Patient Education and Counseling 100 (2017) 411–424 Contents lists available at ScienceDirect Patient Education and Counseling journal homepage: www.elsevier.com/locate/pateducou Review article Culture and nonverbal expressions of empathy in clinical settings: A systematic review Áine Loriéa,1, Diego A. Reineroa,b,1, Margot Phillipsa , Linda Zhanga , Helen Riess, M.D.a,* a b Massachusetts General Hospital/Harvard Medical School, Empathy and Relational Science Program, Department of Psychiatry, Boston, MA, USA New York University, Department of Psychology, New York, NY, USA A R T I C L E I N F O A B S T R A C T Article history: Received 10 December 2015 Received in revised form 22 July 2016 Accepted 23 September 2016 Objective: To conduct a systematic review of studies examining how culture mediates nonverbal expressions of empathy with the aim to improve clinician cross-cultural competency. Methods: We searched three databases for studies of nonverbal expressions of empathy and communication in cross-cultural clinical settings, yielding 16,143 articles. We examined peer-reviewed, experimental or observational articles. Sixteen studies met inclusion criteria. Results: Nonverbal expressions of empathy varied across cultural groups and impacted the quality of communication and care. Some nonverbal behaviors appeared universally desired and others, culturally specific. Findings revealed the impact of nonverbal communication on patient satisfaction, affective tone, information exchange, visit length, and expression decoding during cross-cultural clinical encounters. Racial discordance, patients’ perception of physician racism, and physician implicit bias are among factors that appear to influence information exchange in clinical encounters. Conclusion: Culture-based norms impact expectations for specific nonverbal expressions within patientclinician dyads. Nonverbal communication plays a significant role in fostering trusting provider-patient relationships, and is critical to high quality care. Practice implications: Medical education should include training in interpretation of nonverbal behavior to optimize empathic cross-cultural communication and training efforts should accommodate norms of local patient populations. These efforts should reduce implicit biases in providers and perceived prejudice in patients. ã 2016 Elsevier Ireland Ltd. All rights reserved. Keywords: Culture Empathy Nonverbal Systematic review Patient-physician relationship Contents 1. 2. 3. 4. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Main findings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. 3.2. Patient satisfaction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Affective tone . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. 3.4. Information exchange . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Visit length . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5. Expression decoding . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6. Cultural preferences for NVBs: qualitative studies . . . . . . . . . . . . . . . . . . 3.7. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4.1. Emotion expression: cultural equivalence or cultural advantage model? Cross-cultural considerations of nonverbal empathy . . . . . . . . . . . . . . . . 4.2. * Corresponding author at: Empathy and Relational Science Program, Department of Psychiatry, Massachusetts General Hospital/Harvard Medical School. Wang Ambulatory Care Center, Suite 812, 15 Parkman Street, Boston, MA, USA. E-mail address: hriess@mgh.harvard.edu (H. Riess). 1 Equal author contribution. http://dx.doi.org/10.1016/j.pec.2016.09.018 0738-3991/ã 2016 Elsevier Ireland Ltd. All rights reserved. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 412 412 416 416 416 416 416 419 419 420 420 420 420 412 5. 6. 7. A. Lorié et al. / Patient Education and Counseling 100 (2017) 411–424 4.2.1. Race . . . . . . . . . . . . . . . Nationality . . . . . . . . . 4.2.2. Gender and occupation 4.2.3. Intergroup and implicit 4.2.4. Limitations . . . . . . . . . . . . . . . . . . . . . . Practice implications . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . Conflict of interest disclosures . . . . . . Author contributions . . . . . . . . . . . . . . Ethical approval . . . . . . . . . . . . . . . . . . Acknowledgments . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . .... .... ... bias .... .... .... .... .... .... .... .... .... .... .... ... .... .... .... .... .... .... .... .... . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1. Introduction There is a critical need for health care providers to offer culturally competent empathic care [1–3]. Increasing diversity in patient populations and the healthcare workforce can generate cross-cultural misunderstandings, contributing to medical errors, lack of trust and adherence to treatment [4–7], and decreased patient satisfaction [8–10]. The U.S. confirms this multicultural trend, reporting that by 2043, no individual racial group within the U.S. will make up a majority [11]. In spite of increasing global diversification [12,13], medical trainees are not adequately prepared to provide cross-culturally competent care [14]. In-group biases (the effect wherein people give preferential treatment to others who are perceived to be in the same group) arise in cross-cultural contexts [15–18] and often disproportionally affect minorities, leading to disparities in treatment, healthcare access, and health outcomes [19–23]. Indeed, a previous literature review of cultural differences in medical communication found that clinicians are more verbally dominant and behave less affectively (e.g., less rapport-building, friendly, or concerned) when interacting with ethnic minority patients compared to White patients [24]. Therefore, competence in cross-cultural communication is becoming increasingly critical in practices and policies of health services, with a corresponding need to train medical personnel in these skills to improve the quality of care and patient outcomes [25]. Empathy, a capacity that includes cognitive and affective components enabling individuals to perceive and respond to verbal and nonverbal emotional cues of others [26] is a key component of effective cross-cultural care [9,20,26–38]. Empathy is expressed both through verbal and nonverbal behavior [39], and nonverbal behavior (NVB) is estimated to account for 60%–90% of communication [40]. The importance of nonverbal empathy in clinical encounters has been highlighted in previous work [41–47], suggesting that clinician warmth and listening results in greater patient satisfaction [48], and that specific NVBs, including head nodding, forward lean, direct body orientation, uncrossed legs and arms, arm symmetry, and mutual gaze, are associated with positive health outcomes [49]. Providers who are more sensitive to nonverbal cues reinforce the perception of physician sincerity, dedication, and competence, which in turn improves utilization of health services, functional status, and the overall provider-patient relationship [50]. Although existing medical, psychological, and sociological literature abounds with research that examines gaps in crosscultural communication, in-group bias, and the need for cultural awareness and training [51–55], there is little research integrating cross-cultural differences and patient-clinician NVB [56–61]. One study that focused on the verbal exchange between patients and clinicians reported difficulty in reliably detecting NVB, as such expressions can be communicated vaguely, downplayed or masked, and veiled by language barriers [62]. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 420 420 420 421 421 421 421 422 422 422 422 423 Levine and Ambady’s [61] review examined the influence of nonverbal behavior on racial disparities in healthcare. The findings suggest that through both historical minority group derogation and clinician disengagement, patient distrust can arise. Moreover, negative stereotyping, and culturally-bound nonverbal expectations obstruct nonverbal communication and engagement in cross-racial patient-clinician encounters [61]. However, this previous review was not systematic and focused primarily on White doctors and African American patients, thus limiting the scope and generalizability of its findings. Our systematic review expands on Levine and Ambady’s work [61] by broadening the cross-cultural context, and systematically examining a wider range of groups that report culturally specific practices of NVB in healthcare. Culture has been defined as a learned system of knowledge, attitudes, beliefs, behaviors, values, and norms that is shared by a group of people, community, kin, or nation [63]. Our systematic review is guided by the following research questions: (1) Are nonverbal expressions in the clinical setting culturally specific or universal? (2) If culturally specific, how does empathic NVB in the clinical setting differ cross-culturally? (3) What are the effects of empathic cross-cultural NVB on patient outcomes? An examination of these questions will reveal some of the complexities of cross-cultural nonverbal communication and empathy, and may subsequently offer solutions to improve provider training, clinician cross-cultural competency, and the reduction of disparities. Our systematic review will conclude with practice implications and recommendations for future research. 