Abstract
Severe postoperative pneumonia can increase the risk of poor outcomes in patients with aneurysmal subarachnoid hemorrhage (aSAH). We aimed to explore the associations of preoperative or postoperative inflammatory markers calculated from blood cell counts with severe pneumonia. This retrospective study was conducted at the First Affiliated Hospital of Yangtze University from January 2019 to June 2023. The associations of neutrophil–lymphocyte ratio (NLR), monocyte–lymphocyte ratio (MLR), platelet–lymphocyte ratio (PLR), systemic immune inflammation index (SII), and systemic inflammation response index (SIRI) with severe pneumonia were analyzed. There were 159 patients with pneumonia and 21 patients without pneumonia. There were 41 patients with severe pneumonia and 118 patients with non-severe pneumonia. The multivariate logistic regression analysis showed that NLR on the first postoperative (OR = 2.574, 95%CI: 1.035–6.403, p = 0.042) and third postoperative days (OR = 4.296, 95%CI: 1.699–10.860, p = 0.002) were associated with severe pneumonia in aSAH patients. Among patients ≥ 60 years, SIRI on the preoperative day (OR = 7.430, 95%CI: 1.443–38.251, p = 0.016) and NLR on the third postoperative day (OR = 4.748, 95%CI: 1.286–17.801, p = 0.020) were associated with severe pneumonia. Among patients < 60 years, NLR on the first postoperative day (OR = 24.149, 95%CI: 3.476–167.747, p = 0.001) was associated with severe pneumonia. The NLR on the first and third postoperative days were possibly associated with severe pneumonia in aneurysmal subarachnoid hemorrhage patients undergoing clipping or embolization surgeries. Dynamic detection of NLR during early perioperative period may help clinicians to predict the development of severe pneumonia.
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10143-024-02295-2/MediaObjects/10143_2024_2295_Fig1_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10143-024-02295-2/MediaObjects/10143_2024_2295_Fig2_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10143-024-02295-2/MediaObjects/10143_2024_2295_Fig3_HTML.png)
![](http://media.springernature.com/m312/springer-static/image/art%3A10.1007%2Fs10143-024-02295-2/MediaObjects/10143_2024_2295_Fig4_HTML.png)
Similar content being viewed by others
Data availability
The data that support the findings of this study are available from the first and corresponding author upon reasonable request.
References
Macdonald RL, Schweizer TA (2017) Spontaneous subarachnoid haemorrhage. Lancet 389:655–666. https://doi.org/10.1016/S0140-6736(16)30668-7
Chen Y, Wright N, Guo Y, Turnbull I, Kartsonaki C, Yang L, Bian Z, Pei P, Pan D, Zhang Y, Qin H, Wang Y, Lv J, Liu M, Hao Z, Wang Y, Yu C, Peto R, Collins R, Li L, Clarke R, Chen Z, China Kadoorie Biobank Collaborative Group (2020) Mortality and recurrent vascular events after first incident stroke: a 9-year community-based study of 0.5 million Chinese adults. Lancet Glob Health 8:e580–e590. https://doi.org/10.1016/S2214-109X(20)30069-3
Samuels OB, Sadan O, Feng C, Martin K, Medani K, Mei Y, Barrow DL (2021) Aneurysmal subarachnoid hemorrhage: trends, outcomes, and predictions from a 15-year perspective of a single neurocritical care unit. Neurosurgery 88:574–583. https://doi.org/10.1093/neuros/nyaa465
Cavallo C, Safavi-Abbasi S, Kalani MYS, Gandhi S, Sun H, Oppenlander ME, Zabramski JM, Nakaji P, Lawton MT, Spetzler RF (2018) Pulmonary complications after spontaneous aneurysmal subarachnoid hemorrhage: experience from Barrow Neurological Institute. World Neurosurg 119:e366–e373. https://doi.org/10.1016/j.wneu.2018.07.166
Savardekar A, Gyurmey T, Agarwal R, Podder S, Mohindra S, Gupta SK, Chhabra R (2013) Incidence, risk factors, and outcome of postoperative pneumonia after microsurgical clipping of ruptured intracranial aneurysms. Surg Neurol Int 4:24. https://doi.org/10.4103/2152-7806.107894
Cui JB, Chen QQ, Liu TT, Li SJ (2018) Risk factors for early-onset ventilator-associated pneumonia in aneurysmal subarachnoid hemorrhage patients. Braz J Med Biol Res 51:e6830. https://doi.org/10.1590/1414-431x20176830
Wang R, Zhang J, He M, Chen H, Xu J (2023) Procalcitonin as a biomarker of nosocomial pneumonia in aneurysmal subarachnoid hemorrhage patients treated in neuro-ICU. Clin Neurol Neurosurg 231:107870. https://doi.org/10.1016/j.clineuro.2023.107870
