Cultural Adaptations of Prolonged Exposure Therapy for Treatment and Prevention of Posttraumatic Stress Disorder in African Americans
Abstract
:1. Introduction
1.1. Posttraumatic Stress Disorder
1.2. PTSD in African Americans
1.2.1. Prevalence
1.2.2. Trauma Cognitions
1.2.3. Treatment Seeking and Barriers to Treatment
1.2.4. Race-Based Trauma
1.3. Psychotherapeutic Treatments for PTSD
2. Prolonged Exposure Therapy for African Americans
2.1. Cultural Education
2.2. Assessment
2.3. Psychoeducation and Preparation for Treatment
2.4. In Vivo Exposure
2.5. Imaginal Exposure
2.6. Processing
3. Case Examples
3.1. Case # 1: PE for Treatment of Racism-Related PTSD
3.2. Case # 2: Culturally Modified PE for Prevention of PTSD
4. Discussion
4.1. Assessment Issues
4.2. Treatment Issues
4.3. Limitations and Future Directions
5. Conclusions
Acknowledgments
Author Contributions
Conflicts of Interest
References
- Association Psychological Association. Diagnostic and Statistical Manual of Mental Disorders: DSM-5; American Psychiatric Association: Washington, DC, USA, 2013. [Google Scholar]
- Friedman, M.J.; Resick, P.A.; Bryant, R.A.; Brewin, C.R. Considering PTSD for DSM-5. Depress. Anxiety 2011, 28, 750–769. [Google Scholar] [CrossRef]
- Williams, M.T.; Cahill, S.; Foa, E. Psychotherapy for post-traumatic stress disorder. In Textbook of Anxiety Disorders, 2nd ed.; Stein, D., Hollander, E., Rothbaum, B., Eds.; American Psychiatric Publishing: Washington, DC, USA, 2010. [Google Scholar]
- Brady, K.T.; Killeen, T.K.; Brewerton, T.; Lucerini, S. Comorbidity of psychiatric disorders and posttraumatic stress disorder. J. Clin. Psychiatry 2000, 61, 22–32. [Google Scholar] [CrossRef]
- Helms, J.E.; Nicolas, G.; Green, C.E. Racism and ethnoviolence as trauma: Enhancing professional training. Traumatology 2012, 16, 53–62. [Google Scholar] [CrossRef]
- Carter, R.T. Racism and psychological and emotional injury: Recognizing and assessing race-based traumatic stress. Couns. Psychol. 2007, 35, 13–105. [Google Scholar] [CrossRef]
- American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders: DSM-IV-TR; American Psychiatric Association: Washington, DC, USA, 2006. [Google Scholar]
- Himle, J.A.; Baser, R.E.; Taylor, R.J.; Campbell, R.D.; Jackson, J.S. Anxiety disorders among African Americans, Blacks of Caribbean Descent, and Non-Hispanic Whites in the United States. J. Anxiety. Disord. 2009, 23, 578–590. [Google Scholar] [CrossRef]
- Williams, M.T.; Gooden, A.M.; Davis, D. African Americans, European Americans, and Pathological Stereotypes: An African-Centered Perspective. In Psychology of Culture; Hayes, G.R., Bryant, M.H., Eds.; Nova Science Publishers: Hauppauge, NY, USA, 2012. [Google Scholar]
- Zoellner, L.A.; Feeny, N.C.; Fitzgibbons, L.A.; Foa, E.B. Response of African American and Caucasian women to cognitive behavioral therapy for PTSD. Behav. Ther. 1999, 30, 581–595. [Google Scholar] [CrossRef]
- Poulin, M.; Silver, C.R. World benevolence beliefs and well-being across the life span. Psychol. Aging 2008, 23, 13–23. [Google Scholar] [CrossRef]
- Williams, M.; Jayawickreme, N.; Sposato, R.; Foa, E.B. Race-Specific associations between trauma cognitions and symptoms of alcohol dependence in individuals with comorbid PTSD and alcohol dependence. Addict. Behav. 2012, 37, 47–52. [Google Scholar] [CrossRef]
