Sex Disparities in the Management and Outcomes of Cardiogenic Shock Complicating Acute Myocardial Infarction in the Young
What is New?
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Younger women with acute myocardial infarction-cardiogenic shock received less frequent coronary angiography (78.3% versus 81.4%), early coronary angiography (49.2% versus 54.1%), percutaneous coronary intervention (59.2% versus 64.0%), and mechanical circulatory support (50.3% versus 59.2%) than young men (all P<0.001).
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Female sex was an independent predictor of higher in-hospital mortality (23.0% versus 21.7%; adjusted odds ratio 1.11 [95% CI, 1.07–1.16]; P<0.001) in young admissions with acute myocardial infarction-cardiogenic shock.
What are the Clinical Implications?
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Younger women had lower acuity of illness, lower use of coronary angiography, and percutaneous coronary intervention and higher in-hospital mortality. Whether decreases in invasive strategies has a causal relationship with outcome needs further study.
Introduction
See Editorial by Vest and Cho
Cardiogenic shock following acute myocardial infarction-cardiogenic shock (AMI-CS) continues to carry a significant morbidity and mortality, despite the advances in the acute cardiovascular care.1–6 CS is the leading cause of death in patients with AMI who reach the hospital alive, with mortality rates of ≈50%, mainly occurring within the first 48 hours on admission.7 This mortality is attributed to cardiac pump failure, leading to persistent hypotension and organ hypoperfusion and subsequent multiorgan failure.2,3,8–10 Prior studies have demonstrated persistent healthcare disparities, including sex-based disparities, in the management and outcomes of patients with AMI-CS.11,12 Women with AMI-CS frequently receive less frequent coronary angiography, percutaneous coronary intervention (PCI), coronary artery bypass grafting, and mechanical circulatory support (MCS) compared with their male counterparts.11,13,14 In spite of that, there is evidence that women might actually derive greater benefit from more aggressive, timely, and appropriate cardiac interventions.4,13–17
A majority of these studies have been conducted in older adults or all comers, and therefore younger patients are frequently under-represented.18,19 In the modern era, with the increased prevalence of obesity and other cardiovascular comorbidities, AMI is increasing in the younger population.14,19,20 There are limited data on the outcomes of AMI-CS in the young population. Whether sex disparities are pervasive in this highly selected group of patients is unclear given that younger women may exhibit fewer traditional atherosclerotic cardiovascular risk factors, higher rates of delayed reperfusion, and have more frequent target lesion failure than age-matched men.18–23 Women are also known to have less obstructive coronary artery disease as a cause for their AMI and whether, in the presence of CS, this makes a difference to outcome is unknown.14,20
Using a nationally representative population, we sought to determine if there are sex disparities in the clinical management and outcomes of AMI-CS in the young. We hypothesized that young women with AMI-CS would receive less frequent cardiac procedures and would have higher in-hospital mortality as compared with young men.
Materials and Methods
The National (Nationwide) Inpatient Sample (NIS) is the largest all-payer database of hospital inpatient stays in the United States. NIS contains discharge data from a 20% stratified sample of community hospitals and is a part of the Healthcare Quality and Utilization Project (HCUP), sponsored by the Agency for Healthcare Research and Quality.24 Information regarding each discharge includes patient demographics, primary payer, hospital characteristics, principal diagnosis, up to 24 secondary diagnoses, and procedural diagnoses. The HCUP-NIS does not capture individual patients but captures all information for a given admission. Institutional Review Board approval was not needed as this database was publicly available and de-identified. These data are available to other authors via the HCUP-NIS database with the Agency for Healthcare Research and Quality.
Using the HCUP-NIS data from 2000 to 2017, a retrospective cohort study of admissions between the ages of 18 and 55 years, with AMI in the primary diagnosis field (International Classification of Diseases-9.0 Clinical Modification 410.x and International Classification of Diseases-10 Clinical Modification I21.x-22.x) and a secondary diagnosis of CS (International Classification of Diseases-9.0 Clinical Modification 785.51, International Classification of Diseases-10 Clinical Modification CM R57.0) were identified. Admissions without data on sex or in-hospital mortality were excluded. The Deyo’s modification of the Charlson Comorbidity Index was used to identify the burden of comorbid diseases (Table I in the Data Supplement).25 Demographic characteristics, hospital characteristics, acute organ failure, coronary angiography, PCI, MCS, and noncardiac organ support use were identified for all admissions using previously used methodologies from our group.1–6,8–10,12,26–38 Early coronary angiography was defined as that performed on hospital day zero; the hospital day the procedure was performed was used to time concomitant procedures.
