Polysubstance mortality trends in White and Black Americans during the opioid epidemic, 1999-2018.

Benzodiazepines Joinpoint trend analysis Opioids Polysubstance mortality Racial disparities Stimulants

Journal

BMC public health
ISSN: 1471-2458
Titre abrégé: BMC Public Health
Pays: England
ID NLM: 100968562

Informations de publication

Date de publication:
07 Jan 2024
Historique:
received: 15 10 2022
accepted: 21 12 2023
medline: 7 1 2024
pubmed: 7 1 2024
entrez: 6 1 2024
Statut: epublish

Résumé

Psychoactive drug combinations are increasingly contributing to overdose deaths among White and Black Americans. To understand the evolving nature of overdose crisis, inform policies, and develop tailored and equitable interventions, this study provides a comprehensive assessment of polysubstance mortality trends by race and sex during the opioid epidemic. We used serial cross-sectional US mortality data for White and Black populations from 1999 through 2018 to calculate annual age-adjusted death rates (AADR) involving any opioid, opioid subtypes, benzodiazepines, cocaine, psychostimulants, or combinations of these drugs, stratified by race and sex. Trend changes in AADR were analyzed using joinpoint regression models and expressed as average annual percent change (AAPC) during each period of the three waves of the opioid epidemic: 1999-2010 (wave 1), 2010-2013 (wave 2), and 2013-2018 (wave 3). Prevalence measures assessed the percent co-involvement of an investigated drug in the overall death from another drug. Polysubstance mortality has shifted from a modest rise in death rates due to benzodiazepine-opioid overdoses among White persons (wave 1) to a substantial increase in death rates due to illicit drug combinations impacting both White and Black populations (wave 3). Concurrent cocaine-opioid use had the highest polysubstance mortality rates in 2018 among Black (5.28 per 100,000) and White (3.53 per 100,000) persons. The steepest increase in death rates during wave 3 was observed across all psychoactive drugs when combined with synthetic opioids in both racial groups. Since 2013, Black persons have died faster from cocaine-opioid and psychostimulant-opioid overdoses. Between 2013 and 2018, opioids were highly prevalent in cocaine-related deaths, increasing by 33% in White persons compared to 135% in Blacks. By 2018, opioids contributed to approximately half of psychostimulant and 85% of benzodiazepine fatal overdoses in both groups. The magnitude and type of drug combinations with the highest death rates differed by race and sex, with Black men exhibiting the highest overdose burden beginning in 2013. The current drug crisis should be considered in the context of polysubstance use. Effective measures and policies are needed to curb synthetic opioid-involved deaths and address disparate mortality rates in Black communities.

Sections du résumé

BACKGROUND BACKGROUND
Psychoactive drug combinations are increasingly contributing to overdose deaths among White and Black Americans. To understand the evolving nature of overdose crisis, inform policies, and develop tailored and equitable interventions, this study provides a comprehensive assessment of polysubstance mortality trends by race and sex during the opioid epidemic.
METHODS METHODS
We used serial cross-sectional US mortality data for White and Black populations from 1999 through 2018 to calculate annual age-adjusted death rates (AADR) involving any opioid, opioid subtypes, benzodiazepines, cocaine, psychostimulants, or combinations of these drugs, stratified by race and sex. Trend changes in AADR were analyzed using joinpoint regression models and expressed as average annual percent change (AAPC) during each period of the three waves of the opioid epidemic: 1999-2010 (wave 1), 2010-2013 (wave 2), and 2013-2018 (wave 3). Prevalence measures assessed the percent co-involvement of an investigated drug in the overall death from another drug.
RESULTS RESULTS
Polysubstance mortality has shifted from a modest rise in death rates due to benzodiazepine-opioid overdoses among White persons (wave 1) to a substantial increase in death rates due to illicit drug combinations impacting both White and Black populations (wave 3). Concurrent cocaine-opioid use had the highest polysubstance mortality rates in 2018 among Black (5.28 per 100,000) and White (3.53 per 100,000) persons. The steepest increase in death rates during wave 3 was observed across all psychoactive drugs when combined with synthetic opioids in both racial groups. Since 2013, Black persons have died faster from cocaine-opioid and psychostimulant-opioid overdoses. Between 2013 and 2018, opioids were highly prevalent in cocaine-related deaths, increasing by 33% in White persons compared to 135% in Blacks. By 2018, opioids contributed to approximately half of psychostimulant and 85% of benzodiazepine fatal overdoses in both groups. The magnitude and type of drug combinations with the highest death rates differed by race and sex, with Black men exhibiting the highest overdose burden beginning in 2013.
CONCLUSIONS CONCLUSIONS
The current drug crisis should be considered in the context of polysubstance use. Effective measures and policies are needed to curb synthetic opioid-involved deaths and address disparate mortality rates in Black communities.

