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Inflammation ( # 2014)

DOI: 10.1007/s10753-014-9978-y

The Relationship Between Inflammatory Marker Levels


and Pulmonary Tuberculosis Severity

Ozlem Abakay,1,2 Abdurrahman Abakay,1 Hadice Selimoglu Sen,1 and Abdullah C. Tanrikulu1

Abstract—We aimed to investigate the correlation between red cell distribution width (RDW), neutro-
phil to lymphocyte ratio (NLR), platelet to lymphocyte ratio (PLR), and other inflammatory markers
with pulmonary tuberculosis (PTB) severity. Seventy patients with active pulmonary tuberculosis were
compared with 50 age-matched and gender-matched healthy controls. The mean age of PTB patients
was 50.4±21.8 years. There were no differences in terms of age, gender, and smoking history between
PTB patients and controls. Patients with advanced PTB had a significantly higher white blood cell count,
neutrophil count, RDW, NLR, and C-reactive protein when compared to patients with mild to moderate
PTB. RDW (17.7 versus 15.7 %, p=0.002) and NLR (4.7 versus 3.1, p=0.009) values were higher in
patients with advanced PTB as opposed to patients with mild to moderate PTB. NLR and RDW levels
may be used as markers of inflammation to help clinically manage patients with TB and to determine
disease severity.

KEY WORDS: inflammatory markers; neutrophil to lymphocyte ratio; pulmonary tuberculosis; radiological extent;
red blood cell distribution width.

INTRODUCTION that C-reactive protein (CRP), platelet count, plateletcrit


(PCT), and platelet distribution width (PDW) may be
Tuberculosis (TB) infections occur by inhaling My- potential biomarkers of PTB severity [3–5].
cobacterium tuberculosis bacilli (MTB). Roughly, 10 % of Red blood cell distribution width (RDW) is a measure
tuberculosis diagnoses are made during the first and second of the size variability of circulating blood cells and is part
decades of life, and this disease affects three times as many of the complete blood count (CBC) panel. It is mainly used
men as women [1]. The progression to active disease as a tool in the differential diagnosis of anemia, but the
results from changes in bacterial virulence and/or an im- RDW may be elevated in any condition in which reticulo-
paired host immune system. The most significant risk cytes are released into the circulation such as inflammatory
factor that promotes the progression of latent to active diseases and sepsis [6, 7]. In addition to diagnosing ane-
disease is contracting HIV while infected with TB [2]. mia, recent studies have demonstrated that RDW also gives
The current understanding of the immunology of myco- information regarding the prognosis of congestive heart
bacterial infections has provided insight into how PTB failure, acute myocardial infarction, pulmonary embolism,
causes self-limited hematological abnormalities. pneumonia, obstructive sleep apnea syndrome, chronic
Developing point-of-care diagnostic testing will obstructive pulmonary disease, sepsis, and other illnesses
greatly benefit public health by decreasing morbidity and [7–11]. It is not completely understood why RDW is
mortality and reducing TB transmission rates. Yet in order elevated in these patients, but it has been suggested that
to develop such a test, it is necessary to determine bio- inflammation contributes to higher RDW levels [11].
markers that are both highly specific and sensitive in White blood cell count (WBC) is a well-known indi-
detecting active TB. Recently, several studies suggested cator of inflammation. In recent years, several studies
investigated the potential role of various leukocyte ratios
1
Department of Chest Diseases, Medical Faculty, Dicle University, in chronic inflammatory diseases [12–15]. The inflamma-
Diyarbakir, Turkey tory response is central to the pathophysiology of PTB. To
2
To whom correspondence should be addressed at Department of Chest the best of our knowledge, an investigation regarding
Diseases, Medical Faculty, Dicle University, Diyarbakir, Turkey. whether the neutrophil to lymphocyte ratio (NLR), platelet
E-mail: o.abakay@hotmail.com to lymphocyte ratio (PLR), and RDW are biomarkers of