2. Methods We searched MEDLINE, PsycINFO, and CINAHL from 1990 through September 18, 2014. An example of our electronic search strategy (MEDLINE) is outlined in Appendix A (PsycINFO and CINAHL search strategies available upon request). The electronic search strategy required that articles: (1) be written in English and published in a peer-reviewed journal; (2) include in the title or abstract at least one word related to culture (e.g., race, ethnicity, immigrant, cross-cultural), clinician-patient communication (e.g., empathy, nonverbal, patient centered) and a clinical setting (e.g., hospital, clinic, primary care). For the review by hand, the inclusion criteria were: (1) experimental or observational studies with adults (age 18) and 10 subjects, written in English and published in a peer-reviewed journal; (2) clinician-patient interactions addressing health problems; (3) an analysis or discussion of cultural components; (4) an analysis or discussion of clinician-patient nonverbal communication. Studies were excluded if: (1) not all four of the inclusion criteria were met; (2) the patients had severe psychiatric, neurologic, or facial impairments obstructing communication; (3) the health problems discussed were addressed through non-traditional medical practice, (4) translators were the main focus of the study. For A. Lorié et al. / Patient Education and Counseling 100 (2017) 411–424 413 Fig. 1. Flow Chart of Study Selection Process. full criteria, see Appendix B. Limitations are presented after the Discussion. Our electronic search yielded 16,143 articles (MEDLINE: 8709; PsycINFO: 3079; CINAHL: 4355). Removing duplicates yielded 16,025 articles. For the initial review, two pairs of authors each independently reviewed half of the titles. A fifth author resolved disagreements between reviewer-pairs (99% reviewer-pair agreement). Articles were included for the next round of review if the title incorporated at least two of the three main content criteria (“culture”, “communication”, “clinical”) and appeared relevant to the study’s goal. This process yielded 1040 articles.1 The second round of review examined the abstracts of these remaining articles, again with two pairs of authors each reviewing one half of the results. Articles were included if the abstract included all three content criteria. A fifth author resolved disagreements between reviewer-pairs (95% reviewer-pair agreement). This yielded 116 articles. This new total included two additional articles that were hand selected from the reference list of informative reviews. The final round examined the full text of each article. Authors made independent judgments as to whether 1 Although this article selection process is common for systematic reviews, we nevertheless performed a sensitivity check on 100 randomly selected results that had previously been excluded (on the basis of the initial title review by two authors) and systematically reviewed the abstracts of each of these articles. This sensitivity check confirmed that none of the 100 articles met our inclusion criteria and provides evidence that our study selection process is indeed robust. the article met inclusion/exclusion criteria with particular focus on quality of nonverbal communication measured. Disagreements were resolved by face-to-face discussion of four authors, leading to consensus judgment. Sixteen articles met our inclusion criteria. This selection process adhered to PRISMA guidelines and is illustrated in Fig. 1. 3. Results The systematic review yielded 16 studies (Table 1). Eleven studies were conducted in the United States; other locations included Canada, Slovenia, Sweden, Australia, and Trinidad and Tobago. Six studies examined White Americans and African Americans [64–69]; other cultural groups studied were Australian Aboriginals, Brazilians, Filipinos, South Asians, and Hispanics. Six studies assessed scenarios in which the patients belonged to a minority culture and clinicians belonged to the dominant culture [67,68, 70–73], and five studies examined combinations of patients and providers in both majority and minority cultures [64–66,69,74]. By contrast, four studies examined scenarios in which the providers belonged to a minority culture [75–78], for example internationally educated nurses or physicians (from countries such as the Philippines (39 total), India (11 total), China (5 total), Korea (3 total), Jordan (1 total), Lebanon (1 total), Nigeria (1 total), and Kenya (1 total)). One study examined providers’ NVBs within the majority culture [79]. 414 Table 1 Overview of studies: sample, setting, methods, and nonverbal behaviors studied (studies are organized in reverse chronological order within study design). Patient sample size (n of each culture) Observation Strategy Instruments Interrater reliability Nonverbal behavior studied Outcomes 7 (7 non-AA physicians) Audiotaped clinic visits RIAS, patient questionnaire 0.98 Emotional tone of patient and physician Patient satisfaction and provider satisfaction, physician verbal dominance, patient centeredness, visit duration, information exchange Computerized tests of physicians' ability to decode facial expressions and vocal tones 1) Facial expression coding system, 2) Vocal tone assessment, 3) Patient satisfaction survey, 4) authordeveloped Patient Adherence survey NR Facial expression decoding accuracy and vocal tones decoding accuracy Patient satisfaction, selfreported patient adherence Audiotaped clinic visits; Implicit Association Tests (IAT) for clinicians Two IATs for measuring racial attitudes and stereotypes, and patient questionnaire 0.86 1 Patient and physician positive affect Implicit race bias and compliance bias of physicians, patient satisfaction, visit length, speech speed, clinician verbal dominance, patient centeredness Study Design Country Practice Havranek et al. [68] Randomized control trial USA Primary care 99 (99 AA) Coelho and Galan [74] Crosssectional USA Hospitals and clinics 30 60 (16 South Asian, 14 (30 South Asian, 30 WA) WA physicians) Cooper et al. [66] Cross sectional USA 2 Primary care clinics 269 (213 AA, 56 WA) 40 (9 AA, 12 Asian, 19 WA physicians) Stepanikova et al. [64] Crosssectional USA 3 Primary care clinics 209 (29 nonWhite, 190 WA) Videotaped 30 (3 non-white, 27 WA clinic visits physicians) Xu et al. [75] Crosssectional USA 2 Hospitals 1 (1 standardized patient) 52 (IENs: 38 Philippines, 5 India, 3 Korea, 3 China, 1 Kenya, 2 NR) Videotaped encounter of nursing intake of a standardized patient Author-developed scales 0.82 Hausmann et al. [67] Crosssectional USA Veterans Affairs Hospitals 353 (100 AA, 253 WA) 63 (63 Orthopedic surgeons) Audiotaped clinic visits RIAS, patient questionnaire 0.68 0.92 Provider warmth/respectfulness Patient-rated visit informativeness, and ease of communicating with the provider Zaletel et al. [79] Crosssectional Slovenia 27 Nursing homes 267 (267 Slovenians) 267 (267 Slovenian care givers) Direct clinical observation by pairs of trained observers Kovacev Non-Verbal Expression Checklist NR Distribution of nonverbal behaviors by gender and professional type Johnson et al. [69] Crosssectional USA General clinics 458 (256 AA, 202 WA) 61 (21 AA, 9 Asian, 30 WA, 1 Other physicians) Audiotaped clinic visits RIAS, patient questionnaires 0.88 0.79 Patient and physician positive affect score: dominance/assertiveness (patient only), interest/attentiveness (both), friendliness/warmth (both), responsiveness/engagement (both), and sympathy/empathy (both) Adaption of the Nonverbal 0.83 0.96 Open body position, eye contact, smile, Patient ease, physician’s Communication in touch mixed signals Doctor–Elderly Patient Transactions (NDEPT) Eye contact, smile, body position, nodding, gesture, hugging, interpersonal space, and therapeutic touch Provider facial expressions, head movements, gestures, body position, silence Global assessment of communication Patient positive affect, physician positive affect, verbal dominance, patientcentered orientation, visit duration and speech speed A. Lorié et al. / Patient Education and Counseling 100 (2017) 411–424 Clinician sample size (n of each culture) Author Patient-rated satisfaction, trust, self-disclosure, recommendation, recall, compliance Student health clinic 116 (97 AA, 19 WA) 2 (1 AA, 1 WA physician in a simulated video) Participants watched 1 of 4 videos Patient questionnaires NR Physician facial expression, distance from patient, concern for patient, understanding of patient Bergman and Qualitative Connaughton [70] USA Prenatal clinic 48 (48 Hispanic) NR (American providers) Semistructured interviews Qualitative NR Physician warmth, friendliness, smile, Patient centered care eye contact, patience, formal greetings approaches, patient trust, provider credibility Williams et al. Qualitative [77] Trinidad and Tobago Medical School N/A 36 (36 medical students) Videotaped focus groups Qualitative NR Eye contact, personal space, body movements, touch, vocal tone Provider perceptions of patient expectations Jain and Qualitative Krieger [76] USA Hospital N/A 12 (Internationally educated resident physicians: 6 India, 2 China, 1 Jordan, 1 Lebanon, 1 Nigeria, 1 Philippines) Semistructured audio-recorded interviews Qualitative NR Eye contact, touch, gestures, warmth Internationally educated resident physicians’ crosscultural strategies Jirwe et al. [78] Qualitative Sweden Nursing school N/A 10 (5 Swedish student nurses, 5 immigrant student nurses) Semistructured audio-recorded interviews Qualitative NR Eye contact, smile, gestures, warmth Swedish and non-Swedish student nurse strategies and difficulties in cross-cultural encounters Shahid et al. [71] Qualitative Australia Varied: recruited from oncology centers 30 (30 Australian Aborigines) NR SemiAustralian providers structured audio-recorded interviews Qualitative NR Patient nodding and silence, physician friendliness Trust, patient perception of physician