The primary outcome was the in-hospital mortality in male and female AMI-CS admissions. Temporal trends of CS prevalence, in-hospital mortality, and use of cardiac procedures were evaluated. Secondary outcomes included hospital length of stay, hospitalization costs, use of do-not-resuscitate status, palliative care referral, and discharge disposition in male and female AMI-CS admissions.
Statistical Analysis
As recommended by HCUP-NIS, survey procedures using discharge weights provided with HCUP-NIS database were used to generate national estimates.39 Using the trend weights provided by the HCUP-NIS, samples from 2000 to 2011 were re-weighted to adjust for the 2012 HCUP-NIS re-design.39 Chi-square/1-way ANOVA and t-tests were used to compare 2/≥2 categorical and continuous variables, respectively. Multivariable logistic regression was used to analyze trends over time (referent year 2000). Univariable analysis for trends and outcomes was performed and was represented as odds ratio (OR) with 95% CI. Multivariable logistic regression analysis incorporating age, sex, race, primary payer status, socioeconomic stratum, hospital characteristics, comorbidities, acute organ failure, AMI-type, cardiac procedures, noncardiac procedures, do-not-resuscitate status, and palliative care referral was performed for assessing temporal trends of prevalence and in-hospital mortality. For the multivariable modeling, regression analysis with purposeful selection of statistically (liberal threshold of P<0.20 in univariate analysis) and clinically relevant variables was conducted. There was a statistically significant interaction between sex and adjusted temporal trends of prevalence and in-hospital mortality (P=0.02 and P=0.04 for interaction, respectively). Multiple subgroup analyses stratifying the population by race, presence of cardiac arrest, type of AMI, receipt of PCI and MCS, were performed to confirm the results of the primary analysis. Given the large sample size, all P values that are statistically significant may not be clinically significant.
The inherent restrictions of the HCUP-NIS database related to research design, data interpretation, and data analysis were addressed using prescribed best practices.39,40 Pertinent considerations include not assessing individual hospital-level volumes (because of changes to sampling design detailed above), treating each entry as an admission as opposed to individual patients, restricting the study details to inpatient factors since the HCUP-NIS does not include outpatient data, and limiting administrative codes to those previously validated and used for similar studies. Two-tailed P<0.05 was considered statistically significant. All statistical analyses were performed using SPSS v25.0 (IBM Corp, Armonk NY).
Results
In the period from January 1, 2000 to December 31, 2017, there were over 11 million AMI admissions, of which 2 540 100 (23.1%) were aged 18 to 55 years. CS complicated 90 648 of these younger admissions (3.6%) with a comparable prevalence between men (67 004; 3.6%) and women (23 644; 3.5%; P<0.001). The 18-year temporal trends of CS prevalence in young AMI admissions by sex are presented in Figure 1A and 1B. CS was noted in 2% to 5% of AMI admissions with a steady increase in trend in both sexes, although men had higher rates of CS compared with young women. Compared with men, women with AMI-CS were more often Black, from a lower socioeconomic status, with higher comorbidity, and were admitted more frequently to rural and small hospitals (all P<0.001; Table 1).