0360-3997/14/0000-0001/0 # 2014 Springer Science+Business Media New York


Abakay, Abakay, Sen, and Tanrikulu

active PTB has not yet been published. As chronic inflam- minimal to mild disease, stage 2 was moderate disease, and
mation has been found to be associated with increased stage 3 was advanced disease [5, 16, 17]. Lesions were
inflammatory marker levels in PTB patient serum, we considered minimal if there was no evidence of cavitation
hypothesized that RDW, NLR, and PLR levels are also
and the lesions were of slight to moderate density located
affected by PTB severity. The objective of this study was to
investigate the relationship between the RDW, NLR, and above the second chondrosternal junction. Moreover, the
PLR and known acute phase reactants in patients with lesions must only involve a segment of one or both lungs,
chest X-ray-confirmed active PTB. and the combined extent of the lesions must be smaller than
the volume of a single lung. Disseminated lesions of slight
characterized moderate disease to moderate density in one
MATERIALS AND METHODS or both lungs, and the collective lesion volume cannot
exceed that of a single lung. In moderate disease, the
lesions may also be densely packed so to appear confluent,
Patients
but areas of high-density lesions cannot take up more than
This is a retrospective chart review study. Data were one third of the volume of one lung. Moreover, the total
collected by scanning Dicle University Hospital patient diameter of cavitations cannot exceed 4 cm in patients with
records archived from January 2011 to December 2013. moderate disease. If lesions were found to be more exten-
In this time frame, there was record of 70 culture-positive sive than moderate disease, then it was considered ad-
pulmonary tuberculosis patients. We then included 50 age- vanced disease. After PTB patients were classified accord-
matched and gender-matched healthy controls. This study ing to stage, they were divided into two groups: group 1
was performed in accordance with the principles of the consisted of patients with mild–moderate disease, and
Declaration of Helsinki and was reviewed and approved by group 2 patients had advanced disease.
the Dicle University Medical Faculty ethics committee.
Patients were excluded from the study if they were Laboratory Analysis
taking antibiotics or had conditions that are known to affect
All laboratory samples were collected before the pa-
WBC counts such as hematologic disorders, chronic in-
tients were started on treatment. Complete blood count
flammatory conditions, severe cardiovascular disease,
analyses were performed with the Beckman Coulter LH-
chronic inflammatory diseases, significant liver disease,
750 Hematology Analyzer (Beckman Coulter, Inc., Fuller-
autoimmune disorders, neoplasms, and being immuno-
ton, CA, USA). In accordance with hospital laboratory
compromised. Further exclusion criteria were if hemogram
policy, the CBC was performed within 1 h of sample
data were missing from the chart, if the patient was mis-
collection. Analyses were performed at room temperature.
takenly diagnosed with PTB, or if the patient was found to
Total WBC, neutrophil, lymphocyte, and platelet counts in
have pulmonary edema during follow-up.
addition to PDW, mean platelet volume (MPV), and RDW
Demographics such as age, gender, current smoking
were determined by performing CBC analyses. The NLR
status, and smoking history were obtained. Clinical data
was defined as the absolute neutrophil count divided by the
such as symptoms, duration of symptoms, and history of
absolute lymphocyte count. The PLR was defined as the
previous TB infections were gathered. Lastly, laboratory
absolute platelet count divided by the absolute lymphocyte
findings including hemogram parameters, serum CRP lev-
count. Serum CRP levels were measured by the
el, and erythrocyte sedimentation rate (ESR) were archived
immunoturbidometric method (Roche Diagnostics,
in the patient files. Symptom duration was defined as the
GmbH, Mannheim, Germany) within 1 h of sample col-
time between symptom onset and diagnosis. Patients were
lection, and a normal CRP value was 0.5 mg/dL.
assigned into the pulmonary TB group once MTB was
cultured from samples obtained from either sputum or
Statistical Analysis
bronchial lavage. A positive diagnosis for active PTB
consisted of detecting acid fast bacilli with Ziehl–Neelsen The Kolmogorov–Smirnov test was used to test
stain from sputum samples and at least one positive culture whether continuous variables conformed to a normal dis-
in Löwenstein–Jensen media using the BACTEC TB 460 tribution. Data that followed a normal distribution were
system. All patients in this study met these criteria for expressed as the mean±one standard deviation. The inde-
active PTB. pendent Student’s t test and the χ2 test or Fisher’s exact test
Patients with PTB were classified according to the were utilized to compare data between patient subgroups.
extent of disease evident on chest radiography: stage 1 was Student’s t test, used to evaluate normally distributed data,
Inflammatory Marker Levels and Pulmonary Tuberculosis Severity

