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Progression of the Radiologic Severity Index Is Associated with Increased Mortality and Healthcare Resource Utilisation in Acute Leukaemia Patients with Pneumonia

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Progression of the Radiologic Severity Index Is Associated with Increased Mortality and Healthcare Resource Utilisation in Acute Leukaemia Patients with Pneumonia BMJ Open Resp Res: first published as 10.1136/bmjresp-2019-000471 on 23 December 2019. Downloaded from Respiratory infection Progression of the Radiologic Severity Index is associated with increased mortality and healthcare resource utilisation in acute leukaemia patients with pneumonia Ajay Sheshadri ,1 Myrna Godoy,2 Jeremy J Erasmus,2 Stephen Gruschkus,3 Arain Hasan,1 Scott E Evans,1 Javier Barreda- Garcia,1 Roy F Chemaly,4 Burton Dickey,1 David Ost1 To cite: Sheshadri A, ABSTRACT Key messages Godoy M, Erasmus JJ, et al. Background Pneumonia is a major cause of mortality Progression of the Radiologic and morbidity, but the development of new antimicrobials Progression of the Radiologic Severity Index (RSI), a Severity Index is associated is lacking. Radiological assessment of pneumonia severity ► reproducible measure of how severe a pneumonia with increased mortality may serve as an effective intermediate endpoint to reduce and healthcare resource is on chest imaging, is associated with increased barriers to successful completion of antimicrobial trials. We utilisation in acute leukaemia morbidity and mortality after pneumonia in immuno- sought to determine whether the Radiologic Severity Index patients with pneumonia. compromised hosts BMJ Open Resp Res (RSI) correlated with mortality and healthcare resource utilisation in patients with acute leukaemia undergoing ► Each one- point increase in RSI is associated with a 2019;6:e000471. doi:10.1136/ 7% increase in mortality, and higher peak RSI mea- by copyright. bmjresp-2019-000471 induction chemotherapy. Methods We measured RSI (range 0–72) on all chest surements are associated with higher daily hospital costs and utilisation of intensive care unit resources. This work was previously radiographs performed within 33 days of induction ► We highlight the potential of the RSI as an interme- presented at the American chemotherapy in 165 haematological malignancy patients diate marker of pneumonia severity in antimicrobial Thoracic Society 2017 with pneumonia. Peak RSI was defined as the highest RSI Conference. score within 33 days of induction. We used extended Cox trials. proportional hazards models to measure the association of Received 1 August 2019 time- varying RSI with all- cause mortality within the first 33 Revised 25 November 2019 days after induction chemotherapy, and logistic regression new antimicrobials has lagged behind the Accepted 27 November 2019 or generalised models to measure the association of RSI emergence of resistant pathogens.4 A major http://bmjopenrespres.bmj.com/ with total daily cost and healthcare resource utilisation. impediment to antimicrobial development is Results After adjustment for clinical variables, each one- the difficulty in proving clinical superiority point increase in RSI was associated with a 7% increase through reductions in mortality, because in all- cause 33- day mortality (HR 1.07, 95% CI 1.05 to death is not always attributable to the pneu- 1.09, p<0.0001). Peak RSI values of 37.5 or higher were 5 associated with 86% higher daily direct costs (p<0.0001), monia itself. Furthermore, pneumonia is asso- more days in intensive care unit (9.9 vs 4.8 days, p=0.001) ciated with substantial long- term morbidity and higher odds for mechanical ventilation (OR 12.1, in proportion to pneumonia severity, and p<0.0001). reductions in long- term morbidity would Conclusions Greater radiological severity as measured by not be captured by an endpoint of short- RSI was associated with increased mortality and morbidity 6 term mortality. As a result of the weakness of on September 30, 2021 by guest. Protected in acute leukaemia patients with pneumonia. RSI is a mortality as an endpoint in studies of antimi- promising intermediate marker of pneumonia severity and crobials, the Food and Drug Administration is well suited for use in antimicrobial trials. © Author(s) (or their (FDA) recommended in 2009 that investiga- employer(s)) 2019. Re- use tors consider non- mortality endpoints when permitted under CC BY- NC. No 7 commercial re- use. See rights designing clinical trials. and permissions. Published by INTRODUCTION A recent international expert panel cited BMJ. Worldwide, over 2.7 million deaths are clinical cure, defined as (1) resolution of For numbered affiliations see attributed to pneumonia annually,1 and the signs and symptoms of pneumonia and (2) end of article. annual cost in the USA has been estimated resolution or stability of radiological signs of at $8.4 billion.2 Although antimicrobial resist- pneumonia, as the most relevant endpoint in