- Brunello, N.; Davidson, J.R.; Deahl, M.; Kessler, R.C.; Mendlewicz, J.; Racagni, G.; Shalev, A.Y.; Zohar, J. Posttraumatic stress disorder: Diagnosis and epidemiology, comorbidity and social consequences, biology and treatment. Neuropsychobiology 2001, 43, 150–162. [Google Scholar]
- Davis, R.G.; Ressler, K.J.; Schwartz, A.C.; Stephens, K.; James, B.; Rebekah, G. Treatment barriers for low-income, urban African Americans with undiagnosed posttraumatic stress disorder. J. Trauma. Stress 2008, 21, 218–222. [Google Scholar] [CrossRef]
- Abdullah, T.; Brown, T.L. Mental illness stigma and ethnocultural beliefs, values, and norms: An integrative review. Clin. Psychol. Rev. 2011, 31, 934–948. [Google Scholar] [CrossRef]
- Williams, M.T.; Domanico, J.; Marques, L.; Leblanc, N.J.; Turkheimer, E. Barriers to treatment among African Americans with obsessive-compulsive disorder. J. Anxiety Disord. 2012, 26, 555–563. [Google Scholar] [CrossRef]
- Lester, K.; Resick, P.A.; Young-Xu, Y.; Artz, C. Impact of race on early treatment termination and outcomes in posttraumatic stress disorder treatment. J. Consult. Clin. Psychol. 2010, 78, 480–489. [Google Scholar] [CrossRef]
- Banks, K.; Kohn-Wood, L. The influence of racial identity profiles on the relationship between racial discrimination and depressive symptoms. J. Black Psychol. 2007, 33, 331–354. [Google Scholar] [CrossRef]
- Blume, A.W.; Lovato, L.V.; Thyken, B.N.; Denny, N. The relationship of microaggressions with alcohol use and anxiety among ethnic minority college students in a historically white institution. Cult. Divers. Ethn. Minor. Psychol. 2012, 18, 45–54. [Google Scholar] [CrossRef]
- Chae, D.H.; Lincoln, K.D.; Jackson, J.S. Discrimination, attribution, and racial group identification: Implications for psychological distress among Black Americans in the National Survey of American Life (2001–2003). Am. J. Orthopsychiatr. 2011, 81, 498–506. [Google Scholar] [CrossRef]
- Pieterse, A.; Todd, N.R.; Neville, H.A.; Carter, R.T. Perceived racism and mental health among Black American adults: A meta-analytic review. J. Couns. Psychol. 2012, 59, 1–9. [Google Scholar] [CrossRef]
- Parham, T.A. Counseling models for African Americans. In Counseling Persons of African Descent; Parham, T.A., Ed.; Sage: Thousand Oaks, CA, USA, 2002; pp. 100–118. [Google Scholar]
- Gaertner, S.L.; Dovidio, J.F. Understanding and addressing contemporary racism: From aversive racism to the common ingroup identity model. J. Soc. Issues 2005, 61, 615–639. [Google Scholar] [CrossRef]
- Franklin, A.J. Invisibility syndrome and racial identity development in psychotherapy and counseling African American men. Couns. Psychol. 1999, 27, 761–793. [Google Scholar] [CrossRef]
- Pierce, C.; Carew, J.; Pierce-Gonzalez, D.; Willis, D. An experiment in racism: TV commercials. In Television and Education; Pierce, C., Ed.; Sage: Beverly Hills, CA, USA, 1978; pp. 62–88. [Google Scholar]
- Sue, D.W.; Capodilupo, C.M.; Torino, G.C.; Bucceri, J.M.; Holder, A.M.; Nadal, K.L.; Esquilin, M. Racial microaggressions in everyday life: Implications for clinical practice. Am. Psychol. 2007, 62, 271–286. [Google Scholar] [CrossRef]
- C’de Baca, J.; Castillo, D.; Qualls, C. Ethnic differences in symptoms among female veterans diagnosed with PTSD. J. Trauma Stress 2012, 25, 353–357. [Google Scholar] [CrossRef]
- Davis, J.J.; Walter, K.H.; Chard, K.M.; Parkinson, R.B.; Houston, W.S. Treatment adherence in cognitive processing therapy for combat-related PTSD with history of mild TBI. Rehabil. Psychol. 2013, 58, 36–42. [Google Scholar] [CrossRef]