Identifiants

pubmed: 38184563
doi: 10.1186/s12889-023-17563-x
pii: 10.1186/s12889-023-17563-x
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

112

Informations de copyright

© 2024. The Author(s).

Références

Wide-ranging online data for epidemiologic research (WONDER). Atlanta, GA: CDC, National Center for Health Statistics; 1999–2020. https://wonder.cdc.gov/controller/saved/D77/D305F620 . Accessed 10 Sep 2022.
Ahmad FB, Rossen LM, Sutton P. Provisional drug overdose death counts. National Center for Health Statistics. 2022. https://www.cdc.gov/nchs/nvss/vsrr/drug-overdose-data.htm . Accessed 20 Aug 2022.
Wilson N, Kariisa M, Seth P, Smith H, Davis NL. Drug and opioid-involved overdose deaths — United States, 2017–2018. MMWR Morb Mortal Wkly Rep. 2020;69:290–7.
pubmed: 32191688 pmcid: 7739981 doi: 10.15585/mmwr.mm6911a4
Centers for Disease Control and Prevention. Understanding the Epidemic. https://www.cdc.gov/opioids/basics/epidemic.html . Accessed 15 Apr 2021.
Kariisa M, Scholl L, Wilson N, Seth P, Hoots B. Drug overdose deaths involving cocaine and psychostimulants with abuse potential — United States, 2003–2017. MMWR Morb Mortal Wkly Rep. 2019;68:388–95.
pubmed: 31048676 pmcid: 6541315 doi: 10.15585/mmwr.mm6817a3
Ciccarone D. The rise of illicit fentanyls, stimulants and the fourth wave of the opioid overdose crisis. Curr Opin Psychiatry. 2021;34:344–50.
pubmed: 33965972 pmcid: 8154745 doi: 10.1097/YCO.0000000000000717
Jones CM, Bekheet F, Park JN, Alexander GC. The evolving overdose epidemic: synthetic opioids and rising stimulant-related harms. Epidemiol Rev. 2020;42:154–66.
pubmed: 33511987 doi: 10.1093/epirev/mxaa011
Dowell D, Noonan RK, Houry D. Underlying factors in drug overdose deaths. JAMA. 2017;318:2295–6.
pubmed: 29049472 pmcid: 6007807 doi: 10.1001/jama.2017.15971
Centers for Disease Control and Prevention. Drug overdose deaths. https://www.cdc.gov/drugoverdose/deaths/other-drugs.html . Accessed 20 Apr 2021.
Cicero TJ, Ellis MS, Kasper ZA. Polysubstance use: a broader understanding of substance use during the opioid crisis. Am J Public Health. 2020;110:244–50.
pubmed: 31855487 pmcid: 6951387 doi: 10.2105/AJPH.2019.305412
Drug Enforcement Administration. 2019 National Drug Threat Assessment. https://www.dea.gov/documents/2020/01/30/2019-national-drug-threat-assessment . Accessed 17 Mar 2021.
Jones CM, Einstein EB, Compton WM. Changes in synthetic opioid involvement in drug overdose deaths in the United States, 2010–2016. JAMA. 2018;319:1819–21.
pubmed: 29715347 pmcid: 6583033 doi: 10.1001/jama.2018.2844
Suzuki J, El-Haddad S. A review: fentanyl and non-pharmaceutical fentanyls. Drug Alcohol Depend. 2017;171:107–16.
pubmed: 28068563 doi: 10.1016/j.drugalcdep.2016.11.033
Blondino CT, Gormley MA, Taylor DDH, Lowery E, Clifford JS, Burkart B, et al. The Influence of co-occurring substance use on the effectiveness of opiate treatment programs according to intervention type. Epidemiol Rev. 2020;42:57–78.
pubmed: 32944731 doi: 10.1093/epirev/mxaa005
O’Brien P, Henke RM, Schaefer MB, Lin J, Creedon TB. Utilization of treatment by Medicaid enrollees with opioid use disorder and co-occurring substance use disorders. Drug Alcohol Depend. 2020;217:108261.
pubmed: 32979735 doi: 10.1016/j.drugalcdep.2020.108261
Lin LA, Bohnert ASB, Blow FC, Gordon AJ, Ignacio RV, Kim HM, et al. Polysubstance use and association with opioid use disorder treatment in the US veterans health administration. Addiction. 2021;116:96–104.
