A Nomogram Predicting Pneumonia After Cardiac Surgery: A Retrospective Modeling Study
A Nomogram Predicting Pneumonia After Cardiac Surgery: A Retrospective Modeling Study
A Nomogram Predicting Pneumonia After Cardiac Surgery: A Retrospective Modeling Study
Abstract
Background Postoperative pneumonia (POP) is the most prevalent of all nosocomial infections in patients who
underwent cardiac surgery. The aim of this study was to identify independent risk factors for pneumonia after cardiac
surgery, from which we constructed a nomogram for prediction.
Methods The clinical data of patients admitted to the Department of Cardiothoracic Surgery of Nanjing Drum Tower
Hospital from October 2020 to September 2021 who underwent cardiac surgery were retrospectively analyzed,
and the patients were divided into two groups according to whether they had POP: POP group (n=105) and non-
POP group (n=1083). Preoperative, intraoperative, and postoperative indicators were collected and analyzed. Logistic
regression was used to identify independent risk factors for POP in patients who underwent cardiac surgery. We
constructed a nomogram based on these independent risk factors. Model discrimination was assessed via area
under the receiver operating characteristic curve (AUC), and calibration was assessed via calibration plot.
Results A total of 105 events occurred in the 1188 cases. Age (>55 years) (OR: 1.83, P=0.0225), preoperative malnu‑
trition (OR: 3.71, P<0.0001), diabetes mellitus(OR: 2.33, P=0.0036), CPB time (Cardiopulmonary Bypass Time) > 135
min (OR: 2.80, P<0.0001), moderate to severe ARDS (Acute Respiratory Distress Syndrome )(OR: 1.79, P=0.0148), use
of ECMO or IABP or CRRT (ECMO: Extra Corporeal Membrane Oxygenation; IABP: Intra-Aortic Balloon Pump; CRRT:
Continuous Renal Replacement Therapy )(OR: 2.60, P=0.0057) and MV( Mechanical Ventilation )> 20 hours (OR: 3.11,
P<0.0001) were independent risk factors for POP. Based on those independent risk factors, we constructed a sim‑
ple nomogram with an AUC of 0.82. Calibration plots showed good agreement between predicted probabilities
and actual probabilities.
Conclusion We constructed a facile nomogram for predicting pneumonia after cardiac surgery with good discrimi‑
nation and calibration. The model has excellent clinical applicability and can be used to identify and adjust modifiable
risk factors to reduce the incidence of POP as well as patient mortality.
Keywords Cardiac surgery, Postoperative pneumonia, Nomogram, Outcomes
†
Kuo Wang and Hai-Tao Zhang contributed equally to this work.
*Correspondence:
Dong‑Jin Wang
dongjin_wang@126.com
Full list of author information is available at the end of the article
© The Author(s) 2024. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which
permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the
original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or
other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line
to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory
regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this
licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecom‑
mons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
Wang et al. Journal of Cardiothoracic Surgery (2024) 19:309 Page 2 of 10
Table 1 Univariate analysis of risk factors of pneumonia after cardiac surgery. Data are n (%) or median (IQR)
No pneumonia Pneumonia P value
(n=1083) (n=105)
renal insufficiency, age (years), left ventricular ejection multiple organs in the body by prolonging the duration of
fraction, hypertension, CPB time, RBC infusion and his- cardiopulmonary bypass. Cardiopulmonary bypass can
tory of cardiac surgery and achieved an AUC of 0.84 [16]. cause ischemia-reperfusion injury and systemic systemic
The incidence of pneumonia in that study was 6.6%. inflammation of cardiomyocytes, resulting in decreased
This study also suggested that cardiopulmonary bypass lung compliance. In addition, blood contact with the duct
lasting more than 2 h was an important cause of post- can also cause inflammation in various parts of the body.
