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Figure 1.  Age Distribution of Patients With e-Cigarette, or Vaping, Product Use–Associated Lung Injury (N = 2315) Compared With the Age Distribution of the US General Population
Age Distribution of Patients With e-Cigarette, or Vaping, Product Use–Associated Lung Injury (N = 2315) Compared With the Age Distribution of the US General Population

Data for patients with known age with e-cigarette, or vaping, product use–associated lung injury (EVALI) are from national EVALI surveillance reports to the Centers for Disease Control and Prevention as of December 17, 2019. Data for the general population are from annual estimates of the resident population by single year of age and sex for the United States from April 1, 2010, to July 1, 2018, by the US Census Bureau. Ages 0 to 12 years were excluded from the graph because no EVALI cases have been reported in that age group.

Figure 2.  Duration Between Symptom Onset and First Hospitalization and Duration of First Hospitalization for Hospitalized or Deceased Patients With e-Cigarette, or Vaping, Product Use–Associated Lung Injury in the US in 2019 (N = 2155), Stratified by Age
Duration Between Symptom Onset and First Hospitalization and Duration of First Hospitalization for Hospitalized or Deceased Patients With e-Cigarette, or Vaping, Product Use–Associated Lung Injury in the US in 2019 (N = 2155), Stratified by Age

A and B, Adolescents (age, 13-17 years) had similar duration between symptom onset and first hospitalization compared with young adults (age, 18 to 24 years) (β = −0.12; 95% CI, −2.33 to 2.09; P = .91) and adults (age, 25-49 years) (β = 0.19; 95% CI, −1.63 to 2.01; P = .84). Adolescents also had similar duration of first hospitalization compared with young adults (β = 0.64; 95% CI, −0.28 to 1.55; P = .17) and adults (β = −0.41; 95% CI, −1.43 to 0.61; P = .43). The horizontal lines within the boxes represent the median, with the lower and upper line of the box representing the first and third quartiles. The outliers represent individual patients whose data points were greater than 1.5 times the interquartile range.

Table 1.  Differences in Demographics and Substance Use Behaviors Between Adolescent and Young Adult or Adult Hospitalized or Deceased Patients With e-Cigarette, or Vaping, Product Use–Associated Lung Injury (N = 2155) in the US in 2019a
Differences in Demographics and Substance Use Behaviors Between Adolescent and Young Adult or Adult Hospitalized or Deceased Patients With e-Cigarette, or Vaping, Product Use–Associated Lung Injury (N = 2155) in the US in 2019a
Table 2.  Differences in Clinical Characteristics Between Adolescent and Young Adult or Adult Hospitalized or Deceased Patients With e-Cigarette, or Vaping, Product Use–Associated Lung Injury (EVALI) (N = 2155) in the US in 2019a
Differences in Clinical Characteristics Between Adolescent and Young Adult or Adult Hospitalized or Deceased Patients With e-Cigarette, or Vaping, Product Use–Associated Lung Injury (EVALI) (N = 2155) in the US in 2019a
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    1 Comment for this article
    EXPAND ALL
    Adolescents' Vaping Epidemic During the Covid 19 Pandemic
    Aki Nilanga Bandara, BSc | Instructor, Faculty of Land and Food System, UBC
    We wholeheartedly agree with the authors that we need to redouble our efforts to prevent adolescents' and young adults’ e cigarette epidemic (1). JUUL appears to be associated with the youth e-cigarette epidemic, attracting new users and facilitating frequent use with their highly addictive nicotine content and appealing flavors (2).

    Investing our resources to enhance tobacco cessation during the Covid 19 pandemic is vital. Like the previous outbreaks of MERS and SARS, COVID-19 attacks the lungs and other parts of the respiratory system. A recent state of art review concluded that the e-cigarette use is significantly and independently associated
    with an increased risk of respiratory illness (3).

    It is very critical and important that health care investments be made to prevent and control Covid 19. New research shows that smoking spurs the lungs to make more ACE2, the protein that the coronavirus uses to enter human cells. This finding may explain why smokers appear to be particularly vulnerable to severe infections. The analysis also indicates that the change is reversible, suggesting that quitting smoking might reduce the risk of a severe coronavirus infection (4). This report further provides welcome evidence to priorities smoking cessation within vulnerable communities.

    The frequency of patient inquiries on e-cigarette is increasing, (5) but most clinicians feel they lack sufficient knowledge to counsel and express interest in learning more (6). Physicians infrequently screen or counsel their adolescent patients about e-cigarette use, even though e-cigarettes often come up during visits. Additional efforts by physicians could help prevent future use by adolescents (7). We suggest a patient-centered strategy to incorporate vaping into routine substance counseling. Health care providers caring for adolescents and young adults should be aware of surging e-cigarette use in this population and, in a preventive health role, should include e-cigarette in substance use counseling (8).

    Nicotine addiction is a pediatric disease (9) and nicotine exposure to the developing adolescent brain has been shown to have long-term cognitive and behavioral impairments (10).Juul uses nicotine salts in its vaping devices to deliver “dramatically higher levels” of nicotine to the brain with less irritation and “Adolescents simply do not stand a chance”(11). The Surgeon General estimates that 5.6 million of today’s youth will die prematurely from a smoking related illness (12).