- Kleim, B.; Grey, N.; Wild, J.; Nussbeck, F.W.; Stott, R.; Hackmann, A.; Clark, D.M.; Ehlers, A. Cognitive change predicts symptom reduction with cognitive therapy for Posttraumatic Stress Disorder. J. Consult. Clin. Psychol. 2013, 81, 383–393. [Google Scholar] [CrossRef]
- Foa, E.B.; Dancu, C.V.; Hembree, E.A.; Jaycox, L.H.; Meadows, E.A.; Street, G.P. A comparison of exposure therapy, stress inoculation training, and their combination for reducing Posttraumatic Stress Disorder in female assault victims. J. Consult. Clin. Psychol. 1999, 67, 194–200. [Google Scholar] [CrossRef]
- Feske, U. Treating low-income and minority women with posttraumatic stress disorder: A pilot study comparing prolonged exposure and treatment as usual conducted by community therapists. J. Interpers. Violence 2008, 23, 1027–1040. [Google Scholar] [CrossRef]
- Institute of Medicine (IOM). Treatment of Posttraumatic Stress Disorder: An Assessment of the Evidence; National Academic Press: Washington, DC, USA, 2008. [Google Scholar]
- Foa, E.B.; Gillihan, S.J.; Bryant, R.A. Challenges and successes in dissemination of evidence-based treatments for posttraumatic stress: Lessons learned from prolonged exposure therapy for PTSD. Psychol. Sci. Publ. Interest 2013, Supplement. 14, 65–111. [Google Scholar] [CrossRef]
- Marshall, R.D.; Suh, E.J. Contextualizing trauma: Using evidence-based treatments in a multicultural community after 9/11. Psychiatri. Q. 2003, 74, 401–420. [Google Scholar] [CrossRef]
- U.S. Department of Health and Human Services. Mental health: Culture, Race, and Ethnicity—A Supplement to mental health: A report of the Surgeon General; U.S. Department of Health and Human Services, Substance Abuse and Mental Health Services Administration, Center for Mental Health Services: Rockville, MD, USA, 2001. [Google Scholar]
- Suite, D.H.; La Bril, R.; Primm, A.; Harrison-Ross, P. Beyond misdiagnosis, misunderstanding and mistrust: Relevance of the historical perspective in the medical and mental health treatment of people of color. J. Natl. Med. Assoc. 2007, 99, 879–885. [Google Scholar]
- Pole, N.; Gone, J.P.; Kulkarni, M. Posttraumatic Stress Disorder among ethnoracial minorities in the United States. Clin. Psychol: Sci. Pract. 2008, 15, 35–61. [Google Scholar] [CrossRef]
- Sue, S.; Fujino, D.C.; Hu, L.; Takeuchi, D.; Zane, N. Community mental health services for ethnic minority groups: A test of the cultural responsiveness hypothesis. J. Consult. Clin. Psychol. 1991, 59, 533–540. [Google Scholar] [CrossRef]
- Utsey, S.O.; Giesbrecht, N.; Hook, J.; Stanard, P.M. Cultural, sociofamilial, and psychological resources that inhibit psychological distress in African Americans exposed to stressful life events and race-related stress. J. Couns. Psychol. 2008, 55, 49–62. [Google Scholar] [CrossRef]
- Helms, J.E. Toward a theoretical explanation of the effects of race on counseling a Black and White Model. Couns. Psychol. 1984, 12, 153–165. [Google Scholar] [CrossRef]
- Chapman, L.K.; DeLapp, R.; Williams, M.T. Impact of Race, Ethnicity, and Culture on the Expression and Assessment of Psychopathology. In Adult Psychopathology and Diagnosis, 7th ed.; Beidel, D.C., Frueh, B.C., Hersen, M., Eds.; John Wiley & Sons: Hoboken, NJ, USA, 2014. [Google Scholar]
- Owen, J.J.; Tao, K.; Leach, M.M.; Rodolfa, E. Clients’ perceptions of their psychotherapists’ multicultural orientation. Psychotherapy 2011, 48, 274–282. [Google Scholar] [CrossRef]
