older to the lack of internationally coordinated research to validate adults and health professionals often assume that pain is part these scales and select the best available solutions, almost every of aging. hospital/clinic and each research center favors its scale. At best, While pain in older adults appears to be a challenging problem the consistent practice has been developed at the national level for many health care professionals, it seems that pain in older and is only described in national guidelines (21). Since age is the adults with dementia is even more so (4). Over 50–60% of the main risk factor for dementia and pain, it is expected that the older population living in care homes in developed countries number of patients with dementia and so much pain will also are affected by dementia (5), while the impact of dementia in grow. These combined circumstances are of great socio-health low-to-middle income countries should not be underestimated relevance since when dementia and pain concur, their individual [i.e., (6)]. About 50% of the 35 million people with dementia and social impact multiply and require transnational solutions. worldwide experience pain on a regular basis. The global burden It is not just that there is already evidence that pain is poorly associated with the aging population projected to happen in treated in dementia. Other questions, which also require an the coming decades demands efforts to counteract its socio- urgent response, are those regarding neurophysiological aspects economic impact but, mostly, on the quality of life of patients, of pain in dementia and pain management throughout the caregivers and families (7). disease, including end-of-life dementia stages. For now, the In fact, there is no evidence to suggest that older adults with lack of validated pain assessment tools in older people with dementia experience less pain than do those without dementia cognitive damage, especially dementia, has thus far impeded (8). Thus, pain in dementia patients is assumed to be at least important advances. as prevalent as in cognitively healthy individuals of the same The COST (European Cooperation in Science and age. The impact that dementia and other types of cognitive Technology) Action TD1005 “Pain Assessment in Patients damage have on the perception and expression of pain has been with Impaired Cognition, especially Dementia” led by Stephan scarcely studied, except in Alzheimer’s disease (9, 10). In this Lautenbacher was established to address the issues related to common form of dementia, extensive evidence indicates that pain assessment and dementia [(20), see also Table 1]. The major pain sensitivity is not only intact but may even be increased. In aim was to develop PAIC, a comprehensive and internationally vascular dementia, the prevalence of pain may be even higher agreed-on assessment toolkit for older adults targeting the due to a promotion of neuropathic pain (11). However, the various subtypes of dementia and various aspects of pain, latest studies indicate that pain is underdiagnosed and under- including pain diagnostics, cognitive examination and guidelines treated in people with cognitive damage, especially dementia for proper assessment. In this context, Working Group 2 (12, 13). Thus, dementia patients receive even less pain treatment (WG2) developed a survey that was designed to explore the than individuals without cognitive impairment, as observed in existing use of pain assessment tools and guidelines and develop many studies. The exact reasons for this poor treatment of an understanding of the practical considerations required to dementia patients have yet to be determined (14). One of the facilitate their use within clinical settings. This survey was most probable reasons for under detection of pain is because, conducted across the central European participating countries, nowadays, the diagnostic tools of pain, their classification, including questions about participants’ knowledge and use of and evaluation, depend largely on self-reports that require the existing pain assessment guidelines, the usage of existing pain intact cognitive and communication skills. Both abilities are lost assessment (observational tools) and the experience health Frontiers in Neurology | www.frontiersin.org 2 November 2020 | Volume 11 | Article 592366 Giménez-Llort et al. Pain Assessment in Dementia TABLE 1 | State-of-art of challenges in pain assessment and management in the instruments and professional’s profile” set up by the members elderly and people with cognitive impairment, especially dementia. of WG2 of the COST Action TD1005 (22) was translated Challenges pain management in aging and cognitive impairment into Spanish using a backward, forward procedure. Minor modifications were necessary to clarify aspects of the different Conditionants of pain management in the elderly levels of qualifications and healthcare settings. 