    Protecting our vulnerable children from nicotine dependence is of paramount importance to clinicians and the health care community. We need to bring every possible advocacy effort to create an environment in which our children could grow without compromising their overall health and wellbeing. Primary care physicians, the pediatricians and other practitioners have the unique power and responsibility to advocate for their patients' health by screening for, offering education on, and promoting cessation of e-cigarette use (13, 14). Pediatricians feel poorly informed about e-cigarettes and are concerned about their potential health effects. While clinical discussions about e-cigarettes are rare, recent increases in their use leaves many clinicians wanting guidance about what to say to patients and families. One-step toward educating the adolescents is to ensure pediatricians and primary care physician have an accurate knowledge of the current best practices for e cigarettes and prevention (14).

    REFERENCES
    (1). Adkins SH, Anderson KN, Goodman AB, et al. Demographics, Substance Use Behaviors, and Clinical Characteristics of Adolescents With e-Cigarette, or Vaping, Product Use-Associated Lung Injury (EVALI) in the United States in 2019 [published online ahead of print, 2020 May 18]. JAMA Pediatr. 2020;e200756.
    (2). Vallone DM, Cuccia AF, Briggs J, Xiao H, Schillo BA, Hair EC.Electronic cigarette and JUULuse among adolescents and young adults. JAMA Pediatr. 2020 Jan 21. doi: 10.1001/jamapediatrics.2019.5436
    (3). Gotts JE, Jordt SE, McConnell R, Tarran R. What are the respiratory effects of e-cigarettes? BMJ. 2019 Sep 30;366:l5275. doi: 10.1136/bmj.l5275
    (4). Smith, J. C., et al., (2020). Cigarette smoke exposure and inflammatory signaling increase the expression of the SARS-CoV-2 receptor ACE2 in the respiratory tract. Developmental Cell- http://dx.doi.org/10.1016/j.devcel.2020.05.012   
    (5). Steinberg MB, Giovenco DP, Delnevo CD. Patient–physician communication regarding electronic cigarettes. Prev Med Rep. 2015; 2:96-98
    (6). England LJ, Anderson BL, Tong VT, et al. Screening practices and attitudes of obstetricians-gynecologists toward new and emerging tobacco products. Am J Obstet Gynecol. 2014; 211:695.e691-697 (7). Pepper JK, Gilkey MB, Brewer NT. Physician counselling of adolescents regarding e-cigarette use. J Adolesc Health. 2015 Dec;57(6):580-6. doi: 10.1016/j.jadohealth.2015.06.017. 
    (8). Hildick-Smith GJ, Pesko MF, Shearer L, Hughes JM, Chang J, Loughlin GM, Ipp LS. . A Practitioner's Guide to Electronic Cigarettes in the Adolescent Population. J Adolesc Health. 2015 Dec;57(6):574-9. doi: 10.1016/j.jadohealth.2015.07.020
    (9). Kessler DA, Natanblut SL, Wilkenfeld JP, Lorraine CC, LindanMayl S, Bernstein IBG, Thompson L. Nicotine addiction: a pediatric disease. J Pediatr. 1997;130:518–524.
    (10). Surgeon General’s report (2016) US Department of Health and Human Services. E-cigarette use among youth and young adults: A report of the Surgeon General-http://e-cigarettes.surgeongeneral.gov/documents/2016_SGR_Full_Report_non-508.pdf.
    (11). The American Academy of Pediatrics- Congressional testimony 2019-https://www.cnbc.com/2019/10/15/pediatrician-to-congress-adolescents-dont-stand-a-chance-against-juul.html
    (12). National Center for Chronic Disease Prevention and Health Promotion (US) Office on Smoking and Health. The Health Consequences of Smoking-50 Years of Progress: A Report of the Surgeon General. Atlanta, GA: Centers for Disease Control and Prevention (US); 2014
    (13). Hildick-Smith GJ, Pesko MF, Shearer L, Hughes JM, Chang J, Loughlin GM, Ipp LS. A practitioner’s guide to electronic cigarettes in the adolescent population. J Adolesc Health. 2015 Dec; 57(6):574-9. doi: 10.1016/j.jadohealth.2015.07.020
    (14). Gorzkowski JA, Whitmore RM, Kaseeska KR, Brishke JK, Klein JD. Pediatrician Knowledge, Attitudes, and Practice Related to Electronic Cigarettes. J Adolesc Health. 2016;59(1):81‐86. doi:10.1016/j.jadohealth.2016.03.036

    Aki Nilanga Bandara- nilangabandara527@gmail.com   
     Dr. Vahid Mehrnoush- mv1361@yahoo.com



    CONFLICT OF INTEREST: Founding Director, Global Coalition for Adolescents’ Unique Tobacco Addictions Related Issues​ https://gcfautari.weebly.com/about.html
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    Original Investigation
    May 18, 2020

    Demographics, Substance Use Behaviors, and Clinical Characteristics of Adolescents With e-Cigarette, or Vaping, Product Use–Associated Lung Injury (EVALI) in the United States in 2019

    Author Affiliations
    • 1National Center for HIV/AIDS, Viral Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention, Atlanta, Georgia
    • 2National Center on Birth Defects and Developmental Disabilities, Centers for Disease Control and Prevention, Atlanta, Georgia
    • 3National Center for Chronic Disease Prevention and Health Promotion, Centers for Disease Control and Prevention, Decatur, Georgia
    • 4Center for Global Health, Centers for Disease Control and Prevention, Atlanta, Georgia
    • 5National Center for Injury Prevention and Control, Centers for Disease Control and Prevention, Atlanta, Georgia
    • 6National Institute for Occupational Safety and Health, Centers for Disease Control and Prevention, Atlanta, Georgia
    • 7Agency for Toxic Substances and Disease Registry, Centers for Disease Control and Prevention, Atlanta, Georgia
    • 8National Center for Emerging and Zoonotic Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia
    JAMA Pediatr. Published online May 18, 2020. doi:10.1001/jamapediatrics.2020.0756
    Key Points

    Question  Do adolescents with e-cigarette, or vaping, product use–associated lung injury (EVALI) differ from adults with EVALI?