knowledge and competence Roberts [72] Qualitative USA Community centers 42 (42 Brazilians) NR American providers Semistructured interviews Qualitative NR Perception of physician warmth, touch Patient satisfaction, patient trust Pasco et al. [73] Qualitative Canada Hospital 24 (24 Filipinos) NR Canadian nurses Semistructured interviews Qualitative NR Touch, eye contact and gaze Crosssectional Patient trust Notes: AA = African American, WA = White Americans, IEN = Internationally educated nurse, MD = physician, RN = Registered nurse, N/A = Not applicable, NR = not reported, NVB = Nonverbal behavior, RIAS = Roter Interaction Analysis System, USA = United States of America. A. Lorié et al. / Patient Education and Counseling 100 (2017) 411–424 USA Aruguete and Roberts [65] 415 416 A. Lorié et al. / Patient Education and Counseling 100 (2017) 411–424 The methods of data analysis varied across the included studies. There were nine quantitative studies and seven qualitative studies. One study was a randomized controlled trial [68]; eight were cross-sectional. Three studies used the Roter Interaction Analysis System (RIAS) to code physician and patient behaviors during clinical encounters [67–69]. Seven studies reported acceptable inter-rater reliability. Sample sizes of quantitative studies ranged from 52 to 458. The seven qualitative studies were based on semistructured interviews or focus groups, and their sample sizes ranged from 10 to 48. Patient and physician age and gender were reported in all of the quantitative studies. Factors inconsistently reported were number of years in host country, level of education, language proficiency, and use of interpreters. Mood or mental state was assessed in two studies [66,68]. Clinical specialties included primary care clinics (5 studies), hospitals (5 studies), specialty clinics (2 studies), nursing home (1 study), medical school (1 study), nursing school (1 study), and community center (1 study). Care providers of different specialties and level of training were studied, including: general providers (3 studies), physicians (8 studies), nurses (2 studies), medical students (1 study), nursing students (1 study), and nursing home caregivers (1 study). 3.1. Main findings Findings of nonverbal behaviors influencing empathic crosscultural care can be grouped into two main categories (Table 2). We focus on quantitative studies demonstrating changes in patient or clinician NVBs in cross-cultural clinical encounters and their outcomes. These include patient satisfaction, affective tone, information exchange, visit length, and expression decoding. Main findings and recommendations from qualitative studies that demonstrate cultural preferences for specific NVBs as part of empathic care are presented in Table 2. clinical encounters were found in several studies. Johnson et al. found that both the patient and physician showed significantly less positive affect during visits with AA patients as compared with White patients (patient positive affect: p < 0.001; physician positive affect: p < 0.02) [69]. Stepanikova et al. found that nonverbal communication in concordant AA–AA dyads was more positive, as indicated by more smile, touch, and open body position, compared to communication in any other racial combination [64]. Cooper et al. found a significant association between physician implicit bias as measured on an Implicit Association Test (IAT) and patient positive affect, where AA patients were less likely to demonstrate positive affect (as observed by coders) as compared to encounters with physicians without implicit race bias (p = 0.04). Higher levels of physician implicit race bias were significantly associated with greater clinician verbal dominance, lower patient positive affect, and poorer ratings of interpersonal care among AA patients [66]. Implicit bias also correlated with significantly higher ratings of physician positive affect during visits with White patients, but there was no significant change in positive affect among White patients. Similarly, Hausmann et al. found that encounters in which patients reported high levels of perceived racism had a significant negative association with coder ratings of nonverbal provider positive affect (B = 0.34, 95% CI = 0.66, 0.01) and with patient positive affect (B = 0.41, 95% CI = 0.073, 0.09) [67]. Havranek et al. [68] further explored how race influences communication in race-discordant clinical encounters. In a randomized controlled trial of the effects of a values affirmation exercise (validation of patient self-worth and concerns) given prior to clinic visits, coder ratings of warmth/friendliness and interactivity were significantly higher in the intervention group, whereas ratings of depression/sadness and distress were significantly higher in the control groups. 3.4. Information exchange 3.2. Patient satisfaction Physician concern, communicated nonverbally, correlated with patient satisfaction in several studies [65,66,68,72,74]. Aruguete et al. showed that physician nonverbal concern, irrespective of patient or physician race, was the best predictor of patient satisfaction (p < 0.001) and positive physician recommendation from the participant (p < 0.001) [65]. When the physician displayed positive emotion, made eye contact, and appeared attentive, physician race was not correlated to participants' evaluations [65]. In another study, poorer decoding of South Asian patients’ facial expressions (regardless of physician race) was correlated with lower visit satisfaction and lower likelihood of adhering to a physician’s recommendations [74]. Similarly, high levels of perceived racism among AA patients interacting with White physicians were associated with low patient ratings of warmth and respectfulness (OR = 0.19, 95% CI = 0.05, 0.72) [67]. Cooper et al. showed that higher rates of physician implicit race bias in racially discordant dyads were correlated with AA patients’ poorer ratings of patient care (e.g., AA patients were less likely to feel that the doctor respects the patient (50.2% vs 34.9%, p = 0.001), were less likely to report liking the physician (46.6% vs 32.7%, p < 0.001), and less likely to recommend the physician (47.3% vs 34.4%, p = 0.001)). Values for trust, feeling the physician likes him or her, and having confidence in the physician were not significant [66]. 3.3. Affective tone Changes in the affective tone (tone of voice, warmth, or responsiveness) of patients and clinicians during cross-cultural Racial discordance, patients’ perception of physician racism, and physician implicit bias are among factors that appear to influence information exchange in clinical encounters. In Havranek et al., AA patients randomized to receive values-affirmation training prior to their clinic visit gave and asked for significantly more information about their medical condition than the control group (p = 0.03) [68]. In racially discordant dyads, physicians were more verbally dominant (p < 0.001) and less patient-centered (p < 0.05) with AA patients than with White patients [69]. Physicians with higher rates of implicit bias predicted significantly more cliniciandominated exchanges irrespective of patient race: (p < 0.05, and p < 0.01) [66,69]. High levels of perceived racism among AA patients were negatively associated with patient ratings of ease of communication (OR = 0.22, 95% CI = 0.07, 0.67) [67]. Perceived racism among White patients was negatively associated with patient ratings of visit informativeness (OR = 0.4, 95% CI = 0.23, 0.71), but not among AAs [67]. 3.5. Visit length Findings for visit length varied. Visit length remained the same despite significant improvements of information exchange after patients received values affirmation training in Havranek et al. Ratings of physicians’ rate of speech, verbal dominance, and patient centeredness did not differ significantly between the intervention and control groups [68]. In another study, higher levels of physician compliance stereotyping (a measure of the implicit association between race and the concept of the A. Lorié et al. / Patient Education and Counseling 100 (2017) 411–424 417 Table 2 Studies' Main Nonverbal Findings (Studies are organized in reverse chronological order within study design). Study Refs. # Havranek [68] et al. (2012) Study Design Research aims Main nonverbal findings Randomized control trial To test the effect of a values affirmation intervention given to AA patients prior to their clinic visit with a non-AA primary care physician Affective tone: overall communication in Values affirmation exercise can the intervention group was significantly improve the experience of AA patients more friendly, interactive, and respectful in primary care visits with non- AA (p = 0.02). Patients were rated as less physicians Greater exchange of medical informadistressed and less depressed (p=0.03) Information exchange: patients in the tion is achieved without increasing visit intervention group requested and length, and overall positive affective provided more information about their tone of patients and physicians is medical condition (p =0.03). significantly greater Visit length: no significant difference Physicians should be aware that their Patient satisfaction: no significant affective tone may be influenced by the difference patient's level of comfort and moniPatient trust: no significant difference toring cues such as instructiveness and friendliness may influence patients' affective tone and exchange of medical information Implications Coelho and Galan (2012) [74] Crosssectional To examine physicians’ abilities to decode nonverbal emotions of Caucasian and South Asian