1. Worse self-report The WG2 developed the survey questions in English. The 2. Pain is comorbid to pluripathology and comorbidities that complicate the survey’s focus was to explore practitioners’ current use and evaluation and treatment 3. More incidence of side effects + more potential for adverse effects and opinions on the usefulness and usability of existing tools to iatrogenesis due to the procedure of treatments identify attitudes toward assessment tools and possible barriers High prevalence, needs and challenges pain diagnosis in cognitive impairment to their implementation. 1. Epidemiology: 80% in nursing homes, 50% at home are in pain Together with sociodemographic data, the survey included 2. Cognitive decline associated to aging/MCI/Neurodegeneration both open-ended and multiple-choice questions about 3. Pain = Discomfort + Burden physical-phychological-social levels 4. Infra-diagnosed participants’ knowledge, use of existing pain assessment 5. Infra-treated tools, and the experience healthcare professionals have of using 6. Loss of verbal communication these tools in daily practice. 7. Equal detection – pathology and stage of dementia influence the perception of The instrument contained 36 questions. In Spain’s final pain and the pain related behavior instrument, five more questions were added to record the level 8. Higher tolerance 9. NPS/BPSD – pain manifests as agitation, shouting, aggression of confidence the professionals had on the scales and their 10. Scales proxi behavior of pain: possible presence/absence, intensity, ability to score pain in patients with no cognitive impairment, behavior frequency, six behavioral dimensions mild cognitive impairment or dementia, and moderate/severe FACS, vocalization, body movements, behavioral changes, cognitive impairment or dementia. physiological changes, physical changes The National Survey was sent online to the sampling frame Key words are indicated in bold. NPS/BPSD, Neuropsychiatric symptoms/Behavioral and consisting of all the hospitals registered at the Spanish National Psychological Symptoms associated to Dementia; FACS, Facial Action Coding System. Health System. An opportunistic sample of nursing homes and day care centers was also included. The survey was conducted care professionals have of implementing the tools. Recently, between February 2015 and November 2017. this survey results in central-north Europe have been reported (22), and here we present the results from southern Europe (Spain). The preliminary analysis on one of the “open questions” DATA COLLECTION regarding the professional concerns on problems experienced in Spain and solutions for its improvement was presented for The National Survey used a probability sample of healthcare discussion with the scientific community of the International professionals. As in the previous study (22), a sample size Psychogeriatric Association in our last IPA International calculation was not performed since the study aimed to describe Congress (23). In the present work, the results of that question the currently used guidelines or observational tools for pain have been further analyzed. assessment amongst older adults with cognitive impairment. Therefore, the aims of the present study were three. First, The response rate was very low, with no answers from the to conduct a preliminary survey in Spain to estimate the southern part of the country. Three rounds of submissions were implementation and use of pain scoring systems in old patients performed. Besides, targeted strategies were adopted to circulate with dementia and their reliability. Second, to survey on the use the link for the web-based questionnaire. Thus, the survey of standards and guidelines for pain assessment in people with was also announced on the COST-Action TD1005 website and cognitive impairment/dementia in Spain and, particularly, of the distributed via the newsletter of other health and mental health use of behavioral assessment scales. Finally, to obtain a detailed professional groups: Sociedad Española de Infermería Geriátrica analysis of the current problems that health/care staff encounter (Spanish Society of Geriatric Nursery), Master in Psychogeriatry and, learning from their experience and opinion, what would UAB, CORE Salut Mental de Catalunya, Germanes Hospitalaries help improve their management. del Sagrat Cor de Jesús de Martorell, UVaMiD Unitat de Valoració de la Memòria i la Demència a Salt - Girona, and Instituto Aragonés de Salud. Respondents were not required METHODS to enter their names in the survey, and therefore it was completed anonymously. Respondents had the opportunity to In the Preliminary Regional Survey, a short online questionnaire stop completion of the survey at any moment, which could result consisting of the “General information about professionals and in an incomplete survey. patients” of the PAIC study was