| Characteristic | Young Men (N=67 004) | Young Women (N=23 644) | P Value |
|---|---|---|---|
| Age, y | 48.8±5.6 | 48.3±6.2 | <0.001 |
| Race | |||
| White | 58.2 | 58.4 | <0.001 |
| Black | 7.5 | 12.0 | |
| Others* | 34.3 | 29.6 | |
| Weekend admission | 29.1 | 27.6 | <0.001 |
| Primary payer | |||
| Medicare | 10.7 | 14.9 | <0.001 |
| Medicaid | 16.9 | 22.9 | |
| Private | 50.9 | 46.3 | |
| Others† | 21.6 | 15.9 | <0.001 |
| Quartile of median household income for zip code | |||
| 0th to 25th | 26.3 | 30.3 | <0.001 |
| 26th to 50th | 26.2 | 27.1 | |
| 51st to 75th | 24.6 | 23.5 | |
| 75th to 100th | 23.0 | 19.1 | |
| Charlson comorbidity index | |||
| Mean | 2.1±1.7 | 2.2±1.7 | <0.001 |
| 0–3 | 84.1 | 80.3 | |
| 4–6 | 14.1 | 18.0 | |
| ≥7 | 1.8 | 1.7 | |
| Comorbidities | |||
| Heart failure | 37.4 | 37.9 | 0.13 |
| CKD | 5.4 | 5.8 | 0.02 |
| Cancer | 1.8 | 3.0 | <0.001 |
| AIDS | 0.8 | 0.3 | <0.001 |
| Chronic lung disease | 11.8 | 17.2 | <0.001 |
| Stroke/TIA | 3.2 | 3.5 | 0.03 |
| Hemiplegia | 0.7 | 0.7 | 0.59 |
| Prior CABG | 1.8 | 1.9 | 0.37 |
| Prior pacemaker | 0.3 | 0.5 | <0.001 |
| Prior ICD | 1.1 | 0.8 | <0.001 |
| Atrial fibrillation | 12.8 | 9.2 | <0.001 |
| SVT | 1.2 | 1.1 | 0.30 |
| Hospital teaching status and location | |||
| Rural | 4.9 | 6.0 | <0.001 |
| Urban nonteaching | 34.5 | 34.1 | |
| Urban teaching | 60.7 | 59.9 | |
| Hospital bed-size | |||
| Small | 7.4 | 7.7 | 0.08 |
| Medium | 22.2 | 21.6 | |
| Large | 70.4 | 70.8 | |
| Hospital region | |||
| Northeast | 15.3 | 15.0 | <0.001 |
| Midwest | 23.3 | 24.6 | |
| South | 41.5 | 43.1 | |
| West | 20.0 | 17.3 | |
Figure 1. Trends in the prevalence and in-hospital mortality in younger acute myocardial infarction-cardiogenic shock (AMI-CS) admissions stratified by sex. A, Unadjusted temporal trends of the proportion of AMI admissions with CS stratified by sex (P<0.001 for trend over time). B, Adjusted odds ratio for admission with AMI-CS by year with 2000 as the referent; adjusted for race, comorbidity, primary payer, socioeconomic status, and hospital characteristics (P<0.001 for trend over time). C, Unadjusted in-hospital mortality in AMI-CS by year of admission, stratified by sex (P<0.001 for trend over time). D, Adjusted multivariate logistic regression for in-hospital mortality temporal trends with 2000 as referent year; adjusted for race, admission year, primary payer status, socioeconomic stratum, hospital characteristics, comorbidities, AMI type, acute organ failure, cardiac arrest, cardiac procedures; noncardiac procedures; do-not-resuscitate status; palliative care referral (P<0.001 for trend over time).
Women with AMI-CS had lower rates of ST-segment elevation AMI-CS presentation (73.0% versus 78.7%), lower rates of acute noncardiac organ failure, and lower rates of cardiac arrest (34.3% versus 35.7%; all P<0.001; Table 2). Compared with men, women received less frequent coronary angiography (78.3% versus 81.4%), early coronary angiography (49.2% versus 54.1%), PCI (59.2% versus 64.0%), coronary artery bypass grafting (18.3% versus 20.1%), and MCS (50.3% versus 59.2%; all P<0.001). Temporal trend analysis showed persistently higher rates of coronary angiography, PCI, and MCS use in men compared with women (Figure 2).
