Monocyte-to-Lymphocyte Ratio Was an Independent Factor of the Severity of Spinal Tuberculosis

Chen, Liyi; Liu, Chong; Liang, Tuo; Ye, Zhen; Huang, Shengsheng; Chen, Jiarui; Sun, Xuhua; Yi, Ming; Jiang, Jie; Chen, Tianyou; Li, Hao; Chen, Wuhua; Guo, Hao; Yao, Yuanlin; Liao, Shian; Yu, Chaojie; Wu, Shaofeng; Fan, Binguang; Gan, Zhaoping; Zhan, Xinli

doi:https://doi.org/10.1155/2022/7340330

Oxidative Medicine and Cellular Longevity

On this page

Abstract Introduction Materials and Methods Results Discussion Conclusion Data Availability Ethical Approval Consent Disclosure Conflicts of Interest Authors’ Contributions Acknowledgments References Copyright Related Articles

Research Article | Open Access

Volume 2022 | Article ID 7340330 | https://doi.org/10.1155/2022/7340330

Monocyte-to-Lymphocyte Ratio Was an Independent Factor of the Severity of Spinal Tuberculosis

Liyi Chen,¹Chong Liu,¹Tuo Liang,¹Zhen Ye,¹Shengsheng Huang,¹Jiarui Chen,¹Xuhua Sun,¹Ming Yi,¹Jie Jiang,¹Tianyou Chen,¹Hao Li,¹and Wuhua Chen¹ et al.

Academic Editor: Ilaria Peluso

Received26 Mar 2022

Accepted26 Apr 2022

Published20 May 2022

Abstract

Purpose. The purpose was to explore the relationship between monocyte-to-lymphocyte ratio (MLR) and the severity of spinal tuberculosis. Methods. A total of 1,000 clinical cases were collected, including 496 cases of spinal tuberculosis and 504 cases of nonspinal tuberculosis. Laboratory blood results were collected, including C-reactive protein (CRP), erythrocyte sedimentation rate (ESR), white blood cells (WBC), hemoglobin (HGB), platelets (PLT), neutrophil count, percentage of neutrophils, lymphocyte count, percentage of lymphocytes, monocyte count, percentage of monocytes, MLR, platelets -to- monocyte ratio (PMR), platelets -to- lymphocyte ratio (PLR), neutrophil -to- lymphocyte ratio (NLR), and platelets -to- neutrophil ratio (PNR). The statistical parameters analyzed by the Least Absolute Shrinkage and Selection Operator (LASSO) and receiver-operating characteristic (ROC) curves were used to construct the nomogram. The nomogram was assessed by C-index, calibration curve, ROC curve, and decision curve analysis (DCA) curve. Results. The C-index of the nomogram in the training set and external validation set was 0.801 and 0.861, respectively. Similarly, AUC was 0.801 in the former and 0.861 in the latter. The net benefit of the former nomogram ranged from 0.1 to 0.95 and 0.02 to 0.99 in the latter nomogram. Furthermore, there was a correlation between MLR and the severity of spinal tuberculosis. Conclusion. MLR was an independent factor in the diagnosis of spinal tuberculosis and was associated with the severity of spinal tuberculosis. Additionally, MLR may be a predictor of active spinal tuberculosis.

1. Introduction

Tuberculosis poses a threat to human health all over the world and a huge economic burden on the people [1]. The incidence of spinal tuberculosis remains high, accounting for about 1%-3% of all tuberculosis [2]. Spinal tuberculosis is the most common type of extrapulmonary tuberculosis, accounting for 50% of skeletal tuberculosis [3]. Various examination methods have different limitations for the diagnosis of tuberculosis. The positive rates of acid-fast staining of sputum smears are usually used to diagnose tuberculosis. However, tuberculosis is easily missed due to the low sensitivity of the positive rate of acid-fast bacilli [4]. Although the culture of Mycobacterium tuberculosis is the gold standard for the diagnosis of tuberculosis, it cannot be used as an early diagnosis due to the low detection rate and long bacterial culture time [5]. In addition, the positive rate of spinal tuberculosis bacterial culture is only 44.39% reported in the literature [6]. Despite the rapid development of genetic testing, the positive rate of Mycobacterium tuberculosis DNA is only 66.67% [4]. Spinal tuberculosis is often diagnosed by pathological examination, but the sensitivity of histopathology of spinal tuberculosis ranges from 40.8% to 56.5% [7]. MLR has been reported in the literature as a predictor of tuberculosis diagnosis [8]. However, whether MLR can be used as a predictor in the diagnosis of spinal tuberculosis has not been reported.