- Terwilliger, J.M.; Bach, N.; Bryan, C.; Williams, M.T. Multicultural vs. colorblind ideology: Implications for mental health and counseling. In Psychology of Counseling; DiFabio, A., Ed.; Nova Science Publishing: Hauppauge, NY, USA, 2013. [Google Scholar]
- Foa, E.B. Posttraumatic Diagnostic Manual; National Computer System: Minneapolis, NY, USA, 1996. [Google Scholar]
- Foa, E.B.; Cashman, L.; Jaycox, L.; Perry, K. The validation of a self-report measure of posttraumatic stress disorder: The Posttraumatic Diagnostic Scale. Psychol. Assess. 1997, 9, 445–451. [Google Scholar] [CrossRef]
- Hood, S.K.; Carter, M.M. A preliminary examination of trauma history, locus of control, and PTSD symptom severity in African American women. J. Black Psychol. 2008, 34, 179–191. [Google Scholar] [CrossRef]
- Powers, M.B.; Gillihan, S.J.; Rosenfield, D.; Jerud, A.B.; Foa, E.B. Reliability and validity of the PDS and PSS-I among participants with PSTD and alcohol dependence. J. Anxiety Disord. 2012, 26, 617–623. [Google Scholar] [CrossRef]
- Constantine, M.G. Racial microaggressions against African American clients in cross-racial counseling relationships. J. Couns. Psychol. 2007, 54, 1–16. [Google Scholar] [CrossRef]
- Resick, P.A.; Galovski, T.E.; Uhlmansiek, M.O.; Scher, C.D.; Clum, G.A.; Young-Xu, Y. A randomized clinical trial to dismantle components of cognitive processing therapy for Posttraumatic Stress Disorder in female victims of interpersonal violence. J. Consult. Clin. Psychol. 2008, 76, 243–258. [Google Scholar] [CrossRef]
- Resick, P.A.; Jordan, C.G.; Girelli, S.A.; Hutter, C.K.; Marhoeder-Dvorak, S.A. The study of behavioral group therapy for sexual assault victims. Behav. Ther. 1988, 19, 385–401. [Google Scholar] [CrossRef]
- Comas-Diaz, L.; Jacobsen, F.M. Ethnocultural allodynia. J. Psychother. Pract. Res. 2001, 10, 246–252. [Google Scholar]
- Chapman, L.K.; Steger, M.F. Race and religion: Differential prediction of anxiety symptoms by religious coping in African American and European American young adults. Depress. Anxiety 2010, 27, 316–322. [Google Scholar] [CrossRef]
- Klonoff, E.A.; Landrine, H. Cross-validation of the Schedule of Racist Events. J. Black Psychol. 1999, 25, 231–255. [Google Scholar] [CrossRef]
- Sellers, R.M.; Rowley, S.A.J.; Chavous, T.M.; Shelton, J.N.; Smith, M.A. Multidimensional Inventory of Black Identity: Preliminary investigation of reliability and construct validity. J. Pers. Soc. Psychol. 1997, 73, 805–815. [Google Scholar] [CrossRef]
- Phinney, J.S. The Multigroup Ethnic Identity Measure: A new scale for use with diverse groups. J. Adolesc. Res. 1992, 7, 156–176. [Google Scholar] [CrossRef]
- Roberts, R.E.; Phinney, J.S.; Masse, L.C.; Chen, Y.R.; Roberts, C.R.; Romero, A. The structure of ethnic identity of young adolescents from diverse ethnocultural groups. J. Early Adolesc. 1999, 19, 301–322. [Google Scholar] [CrossRef]
- Williams, M.T.; Chapman, L.K.; Wong, J.; Turkheimer, E. The Role of Ethnic Identity in Symptoms of Anxiety and Depression in African Americans. Psychiatry Res. 2012, 199, 31–36. [Google Scholar] [CrossRef]
- Landrine, H.; Klonoff, E.A. The Schedule of Racist Events: A measure of racial discrimination and a study of its negative physical and mental health consequences. J. Black Psychol. 1996, 22, 144–168. [Google Scholar] [CrossRef]
- Landrine, H.; Klonoff, E.A. frican-American Acculturation: Deconstructing Race and Reviving Culture; Sage: Thousand Oaks, CA, USA, 1996. [Google Scholar]