Zhang X, Zhang S, Wang C, Liu R, Li A (2022) High neutrophil-to-albumin ratio predicts postoperative pneumonia in aneurysmal subarachnoid hemorrhage. Front Neurol 13:840858. https://doi.org/10.3389/fneur.2022.840
Xu M, Zhang L, Wang J, Cheng L, Chen C, Li S, Dai H, Zhao P, Hang C (2023) Pre-operative prognostic nutrition index and post-operative pneumonia in aneurysmal subarachnoid hemorrhage patients. Front Neurol 14:1045929. https://doi.org/10.3389/fneur.2023.1045929
Hu SQ, Hu JN, Chen RD, Yu JS (2022) A predictive model using risk factor categories for hospital-acquired pneumonia in patients with aneurysmal subarachnoid hemorrhage. Front Neurol 13:1034313. https://doi.org/10.3389/fneur.2022.1034313
Shi Y, Huang Y, Zhang TT, Cao B, Wang H, Zhuo C, Ye F, Su X, Fan H, Xu JF, Zhang J, Lai GX, She DY, Zhang XY, He B, He LX, Liu YN, Qu JM (2019) Chinese guidelines for the diagnosis and treatment of hospital-acquired pneumonia and ventilator-associated pneumonia in adults (2018 Edition). Thorac Dis 11:2581–2616. https://doi.org/10.21037/jtd.2019.06.09
Rotstein C, Evans G, Born A, Grossman R, Light RB, Magder S, McTaggart B, Weiss K, Zhanel GG (2008) Clinical practice guidelines for hospital-acquired pneumonia and ventilator-associated pneumonia in adults. Can J Infect Dis Med Microbiol 19:19–53. https://doi.org/10.1155/2008/593289
Yuan K, Li R, Zhao Y, Wang K, Lin F, Lu J, Chen Y, Ma L, Han H, Yan D, Li R, Yang J, He S, Li Z, Zhang H, Ye X, Wang H, Li H, Zhang L, Shi G, Zhou J, Zhao Y, Zhang Y, Li Y, Wang S, Chen X, Zhao Y, Hao Q (2022) Pre-operative predictors for post-operative pneumonia in aneurysmal subarachnoid hemorrhage after surgical clipping and endovascular coiling: a single-center retrospective study. Front Neurol 13:893516. https://doi.org/10.3389/fneur.2022.893516
Wang R, Zhang J, He M, Xu J (2022) A novel risk score for predicting hospital acquired pneumonia in aneurysmal subarachnoid hemorrhage patients. Int Immunopharmacol 108:108845. https://doi.org/10.1016/j.intimp.2022.108845
Zhao H, Shang F, Qi M, Xu Y, Wang N, Qu X (2022) Related factors and a threshold of the maximum neuron-specific enolase value affecting the prognosis of patients with aneurysmal subarachnoid hemorrhage. Appl Bionics Biomech 2022:7596426. https://doi.org/10.1155/2022/7596426
Li M, Xie L (2021) Correlation between NLR, PLR, and LMR and disease activity, efficacy assessment in rheumatoid arthritis. Evid Based Complement Alternat Med 4433141. https://doi.org/10.1155/2021/4433141
Enersen CC, Egelund GB, Petersen PT, Andersen S, Ravn P, Rohde G, Lindegaard B, Jensen AV (2023) The ratio of neutrophil-to-lymphocyte and platelet-to-lymphocyte and association with mortality in community-acquired pneumonia: a derivation-validation cohort study. Infection 51:1339–1347. https://doi.org/10.1007/s15010-023-01992-2
Liao D, Li J, Lv J, Sun T, Deng S (2020) Evaluation of the diagnostic value of peripheral blood parameters for neonatal pneumonia. Clin Lab 66. https://doi.org/10.7754/Clin.Lab.2020.200407
Zawiah M, Hayat Khan A, Abu Farha R, Usman A, Bitar AN (2023) Neutrophil-lymphocyte ratio, monocyte-lymphocyte ratio, and platelet-lymphocyte ratio in stroke-associated pneumonia: a systematic review and meta-analysis. Curr Med Res Opin 39:475–482. https://doi.org/10.1080/03007995.2023.2174327
Li C, Tian W, Zhao F, Li M, Ye Q, Wei Y, Li T, Xie K (2018) Systemic immune-inflammation index, SII, for prognosis of elderly patients with newly diagnosed tumors. Oncotarget 9:35293–35299. https://doi.org/10.18632/oncotarget.24293
Yang C, Li ZQ, Wang J (2023) Association between systemic immune-inflammation index (SII) and survival outcome in patients with primary glioblastoma. Medicine (Baltimore) 102:e33050. https://doi.org/10.1097/MD.0000000000033050
Palacka P, Slopovsky J, Obertova J, Chovanec M, Rejlekova K, Sycova-Mila Z, Kollarik B, Mardiak J, Mego M (2021) Survival prediction by baseline systemic immune-inflammation index (SII) and its changes during first-line platinum-based treatment in a caucasian population of patients with metastatic urothelial carcinoma (MUC). Anticancer Res 41:5749–5759. https://doi.org/10.21873/anticanres.15391