| Characteristic | Young Men (N=67 004) | Young Women (N=23 644) | P Value |
|---|---|---|---|
| Acute organ failure | |||
| Respiratory | 42.8 | 43.7 | 0.71 |
| Renal | 27.4 | 21.9 | <0.001 |
| Hepatic | 10.5 | 8.8 | <0.001 |
| Hematologic | 10.4 | 10.3 | 0.70 |
| Neurologic | 16.6 | 16.6 | 0.98 |
| Takotsubo cardiomyopathy | 0.1 | 0.7 | <0.001 |
| Ischemic stroke | 2.4 | 2.6 | 0.09 |
| Intracranial hemorrhage | 0.6 | 0.8 | 0.02 |
| Intravascular ultrasound | 2.1 | 2.1 | 0.81 |
| Coronary thrombectomy | 2.4 | 2.1 | 0.01 |
| Pulmonary artery catheterization | 7.5 | 7.4 | 0.64 |
| Mechanical circulatory support | |||
| Total | 59.2 | 50.3 | <0.001 |
| IABP | 54.7 | 47.0 | <0.001 |
| pLVAD | 4.2 | 3.0 | <0.001 |
| ECMO | 1.9 | 1.6 | <0.001 |
| Invasive mechanical ventilation | 41.7 | 43.2 | <0.001 |
| Noninvasive ventilation | 2.5 | 2.3 | 0.08 |
| Hemodialysis | 2.6 | 1.8 | <0.001 |
| Fiberoptic bronchoscopy | 3.6 | 3.0 | <0.001 |
| Electroencephalogram | 0.7 | 0.9 | 0.002 |
Figure 2. Trends in the use of coronary angiography, percutaneous coronary intervention (PCI), pulmonary artery catheterization (PAC), and mechanical circulatory support (MCS) in younger acute myocardial infarction-cardiogenic shock (AMI-CS) admissions stratified by sex. Eighteen-year trends in the use of coronary angiography (A), PCI (B), PAC (C), and MCS (D) in younger AMI-CS admissions stratified by sex; all P<0.001 for trend over time.
Compared with men, women had a higher unadjusted in-hospital mortality (23.0% versus 21.7%, unadjusted OR, 1.16 [95% CI, 1.10–1.22]; P<0.001). The 15-year unadjusted and adjusted temporal trends of in-hospital mortality in AMI-CS stratified by sex are presented in Figure 1C and 1D. Despite significant decreases in in-hospital mortality over time in both men and women, after adjustment for race, admission year, primary payer status, socioeconomic stratum, hospital characteristics, comorbidities, AMI type, acute organ failure, cardiac arrest, cardiac procedures; noncardiac procedures; do-not-resuscitate status; palliative care referral, women had significantly higher in-hospital mortality than men throughout the early part of the study period. In a multivariable logistic regression for in-hospital mortality in young AMI-CS admissions, female sex was an independent predictor of higher in-hospital mortality (OR 1.11 [95% CI, 1.07–1.16]; P<0.001; Table II in the Data Supplement). In stratified prespecified subgroup analyses (Figure 3), female sex was an independent predictor of higher in-hospital mortality in admissions of White race, with concomitant cardiac arrest, ST-segment elevation AMI-CS presentation and those not receiving PCI or MCS. Women had comparable rates of do-not-resuscitate status use, palliative care referral, and hospital length of stay to men (Table 3). However, compared with men, women had lower hospitalization costs and less frequent discharges to home (Table 3).
| Characteristic | Young Men (N=67 004) | Young Women (N=23 644) | P Value |
|---|---|---|---|
| In-hospital mortality | 21.7 | 23.0 | <0.001 |
| Length of stay, d | 10.3±12.5 | 10.6±13.3 | 0.001 |
| Hospitalization costs (USD) | 167 669±208 577 | 156 372±198 452 | <0.001 |
| Do-not-resuscitate status use | 2.9 | 2.9 | 0.64 |
| Palliative care referral | 3.1 | 3.1 | 0.85 |
| Discharge disposition | |||
| Home | 64.1 | 57.2 | |
| Hospital transfer | 11.3 | 11.9 | |
| Skilled nursing facility | 10.8 | 13.7 | |
| Home with home health care | 12.7 | 16.4 | |
| Against medical advice | 1.1 | 0.8 | |
Figure 3. Multivariate predictors of in-hospital mortality in younger women with acute myocardial infarction-cardiogenic shock (AMI-CS) compared with younger men. Multivariable-adjusted odds ratios (95% CIs)* for in-hospital mortality in the women stratified by race, presence of cardiac arrest, type of AMI, receipt of percutaneous coronary intervention (PCI) and mechanical circulatory support (MCS); all P<0.001. *Adjusted race, year of admission, primary payer, socioeconomic status, hospital location/teaching status, hospital bedsize, hospital region, comorbidity, type of AMI, acute organ failure, cardiac arrest, coronary angiography, PCI, coronary artery bypass grafting; pulmonary artery catheterization, MCS, mechanical ventilation; hemodialysis; do-not-resuscitate status; palliative care referral. NSTEMI indicates non-ST-elevation myocardial infarction; and STEMI, ST-elevation myocardial infarction.