    Findings  A total of 2155 patients were included in this cross-sectional study. Based on national surveillance data, adolescents with EVALI are more likely than adults with EVALI to report the use of informally sourced e-cigarette or vaping products that contain tetrahydrocannabinol and to have attention-deficit/hyperactivity disorder, asthma, and gastrointestinal and constitutional symptoms.

    Meaning  Public health and clinical efforts could include messaging to adolescents about the risks of tetrahydrocannabinol-containing e-cigarette or vaping products, especially those obtained from informal sources, and their association with EVALI.

    Abstract

    Importance  To date, limited information is available on the characteristics of adolescents with e-cigarette, or vaping, product use–associated lung injury (EVALI).

    Objective  To inform public health and clinical practice by describing differences in demographics, substance use behaviors, and clinical characteristics of EVALI among adolescents compared with adults.

    Design, Setting, and Participants  Surveillance data reported to the Centers for Disease Control and Prevention during the 2019 EVALI outbreak were used to calculate adjusted prevalence ratios (aPRs) with 95% CIs and to test differences between 360 hospitalized or deceased adolescents vs 859 young adults and 936 adults with EVALI (N = 2155).

    Main Outcomes and Measures  Demographics, substance use behaviors, and clinical characteristics.

    Results  Included in this cross-sectional study were 360 hospitalized or deceased adolescents (age range, 13-17 years; 67.9% male) vs 859 young adults (age range, 18-24 years; 72.4% male) and 936 adults (age range, 25-49 years; 65.6% male) with EVALI. Adolescents diagnosed as having EVALI reported using any nicotine-containing (62.4%), any tetrahydrocannabinol (THC)-containing (81.7%), and both (50.8%) types of e-cigarette or vaping products. Informal sources for obtaining nicotine-containing and THC-containing e-cigarette or vaping products were more commonly reported by adolescents (50.5% for nicotine and 96.5% for THC) than young adults (19.8% for nicotine [aPR, 2.49; 95% CI, 1.78-3.46] and 86.9% for THC [aPR, 1.11; 95% CI, 1.05-1.18]) or adults (24.3% for nicotine [aPR, 2.06; 95% CI, 1.49-2.84] and 75.1% for THC [aPR, 1.29; 95% CI, 1.19-1.40]). Mental, emotional, or behavioral disorders were commonly reported; a history of attention-deficit/hyperactivity disorder was almost 4 times more likely among adolescents (18.1%) than adults (4.9%) (aPR, 3.74; 95% CI, 1.92-7.26). A history of asthma was more likely to be reported among adolescents (43.6%) than adults (28.3%) (aPR, 1.53; 95% CI, 1.14-2.05). Gastrointestinal and constitutional symptoms were more common in adolescents (90.9% and 97.3%, respectively) than adults (75.3% and 94.5%, respectively) (aPR, 1.20; 95% CI, 1.13-1.28 and aPR, 1.03; 95% CI, 1.00-1.06, respectively). Because of missing data, percentages may not be able to be calculated from data provided.

    Conclusions and Relevance  Public health and clinical professionals should continue to provide information to adolescents about the association between EVALI and THC-containing e-cigarette or vaping product use, especially those products obtained through informal sources, and that the use of any e-cigarette or vaping product is unsafe. Compared with adults, it appears that adolescents with EVALI more frequently have a history of asthma and mental, emotional, or behavioral disorders, such as attention-deficit/hyperactivity disorder, and report nonspecific problems, including gastrointestinal and constitutional symptoms; therefore, obtaining a confidential substance use history that includes e-cigarette or vaping product use is recommended.

    Introduction

    Since August 2019, the Centers for Disease Control and Prevention (CDC), US Food and Drug Administration (FDA), and state, local, and territorial health departments have been investigating a national outbreak of e-cigarette, or vaping, product use–associated lung injury (EVALI).1 As of December 17, 2019, a total of 2506 hospitalized or deceased cases of EVALI, including 54 deaths from 27 states, had been reported to the CDC. Evidence indicates that EVALI is associated with e-cigarette or vaping products that contain tetrahydrocannabinol (THC) (the primary psychoactive ingredient in marijuana), particularly those obtained through informal sources (eg, family, friends, and in-person or online dealers): 82% of patients with EVALI reported using THC products and 78% reported obtaining their products from only informal sources.2-6 Vitamin E acetate, a cutting or diluting agent sometimes used in THC-containing products, has been found in THC-containing e-cigarette or vaping products tested by the FDA and state laboratories and in bronchoalveolar lavage fluid from patients with EVALI tested by the CDC, suggesting an association between vitamin E acetate and EVALI.7,8 The 2019 EVALI outbreak affected adolescents and young adults, with 16% of reported cases among patients aged 13 to 17 years and 38% among patients aged 18 to 24 years.4