pubmed: 32428386 doi: 10.1111/add.15116
Chan B, Freeman M, Kondo K, Ayers C, Montgomery J, Paynter R, et al. Pharmacotherapy for methamphetamine/amphetamine use disorder—a systematic review and meta-analysis. Addiction. 2019;114:2122–36.
pubmed: 31328345 doi: 10.1111/add.14755
Chan B, Kondo K, Freeman M, Ayers C, Montgomery J, Kansagara D. Pharmacotherapy for cocaine use disorder—a systematic review and meta-analysis. J Gen Intern Med. 2019;34:2858–73.
pubmed: 31183685 pmcid: 6854210 doi: 10.1007/s11606-019-05074-8
Fairbairn N, Coffin PO, Walley AY. Naloxone for heroin, prescription opioid, and illicitly made fentanyl overdoses: challenges and innovations responding to a dynamic epidemic. Int J Drug Policy. 2017;46:172–9.
pubmed: 28687187 pmcid: 5783633 doi: 10.1016/j.drugpo.2017.06.005
Meghani SH, Byun E, Gallagher RM. Time to take stock: a meta-analysis and systematic review of analgesic treatment disparities for pain in the United States. Pain Med. 2012;13:150–74.
pubmed: 22239747 doi: 10.1111/j.1526-4637.2011.01310.x
Pletcher MJ, Kertesz SG, Kohn MA, Gonzales R. Trends in opioid prescribing by race/ethnicity for patients seeking care in US emergency departments. JAMA. 2008;299:70–8.
pubmed: 18167408 doi: 10.1001/jama.2007.64
James K, Jordan A. The opioid crisis in black communities. J Law Med Ethics. 2018;46:404–21.
pubmed: 30146996 doi: 10.1177/1073110518782949
Alexander MJ, Kiang MV, Barbieri M. Trends in black and white opioid mortality in the United States, 1979–2015. Epidemiology. 2018;29:707–15.
pubmed: 29847496 pmcid: 6072374 doi: 10.1097/EDE.0000000000000858
Substance Abuse and Mental Health Services Administration. The Opioid Crisis and the Black/African American Population: An Urgent Issue. 2020. https://store.samhsa.gov/product/The-Opioid-Crisis-and-the-Black-African-American-Population-An-Urgent-Issue/PEP20-05-02-001 . Accessed 30 Mar 2021.
Jordan A, Mathis M, Haeny A, Funaro M, Paltin D, Ransome Y. An evaluation of opioid use in black communities: a rapid review of the literature. Harv Rev Psychiatry. 2021;29:108–30.
pubmed: 33666395 pmcid: 8335706 doi: 10.1097/HRP.0000000000000285
Furr-Holden D, Milam AJ, Wang L, Sadler R. African Americans now outpace whites in opioid-involved overdose deaths: a comparison of temporal trends from 1999 to 2018. Addiction. 2021;116:677–83.
pubmed: 32852864 doi: 10.1111/add.15233
Kariisa M, Seth P, Scholl L, Wilson N, Davis NL. Drug overdose deaths involving cocaine and psychostimulants with abuse potential among racial and ethnic groups – United States, 2004–2019. Drug Alcohol Depend. 2021;227:109001.
pubmed: 34492555 doi: 10.1016/j.drugalcdep.2021.109001
Johnson K, Jones C, Compton W, Baldwin G, Fan J, Mermin J, et al. Federal response to the opioid crisis. Curr HIV/AIDS Rep. 2018;15:293–301.
pubmed: 29968173 doi: 10.1007/s11904-018-0398-8
Ruhm CJ. Nonopioid overdose death rates rose almost as fast as those involving opioids, 1999–2016. Health Aff. 2019;38:1216–24.
doi: 10.1377/hlthaff.2018.05522
von Elm E, Altman DG, Egger M, Pocock SJ, Gøtzsche PC, Vandenbroucke JP. The strengthening the reporting of observational studies in epidemiology (STROBE) statement: guidelines for reporting observational studies. Int J Surg. 2014;12:1495–9.
doi: 10.1016/j.ijsu.2014.07.013