- Pargament, K.I.; Smith, B.W.; Koenig, H.G.; Perez, L. Patterns of positive and negative religious coping with major life stressors. J. Sci. Stud. Relig. 1998, 37, 710–724. [Google Scholar] [CrossRef]
- Egbert, N.; Mickley, J.; Coeling, H. A review and application of social scientific measures of religiosity and spirituality: Assessing a missing component in health communication research. Health Commun. 2004, 16, 7–27. [Google Scholar] [CrossRef]
- Chatters, L.M.; Taylor, R.J.; Jackson, J.S.; Lincoln, K.D. Religious Coping among African Americans, Caribbean Blacks and Non-Hispanic Whites. J. Community Psychol. 2008, 36, 371–386. [Google Scholar] [CrossRef]
- Beck, A.T.; Steer, R.A.; Brown, G.K. Manual for Beck Depression Inventory-II (BDI-II); Psychological Corporation: San Antonio, TX, USA, 1996. [Google Scholar]
- Dutton, G.R.; Grothe, K.B.; Jones, G.N.; Whitehead, D.; Kendra, K.; Brantley, P.J. Use of the Beck Depression Inventory-II with African American primary care patients. Gen. Hosp. Psychiatr. 2004, 26, 437–442. [Google Scholar] [CrossRef]
- Joe, S.; Woolley, M.E.; Brown, G.K.; Ghahramanlou-Holloway, M.; Beck, A.T. Psychometric properties of the Beck Depression Inventory-II in low-income, African American suicide attempters. J. Pers. Assess. 2008, 90, 521–523. [Google Scholar] [CrossRef]
- Foa, E.B.; Hembree, E.A.; Rothbaum, B. Prolonged Exposure Therapy for PTSD: Emotional Processing of Traumatic Experiences: Therapist Guide; Oxford University Press: New York, NY, USA, 2007. [Google Scholar]
- Mendoza, D.B.; Williams, M.T.; Chapman, L.K.; Powers, M. Minority inclusion in randomized clinical trials of panic disorder. J. Anxiety Disord. 2012, 26, 574–582. [Google Scholar] [CrossRef]
- Harrington, E.F.; Crowther, J.H.; Shipherd, J.C. Trauma, binge eating, and the “strong Black woman”. J. Consult. Clin. Psychol. 2010, 78, 469–479. [Google Scholar] [CrossRef]
- Buser, J.K. Treatment-seeking disparity between African Americans and Whites: Attitudes toward treatment, coping resources, and racism. J. Multicult. Counsel. Dev. 2009, 37, 94–104. [Google Scholar] [CrossRef]
- Ruggles, S. The origins of African-American family structure. Am. Socio. Rev. 1994, 59, 136–151. [Google Scholar] [CrossRef]
- Billingsley, A.; Caldwell, C. The church, the family and the school in the African American community. J. Negro Educ. 1991, 60, 427–440. [Google Scholar] [CrossRef]
- Neal-Barnett, A.M.; Stadulis, R.; Payne, M.R.; Crosby, L.; Mitchell, M.; Williams, L.; Williams-Costa, C. In the company of my sisters: Sister circles as an anxiety intervention for professional African American women. J. Affect. Disord. 2011, 129, 213–218. [Google Scholar] [CrossRef]
- Baldwin, J.A.; Bell, Y.R. The African Self-Consciousness Scale: An Africentric personality questionnaire. West J. Black Stud. 1985, 9, 61–68. [Google Scholar]
- Jackson, A.P.; Sears, S.J. Implications of an Africentric worldview in reducing stress for African American women. J. Couns. Dev. 1992, 71, 184–190. [Google Scholar] [CrossRef]
- Akbar, N. Mental disorder among African Americans. In Black Psychology, 3rd ed.; Jones, R., Ed.; Cobb & Henry: Berkeley, CA, USA, 1991; pp. 339–352. [Google Scholar]
- Mental health defined Africentrically. In African Psychology in Historical Perspective and Related Commentary; Azibo, D.A. (Ed.) Africa World Press: Trenton, NJ, USA, 1996; pp. 47–56.