or the Mann–Whitney U test, used to evaluate data that do Table 2. Comparison of Laboratory Results Between PTB Patients and
Controls
not conform to a normal distribution, was used to compare
data between two groups. The Spearman test was used to Parameter PTB patients Controls p value
assess the correlation between variables. Statistical (n=70) (n=50)
analyses were performed with the Statistical Package for
Social Sciences version 15 for the Windows® operating WBC count (×109/μL) 9.5±3.3 9.7±1.9 NS
Neutrophil count (×109/μL) 6.6±2.8 5.7±1.4 0.033
system (SPSS® Inc. Chicago, IL, USA). Two-tailed statis-
Lymphocyte count (×109/μL) 2.2±1.7 3.5±0.9 <0.001
tical significance testing was performed, and p values less Platelet count (×109/μL) 352.3±111.0 257.2±99.0 <0.001
than 0.05 were considered significant. PDW (%) 17.3±1.2 10.9±3.2 <0.001
MPV (fL) 7.4±1.3 7.6±1.2 NS
RDW (%) 16.6±2.6 12.5±1.4 <0.001
NLR 3.9±2.6 1.6±0.3 <0.001
RESULTS PLR 201.1±111.3 78.7±39.2 <0.001
CRP (mg/dL) 6.1±4.2 0.3±0.2 <0.001
ESR (mm/h) 39.8±21.2 5.8±2.1 <0.001
A total of 70 patients diagnosed with PTB and 50 age-
matched and gender-matched healthy control subjects were Data are expressed as the mean±one standard deviation
included in this study. For the PTB patients, the mean age PTB pulmonary tuberculosis, NLR neutrophil to lymphocyte ratio, PLR
platelet to lymphocyte ratio, NS not significant, CRP C-reactive protein,
was 50.4±21.8 years, and ages ranged from 18 to 82 years; ESR erythrocyte sedimentation rate, PDW platelet distribution width,
the average age for controls was 48.5±14.6 years ranging ESR erythrocyte sedimentation rate
from 19 to 86 years. In PTB group, 67 % of patients were
male, and 66 % of patients were male in the control group. WBC count, neutrophil count, RDW, NLR, CRP, and
Thirty-seven (52.8 %) of the PTB patients were smokers. ESR when compared to patients with mild to moderate
During the diagnosis, 66 (94 %) patients had cough, 54 disease (Table 3). The RDW (17.7 versus 15.7 %) and
(77 %) had dyspnea, and 40 (57 %) had weight loss. NLR (4.7 versus 3.1) values were found to be higher in
Demographic and clinical characteristics of both patient the advanced PTB group than in patients with mild to
and control groups are shown in Table 1. There were no moderate PTB.
differences in age, gender, and smoking history between Spearman’s correlation analysis showed a signif-
PTB patients and control subjects (p>0.05). icant correlation between NLR and the serum CRP
Neutrophil count, platelet count, RDW, PDW, NLR,
PLR, ESR, and CRP values were significantly higher in
PTB group when compared to the control group (Table 2). Table 3. Comparison of Laboratory Results Between Patients with Mild
Patients with advanced PTB had a significantly higher to Moderate and Advanced PTB

Parameter Mild to moderate Advanced PTB p value


Table 1. Demographic and Clinical Characteristics PTB (n=37) (n=33)