Ingram DD, Malec DJ, Makuc DM, et al. National Center for Health Statistics Guidelines for Analysis of Trends. Vital Health Stat 2(179). 2018. https://www.cdc.gov/nchs/data/series/sr_02/sr02_179.pdf . Accessed 2 Mar 2020.
Centers for Disease Control and Prevention. National Center for Health Statistics. Mortality multiple cause files. https://www.cdc.gov/nchs/data_access/vitalstatsonline.htm#Mortality_ . Accessed 10 Mar 2020.
Jones CMC, Baldwin GT, Compton WM. Recent increases in cocaine-related overdose deaths and the role of opioids. Am J Public Health. 2017;107:430–2.
doi: 10.2105/AJPH.2016.303627
National Cancer Institute. Joinpoint Regression Program (Version 4.8.0.1) [computer software]. 2020.
Centers for Disease Control and Prevention. U.S. Census Populations With Bridged Race Categories 1999 to 2018 request. https://www.cdc.gov/nchs/nvss/bridged_race.htm . Accessed 13 Mar 2020.
Curtin LR, Klein RJ. Direct standardization (age-adjusted death rates). Healthy People 2000 Stat Notes. 1995:1–10.
Levy B, Paulozzi L, Mack KA, Jones CM. Trends in opioid analgesic prescribing rates by specialty, U.S., 2007–2012. Am J Prev Med. 2015;49:409–13.
pubmed: 25896191 pmcid: 6034509 doi: 10.1016/j.amepre.2015.02.020
Bachhuber MA, Hennessy S, Cunningham CO, Starrels JL. Increasing benzodiazepine prescriptions and overdose mortality in the United States, 1996–2013. Am J Public Health. 2016;106:686–8.
pubmed: 26890165 pmcid: 4816010 doi: 10.2105/AJPH.2016.303061
Hwang CS, Kang EM, Kornegay CJ, Staffa JA, Jones CM, McAninch JK. Trends in the concomitant prescribing of opioids and benzodiazepines, 2002–2014. Am J Prev Med. 2016;51:151–60.
pubmed: 27079639 doi: 10.1016/j.amepre.2016.02.014
Patrick SW, Fry CE, Jones TF, Buntin MB. Implementation of prescription drug monitoring programs associated with reductions in opioid-related death rates. Health Aff. 2016;35:1324–32.
doi: 10.1377/hlthaff.2015.1496
Zhang VS, Olfson M, King M. Opioid and benzodiazepine coprescribing in the United States before and after US food and drug administration boxed warning. JAMA Psychiat. 2019;76:1208–10.
doi: 10.1001/jamapsychiatry.2019.2563
Green TC, Gilbert M. Counterfeit medications and fentanyl. JAMA Intern Med. 2016;176:1555–7.
pubmed: 27533891 doi: 10.1001/jamainternmed.2016.4310
LaRue L, Twillman RK, Dawson E, Whitley P, Frasco MA, Huskey A, et al. Rate of fentanyl positivity among urine drug test results positive for cocaine or methamphetamine. JAMA Netw Open. 2019;2:e192851.
pubmed: 31026029 pmcid: 6487565 doi: 10.1001/jamanetworkopen.2019.2851
Carroll JJ, Marshall BDL, Rich JD, Green TC. Exposure to fentanyl-contaminated heroin and overdose risk among illicit opioid users in Rhode Island: a mixed methods study. Int J Drug Policy. 2017;46:136–45.
pubmed: 28578864 pmcid: 5560423 doi: 10.1016/j.drugpo.2017.05.023
Gladden RM, O’Donnell J, Mattson CL, Seth P. Changes in opioid-involved overdose deaths by opioid type and presence of benzodiazepines, cocaine, and methamphetamine — 25 states, July–December 2017 to January–June 2018. MMWR Morb Mortal Wkly Rep. 2019;68:737–44.
pubmed: 31465320 pmcid: 6715260 doi: 10.15585/mmwr.mm6834a2
Hoots B, Vivolo-Kantor A, Seth P. The rise in non-fatal and fatal overdoses involving stimulants with and without opioids in the United States. Addiction. 2020;115:946–58.
pubmed: 31912625 doi: 10.1111/add.14878
Hoopsick RA, Homish GG, Leonard KE. Differences in opioid overdose mortality rates among middle-aged adults by race/ethnicity and sex, 1999–2018. Public Health Rep. 2021;136:192–200.