patients, and to test the hypothesis that this ability correlates with patient satisfaction and patient adherence Physicians can have difficulty interFacial and vocal tone decoding accuracy: South Asian physicians were no preting South Asian nonverbal cues better at decoding the facial expressions which is correlated with poorer patient or vocal tones of South Asian patients, and satisfaction and poorer patient adherboth South Asian and Caucasian ence Physicians should be trained to physicians were better at decoding Caucasian nonverbal stimuli (p < 0.001) improve awareness of differences in Patient satisfaction: South Asian South Asian facial and vocal tone patients were more likely to be expression dissatisfied with the quality of care provided by their physician (p = 0.032) Patient adherence: South Asian patients reported they were less likely to adhere to recommendations (p < 0.001) Cooper et al. (2012) [66] Crosssectional To examine associations of clinician’s implicit attitudes about race with visit communication and patient ratings of care Training to improve clinician awarePositive Affect: clinician race bias was associated with lower patient positive ness of implicit race bias. affect among Black patients and higher Physician self-awareness can reduce physician positive affect among White implicit race and compliance bias, with patients improvements in overall communicaPhysician verbal dominance: clinician tion and patient ratings of care, parrace bias was associated with greater ticularly among Black patients physician verbal dominance among Black patients and White patients Visit length and speech speed: clinician race compliance bias was associated with longer visits and slower speech among Black patients and faster visits and faster speech among White patients Patient Satisfaction: greater clinician race bias was associated with lower Black patient ratings of clinician respect, liking, (p < 0.001) or recommending physician (p = 0.001) [64] Stepanikova et al. (2012) Crosssectional To examine the influence of race of physicians with patients who are over 65 years old, on nonverbal communication during medical interviews Open body posture, smile and touch: Concordant race resulted in high use of smile, touch, and open body position for both AA and White physicians, and was highest in AA–AA dyads compared to the average across other dyads (open body posture: p < 0.001; smile: p = 0.048; touch: p < 0.001). Discordant race in AA physicians with White patients resulted in highest use of smile and gaze with lowest use of open body position. Eye contact: White physicians made more eye contact with White patients as compared to their AA patients but it was only marginally significant (p = 0.08) Training in nonverbal behavior across all races with specific focus on open body posture and awareness to avoid sending mixed nonverbal messages, especially in race discordant visits Xu et al. (2012) Crosssectional To evaluate nonverbal communication behaviors of internationally educated nurses (IENs) in the United States Therapeutic touch (p < 0.01), interpersonal space (p < 0.01), and eye contact (p < 0.05) were positively correlated to overall global impression score Provide targeted communication training to newly arrived/hired IENs with focus on therapeutic touch, interpersonal space, and eye contact to improve patient rating of overall clinical care [75] 418 A. Lorié et al. / Patient Education and Counseling 100 (2017) 411–424 Table 2 (Continued) Study Refs. # Study Design Research aims Main nonverbal findings Implications Hausmann [67] et al. (2011) Crosssectional To examine the relationship between AA Listening: Feeling that a physician did not Increase physician awareness of uninand White patients’ perceptions of listen was the most common form of tentional biases discrimination from past healthcare perceived racism expressed by both races Training to improve positive affective encounters and patient-provider Affective tone: less positive nonverbal tone, listening, and how to counter communication during a subsequent affect among patients (Beta = 0.41, 95% negative emotion states through rolemedical visit CI = 0.73, 0.09) and providers playing or mindfulness (Beta = 0.34, 95% CI = 0.66, 0.01) was associated with high levels of perceived racism among AA patients Warmth/respectfulness: high levels of perceived racism was associated with low patient ratings of provider warmth/ respectfulness (OR = 0.19, 95% CI = 0.05, 0.72) and ease of communication (OR = 0.22, 95% CI = 0.07, 0.67). Perceived classism yielded similar results Zaletel et al. (2012) [79] Crosssectional To quantify nonverbal communication of Smile: No significant difference in rates of caregivers in Slovenian nursing homes smiling between gender or type of caregiver Eye contact: No significant difference in rates of eye contact between gender or type of caregiver Gestures: associated with gender and type of caregiver, with nurses and females manifesting fewer negative expressions (p = 0.034) Johnson et al. (2004) [69] Crosssectional To examine the association between patient race/ethnicity and patientphysician communication Affective tone: overall physician affective tone was less positive with AA compared with White patients, and AA patient affective tone was less positive compared with White patients (p = 0.02) Verbal dominance: physicians were 23% more verbally dominant with AA patients than with White patients (p < 0.001) Patient-centeredness: content was 33% less patient-centered with AA patients (p < 0.5) Training to improve clinician communication skills including affective communication (e.g., rapport-building, minimizing verbal dominance), and empowering minorities for active participation in health care Aruguete and Roberts (2002) [65] Crosssectional Smile, facial expression, eye contact, To examine the impact of race (AA vs. White) and nonverbal communication on attentiveness, personal space patient evaluations (sitting < 2 feet from patient), and posture (forward lean): physician display of nonverbal concern via these behaviors was the best predictor of patient satisfaction (p < 0.001) and positive physician recommendation (p < 0.001), regardless of physician race Increase nonverbal skills training for students and practitioners in same and discordant race encounters, with focus on behaviors that communicate nonverbal concern Friendliness: Patients expressed preference for friendly (“amable”) providers Smile: a smile may convey warmth, professionalism, and confidence that the provider was competent Eye contact: patients sought sustained eye contact together with a smile as signs of provider professionalism and warmth Training to improve awareness of local cultures' expectations for patientcentered communication: e.g., Hispanic women in prenatal clinic visits expressed preferences for physician friendliness, attentiveness, and patience/not rushing Qualitative Bergman and [70] Connaughton (2013) To understand the experience and expectations of Hispanic women in prenatal clinics Williams et al. [77] (2013) Qualitative To understand the challenges of teaching Eye Contact: in Tobago, it is considered nonverbal communication skills in a disrespectful to look into the eyes of an Caribbean medical school elder Personal Space: in the Bahamas and Jamaica, closer proximities are considered invasive rather than reassuring [76] Qualitative To understand the communication strategies international medical graduates use in medical interactions to overcome language and cultural barriers Jain and Krieger (2011) Internationally educated physicians expressed difficulty knowing how to respond to patients' emotions after giving bad news because in their culture physicians disclose medical information to family members rather than to the Training to improve rates of positive nonverbal communication Traditional (Western) teaching of physician nonverbal behavior did not reflect the diversity of patient preferences in Caribbean cultures Medical education should address culturally specific norms for nonverbal communication Training to improve communication strategies of internationally educated physicians early in their career, with focus on disclosure of medical information and addressing patients' negative emotions when giving bad news A. Lorié et al. / Patient Education and Counseling 100 (2017) 411–424 419 Table 2 (Continued) Study Refs. # Study Design Research aims Main nonverbal findings Implications patient directly. They may compensate for intercultural differences and language barriers with several strategies, including repeating information using non-verbal communication such as eye contact, friendliness, smile, vocally conveying warmth and care, respectful silence, and supportive touch Jirwe et al. (2010) [78] Qualitative To understand the experiences of student Lack of skills and language barriers can nurses' cross-cultural communication result in patient and nurse dissatisfaction. with patients Communication strategies included mirroring the patient’s emotions, using pictures and using body language (smile, eye contact, touch). Nurses who had immigrated to Sweden expressed more confidence communicating in crosscultural encounters than Swedish nurses Training to improve nursing skills, confidence, and satisfaction, including use of smile, touch, eye contact, and mirroring patient expressions Shahid et al. (2009) [71] Qualitative To report Aboriginal patients' views about effective communication between Aboriginal people and cancer providers in Australia Warmth: Aboriginal patients tended to act reserved and viewed many physicians as lacking compassion and warmth Silence: Aboriginal