Bhat 2013
Bhat 2013
Tariq Bhat*1, Sumaya The role of inflammatory markers in cardiovascular diseases has been studied extensively and a
Teli2, Jharendra consistent relationship between various inflammatory markers and cardiovascular diseases has
Rijal3, Hilal Bhat4, been established in the past. Neutrophil to lymphocyte ratio (NLR) is a new addition to the long
list of these inflammatory markers. NLR, which is calculated from complete blood count with
Muhammad Raza3,
differential, is an inexpensive, easy to obtain, widely available marker of inflammation, which
Georges Khoueiry1, can aid in the risk stratification of patients with various cardiovascular diseases in addition to
Mustafain Meghani3, the traditionally used markers. It has been associated with arterial stiffness and high coronary
Muhammad Akhtar1 calcium score, which are themselves significant markers of cardiovascular disease. NLR is reported
and Thomas as an independent predictor of outcome in stable coronary artery disease, as well as a predictor
Costantino1 of short- and long-term mortality in patients with acute coronary syndromes. It is linked with
1
Division of Cardiology, Staten Island
increased risk of ventricular arrhythmias during percutaneous coronary intervention (PCI) and
University Hospital New York, 475 higher long-term mortality in patients undergoing PCI irrespective of indications of PCI. In
Seaview Ave, Staten Island, New York, patients admitted with advanced heart failure, high NLR was reported with higher inpatient
NY 10305, USA mortality. Recently, NLR has been reported as a prognostic marker for outcome from coronary
2
University of Sheffield, School of
Medicine, Sheffield, UK artery bypass grafting and postcoronary artery bypass grafting atrial fibrillation.
3
Department of Medicine, Staten Island
University Hospital New York, 475 Keywords: cardiovascular disease • neutrophil to lymphocyte ratio
Seaview Ave, Staten Island, New York,
NY 10305, USA
4
Department of Medicine, SK Institute Multiple studies have shown a strong and con- Significant evidence has suggested a possible role
of Medical Sciences, Soura, Kashmir,
sistent relationship between inflammation mark- of N count as an independent prognostic factor
India
*Author for correspondence: ers and cardiovascular diseases [1–6] . C-reactive in both acute as well as chronic cardiovascular
Tel.: +1 718 226 9000 protein (CRP) has been studied extensively diseases, which is also supported by some labora-
[email protected]
among all the inflammatory markers and has tory studies explaining different mechanism of
still been in focus in recent studies [3,7] . Being this association [8] . Elevated M count was also
a simple, readily available and inexpensive test, found to carry increased risk in cardiovascular
total white blood cell (WBC) count, has been diseases [10] . The recent remarkable observation
in focus for the last two decades and it has been has been that a ratio of N to L count (NLR) has
suggested in multiple studies that a high level a greater predictability than total WBC count
of total WBC count is not only an independent or N count as a marker in cardiovascular dis-
risk factor for major cardiovascular diseases but eases and is slowly emerging as an independent
can prognosticate outcome of many cardiovas- useful prognostic parameter in cardiovascular
cular diseases [1,4,6,8] . Despite all these studies, diseases [11,12] .
total WBC count has not been explored and The predictive superiority of NLR may be due
exploited for its utility in predicting cardiovas- to many reasons including the fact that it is less
cular risk. It has recently been proposed as one likely to be influenced by various physiological
of the potential biomarkers for risk assessment conditions such as dehydration and exercise,
in cardiovascular disease [9] . even though these conditions may affect abso-
There has been a recent focus on differential lute number of individual cell types. Second
white cell count, and identification of a particu- and most importantly, NLR is a ratio of two
lar cell type (neutrophil [N], lymphocyte [L] different yet complementary immune pathways,
and monocyte [M]) as a stronger predictor of thus integrating the deleterious effects of Ns,
cardiovascular risk than the total WBC count. which are responsible for active nonspecific
inflammation and lymphopenia, which is a marker of poor gen- angiography, NLR was higher in the progressive group (5.0 ± 5.1
eral heath and physiological stress [13] . Thus, NLR, being an vs 3.2 ± 3.0; p = 0.001) compared with the nonprogressive group
integrated reflection of two important and opposite immune and progression rate of atherosclerosis was significantly higher
pathways, is more predictive than either parameter alone. (56 vs 39%; p = 0.03) in patients with high NLR [14] .