MLR is closely associated with the expression of inflammatory factors in many diseases. Mehmet et al.’s study showed that MLR was not only positively correlated with microalbuminuria but also was determined as an independent factor of diabetic kidney injury by logistic regression analysis [9]. Aktas et al. found that MLR was involved in the inflammatory process of hepatic steatosis, and MLR was significantly higher in the hepatic steatosis group than in the control group [10]. MLR was significantly higher in irritable bowel syndrome, which may be a new inflammatory marker for irritable bowel syndrome diagnosed by laboratory examination [11]. In addition, MLR as an inflammatory marker was significantly different between colorectal cancer with and without metastasis, which may predict colorectal cancer metastasis [12]. Interestingly, COVID-19 is widespread around the world, and MLR as a marker of hematologic inflammation is a predictor involving diagnosis and clinical prognosis of the COVID-19 infection [13]. We hypothesized that MLR is also responsible for inflammatory factors in spinal tuberculosis.

ESR and CRP are usually highly expressed in inflammatory diseases and are used to assess the degree of infection of the disease [14]. Increasing ESR during treatment indicates severe spinal tuberculosis and poor prognosis [15]. CRP is as high as 41.9 mg/L before surgery for severe spinal tuberculosis and ESR is as high as 51.4 mm/h [16]. MLR has been confirmed as an inflammation marker in tuberculosis, and high levels of MLR are associated with severe tuberculosis [17]. However, the findings of Van et al. did not support the hypothesis that MLR was associated with tuberculin skin test positivity [18]. There are still contradictions in the association between MLR and tuberculosis. Furthermore, the association between MLR and the severity of spinal tuberculosis has not been reported.

In this paper, a total of 1,000 clinical data are collected, including training set data and external validation set data. We mainly discussed the diagnosis of MLR in spinal tuberculosis and the relationship between MLR and the severity of spinal tuberculosis. Furthermore, we also explored MLR as a predictor of active spinal tuberculosis.

2. Materials and Methods

2.1. Patients

All written consents were obtained from patients with spinal tuberculosis. The inclusion criteria for spinal tuberculosis cases were as follows: (1) diagnosed with spinal tuberculosis by postoperative pathological examination. (2) No disease that affected blood tests. (3) Complete information. The exclusion criteria for spinal tuberculosis cases were as follows: (1) denied spinal tuberculosis by postoperative pathological examination. (2) Had diseases that affected blood tests. (3) Existence of immune-related diseases. Active spinal tuberculosis was defined based on moderate to severe dysfunction. This article was approved by the Ethics Committee of the First Affiliated Hospital of Guangxi Medical University.

2.2. Data Collection

Clinical data were collected from our hospital’s electronic medical record database from June 2012 to June 2021. 1000 clinical data were collected. These data were divided into a training set (700 cases) and an external validation set (300 cases) according to different periods. General information was collected, including gender, age, and body mass index (BMI). Laboratory blood results were collected, including CRP, ESR, WBC, HGB, PLT, neutrophil count, percentage of neutrophils, lymphocyte count, percentage of lymphocytes, monocyte count, percentage of monocytes, MLR, PMR, PLR, NLR, and PNR. The clinical score was evaluated by two senior specialist physicians, including ODI, VAS, and ASIA score.

2.3. Statistical Analysis

R software (version 4.1.1) and GraphPad Prism software (version 8.0) were used in this article. -test was used to compare the two sets of data. The one-way ANOVA test was used to compare multiple sets of data. LASSO regression selected parameters with nonzero coefficients to obtain optimal lambda. Then, the parameters with AUC>0.6 were selected by the ROC curve. The predictive ability and accuracy of the nomogram were assessed by the C-index, calibration curve, ROC curve, and DCA curve. The external verification method further evaluated the predictive ability of the nomogram. Correlation analysis of data with normal distribution was used Pearson test, while Spearman test was used for data with non-normal distribution. All continuous variables were represented by mean ± standard deviation (SD). less than 0.05 was defined as a statistical difference.