Characteristics PTB patients Controls p value WBC count 8.6±2.7 10.6±3.6 0.01
(n=70) (n=50) (×109/μL)
Neutrophil count 5.5±2.4 7.7±2.8 0.001
Age, years 50.4±21.8 48.5±14.6 NS (×109/μL)
Gender: male/female, n/n 47/23 32/18 NS Lymphocyte count 2.2±0.9 2.2±2.3 NS
Current smoker, n 37 25 NS (×109/μL)
Smoking history, packet/years 13.9 11.2 NS Platelet count 350.4±111.9 354.5±111.7 NS
Mean symptom duration, 1.5 – – (×109/μL)
months PDW (%) 17.4±1.2 17.2±1.3 NS
Symptoms, n (%) MPV (fL) 7.4±1.3 7.3±1.2 NS
Cough 66 (94) – – RDW (%) 15.7±2.1 17.7±2.7 0.002
Dyspnea 54 (77) – – NLR 3.1±2.2 4.7±2.8 0.009
Weight loss 40 (57) – – PLR 189.2±104.2 214.5±118.9 NS
Fever 35 (50) – – CRP (mg/dL) 4.1±4.0 8.2±3.4 <0.001
Hemoptysis 21 (30) – – ESR (mm/h) 34.3±19.6 46.0±21.6 0.021
Previous TB infection, n (%) 18 (26) – –
Data are expressed as the mean±one standard deviation. For abbrevia-
NS not significant, TB tuberculosis tions, refer to the legend of Table 2
Abakay, Abakay, Sen, and Tanrikulu

level (r=0.257; p=0.032) (Fig. 1). There is a positive


correlation between NLR and ESR (r=0.317; p=0.008)
(Fig. 2).

DISCUSSION

Inflammation plays a significant role in the pathogen-


esis of PTB. Yaranal et al. demonstrated that hematological
abnormalities are more commonly observed in cases of
severe tuberculosis. Most often, it was observed that pa-
tients with severe tuberculosis had anemia, elevated ESR,
and thrombocytosis [18]. Other studies also reported that
patients with advanced pulmonary TB demonstrated ane-
mia, leukocytosis, elevated ESR, and thrombocytosis [5,
19–23]. In our study, we found that NLR, RDW, ESR, and
CRP values are higher in patients with advanced stage PTB Fig. 2. Correlation between the NLR and erythrocyte sedimentation rate
when compared to patients with mild to moderate PTB. (ESR) levels in study subjects (r=0.317; p=0.008).
These data suggest that the inflammatory response
mounted in patients with severe PTB tends to be greater.
Moreover, besides CRP and ESR, the NLR may be a useful WBC count is a marker of inflammation, and NLR
marker by itself and may be used to distinguish between may be used to predict the prognosis of patients with
patients with advanced PTB and mild to moderate PTB. systemic inflammatory diseases [25–27]. Gary et al. inves-
The NLR may be easily obtained from routine labo- tigated NLR and its association with critical limb ischemia
ratory testing, and this simple ratio may be determined in (CLI) in patients with peripheral arterial occlusive disease
many hospitals. Additionally, the NLR is an easier and less (PAOD) [28]. It was determined that an elevated NLR is
expensive test to perform as compared to other inflamma- significantly associated with a high risk of CLI and other
tory biomarkers such as CRP and procalcitonin [24]. vascular health problems. Holub et al. assessed the sensi-
tivity and specificity of the NLR in diagnosing community-
acquired bacterial pneumonia in patients hospitalized with
a febrile illness. It was suggested that the NLR may serve
as a simple marker that may aid in discriminating between
severe bacterial and viral infections [29]. Yoon et al. in-
vestigated the usefulness of the NLR in differentiating
between pulmonary TB from bacterial community-
acquired pneumonia (CAP). They showed that serum
NLR levels were significantly lower in patients with pul-
monary TB than in patients with bacterial CAP [30]. In our
study, we found that NLR levels were significantly higher
in patients with advanced PTB as opposed to patients with
mild to moderate PTB.
RDW is a biomarker that has been mostly studied
in cardiac diseases, pneumonia, and pulmonary em-
bolism [8–11, 31]. Ozsu et al. demonstrated that obstruc-
tive sleep apnea syndrome patients have an elevated
RDW when compared with controls. They found that
RDW was an independent predictor of cardiovascular
Fig. 1. Correlation between the NLR and serum CRP levels in study su- diseases in obstructive sleep apnea syndrome (OSAS)
bjects (r=0.257; p=0.032). patients, but there was no association between OSAS
Inflammatory Marker Levels and Pulmonary Tuberculosis Severity