In this brief review, the authors will provide a useful summary
of the evidence available in literature about the association of NLR & acute coronary syndrome
NLR with various cardiovascular diseases and its possibility of Acute coronary syndrome (ACS) is one of the commonest admit-
emerging as a cheap, reliable and independent prognostic marker ting diagnoses in the emergency department all over the USA.
of cardiovascular disease. Approximately 6 million emergency room visits per year are for
chest pain in USA [17] . Owing to the high mortality of ACS,
NLR & stable coronary artery disease different modalities have been utilized to increase the efficacy of
Elevated NLR, independently and in interaction with other identifying them earlier, which include use of high-sensitive tro-
disease markers and risk factors, is a significant predictor of ponin; emergency-room-based computed tomography coronary
mortality in stable coronary artery disease (CAD), as well as its angiographic evaluation of chest pain and creation of separate
development and progression [11,12,14–16] . Horne et al. were among fast-track chest pain unit [18–20] . The question of whether NLR
the first to observe the significance of NLR in stable CAD. In on admission has any diagnostic utility in patients admitted
their prospective observational study, more than 3000 patients with chest pain was studied by Zazula et al. Patients diagnosed
without acute myocardial infarction (MI) and with angiographi- with noncardiac chest pain reported lowest admission NLR
cally assessed CAD were followed for more than 6 years [11] . The (3 ± 1.6), followed by unstable angina (3.6 ± 2.9), non-ST-ele-
predictive ability for death/MI of quartile (Q) 4 versus Q1 total vation MI (4.8 ± 3.7) and ST-elevation MI (STEMI) (6.9 ± 5.7)
WBC, N, L and M counts, and NLR were assessed using Cox (p < 0.0001) [21] . NLR above 5.7 reported 91% specificity and
regressions. Total WBC count was confirmed to be an inde- 4.51 odds ratio for the final diagnosis of ACS when compared
pendent predictor of death/MI in patients with or at high risk with the groups with NLR <3.0 (p < 0.001) [21] . Being an inex-
for CAD, but greater predictive ability is provided by high N pensive and reproducible predictive marker, NLR can be of rel-
(Q4 > 6.6 × 103/μl) or low L counts. The greatest risk prediction evance while evaluating chest pain. Elevated CRP and NLR,
is given by the N/L ratio, with Q4 versus Q1 (>4.71 vs >1.96) markers of underlying acute-phase inflammation, serve as indica-
increasing the hazard by 2.2-fold. They reported that incremental tor for thrombus formation in patients with acute MI. Compared
improvement in risk prediction achieved with WBC differential with the patients with acute MI and no thrombus formation,
was similar to or greater than that reported for high-sensitive the levels of high-sensitivity CRP, total N count and NLR were
CRP [11] . Another prospective study analyzed the predictive abil- substantially higher (p < 0.05) in the patients with acute MI and
ity for cardiac events of differential WBC against established risk thrombus formation [22] .
factors in angiographically proven CAD patients. They evaluated Risk stratification and prediction of outcome is of enormous
complete blood count, and other biomarkers of inflammation: importance in management of CAD. There are multiple scor-
(CRP and serum iron), fasting glucose, total, HDL and LDL ing systems in clinical practice utilized for risk stratification of
cholesterol) and established risk factors in 422 patients. High patients diagnosed with ACS. NLR itself is not part of any risk
NLR (5.19 ± 3.81), together with CRP, left ventricular ejection stratification scoring system even though multiple studies have
fraction, fasting glucose, HDL and serum iron, was associated elucidated this association. High NLR has been associated with
with significantly (p = 0.02) increased cardiac death and nonfatal poor outcomes in patients with ACS [23] . In-hospital mortality
MI in patients with stable CAD on a 3-year follow-up. Event-free (8.5 vs 1.8%; p = 0.013) and 6-month mortality (11.5 vs 2.5%;
survival according to NLR tertiles was 99% for the first tertile p < 0.001) were found to be significantly higher in patients with
(1.23 ± 0.26), 96.5% for the second (2.05 ± 0.29) and 88.8% for ACS with high NLR compared with those with low NLR [24] .