3. Results

3.1. The Diagnostic of MLR in Spinal Tuberculosis

700 clinical cases were collected to construct the training set, including 347 cases of spinal tuberculosis (Figures 1–3) and 353 cases of nonspinal tuberculosis (Figures 4–6). There were statistically different parameters between the two groups, including gender, age, BMI, ESR, WBC, HGB, PLT, neutrophil count, lymphocyte count, percentage of lymphocytes, percentage of monocytes, MLR, PLR, NLR, and PNR (Table 1). These parameters were included in the LASSO regression analysis (Figures 7(a) and 7(b)). The optimal lambda and nonzero coefficient parameters were selected by LASSO regression and were included in the ROC analysis (Figure 7(c)). In the training set, the parameters with AUC greater than 0.6 in the ROC curve were age (AUC =0.735), PLR (AUC =0.642), MLR (AUC =0.663), and percentage of monocytes (AUC =0.652). Similarly, the AUC of these parameters in the external validation set was 0.801, 0.706, 0.737, and 0.687, respectively (Figure 7(d)). These parameters were used to construct a nomogram. The predictive ability of the nomogram ranged from 0.01 to 0.99 in the training set (Figure 8). Similarly, the nomograms in the external validation set had the same predictive ability (Figure 9). The C-index in the training set was 0.801 and that was 0.861 in the external validation set. The observations in the calibration curve were highly similar to the ideal values, whether in the training set (Figure 10(a)) or the external validation set (Figure 10(b)). AUC was 0.801 in the training set (Figure 10(c)) and that was 0.861 in the external validation set (Figure 10(d)). The net benefit of this nomogram ranged from 0.1 to 0.95 in the training set (Figure 10(e)). Similarly, the benefit rate was also very high in the external verification set, ranging from 0.02 to 0.99 (Figure 10(f)).

(a)

(b)

(a)

(b)

(c)

(a)

(b)

(c)

(d)

(e)

(a)

(b)

(a)

(b)

(c)

(a)

(b)

(c)

(d)

(e)

(a)

(b)

(c)

(d)

(a)

(b)

(c)

(d)

(e)

(f)

3.2. MLR Was Closely Related to the Severity of Spinal Tuberculosis

496 cases of spinal tuberculosis were included. Cases were divided into high ODI group (score≥20) and low ODI group (score<20) according to the ODI score. There were statistically different parameters between the two groups, including age, ESR, HGB, percentage of neutrophils, lymphocyte count, percentage of lymphocytes, MLR, PLR, and NLR (Table 2). The MLR of the high ODI group was significantly higher than that of the low ODI group (Figure 11(a)). Cases were divided into low VAS group (score≤7) and high VAS group (score>7) according to the VAS score. There were statistically different parameters between the two groups, including age, PLR, and MLR. The MLR of the high VAS group was significantly higher than that of the low VAS group (Figure 11(b)). Cases were divided into five grades according to the ASIA classification. Parameters that were statistically different in ASIA included age, ESR, percentage of monocytes, and MLR (Figure 11(c)). MLR was related to ESR (Figure 11(d)) and CRP (Figure 11(e)). ESR was higher in the high ODI score group than in the low ODI score group (Figure 12(a)). Similarly, the level of ESR was statistically different in ASIA (Figure 12(c)). However, the level of ESR was not statistically different between the high VAS score group and the low VAS score group (Figure 12(b)). In the statistical analysis of ODI score, VAS score, and ASIA, there was no statistical difference in CRP level (Figure 12).

(a)

(b)

(c)

(d)

(e)

(a)

(b)

(c)

(d)

(e)

(f)

3.3. MLR as a Predictor of Active Spinal Tuberculosis

Active spinal tuberculosis was defined based on moderate to severe dysfunction. Parameters with statistical differences were included in the ROC curve analysis, including age, ESR, HGB, percentage of neutrophils, lymphocyte count, percentage of lymphocytes, MLR, PLR, and NLR. Parameters with AUC>0.6 were selected to construct the nomogram, including age, percentage of lymphocytes, MLR, and PLR (Figure 13(a)). The ability of the nomogram to predict active spinal tuberculosis ranged from 0.1 to 0.9 (Figure 13(b)). The observed value and the ideal value were consistent in the calibration curve (Figure 13(c)). AUC was 0.69 by ROC curve analysis (Figure 13(d)).