sent to an opportunistic sample of healthcare professionals (nurses and physicians) from hospitals, nursing homes, and daycare centers in Catalonia, ANALYSIS Aragón and Comunitat Valenciana, three neighboring Spanish autonomous communities. Quantitative data were analyzed using SPSS version 25, and After this preliminary survey, the self-administered descriptive statistics were performed. For the multiple-choice “Questionnaire about the use of standards/guidelines, answers, valid percentages were used given the variation in the Frontiers in Neurology | www.frontiersin.org 3 November 2020 | Volume 11 | Article 592366 Giménez-Llort et al. Pain Assessment in Dementia number of responses per question. The open-ended questions Pain Education were analyzed using content analysis. The comments to the open- Only 14% of participants have ever received post-registration ended questions were analyzed using deductive classification and education relating to pain assessment in people with cognitive superordinate categories created with an open matrix (24). A impairment. Similarly, only 19% reported that case conferences consensual agreement was evaluated by having a peer group or multidisciplinary team meetings are held about managing reviewing the data to verify the responses on the open-ended pain in cognitive impairment. Accordingly (see Figure 2A), 58% questions and categories. In case of disagreement between the of professionals reported feeling very (32%) or slightly (27%) two researchers, it was agreed upon to discuss the differences and dissatisfied with their knowledge about this important issue, seek for consensus. despite their efforts to do it well, paying special attention and taking into account the family and caregivers reports. Thus, there are few opportunities for multidisciplinary team meetings or specialized pain education, mostly thanks to pain committees RESULTS and online courses of pain education for health professionals. However, health professionals that received them reported high Preliminary Regional Survey satisfaction with their knowledge and management of pain. In the preliminary regional survey, 64 professionals from Catalonia, Aragón, and Comunitat Valenciana answered the questionnaire; they were mostly women +30 years old, mainly Use of Standards/Guidelines physicians and nurses. Of both sexes, their patients were mostly On the use of rules and guidelines, self-reporting pain assessment +60 years old, diagnosed with Alzheimer’s disease, vascular, or tools were the most recommended (50%) for people able to mixed dementias and + 3Reisberg GDS stage. The duration of use self-report (i.e., with mild dementia/cognitive impairment) acquaintance with the patients was high since most of them (Figure 3A). However, a high percentage (35.7%) of their were institutionalized patients. The 51.6% of professionals asked institutions do not recommend a tool (Figure 3A); this increased scored their capacity to evaluate pain between 7 and 8, with to 59% for those unable to use self-report (Figure 3B). nurses self-reporting a higher score than physicians. 59.7% of Interestingly, behavioral/observational instruments (e.g., Abbey, professionals use pain scale (mostly EVA and observational PainAD) were poorly recommended in people with dementia scales), being bit more used in nursing homes than in hospitals. with mild (12.5%, Figure 3A) to moderate/severe conditions Forty-five percentage of professionals used the pain instruments (17%, Figure 3B). daily or at least once per week. Overall, the reliability given to In fact, when asking about the source of recommendations, the scales was 1 or 2 ranks lower than for their own professional the participants informed that the use of national/international ability to detect pain in the patients (Figure 1). standards/guidelines in their institutions or the existence of local policies for pain assessment in people with cognitive impairment associated to dementia was poor (Figure 4A). Thus, more than Participants in the National Survey half of professionals (65%) indicated no guidelines or local policy The results summarize the answers of 64 Spanish health (48%) or did not know if their institution had any (17%), in professionals working with older people with cognitive contrast to that 35% of professionals that use a local policy impairment (dementia). Despite respondents having the and/or national/international guidelines (Figure 4A). The ratio opportunity to stop completing the survey at any moment, which of organizations reporting auditing pain assessment in older could result in an incomplete survey, all the submissions were people with dementia was low, as it could only be confirmed by completed surveys. Noticeable, nor submissions were received 9% of participants (Figure 4A). from the southern area of Spain in any of the three rounds. Figure 2 depicts the participants (Figure 2A), institutional (Figure 