operative POP, which may be related to the damage to Kilic et al. found that patients who received CPB for more
Wang et al. Journal of Cardiothoracic Surgery (2024) 19:309 Page 6 of 10
Table 2 Multivariate analysis of risk factors for pneumonia after cardiac surgery
Coefficients () Exp () 95% CI P value Standard error
than 100 minutes had a 1.7-fold increased risk of various as endotracheal intubation and duration of mechanical
complications and POP after cardiac surgery [10]. Allou ventilation (MV), but also due to impaired local (alveolar)
et al. also reported a positive correlation between CPB and systemic defenses, as well as other specific and non-
duration and POP after cardiac surgery, and in multivari- specific factors [19]. We also found that use of ECMO or
ate analyses, the risk of POP increased significantly with IABP or CRRT was independent risk factor for POP. Cas-
increasing CPB duration [17]. telli et al. report that patients who require IABP support
Acute respiratory distress syndrome (ARDS) recom- after cardiac surgery are more likely to develop postop-
bines a family of disorders with consequences of pneu- erative pneumonia because low cardiac output is harm-
monia, alveolar damage, and pulmonary edema [18, 19]. ful to the immune system [20]. Bizzarro et al. reported
Regardless of the initial lung injury, patients with ARDS a high prevalence of nosocomial infections of 21% in
are prone to lung infection [18]. While may be due to patients requiring ECMO support, with lung infections
bronchial contamination due to traditional factors such being the most common [21]. In addition, critically ill
Wang et al. Journal of Cardiothoracic Surgery (2024) 19:309 Page 7 of 10
patients treated with CRRT are at risk of lung infection with postoperative pneumonia may be associated with
[22]. Patients requiring IABP, ECMO, and/or CRRT are concomitant critical illness, prolonged mechanical sup-
usually in a state of low cardiac output leading to require- port, mechanical ventilation (MV) and ICU stay, and
ment of such support devices and the harmful effects on impairment of the immune system that promotes the
the immune system. These increased rates of infection release of inflammatory mediators [20–22]. Extended
Wang et al. Journal of Cardiothoracic Surgery (2024) 19:309 Page 8 of 10
Fig. 4 The curve of the incidence of pneumonia with prolonged hospitalization in patients with malnutrition or not
mechanical ventilation has been reported in many studies pneumonia, with Acinetobacter baumannii having the
to be strongly associated with an increased risk of POP, highest detection rate [26]. Anti-infective therapy should
which is associated with damage to respiratory defense be actively given to reduce the level of inflammatory fac-
mechanisms caused by endotracheal intubation [23]. tors in the blood, improve the patient’s immunity, and
We found that malnutrition was a risk factors affecting reduce the probability of MDRO infection in patients
POP, however, previous studies have rarely looked at the with postoperative pneumonia.
relationship between malnutrition and POP. Malnutri- The nomogram models can be used in the clinic for
tion is a complex organismal state and is recognized as joint diagnosis or prediction of disease risk or progno-
a prognostic risk factor for cardiovascular disease [24]. sis by multiple indicators. In addition, the nomogram
A study published by Chermesh et al. demonstrated a models can provide an accurate digital survival or risk
high risk of complex postoperative course, prolonged probability for each patient, which can assist clini-
ICU stay, and increased 3-year mortality in a popula- cians in decision-making and reflect the idea of indi-
tion of malnourished cardiac patients [25]. These factors vidualized medicine. Previous studies have shown that
contribute to postoperative pneumonia. Timely identi- preoperative respiratory physiotherapy and subglottic
fication of patients with malnutrition or at risk of mal- secretion drainage significantly reduce the incidence
nutrition and active and effective nutritional therapy is of POP, pulmonary atelectasis, and other complica-
important for improving the clinical prognosis of cardiac tions [27–29]. In addition, a growing number of studies
surgery patients. have found that aggressive and systematic preopera-
In addition, multidrug-resistant organisms (MDRO) tive oral care plays an important role in preventing and
have become the major bacterial group responsible for minimizing the development of POP after cardiovascu-
pneumonia infections in postoperative cardiac patients lar surgery, with tooth brushing being one of the most
due to bacterial mutations and overuse of antimicro- acceptable and common measures [30, 31]. However, it
bial drugs. A study showed that postoperative pneumo- may not be appropriate to apply these measures to all
nia caused by multidrug-resistant microorganisms was patients without selection, as some measures are time-
associated with adult patients with renal disease, longer consuming, expensive, and laborious. Therefore, the
intraoperative extracorporeal circulation time, and premise of nomogram application is that there must
postoperative nasogastric tubes, with Gram-negative be clear clinical problems and model construction, and
bacilli being the predominant pathogens in patients with its performance and limitations need to be understood
Wang et al. Journal of Cardiothoracic Surgery (2024) 19:309 Page 9 of 10
before being applied to clinical decision-making. Only Availability of data and materials
The datasets generated and/or analyzed during the current study are not pub‑
in this way can nomogram be better applied to the licly available [some patients did not allow us to publish their medical records]
clinic. but are available from the corresponding author upon reasonable request.