Discussion
In this study of young AMI-CS admissions, we observed that women were more likely to be Black, with higher comorbidity, and have a lower frequency of noncardiac organ failure and cardiac arrest compared with men. Younger women underwent less frequent coronary angiography, PCI and MCS utilization compared with younger men. Female sex was an independent predictor of higher in-hospital mortality, with a consistently higher temporal trend during this 18-year period. Female sex was a predictor of higher in-hospital mortality in high-risk subgroups such as those with ST-segment elevation AMI-CS presentation, with concomitant cardiac arrest, and those not receiving PCI or MCS support.
There are limited data on sex-specific outcomes in AMI-CS. Studies analyzing all patients, the majority of whom are elderly, with AMI-CS from IABP-SHOCK II (The Intraaortic Balloon Pump in Cardiogenic Shock II), SHOCK (Should We Emergently Revascularize Occluded Coronaries for Cardiogenic Shock) registry, and CULPRIT-SHOCK trials (The Culprit Lesion Only PCI Versus Multivessel PCI in Cardiogenic Shock) did not show difference in mortality between women and men.21,22,41 These studies noted women have higher comorbidity, more frequent adverse clinical events, higher rates of mechanical complications and received guideline-directed therapies less often as in this study but concluded that they derived similar benefits from use of revascularization and had comparable in-hospital outcomes.21–23,41 In contrast, prior work from our group has demonstrated that older (≥75 years) women do worse than men with AMI-CS.11
As compared with these populations, younger AMI patients are unique in their varied etiology of AMI, lower comorbidity burden, greater prevalence of high-risk lifestyle behaviors, and lower healthcare utilization.20 It is unclear if similar sex disparities are noted in younger women with AMI-CS compared with younger men. In one study of patients with AMI ≤45 years, Bandyopadhyay et al19 found that despite having a higher comorbidity burden, women had comparable in-hospital mortality and lower rates of CS compared with men. Epps et al18 have noted that young women, despite having less severe disease on coronary angiography, are at higher risk for target vessel and target lesion failure. In the VIRGO study (Variation in Recovery: Role of Gender on Outcomes of Young AMI Patients), female sex was associated with reperfusion delay in young patients with ST-segment elevation AMI.16 Taken in aggregate, these findings suggest that sex-specific disparities exist in young patients with AMI. Our study adds to this literature by specifically evaluating AMI-CS admissions. We note higher in-hospital mortality in young women with AMI-CS. In addition to the potential reasons as stated above, this current analysis indicates that (1) women had a worse comorbidity profile, higher rates of prior chronic kidney disease and cancer, and greater use of invasive mechanical ventilation, all of which portent a poor prognosis and may have served as a deterrent for performance of invasive procedures (Table 1)9; (2) despite an increase in the uptake of coronary angiography, early coronary angiography and PCI over time, women consistently received these therapies less frequently; (3) women had a lower socioeconomic status, which is associated with lower access to healthcare resources and poorer baseline management of comorbidities before hospitalization; (4) it is conceivable that consistent with prior literature, women present with delayed and atypical symptoms and are often misdiagnosed resulting in less-frequent guideline-directed care14,20; and (5) a significant portion of young women were admitted to small and rural hospitals, which we have previously shown to be associated with worse outcomes in AMI-CS.1,5 It is important to note that the etiology of AMI-CS in this young population could not be assessed in this study, and further details are needed to clarify the etiology given the high rates of nonplaque rupture mechanisms in this population.14,20 Last, hospital-level disparities in this population are worthy of further evaluation for future studies.
In addition to poor outcomes, women typically receive less frequent cardiac procedures, including PCI, coronary artery bypass grafting, and MCS.11,12,33,35,37 The majority of these studies included older women with a few studies assessing management in younger women.42 In AMI admissions ≤45 years, women received less PCI, coronary artery bypass grafting, and were less likely to undergo timely PCI within 24 hours of presentation as compared with men.19 Prior work from our group has noted younger age, male sex, lower comorbidity, and cardiac arrest to independently predicted MCS-assisted PCI in AMI-CS.33 Consistent with these data, in the current study, we noted younger women to receive less frequent coronary angiography, PCI, and MCS in AMI-CS. It is conceivable that lower rates of acute organ failure might explain the lower MCS use. However, prior data have shown that clinicians worry about higher complications with large-bore MCS in women because of smaller caliber of femoral vessels, lower body surface area, and higher rates of bleeding.13,14,34 As noted in this study, females has higher rates of intracranial hemorrhages suggestive of higher rates of complications from both antiplatelet/anticoagulation therapies and MCS use.