pubmed: 33211981 doi: 10.1177/0033354920968806
Phelan JC, Link BG. Is racism a fundamental cause of inequalities in health? Annu Rev Sociol. 2015;41:311–30.
doi: 10.1146/annurev-soc-073014-112305
Andraka-Christou B. Addressing racial and ethnic disparities in the use of medications for opioid use disorder. Health Aff. 2021;40:920–7.
doi: 10.1377/hlthaff.2020.02261
Cummings JR, Wen H, Ko M, Druss BG. Race/ethnicity and geographic access to Medicaid substance use disorder treatment facilities in the United States. JAMA Psychiat. 2014;71:190–6.
doi: 10.1001/jamapsychiatry.2013.3575
Goedel WC, Shapiro A, Cerdá M, Tsai JW, Hadland SE, Marshall BDL. Association of racial/ethnic segregation with treatment capacity for opioid use disorder in counties in the United States. JAMA Netw Open. 2020;3:1–10.
doi: 10.1001/jamanetworkopen.2020.3711
Guadamuz JS, Wilder JR, Mouslim MC, Zenk SN, Alexander GC, Qato DM. Fewer pharmacies in black and hispanic/latino neighborhoods compared with white or diverse neighborhoods, 2007–15. Health Aff. 2021;40:802–11.
doi: 10.1377/hlthaff.2020.01699
Martha Hostetter and Sarah Klein, “Understanding and Ameliorating Medical Mistrust Among Black Americans,” Transforming Care. Commonwealth Fund. 2021. https://doi.org/10.26099/9grt-2b21 .
Saloner B, Cook BL. Blacks and hispanics are less likely than whites to complete addiction treatment, largely due to socioeconomic factors. Health Aff. 2013;32:135–45.
doi: 10.1377/hlthaff.2011.0983
Latimore AD, Bergstein RS. “Caught with a body” yet protected by law? Calling 911 for opioid overdose in the context of the Good Samaritan Law. Int J Drug Policy. 2017;50:82–9.
pubmed: 29040841 doi: 10.1016/j.drugpo.2017.09.010
Camplain R, Sabo S, Baldwin JA, Camplain C, Pro G, Trotter RT, et al. Racial/ethnic differences in drug- and alcohol-related arrest outcomes in a Southwest County from 2009 to 2018. Am J Public Health. 2020;110:S85–92.
pubmed: 31967892 pmcid: 6987943 doi: 10.2105/AJPH.2019.305409
Mital S, Wolff J, Carroll JJ. The relationship between incarceration history and overdose in North America: a scoping review of the evidence. Drug Alcohol Depend. 2020;213:108088.
pubmed: 32498032 pmcid: 7683355 doi: 10.1016/j.drugalcdep.2020.108088
Center for Behavioral Health Statistics and Quality. Results from the 2019 National Survey on Drug Use and Health: Detailed Tables. Rockville, MD: Substance Abuse and Mental Health Services Administration. 2020. https://www.samhsa.gov/data/report/2019-nsduh-detailed-tables . Accessed 10 Aug 2021.
Cicero TJ, Wong G, Tian Y, Lynskey M, Todorov A, Isenberg K. Co-morbidity and utilization of medical services by pain patients receiving opioid medications: data from an insurance claims database. Pain. 2009;144:20–7.
pubmed: 19362417 pmcid: 2710243 doi: 10.1016/j.pain.2009.01.026
Fillingim RB, King CD, Ribeiro-Dasilva MC, Rahim-Williams B, Riley JL. Sex, gender, and pain: a review of recent clinical and experimental findings. J Pain. 2009;10:447–85.
pubmed: 19411059 pmcid: 2677686 doi: 10.1016/j.jpain.2008.12.001
McHugh RK, Votaw VR, Sugarman DE, Greenfield SF. Sex and gender differences in substance use disorders. Clin Psychol Rev. 2018;66:12–23.
pubmed: 29174306 doi: 10.1016/j.cpr.2017.10.012
Statistical methods: Suppression of rates and counts. Centers for Disease Control and Prevention. https://www.cdc.gov/cancer/uscs/technical_notes/stat_methods/suppression.htm . Accessed 7 Nov 2023.