severity and RDW [32]. Kurt et al. investigated the In conclusion, it is imperative to identify novel bio-
relationship of MPV, PDW, and RDW with OSAS markers that help indicate the severity of inflammation in
severity, yet no correlation was identified [33]. Yet in patients with PTB so as to identify active TB or disease
our study, we found that there is a significant in- reactivation. To the best of our knowledge, this is the first
crease in RDW in patients with advanced PTB when clinical study demonstrating that the NLR, PLR, and RDW
contrasted with patients with mild to moderate PTB. become elevated in patients with PTB. Hence, NLR and
As such, there was a positive relationship between RDW may be used as markers of inflammation in the
PTB severity and RDW. clinical management of patients with PTB as these bio-
Reactive thrombocytosis in patients with PTB has markers are quickly, cheaply, and easily obtained with
been shown to be correlated with increased disease routine CBC analysis.
severity and higher levels of other acute phase reac-
tants [4, 34]. Tozkoparan et al. determined that the
platelet count and related indices including PDW, Conflict of Interest. The authors declare that there are no
MPV, and PCT were higher in patients with active conflicts of interest.
PTB than in patients with pneumonia or inactive
tuberculosis. They found that these platelet-related
indices decreased following treatment. These data sug- Funding. This research received no specific grant from
gested that an increase in platelet count and its asso- any funding agency in the public, commercial, or not-for-
ciated indices may be used to aid in determining profit sectors.
whether tuberculosis infection is becoming activated
[3]. In our study, platelet count and the PLR level
were higher in patients with PTB as opposed to con-
trols. However, no significant difference was found in
platelet count and the PLR level between patients with
mild to moderate and advanced PTB. REFERENCES
The NLR and PLR are associated with a poorer
prognosis in various diseases. Sunbul et al. investigat- 1. WHO 2010–2011 TB factsheet. Available at: www.who.int/tb/
publications/2010/factsheet_tb_2010_rev21feb11.pdf/ Accessed
ed the association between NLR and PLR in patients 18 Feb 2014.
with dipper versus non-dipper hypertension. They 2. Nunn, P., B. Williams, K. Floyd, C. Dye, G. Elzinga, et al. 2005.
found that patients with non-dipper hypertension had Tuberculosis control in the era of HIV. Nature Reviews Immunology
5: 819–826.
significantly higher NLR and PLR levels when com- 3. Tozkoparan, E., O. Deniz, E. Ucar, H. Bilgic, and K. Ekiz. 2007.
pared to patients with dipper hypertension [35]. Changes in platelet count and indices in pulmonary tuberculosis. Clin-
Yavuzcan et al. compared preoperative MPV values ical Chemistry and Laboratory Medicine 45: 1009–1013.
4. Unsal, E., S. Aksaray, D. Köksal, and T. Sipit. 2005. Potential role of
and other systemic inflammatory response markers, interleukin 6 in reactive thrombocytosis and acute phase response in
namely the NLR and PLR, between patients with ad- pulmonary tuberculosis. Postgraduate Medical Journal 81: 604–607.
vanced stage endometriosis with endometrioma and 5. Sahin, F., E. Yazar, and P. Yildiz. 2012. Prominent features of
platelet count, plateletcrit, mean platelet volume and platelet
patients with a benign adnexal mass. They demonstrat- distribution width in pulmonary tuberculosis. Multidisciplinary
ed that MPV, NLR, and PLR values are not useful in Respiratory Medicine 7: 38.
distinguishing patients with advanced stage endometri- 6. Hotchkiss, R.S., and I.E. Karl. 2003. The pathophysiology and treat-
ment of sepsis. New England Journal of Medicine 348: 138–150.
osis and those with benign disease, even though ad- 7. Jo, Y.H., K. Kim, J.H. Lee, et al. 2013. Red cell distribution width is a
vanced endometriosis is characterized by severe in- prognostic factor in severe sepsis and septic shock. American Journal of
flammation [36]. Feng et al. investigated the prognos- Emergency Medicine 31: 545–548.
8. Sincer, I., A. Zorlu, M.B. Yilmaz, et al. 2012. Relationship between red
tic value of the NLR and PLR in patients with small cell distribution width and right ventricular dysfunction in patients with
cell carcinoma of the esophagus. They reported that chronic obstructive pulmonary disease. Heart & Lung 41: 238–
PLR was superior to NLR in predicting small cell 243.
9. Felker, G.M., L.A. Allen, S.J. Pocock, et al. 2007. Red cell distribution
carcinoma prognosis [37]. In our study, we showed width as a novel prognostic marker in heart failure: data from the
that there is a significant increase in NLR and PLR CHARM Program and the Duke Databank. Journal of the American
values in patients with pulmonary tuberculosis when College of Cardiology 50: 40–47.
10. Dabbah, S., H. Hammerman, W. Markiewicz, et al. 2010. Relation
compared to healthy controls. However, PLR was not between red cell distribution width and clinical outcomes after acute
associated with PTB severity. myocardial infarction. American Journal of Cardiology 105: 312–317.
Abakay, Abakay, Sen, and Tanrikulu