    The 2019 EVALI outbreak occurred in the context of an epidemic of e-cigarette or vaping product use among US adolescents.9 In 2019, 27.5% of high school students used e-cigarettes during the past 30 days.10 As of 2016, an estimated one-third of US middle and high school students who ever used e-cigarettes had used marijuana in these products.11 Furthermore, the proportion of high school students who reported use of THC-containing e-cigarette or vaping products during the past month increased from 7.5% in 2018 to 14% in 2019 based on survey results.12 Adolescent and young adult nicotine and THC use can alter neurodevelopment in the long term and may lead to increased risk of substance use disorder and cognitive difficulties.13-16

    Adolescents who develop EVALI may have characteristics that differ from those of young adults or adults with EVALI, such as how THC-containing products are obtained, medical history, and the frequency of initial symptoms. These differences may be important for tailoring EVALI-related prevention strategies, including messaging to adolescents through public health communication campaigns and by clinicians. Although characteristics of all patients with EVALI have been reported,4,17-19 demographic, substance use, and clinical characteristics of adolescents with EVALI have not been separately described. We used surveillance data reported to the CDC during the 2019 EVALI outbreak to describe demographic characteristics, substance use behaviors, and clinical characteristics of 360 hospitalized or deceased adolescents vs 859 young adults and 936 adults with EVALI (N = 2155).

    Methods
    Patients and Data Collection

    Using case definitions and data collection tools developed by the CDC in collaboration with state health departments and the Council of State and Territorial Epidemiologists, jurisdictions voluntarily reported confirmed and probable hospitalized cases of EVALI and EVALI-associated deaths to the CDC as part of a national surveillance strategy for the 2019 EVALI outbreak. The EVALI surveillance was determined to be a nonresearch, public health surveillance activity exempt from institutional review board review by the CDC. Jurisdictions submit data from medical record abstractions and, if possible, patient interviews. Proxies (eg, parents) may be interviewed if patients are too ill or have died. Protocols for informed consent for medical record abstraction and patient interview were obtained at the jurisdictional level in accordance with jurisdictional practices for public health practice activities. The present cross-sectional study is limited to hospitalized or deceased patients with EVALI with known age younger than 50 years reported to the CDC as of December 17, 2019. At the time of this analysis, EVALI cases had been reported from all 50 states, the District of Columbia, the US Virgin Islands, and Puerto Rico. Patients with EVALI who were 50 years or older were excluded because they have a higher burden of chronic medical conditions and other risk factors for adverse EVALI-associated outcomes.20,21 The analytic sample included 2155 patients with EVALI.

    Data collected by the CDC include the following: e-cigarette or vaping product use, frequency, and product source; the use of nicotine-containing or combustible marijuana products; medical history; EVALI-compatible symptoms; and clinical course of the lung injury. Analytic demographic characteristics included sex (male or female) and race/ethnicity (non-Hispanic white or other race/ethnicity). Specific races/ethnicities were reported by jurisdictions based on medical record abstraction or patient interview but were further collapsed for this analysis because of small cell sizes for specific racial/ethnic categories by patient age group. Substance use history data included the following: nicotine use in the past 90 days (any use, exclusive use, or daily use of nicotine-containing e-cigarette or vaping product or any use of combustible tobacco); THC use in the past 90 days (any use, exclusive use, or daily use of THC-containing e-cigarette or vaping product or any use of combustible marijuana); and source of e-cigarette or vaping products, including formal sources (dispensary, vape or smoke shop, pop-up shop, or grocery, drug, or convenience store) and informal sources (family or friend, illicit dealer, or online). Medical history data included a history of any mental, emotional, or behavioral disorder; diabetes; any heart disease; any chronic respiratory disease; EVALI symptoms reported (respiratory, gastrointestinal, and constitutional); and EVALI clinical course and treatment (location of first reported EVALI clinical encounter, corticosteroid treatment, intensive care unit admission, and intubation).

    Statistical Analysis

    The age distribution of patients with EVALI was compared with the 2018 US Census population estimates to better understand the burden by age.22 Selected demographic characteristics, substance use behaviors, medical history, and clinical course of EVALI for adolescents were compared with those for young adults and adults with EVALI. Because of missing data within each specific age stratum, percentages may not be able to be calculated from the counts provided. Adjusted prevalence ratios (aPRs) and 95% CIs were calculated using Poisson regression models with robust SEs23,24; binary outcomes were modeled with the log-link function and continuous outcomes with the identity link function. All models were adjusted for patient sex because of differences in distribution of sex by age; no other demographic characteristics were included in model adjustments because of percentage of item-level missingness. Analyses were performed using SAS, version 9.4 (SAS Institute Inc). A threshold of 2-sided P < .05 was used to define statistical significance.

    Results

    Included in this cross-sectional study were 360 hospitalized or deceased adolescents (age range, 13-17 years; 67.9% male) vs 859 young adults (age range, 18-24 years; 72.4% male) and 936 adults (age range, 25-49 years; 65.6% male) with EVALI. Compared with the US general population, patients with EVALI are disproportionately adolescents (16% vs 8%) or young adults (37% vs 11%) (Figure 1). A high proportion of adolescents with EVALI were non-Hispanic white (66.3%). Demographics for adolescents (n = 360), young adults (n = 859), and adults (n = 936) with EVALI are listed in Table 1.