- Kambon, K.K. The African Personality in America: An African-Centered Framework; Nubian Nation: Tallahassee, FL, USA, 1992. [Google Scholar]
- McLean, C.P.; Foa, E.B. Prolonged exposure therapy for post-traumatic stress disorder: A review of evidence and dissemination. Exp. Rev. Neurother. 2011, 11, 1151–1163. [Google Scholar] [CrossRef]
- Carter, R.T.; Forsyth, J.M. A guide to the forensic assessment of race-based traumatic stress reactions. J. Am. Acad. Psychiatr. 2009, 37, 28–40. [Google Scholar]
- Jaycox, L.H.; Foa, E.B. Obstacles in implementing exposure therapy for PTSD: Case discussions and practical solutions. Clin. Psychol. Psychother. 1996, 3, 176–184. [Google Scholar] [CrossRef]
- Foa, E.B.; Zoellner, L.A.; Feeny, N.C.; Hembree, E.A.; Alvarez-Conrad, J. Does imaginal exposure exacerbate PTSD symptoms? J. Consult. Clin. Psychol. 2002, 70, 1022–1028. [Google Scholar] [CrossRef]
- Foa, E.B.; Huppert, J.; Cahill, S.P. Emotional processing theory: An update. In Pathological Anxiety: Emotional Processing in Etiology and Treatment; Rothbaum, B., Ed.; Guilford Press: New York, NY, USA, 2006; pp. 3–24. [Google Scholar]
- Cokley, K.; Hall-Clark, B.; Hicks, D. Ethnic minority-majority status and mental health: The mediating role of perceived discrimination. J. Ment. Health Counsel. 2011, 33, 243–263. [Google Scholar]
- Smith, W.A.; Allen, W.R.; Danley, L.L. Assume the Position…You Fit the Description: College Students Experiences and Racial Battle Fatigue Among African American Male College Students. Am. Behav. Sci. 2007, 51, 551–578. [Google Scholar] [CrossRef]
- Woodger, D.; Cowan, J. Institutional racism in healthcare services: Using mainstream methods to develop a practical approach. Ethn. Inequal. Health Soc. Care 2010, 3, 36–44. [Google Scholar] [CrossRef]
- Rothbaum, B.O.; Kearns, M.C.; Price, M.; Malcoun, E.; Davis, M.; Ressler, K.J.; Lang, D.; Houry, D. Early intervention may prevent the development of posttraumatic stress disorder: A randomized pilot civilian study with modified prolonged Exposure. Biol. Psychiatr. 2012, 72, 957–963. [Google Scholar] [CrossRef]
- Pyke, K.D. What is internalized racial oppression and why don’t we study it? Acknowledging racism’s hidden injuries. Sociol. Perspectives 2010, 53, 551–572. [Google Scholar] [CrossRef]
- Malcoun, E.; Williams, M.T.; Bahojb-Nouri, L.V. Assessment of posttraumatic stress disorder in African Americans. In Guide to Psychological Assessments with African Americans; Benuto, L., Leany, B.D., Eds.; Springer: New York, NY, USA, 2015; forthcoming. [Google Scholar]
© 2014 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/3.0/).
Share and Cite
Williams, M.T.; Malcoun, E.; Sawyer, B.A.; Davis, D.M.; Nouri, L.B.; Bruce, S.L. Cultural Adaptations of Prolonged Exposure Therapy for Treatment and Prevention of Posttraumatic Stress Disorder in African Americans. Behav. Sci. 2014, 4, 102-124. https://doi.org/10.3390/bs4020102
Williams MT, Malcoun E, Sawyer BA, Davis DM, Nouri LB, Bruce SL. Cultural Adaptations of Prolonged Exposure Therapy for Treatment and Prevention of Posttraumatic Stress Disorder in African Americans. Behavioral Sciences. 2014; 4(2):102-124. https://doi.org/10.3390/bs4020102
Chicago/Turabian StyleWilliams, Monnica T., Emily Malcoun, Broderick A. Sawyer, Darlene M. Davis, Leyla Bahojb Nouri, and Simone Leavell Bruce. 2014. "Cultural Adaptations of Prolonged Exposure Therapy for Treatment and Prevention of Posttraumatic Stress Disorder in African Americans" Behavioral Sciences 4, no. 2: 102-124. https://doi.org/10.3390/bs4020102
APA StyleWilliams, M. T., Malcoun, E., Sawyer, B. A., Davis, D. M., Nouri, L. B., & Bruce, S. L. (2014). Cultural Adaptations of Prolonged Exposure Therapy for Treatment and Prevention of Posttraumatic Stress Disorder in African Americans. Behavioral Sciences, 4(2), 102-124. https://doi.org/10.3390/bs4020102