(a)

(b)

(c)

(d)

(e)

(f)

4. Discussion

The incidence of spinal tuberculosis in newborns has increased from 14% to 45.2%, posing a huge threat to humans [1, 19, 20]. Despite the rapid advancement of modern experimental technology, the positive detection rate of spinal tuberculosis is still not high. Diagnosis of spine tuberculosis usually uses the following methods: acid-fast tuberculosis smear, acid-fast tuberculosis DNA test, culture of mycobacterium tuberculosis, immunohistochemistry. However, the diagnostic value of MLR in spinal tuberculosis has not been reported.

MLR is significantly expressed in many diseases. MLR was used as a predictor of prostate cancer diagnosis and the AUC was 0.852 [21]. MLR>0.35 was associated with the overall survival rate of glioma patients [22]. High expression of MLR was detected in inflammatory diseases. High MLR expression was associated with mortality in acute respiratory distress syndrome [23]. MLR was significantly higher in patients with advanced knee synovitis than in early patients [23]. Our study found that MLR in the training set was statistically different between spinal tuberculosis and nonspinal tuberculosis. MLR was used as a predictor of spinal tuberculosis diagnosis, and its AUC was 0.663 by ROC curve analysis. The results of Sukson et al. showed that MLR was used as a predictor in the diagnosis of tuberculous pleuritis and the AUC was 0.91 [24]. Monocytes promoted the expression level of immune checkpoints and lead to latent tuberculosis infection [25]. MLR may affect the immune response of tuberculosis patients during the process of mycobacterium tuberculosis replication and progression to tuberculosis [26–28].

The severity of spinal tuberculosis had been reported to be associated with vitamin D receptor (VDR), osteopontin (OPN), and bone morphogenetic protein-4 (BMP-4) gene polymorphism [29]. Osteopontin mediated inflammation by regulating immune cells [30]. Our results found that MLR was associated with the severity of spinal tuberculosis. Osteopontin might have been involved in regulating MLR to promote the progression of spinal tuberculosis. A previous study also reported that the concentration of OPN in tuberculosis plasma was higher than that of healthy patients [31]. VDR was associated with the clinical severity of spinal tuberculosis [29]. It may be that VDR regulated the expression of multiple genes in monocytes [32]. MLR was closely related to the severity of the disease by promoting the activation of macrophages [33]. The results of our study were consistent with the finding that MLR was a marker of the severity of spinal tuberculosis.

ESR and CRP were used as inflammatory markers, usually used to assess the degree of inflammation of the disease [34]. In multidrug-resistant tuberculosis, ESR and CRP were as high as 62.03 mm/h and 83.24 mg/L, respectively, which were significantly higher than the ESR (37.20 mm/h) and CRP (50.02 mg/L) levels in drug-susceptible tuberculosis [35]. The expression of CRP was significantly increased in patients with advanced tuberculosis, but it lacked value in the diagnosis of early tuberculosis [36–38]. However, ESR and CRP also increased significantly in community-acquired pneumonia [39]. This made the diagnosis of spinal tuberculosis combined with community-acquired pneumonia more difficult. Our research showed that ESR and CRP had little contribution to the diagnosis of spinal tuberculosis and the severity of the disease. Our findings provided a distinction between the diagnosis of spinal tuberculosis and community-acquired pneumonia.

MLR had been reported as a marker for active diseases, such as systemic lupus erythematosus [40]. MRL had also been reported to increase expression levels in active gout [33]. Monocytes promoted the release of inflammatory mediators after pathogen invasion, and then transform into macrophages to participate in the immune response [41]. Inflammation was associated with low lymphocyte count [42]. Therefore, the increase in monocyte count and the decrease in lymphocyte count in inflammatory diseases lead to the imbalance of the MLR. Our findings also found that increased MLR was associated with the diagnosis of spinal tuberculosis, clinical severity, and active spinal tuberculosis.