Correspondence to 8 Dr Ajay Sheshadri; ance is a major barrier to the successful treat- pneumonia trials. Radiological progression 3 ASheshadri@ mdanderson. org ment of pneumonia, the development of of pneumonia would therefore constitute a Sheshadri A, et al. BMJ Open Resp Res 2019;6:e000471. doi:10.1136/bmjresp-2019-000471 1 BMJ Open Resp Res: first published as 10.1136/bmjresp-2019-000471 on 23 December 2019. Downloaded from Open access 9 10 failure to achieve clinical cure, but tools to precisely Table 1 Scoring algorithm for the RSI quantify radiological severity have only recently been developed.11–13 We have previously shown that radiolog- Extent of Predominant volumetric ical severity could be precisely and reliably quantified radiological radiological using the Radiologic Severity Index (RSI), a semiquan- 13 pattern in the Pattern involvement Volumetric titative scoring tool. RSI ranges from 0 to 72, and each lung zone score (%) score one- point increase in RSI was associated with a 13% increase in the hazard for 30-day mortality in a high-risk Normal lung 1 0 (normal) 0 cohort of haematological malignancy (HM) patients with Ground glass 2 1–24 1 parainfluenza pneumonia. Furthermore, we showed that opacities RSI progression improved estimates of mortality risk Consolidation 3 25–49 2 in immunocompromised HM patients with respiratory 50–74 3 syncytial virus pneumonia as compared with using only 75–100 4 validated immunodeficiency indices.12 Finally, unlike qualitative assessments of severity, we found that RSI was Radiologic Severity Index (RSI) scores are calculated by multiplying the predominant pattern for each lung zone by the highly reliable when scored by experienced radiologists extent of volumetric radiological involvement for that zone. The 12–15 or pulmonary experts. Therefore, RSI is a promising sum of scores from all six zones gives the final RSI, ranging from marker of disease severity in patients with pneumonia that 0 to 72. can be reliably measured with a simple chest radiograph. Reductions in radiological severity by way of an effec- tive antimicrobial treatment may potentially correlate the first appearance of radiological infiltrates consistent with lower long- term morbidity or lower costs associ- with infection as identified by a senior thoracic radiolo- ated with pneumonia. We previously published that in gist (MG and JJE). All clinical and oncological data were patients with HM undergoing induction chemotherapy collected prospectively from a database of patients with for acute myeloid leukaemia (AML), acute lymphoblastic acute leukaemia. Bacterial and fungal organisms were leukaemia (ALL) or high-risk myelodysplastic syndrome identified using culture- based assays, while viral organ- (MDS), 33- day mortality after pneumonia was nearly isms were identified using direct fluorescent antibody by copyright. 17%.16 Pneumonia was the strongest predictor of death assays. Chemotherapy was defined as intensive when after induction chemotherapy and was associated with a cytarabine was used in a dose of 500 mg/m2 or greater 49% increase in hospital costs. We sought to determine daily as part of the regimen. Data on days in the hospital (1) whether RSI could predict the risk for mortality or ICU, hospital charges and costs, and daily absolute among the subset of patients with leukaemia who devel- neutrophil counts (ANC) were obtained from institu- oped pneumonia, (2) whether higher RSI was associated tional databases. Further details on the calculation of with a higher utilisation of hospital and intensive care charges and costs were previously published in an online unit (ICU) resources after pneumonia and (3) whether supplementary appendix.16 increasing RSI correlated with higher hospital costs. http://bmjopenrespres.bmj.com/ Radiological scoring METHODS Two senior thoracic radiologists (MG and JJE) calculated Study design RSI for each chest radiograph performed within 33 days We had previously conducted a retrospective cohort of induction chemotherapy.13 Table 1 illustrates how RSI study of pneumonia incidence in adult patients with is calculated. Briefly, chest radiographs were divided into AML, ALL or MDS between 1 January 2005 and 30 three zones in each lung (six in total): upper (above the September 2009.16 In the current study, we examined carina), middle (below the carina and above the inferior data from the prior study in the subset of patients with pulmonary vein) and lower (below the inferior pulmo- leukaemia who developed pneumonia within 33 days nary vein) in both lungs (figure 1). Pulmonary infiltrates on September 30, 2021 by guest. Protected of induction chemotherapy. We defined pneumonia as were scored on a 3- point scale based on the predominant the presence of fever (temperature >38.3°C), cough, pattern in that zone—normal attenuation: 1; ground dyspnoea or hypoxaemia, and thoracic imaging findings glass opacities (GGOs): 2; consolidation: 3. Consolida- consistent
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