patients expressed reluctance to admit to difficulty understanding their physicians and lacked the confidence to ask questions Head Nod: Aboriginal patients may nod rather than admit lack of understanding Improve awareness of meaning of Aboriginal patients' silence and nodding, and further integrate Aboriginal clinical support and interpreters in cancer care Roberts (2007) [72] Qualitative To understand what health practices and Warmth: Brazilian immigrants beliefs are common among Brazilian experienced U.S. clinicians as lacking immigrant patients warmth and desired more personal warmth from their providers (“carinho”) Personal space: preference for more physical closeness from providers Touch: preference for a hug or a kiss over a handshake Smile and eye contact: can convey warmth. Clinician “coldness” can be interpreted by absence of a smile or eye contact Lengthen clinical encounters and consider if the patient expects or desires more warmth in nonverbal and verbal behavior from clinicians Pasco et al. (2004) [73] Qualitative To identify Filipino-Canadian values that impact patient-nurse interactions Improve nurse awareness of use of gaze and touch to build relationships with hospitalized Filipino patients Touch by nurses helps develop trust in hospitalized Filipino patients. Patients experience a nurses' touch as conveying respect for the patient Eye contact: direct eye contact is valued; lowered eyes may mean respect or shame and is context-dependent. A head-to-toe gaze by a nurse can be perceived as demeaning Notes: AA = African American, IEN = Internationally educated nurse, vs = versus. “compliant patient”) were associated with longer visits, slower speech, less patient centeredness, poorer ratings of interpersonal care and lower ratings of patient positive affect among AA patients [66]. In contrast, Johnson et al. showed no difference in speech speed or visit duration when medical visits between AA or White patients were compared [69]. 3.6. Expression decoding One study of physicians’ ability to identify nonverbal emotional cues across races was included in our review [74]. South Asian physicians were no better at decoding facial expressions or vocal tones of South Asian or Caucasian patients than Caucasian physicians. Physicians, regardless of their ethnicity, were more accurate at rating Caucasian patients’ facial expressions and vocal tones than South Asian faces and voice tones. Therefore, assumptions cannot be made regarding greater attunement to NVB between similar groups, as the accuracy in NVB decoding appears to be related more to the influence of the dominant culture. 3.7. Cultural preferences for NVBs: qualitative studies The qualitative studies included in our review revealed explicit patient preferences and expectations for certain NVBs as part of empathic care [70–73,76–78]. They are summarized in Table 2. 4. Discussion Our systematic review results indicate that nonverbal expressions of empathy are essential components of cross-cultural clinical competency and quality care. However, optimal expression of empathic NVB can vary across cultural groups, especially in culturally diverse clinical settings. It appears that culture mediates nonverbal empathic expression on several levels, including race, nationality, gender, and occupation [64,66,67,69,71,74,79]. Greater 420 A. Lorié et al. / Patient Education and Counseling 100 (2017) 411–424 attention to and skill with interpreting and expressing NVB across such cultural groups can improve the provider-patient relationship and help to diminish disparities in quality of care. Several theories inform the interpretation of our findings, discussed below. 4.1. Emotion expression: cultural equivalence or cultural advantage model? Extensive research suggests that the expressions of six basic emotions (happiness, sadness, anger, fear, disgust, and surprise) are universal [80],2 though members of the same national or ethnic group may be more able to identify these facially-expressed emotions [82]. There has also been debate as to whether empathy, which encompasses the detection and expression of a broad range of emotions, is a capacity that can be expressed and understood universally (cultural equivalence model) or is subject to cultural norms (cultural advantage model) [58]. This raises the concern of whether specific nonverbal expressions of empathy may be universally interpreted or culturally dependent. For example, culturally determined power and status dynamics may drive certain expectations of nonverbal deference to authority figures, such as reduced or avoidance of direct eye contact with physicians. Such culturally dependent expectations of behavior, as revealed through NVB, may become more pronounced in cross-cultural patient-clinician encounters, risking further miscommunication within and between different cultural groups. These communication missteps may discourage patient participation, reduce shared decision-making and diminish patient-centered care, which could negatively impact the quality of care and ultimately, healthcare outcomes. for specific nonverbal expressions (e.g., gaze and proximity) that are context dependent [70,72,73,77]. Western physicians must take caution in cross-cultural contexts not to misinterpret acts of nodding or silence as signs of mutual understanding as these patient expressions could instead be masking confusion or suppressing emotions [71]. Missing or inaccurately decoding such NVB in a cross-cultural context may overlook patients’ physiological and psychological distress and could also decrease clinicians’ diagnostic acumen. Specific NVBs, such as eye contact, may also have various meanings. For example, a Filipino Canadian community voiced preference for more direct eye contact from providers, especially if the provider is giving instructions [73]. This same group also cautioned against the use of lowered eye contact, which can symbolize respect or shame depending on the context, as well as head-to-foot gaze, which could be interpreted as demeaning [73]. However, in direct contrast, a study with Caribbean medical students cautioned against the use of direct eye contact with some Caribbean elderly as this could be interpreted as a sign of disrespect [77]. In multiple studies, open body posture was assessed [64,65,75,77,79] and associated with patient ratings of clinician warmth and overall care. Proximity to the patient was generally viewed as empathic (e.g., Brazilians preferred closer proximity and warmth), although Williams et al. noted certain constraints by gender and age in Caribbean cultures (Table 2). These nuanced results further highlight that although training is often shaped by the dominant culture, it should be tailored to the norms of the local population. Therefore, a provider’s use and awareness of specific NVBs should be aligned with the specific cultural norms of patients to enhance both information exchange and patient satisfaction. 4.2. Cross-cultural considerations of nonverbal empathy 4.2.1. Race Whereas our review’s search terms aimed to capture a broad representation of cultural groups, our search ultimately yielded a predominance of American reports that focused on race as the cultural variable of interest in the patient-clinician encounter. This emphasis on race may reflect perceived racial bias in the U.S., belying a lengthy historical context of minority group oppression. Nonetheless, cross-racial communication issues may also extend to other cross-cultural communication contexts, particularly those examining group prejudices. Race plays a role in physicians’ NVB and its influence is best understood when physician race and patient race are considered jointly [64]. One study showed that AA physicians exhibited more positive NVB with AA patients than White physicians, in contrast to mixed positive and negative signals found between AA physicians interacting with White patients [64]. These findings suggest that NVB exists at both conscious and unconscious levels of awareness. In another study, high levels of perceived past discrimination by AA patients were correlated with a perceived lack of White physician’s positive affective tone and overall worse care [67]. This implies that clinicians working with discordant groups should be especially aware that past experiences of discrimination could influence how patients perceive the clinician’s nonverbal displays. 4.2.2. Nationality Differences in empathic nonverbal expressions were shown across cultural groups [64–68,73,74,79,83]; however, each cultural group valued and/or employed positive nonverbal signals. Some studies indicated that particular cultural groups have preferences 2 Also see Ref. [81]. L.F. Barrett, Are emotions natural kinds, Perspect. Psychol. Sci. 1, 2006, 28–58. 