In addition, PLR is also a marker of inflammation and is significantly expressed in a variety of diseases. Mehmet et al.’s study showed that PLR as an inflammatory factor was significantly higher in advanced fibrosis 119 (61-1547) % than in mild fibrosis 99.5 (36-259) %, with a significant difference between the two groups [43]. Hamdi et al.’s study showed that PLR was positively correlated with CRP and ESR in the thyroid conditions, which could predict the thyroid conditions with high uptake or normal uptake [44]. The expression of PLR in malignant thyroid nodules was higher than that in benign thyroid nodules, and there was a positive correlation with TSH [45]. In addition, PLR expression was significantly higher in diabetes mellitus than in healthy patients, and there was a positive correlation between PLR and HbA1c [46]. Similarly, we also found that PLR, as an inflammatory factor, was significantly higher in spinal tuberculosis than in nonspinal tuberculosis in this study (). However, the AUC of MLR (0.663) in diagnosing spinal tuberculosis was higher than that of PLR (0.642) in the training set. The former (0.737) is also higher than the latter (0.706) in the verification set.

However, this study still had some limitations. (1) This topic was single-center research. (2) Blood tests were only collected at a single time point, and blood tests at multiple time points were more convincing.

5. Conclusion

MLR as an independent factor was associated with the diagnosis of spinal tuberculosis and the severity of spinal tuberculosis. Furthermore, MLR may be a predictor of active spinal tuberculosis.

Data Availability

The original contributions presented in the study are included in the article, further inquiries can be directed to the corresponding author/s.

Ethical Approval

All procedures were performed in accordance with relevant guidelines. This paper has been approved by the ethics committee of The First Affiliated Hospital of Guangxi Medical University.

Written informed consent of patients has been obtained for this study. The patient provided consent for publication of the data and images.

Disclosure

Funding bodies had no role in the study design, collection, analysis, and interpretation of the data or in writing the manuscript.

Conflicts of Interest

All authors declare no conflicts of interest.

Authors’ Contributions

Liyi Chen and Chong Liu wrote the article and prepared Figures 1–13 and Tables 1 and 2. Zhaoping Gan and Xinli Zhan contributed equally to this work. Zhaoping Gan should be considered co-corresponding author. Liyi Chen and Chong Liu contributed equally to this work and co-first authors. All authors reviewed the article.

Acknowledgments

This work was sponsored by the National Natural Science Foundation of China (81560359) and National Natural Science Foundation of China (81860393).