11. Braun, E., E. Domany, Y. Kenig, et al. 2011. Elevated red cell distri- lymphocyte ratio as a predictor of disease severity in ulcerative colitis.
bution width predicts poor outcome in young patients with community Journal of Clinical Laboratory Analysis 27: 72–76.
acquired pneumonia. Critical Care 15: R194. 26. Okyay, G.U., S. Inal, K. Oneç, R.E. Er, O. Paşaoğlu, H. Paşaoğlu, U.
12. Thomsen, M., T.S. Ingebrigtsen, J.L. Marott, M. Dahl, P. Lange, J. Derici, and Y. Erten. 2013. Neutrophil to lymphocyte ratio in evalua-
Vestbo, et al. 2013. Inflammatory biomarkers and exacerbations in tion of inflammation in patients with chronic kidney disease. Renal
chronic obstructive pulmonary disease. JAMA 309: 2353–2361. Failure 35: 29–36.
13. Goldenberg, A.S. 1996. Hematologic abnormalities and mycobacterial 27. Güngör B, Ozcan KS, Erdinler I, Ekmekçi A, Alper AT, Osmonov D,
infection. In Tuberculosis, ed. N.R. Williams and G.M. Stuart, Calık N, Akyuz S, Toprak E, Yılmaz H, Yıldırım A, Bolca O.
645–647. Boston: Little – Brown Company. Elevated levels of RDW is associated with non-valvular atrial fibril-
14. Ahsen, A., M.S. Ulu, S. Yuksel, K. Demir, M. Uysal, M. Erdogan, lation. J Thromb Thrombolysis 2013.
et al. 2013. As a new inflammatory marker for familial Mediterranean 28. Gary, T., M. Pichler, K. Belaj, F. Hafner, A. Gerger, H. Froehlich, P.
fever: neutrophil-to-lymphocyte ratio. Inflammation 36: 1357–1362. Eller, E. Pilger, and M. Brodmann. 2013. Neutrophil-to-lymphocyte
15. Ertaş, G., O. Sönmez, M. Turfan, S. Kul, E. Erdoğan, A. Tasal, et al. ratio and its association with critical limb ischemia in PAOD patients.
2013. Neutrophil/lymphocyte ratio is associated with thromboembolic PLoS One 8: e56745.
stroke in patients with non-valvular atrial fibrillation. Journal of the 29. Holub, M., O. Beran, N. Kaspříková, and P. Chalupa. 2012. Neutro-
Neurological Sciences 324: 49–52. phil to lymphocyte count ratio as a biomarker of bacterial infections.
16. 1961. National Tuberculosis Association of the USA: Diagnostic Central European Journal of Medicine 7: 258–261.
standards and classification of tuberculosis. New York: National 30. Yoon, N.B., C. Son, and S.J. Um. 2013. Role of the neutrophil-
Tuberculosis Association. lymphocyte count ratio in the differential diagnosis between pulmo-
17. Seaton, A., D. Seaton, and A.G. Leitch. 1989. Crofton and Douglas’s nary tuberculosis and bacterial community-acquired pneumonia.
respiratory diseases, 4th ed, 409–410. Oxford: Blackwell. Annals of Laboratory Medicine 33: 105–110.
18. Yaranal, P.J., T. Umashankar, and S.G. Harish. 2013. Hematological 31. Ozsu, S., Y. Abul, S. Gunaydin, A. Orem, and T. Ozlu. 2014. Prog-
profile in pulmonary tuberculosis. International Journal of Health and nostic value of red cell distribution width in patients with pulmonary