Yorulmaz A, Hayran Y, Akpinar U, Yalcin B (2020) Systemic immune-inflammation index (SII) predicts increased severity in psoriasis and psoriatic arthritis. Curr Health Sci J 46:352–357. https://doi.org/10.12865/CHSJ.46.04.05
Trifan G, Testai FD (2020) Systemic immune-inflammation (SII) index predicts poor outcome after spontaneous supratentorial intracerebral hemorrhage. J Stroke Cerebrovasc Dis 29:105057. https://doi.org/10.1016/j.jstrokecerebrovasdis.2020.105057
Liu X, Guan G, Cui X, Liu Y, Liu Y, Luo F (2021) Systemic immune-inflammation index (SII) can be an early indicator for predicting the severity of acute pancreatitis: a retrospective study. Int J Gen Med 14:9483–9489. https://doi.org/10.2147/IJGM.S343110
Chen Y, Lian BQ, Peng L, Ding CY, Lin YX, Yu LH, Wang DL, Kang DZ (2020) Neutrophil to lymphocyte ratio is a prognosis factor for post-operative pneumonia in aneurysmal subarachnoid hemorrhage patients. Chin Med J (Engl) 134:682–689. https://doi.org/10.1097/CM9.0000000000001304
Le Roux PD, Elliott JP, Newell DW, Grady MS, Winn HR (1996) Predicting outcome in poor-grade patients with subarachnoid hemorrhage: a retrospective review of 159 aggressively managed cases. J Neurosurg 85:39–49. https://doi.org/10.3171/jns.1996.85.1.0039
Lanzino G, Kassell NF, Germanson TP, Kongable GL, Truskowski LL, Torner JC, Jane JA (1996) Age and outcome after aneurysmal subarachnoid hemorrhage: why do older patients fare worse? J Neurosurg 85:410–418. https://doi.org/10.3171/jns.1996.85.3.0410
Jiao J, Yang XY, Li Z, Zhao YW, Cao J, Li FF, Liu Y, Liu G, Song BY, Jin JF, Liu YL, Wen XX, Cheng SZ, Yang LL, Wu XJ, Sun J (2019) Incidence and related factors for hospital-acquired pneumonia among older bedridden patients in China: a hospital-based multicenter registry data based study. Front Public Health 7:221. https://doi.org/10.3389/fpubh.2019.00221
Shi T, Denouel A, Tietjen AK, Lee JW, Falsey AR, Demont C, Nyawanda BO, Cai B, Fuentes R, Stoszek SK, Openshaw P, Campbell H, Nair H, RESCEU Investigators (2020) Global and regional burden of hospital admissions for pneumonia in older adults: a systematic review and meta-analysis. J Infect Dis 222:S570–S576. https://doi.org/10.1093/infdis/jiz053
Okazaki T, Ebihara S, Mori T, Izumi S, Ebihara T (2020) Association between sarcopenia and pneumonia in older people. Geriatr Gerontol Int 20:7–13. https://doi.org/10.1111/ggi.13839
Fukushima T, Watanabe N, Okita Y, Yokota S, Matsuoka A, Kojima K, Kurita D, Ishiyama K, Oguma J, Kawai A, Daiko H (2023) The evaluation of the association between preoperative sarcopenia and postoperative pneumonia and factors for preoperative sarcopenia in patients undergoing thoracoscopic-laparoscopic esophagectomy for esophageal cancer. Surg Today 53:782–790. https://doi.org/10.1007/s00595-022-02620-6
Kim MY, Kim SY, Shin HJ, Kweon KH, Park J, Kim NY (2023) Effect of sarcopenia on pneumonia after endoscopic submucosal resection in patients aged ≥65 years: a retrospective study. Cancers (Basel) 15:4753. https://doi.org/10.3390/cancers15194753
Acknowledgements
We thank Dr. Jie Min, Dr. Yong Yang, and Ms. Fangju Mao (The First Affiliated Hospital of Yangtze University, Jingzhou, China) for their professional technology in the clinical field.
Author information
Authors and Affiliations
Contributions
X.W. contributed to the conceptualization. X.W. and J.Z. contributed to the methodology. X. W., Y. Z. and J.Z. contributed to the data curation. X.W. contributed to the formal analysis. X. W. and Y. Z. wrote the main manuscript. L.D. contributed to the writing—review and editing.
Corresponding author
Ethics declarations
Ethics approval
This study was approved by the Ethics Committee of the First Affiliated Hospital of the Yangtze University. The ethics committee waived the requirement for informed consent due to the retrospective nature of the study.
Competing interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Wang, X., Zhao, Y., Zhao, J. et al. Neutrophil–lymphocyte ratio on first and third postoperative days: associated with severe pneumonia in aneurysmal subarachnoid hemorrhage patients undergoing surgeries. Neurosurg Rev 47, 70 (2024). https://doi.org/10.1007/s10143-024-02295-2
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s10143-024-02295-2