References

J. Chakaya, M. Khan, F. Ntoumi et al., “Global tuberculosis report 2020 - reflections on the Global TB burden, treatment and prevention efforts,” International Journal of Infectious Diseases, vol. 113, pp. S7–S12, 2021.
View at: Publisher Site | Google Scholar
R. N. Dunn and M. Ben Husien, “Spinal tuberculosis,” Bone and Joint Journal, vol. 100-B, no. 4, pp. 425–431, 2018.
View at: Publisher Site | Google Scholar
C. H. Chen, Y. M. Chen, C. W. Lee, Y. J. Chang, C. Y. Cheng, and J. K. Hung, “Early diagnosis of spinal tuberculosis,” Journal of the Formosan Medical Association, vol. 115, no. 10, pp. 825–836, 2016.
View at: Publisher Site | Google Scholar
C. Li, L. Liu, and Y. Tao, “Diagnosis and treatment of congenital tuberculosis: a systematic review of 92 cases,” Orphanet Journal of Rare Diseases, vol. 14, no. 1, p. 131, 2019.
View at: Publisher Site | Google Scholar
R. E. Colman, J. Anderson, D. Lemmer et al., “Rapid drug susceptibility testing of drug-resistant mycobacterium tuberculosis isolates directly from clinical samples by use of amplicon sequencing: a proof-of-concept study,” Journal of Clinical Microbiology, vol. 54, no. 8, pp. 2058–2067, 2016.
View at: Publisher Site | Google Scholar
L. Tang, S. Feng, R. Gao et al., “A comparative study on the role of Xpert MTB/RIF in testing different types of spinal tuberculosis tissue specimens,” Genetic Testing and Molecular Biomarkers, vol. 21, no. 12, pp. 722–726, 2017.
View at: Publisher Site | Google Scholar
Y. Yu, Y. Kong, J. Ye, and A. Wang, “Performance of conventional histopathology and GeneXpert MTB/RIF in the diagnosis of spinal tuberculosis from bone specimens: a prospective clinical study,” Clinical Biochemistry, vol. 85, pp. 33–37, 2020.
View at: Publisher Site | Google Scholar
S. Gatechompol, J. Sophonphan, S. J. Kerr et al., “Monocyte-to-lymphocyte ratio as a predictor of TB among people living with HIV,” The International Journal of Tuberculosis and Lung Disease: the Official Journal of the International Union against Tuberculosis and Lung Disease, vol. 25, no. 11, pp. 933–938, 2021.
View at: Publisher Site | Google Scholar
M. Z. Kocak, G. Aktas, T. T. Duman et al., “Monocyte lymphocyte ratio as a predictor of diabetic kidney injury in type 2 diabetes mellitus; the MADKID study,” Journal of Diabetes & Metabolic Disorders, vol. 19, no. 2, pp. 997–1002, 2020.
View at: Publisher Site | Google Scholar
G. Aktas, T. T. Duman, O. Kurtkulagi et al., “Liver steatosis is associated both with platelet distribution width, neutrophil lymphocyte and monocyte lymphocyte ratios,” Primary Health Care Open Access, vol. 10, no. 4, 2020.
View at: Google Scholar
G. Aktas, T. Duman, B. Atak et al., “Irritable bowel syndrome is associated with novel inflammatory markers derived from hemogram parameters,” Family Medicine and Primary Care Review, vol. 22, no. 2, pp. 107–110, 2020.
View at: Publisher Site | Google Scholar
O. Catal, B. Ozer, M. Sit, G. Aktas, and H. Erkol, “The role of monocyte to lymphocyt ratio in predicting metastasis in rectal cancer,” Annals of Medical Research, vol. 28, no. 3, pp. 0527–0531, 2021.
View at: Publisher Site | Google Scholar
G. Aktas, “Hematological predictors of novel Coronavirus infection,” Revista da Associação Médica Brasileira, vol. 67, Supplement 1, pp. 1-2, 2021.
View at: Google Scholar
C. Bray et al., “Erythrocyte sedimentation rate and C-reactive protein measurements and their relevance in clinical medicine,” WMJ, vol. 115, no. 6, pp. 317–321, 2016.
View at: Google Scholar
J. Kim, J. Y. Ahn, S. J. Jeong et al., “Prognostic factors for unfavourable outcomes of patients with spinal tuberculosis in a country with an intermediate tuberculosis burden,” The Bone & Joint Journal, vol. 101-B, no. 12, pp. 1542–1549, 2019.
View at: Publisher Site | Google Scholar
W. Wu, Z. Li, R. Lin, S. Wang, and J. Lin, “Single-stage posterior-only debridement, decompression and interbody fusion for the treatment of thoracolumbar spinal tuberculosis complicated with psoas abscesses,” BMC Surgery, vol. 21, no. 1, p. 84, 2021.
View at: Publisher Site | Google Scholar