Rehabilation Sciences 2: 50–55. embolism. Clinical and Applied Thrombosis/Hemostasis 20: 365–370.
19. Bazick, H.S., D. Chang, K. Mahadevappa, et al. 2011. Red cell 32. Ozsu, S., Y. Abul, A. Gulsoy, Y. Bulbul, S. Yaman, and T. Ozlu. 2012.
distribution width and all-cause mortality in critically ill patients. Red cell distribution width in patients with obstructive sleep apnea
Critical Care Medicine 39: 1913–1921. syndrome. Lung 190: 319–326.
20. Baynes, R.D., H. Flax, T.H. Bothwell, W.R. Bezwoda, A.P. MacPhail, 33. Kurt, O.K., and N. Yildiz. 2013. The importance of laboratory param-
P. Atkinson, et al. 1986. Haematological and iron-related measure- eters in patients with obstructive sleep apnea syndrome. Blood
ments in active pulmonary tuberculosis. Scandinavian Journal of Coagulation and Fibrinolysis 24: 371–374.
Haematology 36: 280–287. 34. Mirsaeidi, M., P. Peyrani, S. Aliberti, G. Filardo, J. Bordon, F. Blasi,
21. Olaniyi, J.A., and Y.A. Aken’Ova. 2003. Haematological profile of et al. 2010. Thrombocytopenia and thrombocytosis at time of hospi-
patients with pulmonary tuberculosis in Ibadan, Nigeria. African talization predict mortality in patients with community-acquired pneu-
Journal of Medicine and Medical Sciences 32: 239–242. monia. Chest 137: 416–420.
22. Das, B.S., U. Devi, C. Mohan Rao, V.K. Srivastava, P.K. Rath, and B.S. 35. Sunbul M, Gerin F, Durmus E, Kivrak T, Sari I, Tigen K, Cincin A.
Das. 2003. Effect of iron supplementation on mild to moderate anaemia 2013. Neutrophil to lymphocyte and platelet to lymphocyte ratio in
in pulmonary tuberculosis. British Journal of Nutrition 90: 541–550. patients with dipper versus non-dipper hypertension. Clin Exp
23. Akintunde, E.O., W.A. Shokunbi, and C.O. Adekunle. 1995. Leuco- Hypertens.
cyte count, platelet count and erythrocyte sedimentation rate in pul- 36. Yavuzcan, A., M. Caglar, Y. Ustun, S. Dilbaz, I. Ozdemir, E. Yildiz, A.
monary tuberculosis. African Journal of Medicine and Medical Ozkara, and S. Kumru. 2013. Evaluation of mean platelet volume,
Sciences 24: 131–134. neutrophil/lymphocyte ratio and platelet/lymphocyte ratio in advanced
24. Kang, Y.A., S.Y. Kwon, H.I. Yoon, J.H. Lee, and C.T. Lee. 2009. Role stage endometriosis with endometrioma. Journal of the Turkish
of C-reactive protein and procalcitonin in differentiation of tuberculo- German Gynecological Association 14: 210–215.
sis from bacterial community acquired pneumonia. Korean Journal of 37. Feng, J.F., Y. Huang, Q. Zhao, and Q.X. Chen. 2013. Clinical signif-
Internal Medicine 24: 337–342. icance of preoperative neutrophil lymphocyte ratio versus platelet
25. Celikbilek, M., S. Dogan, O. Ozbakır, G. Zararsız, H. Kücük, S. lymphocyte ratio in patients with small cell carcinoma of the esoph-
Gürsoy, A. Yurci, K. Güven, and M. Yücesoy. 2013. Neutrophil– agus. ScientificWorldJournal 2013: 504365.

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