Declarations
Limitations and future directions
Ethics approval and consent to participate
Our study also has some limitations. First, the data for Ethical approval was obtained from Medical Ethics Committee of Affiliated
this study were derived from a single-center database, Nanjing Drum Tower Hospital, Nanjing University Medical College, in accord‑
with a single patient source, a small study sample size, ance with the principles of the Declaration of Helsinki on September 23, 2020
(2020-249-01). All included patients were required to provide written informed
and the specific cardiac surgical procedures. Second, we consent.
lack external validation of the model, which may limit its
generalizability. Third, we established standardized diag- Consent for publication
Not applicable.
nostic criteria for POP before the start of the study, but
there may be some degree of variability and subjectivity Competing interests
in clinical diagnosis. For example, although we strictly The authors declare no competing interests.
abide by the principles of sputum culture, but because in Author details
the retention process is susceptible to oropharyngeal col- 1
Department of Cardio‑Thoracic Surgery, Nanjing Drum Tower
onization bacteria contamination, its quality is difficult to Hospital,Affiliated Clinical College of Xuzhou Medical University, Nan‑
jing 210008, Jiangsu, China. 2 Department of Cardio‑Thoracic Surgery, Nanjing
ensure, false positive rate, may be poorly in line with the Drum Tower Hospital, Chinese Academy of Medical Science & Peking Union
diagnosis of clinical infections, and cannot be 100% guar- Medical College, Nanjing 210008, Jiangsu, China. 3 Department of Cardio‑Tho‑
antee of sputum culture positive. This can lead to over- racic Surgery, Nanjing Drum Tower Hospital, Affiliated Hospital of Medical
School, Nanjing University, Nanjing 210008, Jiangsu, China.
estimation or underestimation of the true incidence of
POP. A well-designed prospective study may be needed Received: 23 July 2023 Accepted: 25 May 2024
in the future to obtain more accurate estimates of the
incidence of POP. Future studies should focus on improv-
ing the generalization and practicability of our results.
References
1. Kinlin LM, Kirchner C, Zhang H, et al. Derivation and validation of a clinical
Conclusion prediction rule for nosocomial pneumonia after coronary artery bypass
graft surgery. Clin Infect Dis. 2010;50(4):493–501. https://doi.org/10.1086/
Three preoperative indicators (age, preoperative mal- 649925.
nutrition, diabetes mellitus), one intraoperative indica- 2. Horvath KA, Acker MA, Chang H, et al. Blood transfusion and infection
tor (CPB > 135 min) and three postoperative indicators after cardiac surgery. Ann Thorac Surg. 2013;95(6):2194–201. https://doi.
org/10.1016/j.athoracsur.2012.11.078.
(moderate to severe ARDS, use of ECMO or IABP or 3. Zardi EM, Chello M, Zardi DM, et al. Nosocomial extracardiac infections
CRRT, MV> 20 hours) were identified as independent after cardiac surgery [J]. Curr Infect Dis Rep. 2022;24(11):159–71. https://
risk factors by multivariate logistic regression analy- doi.org/10.1007/s11908-022-00787-0.
4. Strobel RJ, Liang Q, Zhang M, et al. A Preoperative Risk Model for Post‑
sis. A facile nomogram for predicting pneumonia after operative Pneumonia After Coronary Artery Bypass Grafting. Ann Thorac
cardiac surgery was constructed and well validated. A Surg. 2016;102(4):1213–9. https://doi.org/10.1016/j.athoracsur.2016.03.
nomogram performed well in terms of calibration and 074.