T. Buttle, C. Y. Hummerstone, T. Billahalli et al., “The monocyte-to-lymphocyte ratio: sex-specific differences in the tuberculosis disease spectrum, diagnostic indices and defining normal ranges,” PloS one, vol. 16, no. 8, article e0247745, 2021.
View at: Publisher Site | Google Scholar
E. Van Ginderdeuren, J. Bassett, C. F. Hanrahan, and A. Van Rie, “Association between monocyte-to-lymphocyte ratio and tuberculin skin test positivity in HIV-positive adults,” PloS one, vol. 16, no. 7, article e0253907, 2021.
View at: Publisher Site | Google Scholar
M. Peghin, D. Rodriguez-Pardo, A. Sanchez-Montalva et al., “The changing epidemiology of spinal tuberculosis: the influence of international immigration in Catalonia, 1993-2014,” Epidemiology and Infection, vol. 145, no. 10, pp. 2152–2160, 2017.
View at: Publisher Site | Google Scholar
S. H. Chen, W. C. Lin, C. H. Lee, and W. Y. Chou, “Spontaneous infective spondylitis and mycotic aneurysm: incidence, risk factors, outcome and management experience,” European Spine Journal, vol. 17, no. 3, pp. 439–444, 2008.
View at: Publisher Site | Google Scholar
Z. Xu, J. Zhang, Y. Zhong et al., “Predictive value of the monocyte-to-lymphocyte ratio in the diagnosis of prostate cancer,” Medicine, vol. 100, no. 38, article e27244, 2021.
View at: Publisher Site | Google Scholar
S. Chim, P. Sanfilippo, T. J. O'Brien, K. J. Drummond, and M. Monif, “Pretreatment neutrophil-to-lymphocyte/monocyte-to-lymphocyte ratio as prognostic biomarkers in glioma patients,” Journal of Neuroimmunology, vol. 361, article 577754, 2021.
View at: Publisher Site | Google Scholar
L. Yang, C. Gao, F. Li et al., “Monocyte-to-lymphocyte ratio is associated with 28-day mortality in patients with acute respiratory distress syndrome: a retrospective study,” Journal of Intensive Care, vol. 9, no. 1, p. 49, 2021.
View at: Publisher Site | Google Scholar
P. Sukson, C. Liwsrisakun, J. Inchai, K. Trongtrakul, and P. Tajarernmuang, “Peripheral blood monocyte to lymphocyte ratio for prediction of tuberculous pleuritis,” International Journal of Infectious Diseases, vol. 112, pp. 212–216, 2021.
View at: Publisher Site | Google Scholar
P. Wang, M. F. Wu, C. Y. Hsu et al., “The dynamic change of immune checkpoints and CD14+ monocytes in latent tuberculosis infection,” Biomedicine, vol. 9, no. 10, p. 1479, 2021.
View at: Publisher Site | Google Scholar
E. Petruccioli, T. J. Scriba, L. Petrone et al., “Correlates of tuberculosis risk: predictive biomarkers for progression to active tuberculosis,” The European Respiratory Journal, vol. 48, no. 6, pp. 1751–1763, 2016.
View at: Publisher Site | Google Scholar
V. Naranbhai, H. A. Fletcher, R. Tanner et al., “Distinct transcriptional and anti-mycobacterial profiles of peripheral blood monocytes dependent on the ratio of monocytes: lymphocytes,” eBioMedicine, vol. 2, no. 11, pp. 1619–1626, 2015.
View at: Publisher Site | Google Scholar
H. Esmail, C. E. Barry 3rd, D. B. Young, and R. J. Wilkinson, “The ongoing challenge of latent tuberculosis,” Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, vol. 369, no. 1645, p. 20130437, 2014.
View at: Publisher Site | Google Scholar
G. Wang, L. Xie, J. Hu et al., “Osteopontin, bone morphogenetic protein-4, and vitamin D receptor gene polymorphisms in the susceptibility and clinical severity of spinal tuberculosis,” Cellular Physiology and Biochemistry: International Journal of Experimental Cellular Physiology, Biochemistry, and Pharmacology, vol. 41, no. 5, pp. 1881–1893, 2017.
View at: Publisher Site | Google Scholar
R. Singh, T. Hui, A. Matsui et al., “Modulation of infection-mediated migration of neutrophils and CXCR2 trafficking by osteopontin,” Immunology, vol. 150, no. 1, pp. 74–86, 2017.
View at: Publisher Site | Google Scholar
B. Shiratori, J. Zhao, M. Okumura et al., “Immunological roles of elevated plasma levels of matricellular proteins in Japanese patients with pulmonary tuberculosis,” International Journal of Molecular Sciences, vol. 18, no. 1, 2017.
View at: Publisher Site | Google Scholar
T. Simakou, R. Freeburn, and F. Henriquez, “Gene expression during THP-1 differentiation is influenced by vitamin D3 and not vibrational mechanostimulation,” Peer J, vol. 9, article e11773, 2021.