4.2.3. Gender and occupation NVB can vary according to gender and profession of the provider, however differences in NVB by gender and occupation are largely unexamined variables in the cross-cultural clinical context, and here we report preliminary findings. Zaletel et al. examined the frequency of NVBs in Slovenian nursing homes and found that male caregivers3 exhibited more negative NVBs (e.g., dropping the eyes, refusing by head shaking, frowning, staring, making grimaces) than female caregivers. Non-physician professional staff exhibited positive NVBs (e.g., making eye contact, smiling, raising the eyebrows, nodding) significantly more frequently than nonprofessional “helpers” [79]. Additionally, gender differences were noted in which female caregivers demonstrated mixed nonverbal patterns with their male patients [79]. Stepanikova et al. found that female physicians delivered highly positive nonverbal messages using smile and gaze but at the same time, their body position was more closed, suggesting a lack of social ease [64]. Studies of internationally educated nurses and physicians found that NVBs served both as barriers and compensatory strategies for empathic clinical care. Xu et al. [75] found that internationally educated nurses in the U.S. used therapeutic touch less frequently and were perceived as less warm by U.S. raters. The cultural norms regarding touch are particularly important to understand, as touch could be perceived as dominating or controlling, or as an expression of warmth and caring depending on the cultural group or cross-cultural context. In contrast, studies of internationally 3 The group of 267 caregivers (27 men, 240 women) consisted of three groups: nursing staff (graduate nurses and nurse assistants), social helpers (auxiliary personnel), and other non-physician professionals (physiotherapists, occupational therapists, social workers). A. Lorié et al. / Patient Education and Counseling 100 (2017) 411–424 421 educated clinicians [76,78] reported that clinicians attempted to compensate for language gaps by using more touch and emphasizing gestures, eye contact, smile, and friendliness to convey care. clinician samples that follow rigorous research methodologies, both in qualitative and quantitative investigations. 4.2.4. Intergroup and implicit bias In addition to racial and ethnic differences, the patientclinician relationship may be regarded as an intergroup interaction as there is an inherent power differential in the patientclinician relationship due to the clinician’s medical knowledge and experience, and the patient’s subordinate role of seeking medical advice. The power differential within the patientclinician relationship or the concept of “professional dominance” [84] can also be affected by various cultural factors, including nationality, socio-economic status, race, gender, and age. Current intergroup research indicates that prejudice toward different cultural groups often stems from implicit in-group biases, which results in favoring or being selective towards members that share the same group identity [85–88]. Our findings indicate that implicit bias can “leak out” through inadvertent negative nonverbal expressions and can be detected in the form of verbal dominance and lower patient positive affective tone [66]. Implicit biases could likewise be revealed in other inadvertent nonverbal expressions, such as closed body position or reduced eye contact [64]. Such culturally determined dynamics can seriously compromise successful clinical care and therefore require greater awareness of these NVBs to advance and strengthen crosscultural competency [24]. Nonverbal communication is a critical component of crosscultural competency, which includes demonstrating respect for patients and fostering empathy and trust. While these competencies appear to be universally valued, there are cultural differences in how they are expressed and reciprocated. Clinicians’ cultural competence can improve by learning the nonverbal norms of the various cultural backgrounds that they serve. There are crosscultural nonverbal practices that appear to be widely desired, such as open body posture, smile, and demonstrations of warmth by facial expression. There are also reports of NVBs that convey culturally different meanings, such as length and directness of eye gaze, meaning of hand gestures, and touch, and these must be used judiciously. This review summarized specific and generally desired NVB’s in the cultural studies that met our inclusion criteria (Appendix B). Specific techniques for training in cultural competency are described below. Empathy is a process that involves both receptive and expressive capacities [26], and clinicians in cross-cultural encounters require skills to perceive patient cues and express culturally sensitive nonverbal behaviors. This can be achieved by promoting clinician awareness of implicit race bias [66,67] and teaching appropriate responses. Specific techniques may include roleplaying, imagery, mindfulness training [67] and nonverbal skills training [26]. Values affirmation exercises prior to race-discordant clinical encounters can also enhance information exchange and perception of providers’ NVBs displays of warmth and respect [68]. Providers more skilled at cross-cultural NVB will also strengthen their perceived dedication and competency amongst patients, as well as help improve their diagnostic abilities by eliciting affective cues and establishing rapport with the patient [89]. These techniques are similar to the empathy training for medical trainees, previously reported, [26], which can be applied to cross-cultural interactions. Finally, how we train medical students and clinicians should reflect the diversity of the populations they serve, rather than the norms of the dominant culture in order to promote diagnostic accuracy, mutual respect, and trust. 5. Limitations This systematic review has several limitations. First, examining the provider-patient relationship, cultural dynamics, and NVB is a complex undertaking and definitions and naming conventions are heterogeneous. Second, we were limited to reviewing full-text articles in English after 1990, thereby potentially excluding relevant studies published pre-1990 or those published in other languages. Pragmatically, we were limited to English-only papers as we did not have ready access to translators or multilingual authors. Although this presents a serious limitation in crosscultural research, one key area of interest is how other cultures convey and perceive empathy via NVB as it relates to interactions with U.S.-based clinicians. As noted in our introduction, the U.S. is becoming more racially diverse and cross-cultural clinical encounters are on the rise. This is of particular interest as our systematic review allows us to make more concrete recommendations for our U.S.-based clinicians. The recent publication dates of many of the cited studies confirm intensified research and clinical interest in this topic due to rapidly changing demographics. Additionally, there were methodological limitations of several studies we examined. Two studies [65,75] included simulated patients, and although this design increases internal validity, it limits external validity. One study used a facial expression computer program to test provider facial expression decoding in lieu of direct clinical observation [74]. The sample sizes of our studies were generally small and insufficiently powered to assess confounding variables such as age, gender, socioeconomic status, clinical setting, language fluency or degree of acculturation. Most studies used convenience samples rather than randomized samples, and most were Western and Eurocentric-based. Furthermore, because members of the dominant culture typically code studies, additional coder bias may have been introduced. Together, these methodological limitations suggest cultural NVB is an important area for further research with larger patient and 6. Practice implications 7. Conclusion Nonverbal communication and culture permeate virtually every aspect of health care delivery, and this review demonstrates that additional research is needed. Some cultural groups have context-dependent preferences for certain NVBs [70,73,77]. This complicates detection and delivery of nonverbal signals among culturally discordant groups. Though culturally specific NVBs of empathy exist, we recognize that culture is dynamic and constantly changing, particularly in cross-cultural environments [90]. Our review of the literature highlights that culture not only shapes norms for NVB in medical encounters, but it also appears to mediate communication itself [64,66,67,71,74,79]. Therefore, greater training efforts are needed to improve perception and interpretation of patients’ NVB, and to enhance clinicians’ awareness of their own displays of empathic NVB. Both undergraduate and graduate medical education initiatives could encourage focus groups and specific training in this emerging area. Medical trainees increasingly represent multinational and multiracial backgrounds, or have worked in medical settings all over the world. Such trainees could be invited to share cultural norms from diverse backgrounds in experiential learning settings to inform traditional patient-doctor courses. Training programs in empathic behavior with patients from all backgrounds are needed. 422 A. Lorié et al. / Patient Education and Counseling 100 (2017) 411–424 Further research in empathic NVB is critical to the global health conversation. Currents in today’s world political landscape are creating additional urgency for training in cross-cultural competence. With massive shifts of minority groups into racially and ethnically dominant cultures, the misinterpretation of cultural norms and NVB can have dire consequences if cultural competence is not made a top priority – consequences not only for individuals and patients, but for populations as a whole. This review serves as a springboard to develop training programs that focus on empathic NVB with special attention to cross-cultural communication. Such training is urgently needed at the undergraduate and graduate level to improve cultural competency nationally and internationally in our increasingly diverse world. Conflict of interest disclosures Dr. Riess reports a financial interest in Empathetics, Inc. No other disclosures were reported. Author contributions Helen Riess had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the review. Study concept and design: Lorié, Phillips, Zhang, Riess Acquisition of data: Lorié, Reinero, Phillips, Zhang, Riess Analysis and interpretation of data: Lorié, Reinero, Phillips, Riess Drafting of the manuscript: Lorié, Reinero, Phillips, Riess Critical revision of the manuscript for intellectual content: Lorié, Reinero, Phillips, Riess Obtained funding: Riess Administrative, technical, or material support: Reinero Study supervision: Riess All authors gave final approval to the submitted paper. Ethical approval No ethical approval was required for the systematic review. Acknowledgments All authors gratefully acknowledge that this project was made possible with a grant from The Arnold P. Gold Foundation and the David Judah Fund. The Arnold P. Gold Foundation and the David Judah Fund had no role in study design, collection, analysis, interpretation of data, writing the report, nor in the decision to submit the report for publication. The authors would also like to thank Carole Foxman, Martha Stone, Lidia Schapira, M.D., and Arielle Gordon-Rowe for their invaluable assistance. 