5. Gelijns AC, Moskowitz AJ, Acker MA, et al. Management practices and
discrimination, and may have good clinical usefulness. major infections after cardiac surgery. J Am Coll Cardiol. 2014;64(4):372–
Through individualized risk assessment and identifi- 81. https://doi.org/10.1016/j.jacc.2014.04.052.
cation of high-risk populations, nomograms can help 6. Chen LF, Arduino JM, Sheng S, et al. Epidemiology and outcome of
major postoperative infections following cardiac surgery: risk factors and
clinicians improve clinical decision-making and help impact of pathogen type. Am J Infect Control. 2012;40(10):963–8. https://
patients make informed decisions. doi.org/10.1016/j.ajic.2012.01.012.
7. Massart N, Mansour A, Ross JT, et al. Mortality due to hospital-
Acknowledgements acquired infection after cardiac surgery. J Thorac Cardiovasc Surg.
None. 2022;163(6):2131–40 e3. https://doi.org/10.1016/j.jtcvs.2020.08.094.
8. Wang DS, Huang XF, Wang HF, et al. Clinical risk score for postopera‑
Authors’ contributions tive pneumonia following heart valve surgery. Chin Med J (Engl).
KW and HTZ carried out the study, participated in the statistical analysis, and 2021;134(20):2447–56. https://doi.org/10.1097/CM9.0000000000
drafted the manuscript. FDF, JP, and TP participated in the statistical analysis. 001715.
DJW conceived of the study, participated in its design and coordination, and 9. Wang D, Huang X, Wang H, et al. Risk factors for postoperative
helped draft the manuscript. All authors have read and approved the final pneumonia after cardiac surgery: a prediction model. J Thorac Dis.
manuscript. 2021;13(4):2351–62. https://doi.org/10.21037/jtd-20-3586.
10. Kilic A, Ohkuma R, Grimm JC, et al. A novel score to estimate the
Funding risk of pneumonia after cardiac surgery. J Thorac Cardiovasc Surg.
None. 2016;151(5):1415–20. https://doi.org/10.1016/j.jtcvs.2015.12.049.
Wang et al. Journal of Cardiothoracic Surgery (2024) 19:309 Page 10 of 10
11. Bonell A, Azarrafiy R, Huong VTL, et al. A Systematic Review and Meta- 31. Nicolosi LN, Del Carmen Rubio M, Martinez CD, Gonzalez NN, Cruz ME.
analysis of Ventilator-associated Pneumonia in Adults in Asia: An Analysis Effect of oral hygiene and 012% chlorhexidine gluconate oral rinse in
of National Income Level on Incidence and Etiology. Clin Infect Dis. preventing ventilator-associated pneumonia after cardiovascular surgery.
2019;68(3):511–8. https://doi.org/10.1093/cid/ciy543. Resp Care. 2014;59:504–9. https://doi.org/10.4187/respcare.02666.
12. Liu J, Liu J, Wang J, et al. Prevalence and impact of malnutrition on
readmission among hospitalized patients with heart failure in China. ESC
Heart Fail. 2022;9(6):4271–9. https://doi.org/10.1002/ehf2.14152. Publisher’s Note
13. Zhang HT, Han XK, Wang CS, et al. Diagnosis of infection after car‑ Springer Nature remains neutral with regard to jurisdictional claims in pub‑
diac surgery (DICS): a study protocol for developing and validating lished maps and institutional affiliations.
a prediction model in prospective observational study. BMJ Open.
2021;11(9):e048310. https://doi.org/10.1136/bmjopen-2020-048310.
14. American Thoracic Society. Infectious Diseases Society of A. Guidelines
for the management of adults with hospital-acquired, ventilator-associ‑
ated, and healthcare-associated pneumonia. Am J Respir Crit Care Med.
2005;171(4):388–416. https://doi.org/10.1164/rccm.200405-644ST.
15. Kalil AC, Metersky ML, Klompas M, et al. Management of Adults With
Hospital-acquired and Ventilator-associated Pneumonia: 2016 Clinical
Practice Guidelines by the Infectious Diseases Society of America and the
American Thoracic Society. Clin Infect Dis. 2016;63(5):e61–111. https://
doi.org/10.1093/cid/ciw353.