View at: Publisher Site | Google Scholar
C. Kadiyoran, O. Zengin, H. A. Cizmecioglu et al., “Monocyte to lymphocyte ratio, neutrophil to lymphocyte ratio, and red cell distribution width are the associates with gouty arthritis,” Acta Medica (Hradec Králové), vol. 62, no. 3, pp. 99–104, 2019.
View at: Publisher Site | Google Scholar
B. L. Muller, D. M. . P. Ramalho, P. F. G. . Santos, E. D. D. Mesquita, A. L. Kritski, and M. M. Oliveira, “Inflammatory and immunogenetic markers in correlation with pulmonary tuberculosis,” Jornal Brasileiro de Pneumologia, vol. 39, no. 6, pp. 719–727, 2013.
View at: Publisher Site | Google Scholar
Y. Wang, C. Hu, Z. Wang, H. Kong, W. Xie, and H. Wang, “Serum IL-1β and IL-18 correlate with ESR and CRP in multidrug-resistant tuberculosis patients,” Journal of Biomedical Research, vol. 29, no. 5, pp. 426–428, 2015.
View at: Publisher Site | Google Scholar
C. Yoon, L. H. Chaisson, S. M. Patel et al., “Diagnostic accuracy of C-reactive protein for active pulmonary tuberculosis: a meta-analysis,” The International Journal of Tuberculosis and Lung Disease, vol. 21, no. 9, pp. 1013–1019, 2017.
View at: Publisher Site | Google Scholar
M. El Amrani, M. Asserraji, A. Bahadi, D. El Kabbaj, and M. Benyahia, “Tuberculosis in hemodialysis,” Medecine et Sante Tropicales, vol. 26, no. 3, pp. 262–266, 2016.
View at: Publisher Site | Google Scholar
M. L. Moraes, D. M. . P. Ramalho, K. N. Delogo et al., “Association of serum levels of iron, copper, and zinc, and inflammatory markers with bacteriological sputum conversion during tuberculosis treatment,” Biological Trace Element Research, vol. 160, no. 2, pp. 176–184, 2014.
View at: Publisher Site | Google Scholar
W. Niu, Y. G. Wan, M. Y. Li, Z. X. Wu, L. G. Zhang, and J. X. Wang, “The diagnostic value of serum procalcitonin, IL-10 and C-reactive protein in community acquired pneumonia and tuberculosis,” European Review for Medical and Pharmacological Sciences, vol. 17, no. 24, pp. 3329–3333, 2013.
View at: Google Scholar
D. Suszek, A. Górak, and M. Majdan, “Differential approach to peripheral blood cell ratios in patients with systemic lupus erythematosus and various manifestations,” Rheumatology International, vol. 40, no. 10, pp. 1625–1629, 2020.
View at: Publisher Site | Google Scholar
A. Refai, S. Gritli, M. R. Barbouche, and M. Essafi, “Mycobacterium tuberculosis virulent factor ESAT-6 drives macrophage differentiation toward the pro-inflammatory M1 phenotype and subsequently switches it to the anti-inflammatory M2 phenotype,” Frontiers in Cellular and Infection Microbiology, vol. 8, p. 327, 2018.
View at: Publisher Site | Google Scholar
F. Gravani, I. Papadaki, E. Antypa et al., “Subclinical atherosclerosis and impaired bone health in patients with primary Sjogren's syndrome: prevalence, clinical and laboratory associations,” Arthritis Research & Therapy, vol. 17, no. 1, p. 99, 2015.
View at: Publisher Site | Google Scholar
M. A. Kosekli, “Mean platelet volume and platelet to lymphocyte count ratio are associated with hepatitis B-related liver fibrosis,” European Journal of Gastroenterology & Hepatology, vol. 34, no. 3, pp. 324–327, 2022.
View at: Publisher Site | Google Scholar
H. Afin and G. Aktas, “Platelet to Lymphocyte and Neutrophil to Lymphocyte Ratios are useful in differentiation of thyroid conditions with normal and increased uptake,” Ethiopian Journal of Health Development, vol. 35, no. 3, pp. 1–5, 2021.
View at: Google Scholar
B. M. Atak, G. B. Kahveci, S. Bilgin, O. Kurtkulagi, and M. A. Kosekli, “Platelet to lymphocyte ratio in differentiation of benign and malignant thyroid nodules,” Experimental Biomedical Research, vol. 4, no. 2, pp. 148–153, 2021.
View at: Publisher Site | Google Scholar
B. Atak, G. Aktas, T. T. Duman, E. Erkus, M. Z. Kocak, and H. Savli, “Diabetes control could through platelet-to-lymphocyte ratio in hemograms,” Revista da Associação Médica Brasileira, vol. 65, pp. 38–42, 2019.
View at: Google Scholar

Copyright

Copyright © 2022 Liyi Chen et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

PDF Download Citation

Download other formats

Order printed copies