10 Touch/or touch*.ti,ab. (28443) 11 smiling/or (smile* or smiling).ti,ab. (3742) 12 (handshake* or shake hand* or hand shake*).ti,ab. (183) 13 lean*.ti,ab. (25884) 14 Posture/or postur*.ti,ab. (75225) 15 or/1-14 (311111) 16 Physician-Patient Relations/(59545) 17 Interpersonal Relations/(54776) 18 “Attitude of Health Personnel”/(90992) 19 Attitude/or additude*.ti,ab. (38762) 20 Trust/or trust.ti,ab. (20571) 21 stereotyping/or stereotyp*.ti,ab. (22961) 22 Personal Satisfaction/or satisf*.ti,ab. (198602) 23 communication barriers/or barrier*.ti,ab. (143193) 24 (doctor patient or patient doctor).ti,ab. (4900) 25 communication/or communicat*.ti,ab. (191659) 26 clinician*.ti,ab. (114903) 27 (patient adj1 physician).ti. (1816) 28 relations*.ti. (181398) 29 Primary Health Care/(53504) 30 medicine/or general practice/or family practice/(88263) 31 or/16-30 (1113105) 32 15 and 31 (37998) 33 exp Ethnic Groups/or ethnic*.ti,ab. (159069) 34 “Minority Groups”/or minorit*.ti,ab. (43777) 35 refugees/or “transients and migrants”/(14289) 36 Racism/or (race* or racial or racism or biracial).ti,ab. (94970) 37 Prejudice/or prejudic*.ti,ab. (24724) 38 Healthcare Disparities/or disparit*.ti,ab. (34508) 39 attitude to health/(72138) 40 health knowledge, attitudes, practice/(71692) 41 (culture* or cultural).ti,ab. (784151) 42 cross-cultural comparison/or cultural characteristics/or cultural competency/or cultural diversity/(44690) 43 exp geographic locations/(3206192) 44 exp Continental Population Groups/(152589) 45 or/33-44 (4116502) 46 32 and 45 (10064) 47 limit 46 to english language (9382) 48 limit 47 to yr = “1990–2014” (8719) 49 animal/(5256927) 50 48 not 49 (8586) 51 humans/and 48 (8330) 52 50 or 51 (8653) NOTE: A second search was run using these same search terms but adding the search statement: “cues/or (cue*1 or clue*1).ti,ab.” to the top of list, and identifying any new results as a consequence of this addition. Appendix B. . Inclusion and Exclusion Criteria Appendix A. . MEDLINE Electronic Search Strategy 1. ) Inclusion Criteria Database: Ovid MEDLINE(R) 1946 to Present 1 Empathy/or empath*.ti,ab. (16415) 2 compassion*.ti,ab. (4567) 3 affect/(24011) 4 eye contact.ti,ab. or Eye Movements/(23679) 5 (gaze* or gazing).ti,ab. (9762) 6 kinesics/or gestures/or (gesture* or body language).ti,ab. (4209) 7 nonverbal communication/or (non-verbal or nonverbal).ti,ab. (9773) 8 facial expression/or facial.ti,ab. (83410) 9 Voice Quality/or voice.ti,ab. (19708) Experimental or observational studies examining each of the following: 1) Communication, for example, “empathy”, “compassion”, “affective” “relationship”, “nonverbal”, “gaze”, “patient satisfaction” 2) Cultural groups, for example, “cross-cultural”, “socio-cultural”, various ethnic, racial, and country groups, “cultural competence”; 3) Clinician-patient interactions addressing health problems. 4) Studies reported in English, peer-reviewed papers, subjects > 18 years old, N 10. A. Lorié et al. / Patient Education and Counseling 100 (2017) 411–424 Exclusion Criteria Commentaries, reviews, dissertations, replies, and book chapters Studies on theoretical, hermeneutics, and concept analysis Studies on patients with severe neurologic impairment and disorders of face and neck that interfere communication Studies on patients with active psychosis or developmental disorders Studies on nonverbal healing through massage or dance therapy Studies on sex therapy/relationship counseling Studies on mother-infant bonding Studies on infants Studies on children Studies on auditory disorders Studies on pharmacy Studies on translator communication References [1] J.T. Berger, Culture and ethnicity in clinical care, Arch. Intern. Med. 158 (1998) 2085–2090. [2] B.B. Briggance, N. Burke, Shaping America's health care professions: the dramatic rise of multiculturalism, West. J. Med. 176 (2002) 62–64. [3] A. Kleinman, L. Eisenberg, B. Good, Culture, illness, and care: clinical lessons from anthropologic and cross-cultural research, Ann. Intern. Med. 88 (1978) 251–258. [4] L.A. Petersen, Racial differences in trust: reaping what we have sown, Med. Care 40 (2002) 81–84. [5] D.H. Thom, B. Campbell, Patient-physician trust: an exploratory study, J. Fam. Pract. 44 (1997) 169–176. [6] D.G. Safran, D.A. Taira, W.H. Rogers, M. Kosinski, J.E. Ware, A.R. Tarlov, Linking primary care performance to outcomes of care, J. Fam. Pract. 47 (1998) 213–220. [7] Kaiser Family Foundation, Race, Ethnicity and Medical Care, A Survey of Public Perceptions and Experiences, (1999) http://kff.org/disparities-policy/pollfinding/race-ethnicity-medical-care-a-survey-of/, (accessed 16.07.21). [8] A. Nelson, Unequal treatment: confronting racial and ethnic disparities in health care, J. Natl. Med. Assoc. 94 (2002) 666–668. [9] B. Freshman, L. Rubino, Emotional intelligence: a core competency for health care administrators, Health Care Manager 20 (2002) 1–9. [10] D.M. Tate, Cultural awareness: bridging the gap between caregivers and Hispanic patients, J. Contin. Educ. Nurs. 34 (2003) 213–217. [11] U.S. Census Bureau, U.S. Census Bureau Projections Show a Slower Growing, Older, More Diverse Nation a Half Century from Now, (2012) https://www. census.gov/newsroom/releases/archives/population/cb12-243.html, (accessed 16.07.21). [12] B. Rechel, P. Mladovsky, D. Ingleby, J.P. Mackenbach, M. McKee, Migration and health in an increasingly diverse Europe, Lancet 381 (2013) 1235–1245. [13] A. Tjale, L. De Villiers, Cultural Issues in Health and Health Care: A Resource Book for Southern Africa, Juta and Company Ltd., Cape Town, 2004. [14] J.S. Weissman, J. Betancourt, E.G. Campbell, E.R. Park, M. Kim, B. Clarridge, et al., Resident physicians' preparedness to provide cross-cultural care, J. Am. Med. Assoc. 294 (2005) 1058–1067. [15] B.K. Cheon, T. Im D-m Harada, J.-S. Kim, V.A. Mathur, J.M. Scimeca, et al., Cultural influences on neural basis of intergroup empathy, Neuroimage 57 (2011) 642–650. [16] M. de Greck, Z. Shi, G. Wang, X. Zuo, X. Yang, X. Wang, et al., Culture modulates brain activity during empathy with anger, Neuroimage 59 (2012) 2871–2882. [17] J.N. Gutsell, M. Inzlicht, Intergroup differences in the sharing of emotive states: neural evidence of an empathy gap, Soc. Cogn. Affect. Neurosci. 7 (2012) 596–603. [18] S. Han, G. Northoff, K. Vogeley, B.E. Wexler, S. Kitayama, M.E. Varnum, A cultural neuroscience approach to the biosocial nature of the human brain, Annu. Rev. Psychol. 64 (2013) 335–359. [19] J.A. Sabin, B.A. Nosek, A.G. Greenwald, F.P. Rivara, Physicians' implicit and explicit attitudes about race by MD race, ethnicity, and gender, J. Health Care Poor Underserved 20 (2009) 896–913. [20] J.R. Betancourt, A.R. Green, J.E. Carrillo, E.R. Park, Cultural competence and health care disparities: key perspectives and trends, Health Affair 24 (2005) 499–505. [21] J.R. Betancourt, J. Corbett, M.R. Bondaryk, Addressing disparities and achieving equity: cultural competence, ethics, and health-care transformation, Chest 145 (2014) 143–148. [22] M. Weathers, E. Frank, L.A. Spell, Differences in the communication of affect: members of the same race versus members of a different race, J. Black Psychol. 28 (2002) 66–77. 423 [23] M. van Ryn, J. Burke, The effect of patient race and socio-economic status on physicians' perceptions of patients, Soc. Sci. Med. 50 (2000) 813–828. [24] B.C. Schouten, L. Meeuwesen, Cultural differences in medical communication: a review of the literature, Patient Educ. Couns. 64 (2006) 21–34. [25] M.R. DiMatteo, R.D. Hays, L.M. Prince, Relationship of physicians' nonverbal communication skill to patient satisfaction, appointment noncompliance, and physician workload, Health Psychol. 5 (1986) 581. [26] H. Riess, J.M. Kelley, R.W. Bailey, E.J. Dunn, M. Phillips, Empathy training for resident physicians: a randomized controlled trial of a neuroscience-informed curriculum, J. Gen. Intern. Med. 27 (2012) 1280–1286. [27] H. Riess, J.M. Kelley, R. Bailey, P.M. Konowitz, S.T. Gray, Improving empathy and relational skills in otolaryngology residents a pilot study, Otolaryngol. Head Neck 144 (2011) 120–122. [28] G.B. Hickson, C.F. Federspiel, J.W. Pichert, C.S. Miller, J. Gauld-Jaeger, P. Bost, Patient complaints and malpractice risk, J. Am. Med. Assoc. 287 (2002) 2951–2957. [29] J.M. Hemmerdinger, S.D. Stoddart, R.J. Lilford, A systematic review of tests of empathy in medicine, BMC Med. Ed. 7 (2007) 24. [30] X. Liu, W. Rohrer, A. Luo, Z. Fang, T. He, W. Xie, Doctor–patient communication skills training in mainland China: a systematic review of the literature, Patient Educ. Couns. 