Arias E, Heron M, Hakes J. The validity of race and hispanic-origin reporting on death certificates in the United States: an update. Vital Health Stat. 2016;2:1–21.
Joshi S, Weiser T, Warren-Mears V. Drug, opioid-involved, and heroin-involved overdose deaths among American Indians and Alaska Natives — Washington, 1999–2015. MMWR Morb Mortal Wkly Rep. 2018;67:1384–7.
pubmed: 30571673 pmcid: 6342552 doi: 10.15585/mmwr.mm6750a2
Ruhm CJ. Corrected US opioid-involved drug poisoning deaths and mortality rates, 1999–2015. Addiction. 2018;113:1339–44.
pubmed: 29430760 doi: 10.1111/add.14144
Buchanich JM, Balmert LC, Williams KE, Burke DS. The effect of incomplete death certificates on estimates of unintentional opioid-related overdose deaths in the united states, 1999–2015. Public Health Rep. 2018;133:423–31.
pubmed: 29945473 pmcid: 6055296 doi: 10.1177/0033354918774330
Clinton HA, Thangada S, Gill JR, Mirizzi A, Logan SB. Improvements in toxicology testing to identify fentanyl analogs and other novel synthetic opioids in fatal drug overdoses, connecticut, January 2016–June 2019. Public Health Rep. 2021;1361_suppl:80S–86S.
doi: 10.1177/00333549211042829
Warner M, Paulozzi LJ, Nolte KB, Davis GG, Nelson LS. State variation in certifying manner of death and drugs involved in drug intoxication deaths. Acad Forensic Pathol. 2013;3:231–7.
doi: 10.23907/2013.029
Centers for Disease Control and Prevention. Increase in fatal drug Overdoses across the United States driven by synthetic opioids before and during the COVID-19 pandemic. CDC Health Alert Network. 2020. https://emergency.cdc.gov/han/2020/han00438.asp . Accessed 3 Jan 2021.
American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, 5th Ed. (DSM-5®). Washington, DC: American Psychiatric Association; 2013.
Peppin JF, Raffa RB, Schatman ME. The polysubstance overdose-death crisis. J Pain Res. 2020;13:3405–8.
pubmed: 33364823 pmcid: 7751289 doi: 10.2147/JPR.S295715
Peiper NC, Clarke SD, Vincent LB, Ciccarone D, Kral AH, Zibbell JE. Fentanyl test strips as an opioid overdose prevention strategy: findings from a syringe services program in the Southeastern United States. Int J Drug Policy. 2019;63:122–8.
pubmed: 30292493 doi: 10.1016/j.drugpo.2018.08.007
Barry CL. Fentanyl and the evolving opioid epidemic: what strategies should policy makers consider? Psychiatr Serv. 2018;69:100–3.
pubmed: 28967324 doi: 10.1176/appi.ps.201700235
Joudrey PJ, Adams ZM, Bach P, Van BS, Chaiton JA, Ehrenfeld L, et al. Methadone access for opioid use disorder during the COVID-19 pandemic within the United States and Canada. JAMA Netw Open. 2021;4:e2118223.
pubmed: 34297070 pmcid: 8303098 doi: 10.1001/jamanetworkopen.2021.18223
Spencer MR, Miniño AM, Warner M. Drug overdose deaths in the United States, 2001–2021. NCHS Data Brief, no 457. Hyattsville, MD: National Center for Health Statistics. 2022. https://doi.org/10.15620/cdc:122556 .
Friedman JR, Hansen H. Evaluation of increases in drug overdose mortality rates in the US by race and ethnicity before and during the COVID-19 pandemic. JAMA Psychiat. 2022;79:379.
doi: 10.1001/jamapsychiatry.2022.0004

Auteurs

Marwa Rawy (M)

University of Wisconsin-Madison, Madison, USA. rawy@wisc.edu.

Gergis Abdalla (G)

Claude Bernard University Lyon 1, Lyon, France.

Kevin Look (K)

University of Wisconsin-Madison, Madison, USA.

Classifications MeSH