    Most adolescent patients with EVALI reported using THC-containing e-cigarette or vaping products (81.7%); this proportion of patients was similar to that of young adults (81.3%) and adults (77.2%) with EVALI (Table 1). Among adolescents reporting the use of THC-containing products, 57.9% reported daily use; this practice was less common compared with young adults (76.5%; aPR, 0.76; 95% CI, 0.64-0.89) and adults (78.0%; aPR, 0.74; 95% CI, 0.63-0.87). Nicotine-containing e-cigarette or vaping product use was more commonly reported among adolescents (62.4%) than adults (46.3%) (aPR, 1.35; 95% CI, 1.20-1.51). Among adolescents with EVALI reporting nicotine-containing product use, daily use was common (74.4%). However, adolescents used nicotine-containing products daily less commonly than adults (91.9%; aPR, 0.81; 95% CI, 0.72-0.91). Daily use of these products was similar among adolescents and young adults. Exclusive nicotine-containing product use was similar across all 3 age categories (range, 10.9%-14.4%; P > .05); exclusive use of THC-containing products was less common among adolescents (28.0%) than adults (37.3%) (aPR, 0.75; 95% CI, 0.61-0.92). Reporting use of both nicotine-containing and THC-containing products was more common among adolescents (50.8%) compared with adults (30.4%) (aPR, 1.66; 95% CI, 1.43-1.94). Combustible marijuana use was more common in adolescents (55.5%) than adults (44.7%) (aPR, 1.25; 95% CI, 1.05-1.47); combustible tobacco use was less common among adolescents (16.8%) than young adults (31.7%) (aPR, 0.53; 95% CI, 0.38-0.75) and adults (40.4%) (aPR, 0.42; 95% CI, 0.29-0.61).

    More adolescent patients with EVALI reported obtaining THC-containing products through informal sources (96.5%) compared with young adults (86.9%) (aPR, 1.11; 95% CI, 1.05-1.18) and adults (75.1%) (aPR, 1.29; 95% CI, 1.19-1.40). Specifically, adolescents obtained THC-containing products more frequently from family or friends (61.0%) than young adults (42.2%) (aPR, 1.41; 95% CI, 1.14-1.75) and adults (40.5%) (aPR, 1.52; 95% CI, 1.22-1.88). Adolescent patients with EVALI also reported obtaining nicotine-containing products more frequently from informal sources (50.5%) than young adults (19.8%) (aPR, 2.49; 95% CI, 1.78-3.46) and adults (24.3%) (aPR, 2.06; 95% CI, 1.49-2.84). Among adolescents with EVALI who reported using nicotine-containing products, most reported obtaining at least some (69.0%) of their nicotine-containing e-cigarette or vaping products through formal sources, such as recreational dispensaries or convenience stores, although less commonly than young adults (92.5%) (aPR, 0.75; 95% CI, 0.65-0.87) or adults (88.9%) (aPR, 0.78; 95% CI, 0.67-0.90).

    Reported history of any mental, emotional, or behavioral disorder was common across all age groups with EVALI in our analysis (range, 41.5%-51.0%). Specifically, attention-deficit/hyperactivity disorder (ADHD) was more commonly reported among adolescents with EVALI (18.1%) compared with young adults (7.9%) (aPR, 2.31; 95% CI, 1.27-4.20) and adults (4.9%) (aPR, 3.74; 95% CI, 1.92-7.26). Adolescents more commonly reported a history of asthma (43.6%) compared with adults (28.3%) (aPR, 1.53; 95% CI, 1.14-2.05); there were no statistically significant differences in having a reported history of asthma between adolescents and young adults (41.1%) (P > .05) (Table 2).

    Respiratory symptoms at initial clinical presentation for EVALI were reported by almost all patients with EVALI regardless of age (range, 95.8%-96.7%). Adolescents more commonly reported gastrointestinal symptoms associated with EVALI (90.9%) compared with adults (75.3%) (aPR, 1.20; 95% CI, 1.13-1.28) (Table 2). Adolescents also more frequently reported constitutional symptoms (eg, fever, chills, and malaise) associated with EVALI (97.3%) compared with adults (94.5%) (aPR, 1.03; 95% CI, 1.00-1.06). No difference was noted between adolescents and young adults for report of respiratory, gastrointestinal, or constitutional symptoms. There were no statistically significant differences between age groups for duration between symptom onset and first hospitalization (Figure 2A). Adolescents less often reported their first EVALI clinical encounter was a hospitalization (80.4%) compared with adults (85.2%) (aPR, 0.95; 95% CI, 0.89-1.00). Adolescents were more commonly admitted to the intensive care unit (46.9%) than young adults (37.6%) (aPR, 1.24; 95% CI, 1.05-1.48). Intubation was less common among adolescents (12.4%) compared with adults (23.1%) (aPR, 0.54; 95% CI, 0.31-0.94). Percentage intubated was similar for adolescents and young adults. There were no statistically significant differences among age groups in whether corticosteroids were administered (Table 2). No statistically significant differences were found between age groups for duration of first hospitalization (Figure 2B).

    Discussion

    Adolescents and young adults are disproportionately affected by EVALI. These age groups comprise 19% of the US general population older than 12 years but contribute to just over 50% of reported EVALI cases. Furthermore, among persons with EVALI, important differences exist in substance use behaviors and clinical characteristics of adolescents compared with young adults and adults. Most adolescents with EVALI reported the use of THC-containing products and more frequently reported obtaining these THC-containing products from informal sources (ie, family, friends, and in-person or online dealers) than young adults or adults with EVALI. Moreover, a history of ADHD was more commonly reported among adolescents with EVALI than among young adults or adults with EVALI; a history of asthma was more commonly reported among adolescents with EVALI than among adults with EVALI. Gastrointestinal and constitutional symptoms were more common for adolescents at clinical presentation, which may complicate the clinical picture and could delay EVALI diagnosis and treatment. These findings can inform public health and clinical professionals’ response to EVALI among adolescents.