Using the HCUP-NIS database between 2001 and 2010, Gupta et al43 showed race to play a larger role in young women with AMI compared with young men. They noted Black race to be associated with higher mortality in all-comers AMI population.43 In our prior work in older patients, we similar noted non-White race to be an independent predictor of worse outcomes in older AMI-CS admissions.11 Data from the SHOCK trial have shown no racial/ethnic differences in AMI-CS patients after adjusting for patient characteristics and use of revascularization.44 In young women ≤55 years, Black women tend to have higher rates of hospitalization and higher mortality compared with White women, even after adjustment for chronic kidney disease, time of presentation, insurance, and treatment in the first 24 hours.14 In contrast, this study found higher in-hospital mortality in young White women. These contrasting findings may be attributable to the acuity and organ failure in AMI-CS, which may predominate over the comorbid conditions in the evaluation of short-term mortality.3 Regardless, the interaction of age, sex, and race are worthy of further careful study in this vulnerable population of critically ill patients with AMI-CS.
Limitations
This study has several limitations, despite the HCUP-NIS database’s attempts to mitigate potential errors by using internal and external quality control measures. The International Classification of Diseases-9.0 Clinical Modification codes for AMI and CS have been previously validated that reduces the inherent errors in the study.45,46 It is conceivable that increased recognition and subsequent coding of CS could have contributed to the increase in prevalence as noted in our study. Important factors such as the delay in presentation from time of onset of AMI symptoms, timing of CS, reasons for not receiving aggressive medical care, timing of multiorgan failure, and treatment-limiting decisions of organ support could not be reliably identified in this database. It is possible that despite best attempts at mitigating confounding by a multivariable analysis, female sex was a marker of greater illness severity because of residual confounding. Echocardiographic data, angiographic variables, and hemodynamic parameters were unavailable in this database, which limits physiological assessments of disease severity. Last, spontaneous coronary artery dissection or coronary spasm, which is noted more frequently in young women presenting with AMI, could not be ascertained in this population because of the nonspecific coding for this etiology.47
Conclusions
In young (≤55 years) AMI-CS admissions, there remain significant sex disparities in the management and outcomes. Younger women had higher comorbidity, lower acuity of illness, lower use of coronary angiography, and PCI and higher in-hospital mortality. Further quantitative and qualitative research is needed in these vulnerable populations to better understand the underlying reasons for these differences in resource utilization in this high-risk population and what can be done to improve the outcome.
| AMI |
acute myocardial infarction |
| CS |
cardiogenic shock |
| CULPRIT-SHOCK |
The Culprit Lesion Only PCI Versus Multivessel PCI in Cardiogenic Shock |
| HCUP |
Healthcare Cost and Utilization Project |
| MCS |
mechanical circulatory support |
| NIS |
National (Nationwide) Inpatient Sample |
| OR |
odds ratio |
| PCI |
percutaneous coronary intervention |
| SHOCK |
Should We Emergently Revascularize Occluded Coronaries for Cardiogenic Shock |
| VIRGO |
Variation in Recovery: Role of Gender on Outcomes of Young AMI Patients |
Acknowledgments
Drs Vallabhajosyula, Ya’Qoub, Cheungpasitporn, Sundaragiri, and Barsness performed study design, literature review, statistical analysis, data management, data analysis, and drafting manuscript. Drs Vallabhajosyula, Ya’Qoub, Singh, Bell, Gulati, Cheungpasitporn, Sundaragiri, Miller, Jaffe, B.J. Gersh, and Drs Holmes and Barsness provided access to data. Drs Singh, Bell, Gulati, Miller, Jaffe, B.J. Gersh, and Drs Holmes and Barsness participated in manuscript revision, intellectual revisions, and mentorship. Drs Vallabhajosyula, Ya’Qoub, Singh, Bell, Gulati, Cheungpasitporn, Sundaragiri, Miller, Jaffe, Gersh, Holmes, and Barsness provided final approval.
Sources of Funding
Dr Vallabhajosyula is supported by the Clinical and Translational Science Award (CTSA) Grant Number UL1 TR000135 from the National Center for Advancing Translational Sciences (NCATS), a component of the National Institutes of Health (NIH). Its contents are solely the responsibility of the authors and do not necessarily represent the official view of NIH.
Footnotes
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