2B) and dementia wards (Figure 2C) profiles. The Use of Observational Pain Assessment participant’s age was normally distributed, from 21 to 65 Tools years old, with 1/3 of the participants being 31–40 years old. As shown in Figure 4B on the use of observational instruments, Concerning their sex, the sample of participants was enriched only 35.7% of participants use them for pain assessment in people in females (64%). There was a similar composition of registered with dementia in the current practice. In fact, EVA, PAINAD- nurses, medical practitioners, and therapeutic professions sp and observational scales were the most commonly used pain (physiotherapists, occupational therapy, psychologists). They assessment scales reported. Overall, the participants find these worked in public and private hospitals, nursing homes, and tools difficult (28%) or very difficult to use (10%), they have day-care centers of 16 different regional areas of Spain (see map medium to high reliability, but none of the participants gave them in Figure 2C). Most of the institutions had a dementia ward a 10 out of 10. Thirty-two percent do not use observational tools. (60.9%), which was specialized in 43.8% of cases (Figure 2C). Regarding the participants opinion about the clinical settings Several types of dementia were referred by participants as those to use of observational instruments (Figure 4C), they informed requesting their professional attention, ranging from 56.1% of that the behavioral pain assessment is mostly (80%) conducted professionals taking care of Alzheimer’s disease patients to 31.6% while caring for a patient and over a period of time involving of them caring for people with Lewy body dementia. rest and movement (61%) or at rest (30%). When asking about Frontiers in Neurology | www.frontiersin.org 4 November 2020 | Volume 11 | Article 592366 Giménez-Llort et al. Pain Assessment in Dementia FIGURE 1 | Preliminary regional survey on the confidence on pain assessment for people without cognitive impairment (A), mild cognitive impairment/dementia (B), and moderate/severe cognitive impairment/dementia (C). preferences, the professionals considered it ideal for a behavioral found in the poor or absent verbal communication and pain assessment to take 3–5 min (43%) or 1–2 min (36%). level of comprehension in such severe cognitive conditions Regarding the utility of the pain items in the observational (14%); the scarce time availability for pain assessment and instruments (Figure 5), facial expression (41%) followed by monitoring confronted to low feasible and time-consuming changes in activity patterns or routines (28%) were considered tools (14%); the lack of specialized pain education and by professionals as essential elements of a behavioral pain poor knowledge of specific tools for this population (12%); assessment. Verbalizations (40%), followed by vocalizations as well as the poor standardization (10%) and reliability (34%), body movements and changes in interpersonal (10%) of the tools, mostly for severe cognitive impairment. interactions (both 32%), and changes in mental status (27%) Also, the professionals referred to difficulties due to the were considered as very useful (see Figures 5A,B). presence of confounding factors, general lack of guidelines In the different institutions, pain assessment amongst people and recommendations, low awareness among the health with cognitive impairment is conducted mostly by registered professionals. nurses and medical practitioners (50%). It is recorded in the When the participants were asked what would help patients’ clinical history and “nursery working sheets,” and its them improve pain assessment in people with cognitive mainly communicated to medical practitioners (59%). Registered impairment/dementia (Figure 6B), their answers focused nurses (43%), family members and other important persons on pain education specialized for this population (28%). apart from family (46%), as well as members of therapeutic They also stated the need for pain assessment tools to be: professional groups (41%) are equally informed of the results of specific (24%), standardized (19%), easy and fast to use (17%), pain assessment. When using a behavioral pain assessment tool, and reliable (10%). More time available (8%), awareness the professionals would prefer to respond to items by rating items and involvement of the teams (5%) were also commonly on a numeric scale (39%), or ticking a simple present/absent referred to as aspects that would benefit pain management in (32%) or selecting categories (i.e., slight moderate/a lot) (23%) cognitive impairment. (see Figure 5C). Challenges and Future Directions Figure 6 details the challenges reported by Spanish professionals DISCUSSION/CONCLUSIONS in assessing pain in cognitive impairment (Figure 6A), and the solutions and recommendations for its improvement Pain assessment among older