    Most adolescents with EVALI (81.7%) reported THC-containing e-cigarette or vaping product use, and almost all adolescents with EVALI (96.5%) reported obtaining THC-containing products from informal sources (ie, family, friends, and in-person, or online dealers). Informal sources were more commonly reported by adolescents with EVALI than by young adults or adults with EVALI. Many adolescents (57.9%) reported daily THC-containing product use. The finding of frequent informally sourced THC-containing product use is consistent with previous national results and with data suggesting that THC-containing e-cigarette or vaping products are associated with most of the EVALI cases and played a major role in the 2019 EVALI outbreak.1,2,4,5,18 Informally sourced THC-containing e-cigarette or vaping products obtained from geographically diverse states have been found to contain vitamin E acetate, a chemical associated with EVALI.7,19 The finding of vitamin E acetate in bronchoalveolar lavage fluid of patients with EVALI but not in the lung fluid of people who do not have EVALI further supports the association between vitamin E acetate and EVALI.8 However, evidence is not sufficient to rule out other chemicals of concern, including those in THC or non-THC products; product sources remain under investigation. There may be more than 1 cause of EVALI.1

    The common occurrence of several specific comorbidities in adolescents with EVALI may inform clinical evaluation and intervention. The prevalence of ADHD among adolescents with EVALI in our study was higher than the prevalence among adolescents in the US general population (18.1% vs 10.5%),25 and adolescents with EVALI reported a history of ADHD between 2 to 4 times more often than young adults or adults with EVALI (18.1% vs 7.9% and 4.9%, respectively). Furthermore, ADHD is associated with risk-taking behaviors, including e-cigarette use26 and other substance use.27-29 Half of adolescents with EVALI reported a history of any co-occurring behavioral health condition; these conditions are common in the overall population of patients with EVALI and are important to consider to optimize clinical care and appropriate referral to behavioral health services.20,21 Addressing these needs in adolescent patients may reduce risk of subsequent substance use disorder.16 Similar to the general population,30 adolescents with EVALI more commonly reported a history of asthma than adult patients with EVALI. Notably, the prevalence of asthma among adolescents with EVALI appears to be higher than that among the general adolescent population (43.6% vs 18.2%),30 which reflects previous reports of higher prevalence of asthma among all patients with EVALI31,32 and may indicate that adolescents with asthma and EVALI more frequently seek hospital care. Our findings support the importance of asking adolescents who are seen with asthma symptoms about e-cigarette or vaping product use and consideration of EVALI in differential diagnoses.

    Adolescents with EVALI were more likely to report experiencing gastrointestinal or constitutional symptoms compared with adults with EVALI. Prior evidence supports a high frequency of gastrointestinal symptoms in patients with EVALI, which are sometimes reported as the reason for obtaining medical care.32 Although the reason is unclear, it is possible that differing patterns of product use by adolescents might play a role. For example, adolescents might be inexperienced e-cigarette users compared with adults and inhale less deeply, leading to increased swallowing of the e-cigarette aerosol and a higher exposure of aerosol constituents to the gastrointestinal system. Additional research is needed to test this hypothesis.33,34 The occurrence of nonspecific gastrointestinal and constitutional symptoms may delay clinical recognition of EVALI given that it is a diagnosis of exclusion. A confidential, accurate substance use history paired with appropriate patient education, including about e-cigarette or vaping product use, is needed to ensure timely diagnosis of EVALI.

    These findings highlight the importance of clinicians working with adolescents to provide education and access to services. Teaching should (1) emphasize the association between THC-containing e-cigarette or vaping product use and EVALI; (2) reinforce that there may be other chemicals of concern aside from vitamin E acetate, including those in products not containing THC, associated with EVALI; and (3) counsel adolescents that any e-cigarette or vaping product use is unsafe.1,35 The identification of common comorbidities, including ADHD and asthma, can inform clinical evaluation and intervention; our findings support the critical need to make tobacco use cessation, substance use screening, and mental health services easily accessible to all youth.20,36,37 Clinician awareness that adolescents commonly report nonspecific gastrointestinal and constitutional symptoms may hasten timely recognition of EVALI.

    When addressing EVALI among youth, it is important for clinicians and public health professionals to distinguish between the 2019 EVALI outbreak and the ongoing US epidemic of youth e-cigarette use. Primarily, EVALI is associated with the use of THC-containing products from informal sources (ie, family, friends, and in-person or online dealers), whereas the youth e-cigarette use epidemic has primarily been associated with the use of nicotine-containing products from formal sources (eg, legal retail establishments). However, each of these epidemics (ie, EVALI and youth e-cigarette use) disproportionately influences young people and is complicated by a multifactorial causation.38 These 2 events (EVALI and youth e-cigarette use) represent opportunities for public health and clinical communities to prevent and reduce the use of e-cigarette or vaping products among adolescent and young adult populations. In 2016, the FDA asserted regulatory authority over e-cigarettes, which required that all e-cigarettes on the market at that time needed to have an authorization from the FDA to be legally marketed. However, the agency subsequently deferred enforcement of the premarket authorization requirements, which means that all e-cigarettes now on the US market are considered illegally marketed and are subject to enforcement. Regardless of whether nicotine, THC, or any other substance is used in an e-cigarette or vaping product, these products are not safe for youth or young adults because of known negative health influences.13-15,35,39

    Limitations

    This study has limitations. Data collection methods varied across jurisdictions, which may have resulted in reporting inconsistencies that could not be accounted for in this analysis. Information was obtained from medical records and patient or proxy interviews, which may be incomplete or subject to social desirability or recall bias. In addition, comparisons with national prevalence data (eg, for asthma) may be inexact given the variability in question framing or the time frame of data collection. This analysis only includes hospitalized or deceased EVALI cases; it is possible that many more adolescents may be affected but not severely enough to require hospitalization. Proxies may not have had complete knowledge about the patient’s exposure history. For medical history, indicators of some conditions (any mental, emotional, or behavioral disorder, including ADHD, posttraumatic stress disorder, and substance use, as well as a history of diabetes, asthma, chronic obstructive pulmonary disease, and obstructive sleep apnea) were created using responses to free-text fields and may not have been reported systematically. Finally, some estimates are based on small sample sizes, and precision in estimates is thus limited; these models should be interpreted with caution.