98 (2015) 3–14. [31] J.R. Betancourt, Cross-cultural medical education: conceptual approaches and frameworks for evaluation, Acad. Med. 78 (2003) 560–569. [32] R.C.-Y. Chung, F. Bemak, The relationship of culture and empathy in crosscultural counseling, J. Couns. Dev. 80 (2002) 154–159. [33] C. Brant, Communication patterns in Indians: verbal and non-verbal, Ann. Sex Res. 6 (1993) 259–269. [34] A.J. Marsella, Counseling and psychotherapy with Japanese Americans: crosscultural considerations, Am. J. Orthopsychiatry 63 (1993) 200–208. [35] J.L. Mitchell, Cross-cultural issues in the disclosure of cancer, Cancer Pract. 6 (1998) 153–160. [36] V.C. Mullin, S.E. Cooper, S. Eremenco, Communication in a South African cancer setting: cross-cultural implications, Int. J. Rehabil. Health 4 (1998) 69–82. [37] Y. Xu, R. Davidhizar, Intercultural communication in nursing education: when Asian students and American faculty converge, J. Nurs. Educ. 44 (2005) 209–215. [38] G. Juckett, Cross-cultural medicine, Am. Fam. Phys. 72 (2005) 2267–2274. [39] H. Riess, G. Kraft-Todd, EMPATHY: a tool to enhance nonverbal communication between clinicians and their patients, Acad. Med. 89 (2014) 1108–1112. [40] A. Mehrabian, Nonverbal Communication, Transaction Publishers, 1977. [41] S.A. Buetow, Something in nothing: negative space in the clinician-patient relationship, Ann. Fam. Med. 7 (2009) 80–83. [42] W.M. Caris-Verhallen, A. Kerkstra, J.M. Bensing, Non-verbal behaviour in nurse-elderly patient communication, J. Adv. Nurs. 29 (1999) 808–818. [43] A. Duffy, Non-verbal communication in cancer and palliative care, Nurs. Times 102 (2006) 30–31. [44] A.F. Hannawa, Shedding light on the dark side of doctor-patient interactions: verbal and nonverbal messages physicians communicate during error disclosures, Patient Educ. Couns. 84 (2011) 344–351. [45] H. Ishikawa, H. Hashimoto, M. Kinoshita, S. Fujimori, T. Shimizu, E. Yano, Evaluating medical students' non-verbal communication during the objective structured clinical examination, Med. Ed. 40 (2006) 1180–1187. [46] L. Kacperek, Clinical. Non-verbal communication: the importance of listening, Br. J. Nurs. 6 (1997) 275–279. http://www.magonlinelibrary.com/doi/abs/ 10.12968/bjon.1997.6.5.275. [47] E.R. Tilson, S.D. Gibson, High-touch patient care in radiology, Semin. Radiol. Technol. 7 (1999) 1. [48] S. Henry, A. Fuhrel-Forbis, M. Rogers, S. Eggly, Association between nonverbal communication during clinical interactions and outcomes: a systematic review and meta-analysis, Patient Educ. Couns. 86 (2012) 297–315. [49] R.S. Beck, R. Daughtridge, P.D. Sloane, Physician-patient communication in the primary care office: a systematic review, J. Am. Board Fam. Pract. 15 (2002) 25–38. [50] D.L. Roter, R.M. Frankel, J.A. Hall, D. Sluyter, The expression of emotion through nonverbal behavior in medical visits, J. Gen. Intern. Med. 21 (2006) S28–S34. [51] J.R. Betancourt, A.R. Green, J.E. Carrillo, O. Ananeh-Firempong, Defining cultural competence: a practical framework for addressing racial/ethnic disparities in health and health care, Public Health Rep. 118 (2003) 293–302. [52] J. Betancourt, M. Cervantes, Cross-cultural medical education in the United States: key principles and experiences, Kaohsiung J. Med. Sci. 25 (2009) 471–478. [53] M.M. Maier-Lorentz, Transcultural nursing: its importance in nursing practice, J. Cult. Divers. 15 (2008) 37–43. [54] G. Flores, Culture and the patient-physician relationship: achieving cultural competency in health care, J. Pediatr. 136 (2000) 14–23. [55] D.W. Sue, C.M. Capodilupo, G.C. Torino, J.M. Bucceri, A. Holder, K.L. Nadal, et al., Racial microaggressions in everyday life: implications for clinical practice, Am. Psychol. 62 (2007) 271. [56] Y.-W. Wang, M.M. Davidson, O.F. Yakushko, H.B. Savoy, J.A. Tan, J.K. Bleier, The scale of ethnocultural empathy: development, validation, and reliability, J. Couns. Psychol. 50 (2003) 221. [57] E.A. Segal, Social empathy: a model built on empathy, contextual understanding, and social responsibility that promotes social justice, J. Soc. Serv. Res. 37 (2011) 266–277. 424 A. Lorié et al. / Patient Education and Counseling 100 (2017) 411–424 [58] J.A. Soto, R.W. Levenson, Emotion recognition across cultures: the influence of ethnicity on empathic accuracy and physiological linkage, Emotion 9 (2009) 874. [59] S. De Maesschalck, M. Deveugele, S. Willems, Language, culture and emotions: exploring ethnic minority patients' emotional expressions in primary healthcare consultations, Patient Educ. Couns. 84 (2011) 406–412. [60] E. Kale, A. Finset, H.-L. Eikeland, P. Gulbrandsen, Emotional cues and concerns in hospital encounters with non-western immigrants as compared with Norwegians: an exploratory study, Patient Educ. Couns. 84 (2011) 325–331. [61] C.S. Levine, N. Ambady, The role of non-verbal behaviour in racial disparities in health care: implications and solutions, Med. Ed. 47 (2013) 867–876. [62] E. Kale, K. Skjeldestad, A. Finset, Emotional communication in medical consultations with native and non-native patients applying two different methodological approaches, Patient Educ. Couns. 92 (2013) 366–374. [63] G. Smith, Communication and culture. In: Holt RaW (Ed.) New York (1966). [64] I. Stepanikova, Q. Zhang, D. Wieland, G. Eleazer, T. Stewart, Non-verbal communication between primary care physicians and older patients: how does race matter, J. Gen. Intern. Med. 27 (2012) 576–581. [65] M.S. Aruguete, C.A. Roberts, Participants' ratings of male physicians who vary in race and communication style, Psychol. Rep. 91 (2002) 793–806. [66] L.A. Cooper, D.L. Roter, K.A. Carson, M.C. Beach, J.A. Sabin, A.G. Greenwald, et al., The associations of clinicians' implicit attitudes about race with medical visit communication and patient ratings of interpersonal care, Am. J. Public Health 102 (2012) 979–987. [67] L.R. Hausmann, M.J. Hannon, D.M. Kresevic, B.H. Hanusa, C. Kwoh, S.A. Ibrahim, Impact of perceived discrimination in healthcare on patient-provider communication, Med. Care 49 (2011) 626–633. [68] E.P. Havranek, R. Hanratty, C. Tate, L.M. Dickinson, J.F. Steiner, G. Cohen, et al., The effect of values affirmation on race-discordant patient-provider communication, Arch. Intern. Med. 172 (2012) 1662–1667. [69] R.L. Johnson, D. Roter, N.R. Powe, L.A. Cooper, Patient race/ethnicity and quality of patient-physician communication during medical visits, Am. J. Public Health 94 (2004) 2084–2090. [70] A.A. Bergman, S.L. Connaughton, What is patient-centered care really: voices of hispanic prenatal patients, Health Commun. 28 (2013) 789–799. [71] S. Shahid, L.D. Finn, S.C. Thompson, Barriers to participation of aboriginal people in cancer care: communication in the hospital setting, Med. J. Aust. 190 (2009) 574–579. [72] T.E. Roberts, Health practices and expectations of Brazilians in the United States, J. Cult. Divers. 14 (2007) 192–197. [73] A.C.Y. Pasco, J.M. Morse, J.K. Olson, Cross-cultural relationships between nurses and filipino Canadian patients, J. Nurs. Scholarsh. 36 (2004) 239–246. [74] K. Coelho, C. Galan, Physician cross-cultural nonverbal communication skills, patient satisfaction and health outcomes in the physician-patient relationship, Int. J. Fam. Med. (2012) (Article ID 376907:5). [75] Y. Xu, S. Staples, J.J. Shen, Nonverbal communication behaviors of internationally educated nurses and patient care, Res. Theory Nurs. Pract. 26 (2012) 290–308. [76] P. Jain, J.L. Krieger, Moving beyond the language barrier: the communication strategies used by international medical graduates in intercultural medical encounters, Patient Educ. Couns. 84 (2011) 98–104. [77] S. Williams, M. Harricharan, B. Sa, Nonverbal communication in a caribbean medical school: touch is a touchy issue, Teach. Learn. Med. 25 (2013) 39–46. [78] M. Jirwe, K. Gerrish, A. Emami, Student nurses experiences of communication in cross-cultural care encounters, Scand. J. Caring Sci. 24 (2010) 436–444. [79] M. Zaletel, A.N. Kovacev, R.P. Mikus, L.Z. Kragelj, Nonverbal communication of caregivers in Slovenian nursing homes, Arch. Gerontol. Geriatr 54 (2012) 94–101. [80] P. Ekman, Emotions Across Cultures. In: Books T, (Ed.) New York (2003). [81] L.F. Barrett, Are emotions natural kinds, Perspect. Psychol. Sci. 1 (2006) 28–58. [82] H.A. Elfenbein, N. Ambady, On the universality and cultural specificity of emotion recognition: a meta-analysis, Psychol. Bull. 128 (2002) 203–235. [83] J.A. Harrigan, R. Rosenthal, Physicians' head and body positions as determinants of perceived rapport, J. Appl. Soc. Psychol. 13 (1983) 496–509. [84] E. Freidson, Profession of medicine: a study of the sociology of applied knowledge. In: Dodd MC, (ed.) New York (1970). [85] M.R. Banaji, A.G. Greenwald, Blindspot Hidden Biases of Good People, Random House Publishing Group, 2013. [86] A.R. Green, D.R. Carney, D.J. Pallin, L.H. Ngo, K.L. Raymond, L.I. Iezzoni, et al., Implicit bias among physicians and its prediction of thrombolysis decisions for black and white patients, J. Gen. Intern. Med. 22 (2007) 1231–1238. [87] H. Tajfel, J.C. Turner, An integrative theory of intergroup conflict. In: Brooks/ Cole, editor. The social psychology of intergroup relations In: W.G. Austin, S. Worchel (Eds.). Monterey, CA (1979) p. 33–47. [88] J.C. Turner, Some current issues in research on social identity and selfcategorization theories, Soc. Identity: Context Commitment Content (1999) 6–34. [89] D.L. Roter, J.A. Hall, N.R. Katz, Relations between physicians' behaviors and analogue patients' satisfaction, recall, and impressions, Med. Care (1987) 437–451. [90] D. Matsumoto, Cultural similarities and differences in display rules, Motiv. Emotion 14 (1990) 195–214.