adults is often neglected or (Figure 6B). In an open question, there was a consensus not done (21, 25, 26). Two-thirds of residents in long among the different professionals that the difficulties were term care facilities have dementia (5). Pain identification, found at three levels: the patient, the professional knowledge measurement, and management confront a series of difficulties and the tools. They pointed out pain management in severe due to the several forms of dementia, their different etiology, cognitive impairment, due to its complexity and diverse neurodegeneration processes, and worsening by the progressive etiology, like raising more concern. The difficulties are currently loss of verbal communication and self-reports. Thus, these Frontiers in Neurology | www.frontiersin.org 5 November 2020 | Volume 11 | Article 592366 Giménez-Llort et al. Pain Assessment in Dementia FIGURE 2 | Participants (A), institutions (B), and dementia wards (C) profiles in the National Survey and geographical distribution of the answers received and panels of professionals. FIGURE 3 | On the use of rules and guidelines for pain assessment in people with mild cognitive impairment (MCI) or mild dementia (A), and cognitive impairment (CI), and severe dementia (B). Frontiers in Neurology | www.frontiersin.org 6 November 2020 | Volume 11 | Article 592366 Giménez-Llort et al. Pain Assessment in Dementia FIGURE 4 | On the use of rules and audition of pain assessment (A), the use of observational instruments (B), and the different conditioning factors on the use of observational instruments for pain assessment in people with dementia (C). persons are more likely not to have their pain assessed for these elderly groups (33, 34). Also, the belief that older adults and therefore undertreated (27). Untreated pain is not only should not be prescribed strong opioids results in avoidance of distressing for the individual, but causes other problems, their use (35, 36). including reduced quality of life, interrupted or poor sleep In the present work, we estimated a low implementation patterns, impaired social interactions, and reduced appetite. and use of pain scoring systems in patients with cognitive Severe pain is less likely to cause wandering but more likely impairment/dementia, probably to the poor reliability given to to display aggressive and agitated behaviors (28). Conversely, them by Spanish professionals. The survey reflected that the treating pain in patients has been reported to have concomitant lack of guidelines is a major problem. Similarly, the ratio of relief of agitation (29). The high number of physical assaults organizations reporting auditions of pain assessment in older on staff working in dementia wards (30) may be related people with dementia to assess care quality was low. The low to unidentified and unmanaged pain and often results in response rate (taking part in the study) and an important antipsychotic medication rather than person-centered care. percentage of uncertain responses (I don’t know) were also In such a case, a worrisome clinical situation arises due to notorious. Most research works never achieve a 100% response the increased mortality risk that has been associated with rate, and reasons for low rates include refusal, ineligibility, antipsychotics in the elder but mostly those with dementia inability to respond, and contact not been possible (37). (15, 16). Therefore, “Pain in Cognitive Impairment, especially Limitations associated with poor response are referred to as each Dementia” is one of the health topics with clear snail effect non-response being liable to sample bias. Here, the participants (poor and slow diagnosis in frail elderly patients) (31) that found observational tools difficult or very difficult to use, an raises growing concern among professionals since the pain in important number do not use them, and many complained these patients is known to be under-detected and under-treated they have low reliability in the advanced stages of the disease. (13, 32). Despite this evidence, statements such as “pain is a Therefore, the current study confirmed many findings from the normal part of the aging process,” “the older person who has original E.U. survey (22). The majority of participants did not dementia cannot feel pain,” or “if an older person does not use national/international standards, guidelines, or local policies verbalize pain, it does not exist” are often displayed amongst or were unsure if their institutions had any pain management health care professionals and result in poor pain management guidelines (E.U. survey, 42, and 17%, respectively). In many other Frontiers in Neurology | www.frontiersin.org 7 November 2020 | Volume 11 | Article 592366 Giménez-Llort et al. Pain Assessment in Dementia FIGURE 5 | Utility of pain items of observational scales for pain assessment in people with dementia (A, main items: facial expression, verbalization, vocalization, body movements; B, changes in interpersonal interactions, activity patterns/routine, mental status), and the professional preference about how to register pain (C). countries globally, pain is not routinely assessed, even though we behavioral pain assessment, the Spanish participants reported have the tools available to help us do this. facial expression as the most important and essential pain An important number of observational scales have been indicator (41%), the original survey found facial expressions were developed so far to assess pain in persons with dementia, and regarded as being less important in the clinical setting (18% their use seems to respond to experience-based confidence in rated as essential). Facial expressions were reported as not easily them (20). The EU-COST-Action “Pain in impaired cognition, observed when providing care, such as washing or moving a especially dementia” selected items out of existing observational patient. Probably, the relevance of facial expressions to infer scales, critically re-assessed their suitability to detect pain in pain depends on cultural aspects on the expressivity (how one dementia. The EU-consortium created an improved “best-of ” expresses) and detection and codification (how one detects from meta-tool built on the knowledge and expertise implemented others) of non-verbal communication, known to be higher in in these scales (38). In both the current study and the E.U. Latin countries. In fact, checklists of non-verbal pain indicators survey, approximately one-third reported using observational (39) do a specific analysis of the facial expression coding system pain assessment tools for older people with dementia (36 vs. (FACS). Most studies on the use of FACS on pain in adults and 34%). Furthermore, in both studies, most of the respondents elderly health conditions, or cognitive deficits and/or chronic complete the observational assessment while providing care for pain, show that it is a reliable and objective tool in the detection the patient and over a period of rest and movement, with a and quantification of pain in all patients (40, 41). preference for short assessments of 3–5 min and numeric or easy Regarding the professional concerns on problems experienced tick scales, as opposed to selecting categories or open-ended in Spain and solutions for its improvement (23), pain questions. In the original survey, participants from the U.K. management in patients with severe cognitive impairment was unsurprisingly demonstrated a preference for the Abbey scale, mostly the one raising more concern. The poor standardization which is simple and easy to apply. In contrast, other countries of practices, poor or lack of guidelines or recommendations in the previous study opted for the Doloplus scale. Interestingly, for the complex and heterogeneous features of the last stages the Spanish survey participants did not choose the Abbey pain of dementia were also considered as limiting point for their scale as a preferred tool. professional activity. Here, the detailed analysis of the answers While there were similarities in the preference for verbal, unveils the specific aspects behind these reasons. First, the vocal, and body movements as being essential elements of a main functional limitation was the poor or absent verbal Frontiers in Neurology | www.frontiersin.org 8 November 2020 | Volume 11 | Article 592366 Giménez-Llort et al. Pain Assessment in Dementia FIGURE 6 | Challenges (A) and Future directions (B) in the pain assessment and management in the cognitively impaired/dementia population. communication of the patient but also of his/her comprehension. professionals who did have multidisciplinary staff meetings Second, the low feasible and time-consuming tools in a regarding pain assessment and specialized pain training reported professional activity with a short time to assess the patients higher satisfaction with their knowledge and pain management. were seen as worsening pain assessment challenges, mostly This study’s findings indicate that training needs are still not in these patients with severe cognitive impairment. Third, being met, despite the clinician’s best efforts to learn. the professionals’ complain about knowledge and education It is evident from the comparable findings that health indicated that the poor knowledge of specific tools for pain professionals across the E.U. struggle with the same challenges in assessment in these populations and the lack of specialized pain assessment in people with dementia. The recommendations pain education were important regrets. Standardization and made by participants from Spain closely align with those made reliability of tools, mostly for severe cognitive impairment, were by authors of the E.U. survey; these include improved pain also mentioned by many professionals, as well as confounding