    Conclusions

    It is important for public health and clinical professionals to continue providing information to adolescents about the association between EVALI and THC-containing e-cigarette or vaping product use, in particular those from informal sources, and that any e-cigarette or vaping product use is unsafe.35 The high prevalence of ADHD, other mental or behavioral health conditions, and asthma among adolescents with EVALI may complicate care and follow-up. Youth should be referred to appropriate treatment for co-occurring conditions and substance use cessation services.20,37 The high proportion of adolescents seen with nonspecific gastrointestinal and constitutional symptoms may delay EVALI diagnosis. It is essential that clinicians caring for adolescents obtain a confidential substance use history that includes e-cigarette or vaping product use.37,40,41 Ultimately, the need for programs and policies to limit youth exposure to e-cigarette products, regardless of nicotine or THC content, is a public health imperative.42

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    Article Information

    Accepted for Publication: February 29, 2020.

    Corresponding Author: Susan H. Adkins, MD, National Center for HIV/AIDS, Viral Hepatitis, STD, and TB Prevention, Centers for Disease Control and Prevention, 1600 Clifton Rd, Mail Stop US8-1, Atlanta, GA 30329 (igc7@cdc.gov).

    Published Online: May 18, 2020. doi:10.1001/jamapediatrics.2020.0756

    Author Contributions: Drs Anderson and Ellington had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Drs Adkins and Anderson are co–first authors.

    Concept and design: Adkins, Anderson, Goodman, Twentyman, Kimball, Evans, Kiernan, Rose, Jones, Ellington, Wiltz.

    Acquisition, analysis, or interpretation of data: Adkins, Anderson, Goodman, Twentyman, Danielson, Kimball, Click, Ko, Weissman, Melstrom, Krishnasamy, King, Ellington, Pollack, Wiltz.

    Drafting of the manuscript: Adkins, Anderson, Goodman, Twentyman, Kimball, Ko, Kiernan, King, Wiltz.

    Critical revision of the manuscript for important intellectual content: Adkins, Anderson, Goodman, Twentyman, Danielson, Kimball, Click, Ko, Evans, Weissman, Melstrom, Krishnasamy, Rose, Jones, King, Ellington, Pollack, Wiltz.

    Statistical analysis: Anderson, Goodman, Twentyman, Danielson, Ko, Melstrom, Ellington, Pollack.

    Administrative, technical, or material support: Adkins, Anderson, Goodman, Twentyman, Click, Ko, Evans, Weissman, Melstrom, King, Ellington, Wiltz.

    Supervision: Adkins, Anderson, Twentyman, Evans, Krishnasamy, Rose, Jones, King, Ellington, Pollack, Wiltz.

    Conflict of Interest Disclosures: None reported.

    Group Information: The Lung Injury Clinical Task Force members are Maleeka Glover, ScD, MPH; Katherine Shealy, MPH; Sarah Reagan-Steiner, MD; and Stacy Thorne, PhD, MPH. The Lung Injury Epidemiology/Surveillance Task Force members are Bailey Wallace, MPH; Don Hayes, MD; Kimberly Thomas, MPH; Chelsea Austin; Matthew Lozier, PhD; Stephanie Thomas; Alissa Cyrus, MPH; Kelsey Coy, MPH; Christina Mikosz, MD; Dustin Currie, PhD; Sierra Graves, MPH; Phillip Salvatore, PhD; Sonal Goyal, PharmD; Denise Hughes; Suzanne Newton, MPH; Rashid Njai, PhD; Geroncio Fajardo, MD; Megan Wallace, PhD; Zheng (Jane) Li, PhD; Amy Board, DrPH; Lindsay Eckhaus, MPH; Elizabeth Carter, MPH; Lindsay Kim, MD; Amena Abbas, MPH; Stephen Soroka, MPH; Adebayo Adebola, MPH; and (from the Council of State and Territorial Epidemiologists) Mia Israel, MPH, and Janet Hamilton, MPH.

    Disclaimer: The findings and conclusions of this article are those of the authors and do not represent the official position of the Centers for Disease Control and Prevention.