16. Wang D, Chen X, Wu J, et al. Development and Validation of Nomogram
Models for Postoperative Pneumonia in Adult Patients Undergoing Elec‑
tive Cardiac Surgery. Front Cardiovasc Med. 2021;8:750828. https://doi.
org/10.3389/fcvm.2021.750828[publishedOnlineFirst:20211011].
17. Allou N, Bronchard R, Guglielminotti J, et al. Risk factors for postoperative
pneumonia after cardiac surgery and development of a preoperative risk
score* [J]. Crit Care Med. 2014;42(5):1150–6.
18. Luyt CE, et al. Pulmonary infections complicating ARDS. Intensive Care
Med. 2020;46(12):2168–83. https://doi.org/10.1007/s00134-020-06292-z.
19. Thompson BT, Chambers RC, Liu KD. Acute respiratory distress syndrome.
N Engl J Med. 2017;377(6):562–72. https://doi.org/10.1056/NEJMra1608
077.
20. Castelli P, et al. Intra-aortic balloon counterpulsation: outcome in cardiac
surgical patients. J Cardiothorac Vasc Anesth. 2001;15(6):700–3. https://
doi.org/10.1053/jcan.2001.28312.
21. Bizzarro MJ, et al. Infections acquired during extracorporeal membrane
oxygenation in neonates, children, and adults. Pediatr Crit Care Med.
2011;12(3):277–81. https://doi.org/10.1097/PCC.0b013e3181e28894.
22. Zuo M, et al. Characteristics and factors associated with nosocomial
pneumonia among patients undergoing continuous renal replacement
therapy (CRRT): A case-control study. Int J Infect Dis. 2018;68:115–21.
https://doi.org/10.1016/j.ijid.2018.01.008.
23. Papazian L, Klompas M, Luyt CE. Ventilator-associated pneumonia in
adults: a narrative review. Intensive Care Med. 2020;46(5):888–906.
https://doi.org/10.1007/s00134-020-05980-0.
24. Hill A, et al. Current Evidence about Nutrition Support in Cardiac Surgery
Patients-What Do We Know? Nutrients. 2018;10(5):597. https://doi.org/10.
3390/nu10050597.
25. Chermesh I, Hajos J, Mashiach T, Bozhko M, Shani L, Nir R-R, et al.
Malnutrition in cardiac surgery: food for thought. Eur J Prev Cardiol.
2014;21(4):475–83. https://doi.org/10.1177/2047487312452969.
26. Wang M, Xu X, Wu S, et al. Risk factors for ventilator-associated pneumo‑
nia due to multi-drug resistant organisms after cardiac surgery in adults
[J]. BMC Cardiovasc Disord. 2022;22(1):465.
27. Katsura M, Kuriyama A, Takeshima T, Fukuhara S, Furukawa TA. Preopera‑
tive inspiratory muscle training for postoperative pulmonary compli‑
cations in adults undergoing cardiac and major abdominal surgery.
Cochrane Database Syst Rev. 2015;10:CD01035. https://doi.org/10.1002/
14651858.CD010356.pub2.
28. Hudson JKC, McDonald BJ, MacDonald JC, Ruel MA, Hudson CCC. Impact
of subglottic suctioning on the incidence of pneumonia after cardiac
surgery: a retrospective observational study. J Cardiothor Vasc An.
2015;29:59–63. https://doi.org/10.1053/j.jvca.2014.04.026.
29. Hulzebos EHJ, Smit Y, Helders PPJM, van Meeteren NLU. Preoperative
physical therapy for elective cardiac surgery patients. Cochrane Db Syst
Rev. 2012;11:D10118. https://doi.org/10.1002/14651858.CD010118.pub2.
30. Akutsu Y, Matsubara H, Shuto K, Shiratori T, Uesato M, Miyazawa Y, et al.
Pre-operative dental brushing can reduce the risk of postoperative pneu‑
monia in esophageal cancer patients. Surgery. 2010;147:497–502. https://
doi.org/10.1016/j.surg.2009.10.048.