education for understanding pain assessment and management factors, and low awareness among health professionals. Most in people with dementia; improved pain assessment tools that are of these challenges pointed out by Spanish professionals agreed fast and easy to use and interpret; and more time allowed for with aspects reported from the original survey (22). There, pain assessment. Efforts to establish more feasible instruments concerns referred to uncertainty about the observation; lack of and policies together with education are key targets of our future information; lack of objectivity; lack of education, knowledge and directions in Spain as they are for other countries. expertise; lack of time; lack of interest and awareness; and lack of Among the limitations of the study, the first to be mentioned available pain tools. In the current survey, the key challenges were is the number of participants, lower than in the center-north similar and focused on difficulties in communicating with the Europe survey, mostly due to the lack of submissions received patient; short time available for pain assessment and monitoring; from an important geographical area. The length and the number lack of specialized pain education and poor knowledge of tools of sensitive questions regarding the use of guidelines probably suitable for this population; poor standardization and reliability was a strong limitation to receive submissions. As mentioned of tools; and general lack of guidance and recommendations. before, despite the chance to stop completing the survey at any Inadequate pain education from both studies came out as a moment, all the submissions were completed surveys. The sex key problem relating to pain assessment in dementia patients. bias of participants, mostly females, was observed but probably In Spain, professionals reported feeling very (32%) or slightly less than expected for the gender bias in healthcare professions. (26%) dissatisfied with their pain assessment knowledge. Health Finally, since there are different types and degrees of dementia, Frontiers in Neurology | www.frontiersin.org 9 November 2020 | Volume 11 | Article 592366 Giménez-Llort et al. Pain Assessment in Dementia a survey requesting answers for each one of them would be AUTHOR CONTRIBUTIONS more specific. The Spanish survey was in clear agreement in the results LG-L and PS: WG2 COST-Action TD1005 development of obtained in center-north Europe, except for considering facial the concept and study design. LG-L, MB, AM-S, and VT-L: expression as a key aspect of observational tools, probably due study conduct, survey and data collection from the different to cultural bias. This convergence in the professional criteria geographical areas. LG-L: data analysis and illustrations. LG-L, through south-center-north Europe is relevant to note because, RD, and PS: drafting manuscript. AB and MB: critical discussion. in Spain, the distribution of the survey to different health All authors participated in the scientific discussions and professional profiles, not always confident with the approach to approved final version of manuscript. patients with severe dementia, could have been a source of bias in the findings and interpretation of the results. FUNDING The results of the present work and the center-north Europe survey (22) were considered as one of the sources of knowledge This work received financial support by Associació Envellir for the PAIC-15 scale, a new internationally agreed-on meta- bé-Saber Envejecer-Healthy Aging/NeusSenderMeler/060614, tool for Pain Assessment in Impaired Cognition, composed Teaming.net/saberenvejecerydemencias, and it’s all for LOVE by a list of 15 observational items that have demonstrated projects Charity Organization 4LOVEprojects/MJ29082020. psychometric quality and clinical usefulness both in their former scales and in their international evaluation (38). Also, these ACKNOWLEDGMENTS surveys’ professional opinions were taken into consideration in the scientific development and discussion of our most recent We thank Core Salut Mental, Delphi panel, and all the work on observational pain assessment in older persons with Spanish health/care professionals that participated in the Survey dementia (42). for providing their professional experience that will help to improve pain assessment and management in dementia in the DATA AVAILABILITY STATEMENT near future. We thank Teaming.net/saberenvejecerydemencias members María Amparo Fernández-Núñez, Jorge Lisbona, The raw data supporting the conclusions of this article will be Carme Balaguero Fite, Gestión Integrada Empresarial SL, for made available by the authors, without undue reservation. their continuous support. REFERENCES 11. Defrin R, Amanzio M, de Tommaso M, Dimova V, Filipovic S, Finn DP, et al. Experimental pain processing in individuals with cognitive 1. 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