    Additional Contributions: We thank the members of the Lung Injury Clinical Task Force and the Lung Injury Epidemiology/Surveillance Task Force, who contributed to data collection and administrative support. The following individuals contributed to data collection efforts (no compensation was provided for these efforts): Sarah Khalidi, MPH, and Sondra Reese, MPH, Alabama Department of Public Health; Eric Q. Mooring, ScD, SM, MPhil, and Joseph B. McLaughlin, MD, MPH, Alaska Division of Public Health; Emily M. Carlson, MPH, and Tiana Galindo, Arizona Department of Health Services; Allison James, DVM, MPH, PhD, Appathurai Balamurugan, MD, DrPH, and Brandy Sutphin, MPH, Arkansas Department of Health; California e-Cigarette, or Vaping, Product Use–Associated Lung Injury Investigation Team, California Department of Public Health; Elyse Contreras, MPH, and Richard Holdman, MD, Colorado Department of Public Health and Environment; Sydney Jones, PhD, MScPH, and Jaime Krasnitski, MPH, Connecticut Department of Public Health; Caroline Judd, MPH, and Amanda Bundek, BS, Delaware Department of Health and Social Services, Division of Public Health; Adrienne Sherman, MPH, and Kenan Zamore, MPH, District of Columbia Department of Health; Heather Rubino, PhD, MS, and Thomas Troelstrup, MPH, Florida Department of Health; Georgia Lung Injury Response Team, Georgia Department of Public Health; Hawaii Department of Health; Kathryn A. Turner, PhD, MPH, Eileen M. Dunne, PhD, and Scott C. Hutton, PhD, MPH, Idaho Division of Public Health; Lori Saathoff-Huber, MPH, and Dawn Nims, MPH, Illinois Department of Public Health; Charles R. Clark, MPH, Sara Hallyburton, MPH, and Kathryn Gaub, DVM, MPH, Indiana State Department of Health; Chris Galeazzi, Nicholas Kalas, MPH, Tom Salter, MBA, MPH, and Tyra Goss, Iowa Department of Public Health; Amie Cook, MPH, and Justin Blanding, MPH, Kansas Department of Health and Environment; Kentucky Department for Public Health; Julie Hand, MSPH, and Theresa Sokol, MPH, Louisiana Department of Health; Maine Center for Disease Control and Prevention; Clifford S. Mitchell, MS, MD, MPH, and Kenneth A. Feder, PhD, Maryland Department of Health; John Bernardo, MD, and Catherine M. Brown, DVM, MSc, MPH, Massachusetts Department of Public Health; Rita Seith, MPH, and Eden V. Wells, MD, MPH, FACPM, Michigan Department of Health and Human Services; Stacy Holzbauer, DVM, MPH, Terra Wiens, MPH, Jo Taylor, DVM, PhD, Cory Cole, MPH, Paige D’Heilly, MPH, Jamie Margetta, MPH, and Ruth Lynfield, MD, Minnesota Department of Health; Paul Byers, MD, and Kathryn Taylor, MD, Mississippi State Department of Health; Valerie Howard, MSW, and George Turabelidze, MD, Missouri Department of Health and Senior Services; Isaiah Reed, MA, MSc, Montana Department of Public Health and Human Services; Matthew Donahue, MD, and Tom Safranek, MD, Nebraska Department of Health and Human Services; Melissa Peek-Bullock, BS, Victoria LeGarde, MPH, and Ashleigh Faulstich, MPH, Nevada Department of Health and Human Services; Suzann Beauregard, RN, Darlene Morse, MS, and Pascal Kalin, MSc, New Hampshire Department of Health and Human Services; Stephen Perez, PhD, RN, and Lisa McHugh, PhD, MPH, New Jersey Department of Health; Joseph T. Hicks, DVM, PhD, and Alex Gallegos, MPH, New Mexico Department of Health; EVALI Investigation Team, New York State Department of Health; Lauren J. Tanz, ScD, Ariel Christensen, MPH, and Aaron Fleischauer, PhD, North Carolina Division of Public Health; Kodi Pinks, MPH, and Tracy Miller, PhD, MPH, North Dakota Department of Health; Courtney Dewart, PhD, MPH, RN, and Kirtana Ramadugu, MPH, Ohio Department of Health; Tracy Wendling, DrPH, and Claire B. Nguyen, MS, Oklahoma State Department of Health; Tasha Poissant, MPH, Amanda Faulkner, MPH, Steve Rekant, DVM, MPH, and Laurel Boyd, MPH, Oregon Health Authority; Kumar Nalluswami, MD, MPH, and Brittany N. Spotts, Pennsylvania Department of Health; Ada Lily Ramírez Osorio, RN, BSN, MBA/HCM, Departamento de Salud de Puerto Rico; Ailis Clyne, MD, James Rajotte, MS, and Morgan Orr, MPH(c), Rhode Island Department of Health; Virginie Daguise, PhD, Sharon Biggers, MPH, CHES, and Daniel Kilpatrick, PhD, MPH, CEPR, South Carolina Department of Health and Environmental Control; Joshua L. Clayton, Jonathan Steinberg, and Kipp Stahl, BSN, RN, South Dakota Department of Health; Kelly Squires, MPH, and Julie Shaffner, MS, MPH, Tennessee Department of Health; Ketki Patel, Varun Shetty, MD, MBA, MS, Haylea Stuteville, MPH, DeLayna Goulding, MPH, and Emily Hall, MPH, Texas Department of State Health Services; Esther M. Ellis, PhD, US Virgin Islands Department of Health; Keegan McCaffery and Jordan Green, MPH, Utah Department of Health; Vermont Department of Health; Lilian Peake, MD, MPH, and Jonathan Falk, MPH, Virginia Department of Health; Trevor Christensen, MPH, and Melanie Payne, MPH, Washington State Department of Health; Shannon McBee, MPH, CHES, and Christy Reed, BSPH, West Virginia Department of Health and Human Resources; Jonathan Meiman, MD, and Ian Pray, PhD, MPH, Wisconsin Department of Health Services; and Melissa Taylor, MPH, Wyoming Department of Health.

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