the third (5.19 ± 3.81) [12] . Over a mean follow-up of 32 months in patients with CAD
In a large Asian cohort of high-risk patients, (patients with who had undergone percutaneous coronary angioplasty, the
diabetes mellitus and metabolic syndrome) NLR was associated best survival was seen in patients with low NLR (1.7 ± 0.5) and
with both metabolic syndrome and risk of ischemic cardiovascu- an increased mortality seen in patients with NLR ≥3.2 ± 0.6
lar diseases [16] . Association between NLR and other established (p < 0.0001) [25] . After adjusting for age, chronic obstructive pul-
indirect markers of cardiovascular disease like coronary calcium monary disease, left ventricular ejection fraction, serum hemo-
score (CCS) was studied in more than 800 Korean adult patients. globin, serum creatinine and lesion severity, the log NLR was an
The degree of atherosclerosis or arterial stiffness, measured by independent significant predictor of long-term mortality (hazard
brachial–ankle pulse-wave velocity and CCS, was associated to ratio; 1.85, p = 0.01) in CAD after percutaneous coronary inter-
NLR as higher scores among the patients with high NLR ≥2.5 vention (PCI) [25] . During median follow-up to 3.6 years in
(p < 0.001 for brachial–ankle pulse-wave velocity and p = 0.032 African–American patients undergoing PCI, mortality rate was
for CCS) [15] . A recent interesting observation about angiographic high with 31.1% in the group with preprocedural NLR ≥3.5
progression of coronary atherosclerosis by Kalay et al. reported whereas it was only 10.4% in the group with preprocedural
that among the patients with CAD requiring repeat coronary NLR <3.5 (p < 0.001) [26] .
Patients with non-STEMI and NLR >4.7 had significantly cohort study, NLR was found to be a significant marker of fre-
higher in-patient and 4-year mortality rate (29.8 vs 8.4%) com- quent decompensation and long-term mortality in patients with
pared with those with NLR <3 (p < 0.0001) [13] . Among the CHF. During 26-month median follow-up of more than 1000
patients with STEMI, long-term mortality was significantly patients with ADHF, a positive trend between death and NLR
higher (47.9 vs 6.4%, p < 0.001) in the group with maximum was observed, 32.8, 23.2 and 14.2% of deaths occurred in patients
NLR compared with those with lowest NLR [27] . Compared with with admission NLR of 9.6 (7.6–13.1), 5.1(4.5–5.8) and 2.8
patient groups with STEMI undergoing PCI who had low NLR (2.2–3.8) (p < 0.001), respectively [40] . Similarly, ADHF patients
and no anemia, and those with low NLR and anemia on admis- with high NLR (≥7.6) had significantly higher 30-day readmission
sion, 6-month mortality was higher (p = 0.036) in those patients rate (p < 0.001) compared with those with lower NLR [40] .
with high NLR and anemia [28] . It clearly suggests that combined
use of hemoglobin level and NLR provides timely information for NLR & coronary artery bypass surgery
early risk stratification in patients with STEMI undergoing PCI. NLR, by integrating information on inflammatory milieu and
In summary, NLR has been consistently shown to be an inde- physiologic stress, can serve as a prognostic marker for post
pendent risk marker for ACS both in the short term as well as operative AF and outcome from coronary artery bypass grafting
long term but similar association was not found by Kruk et al. (CABG) surgery. Elevated preoperative NLR has been associ-
in their more than 1000 with unselected patients STEMI, only ated with worse outcome after CABG. During 3.6-year follow-
high-sensitivity CRP and WBC count independent of each up in patients undergoing CABG, mortality (hazard ratio: 1.13,
other predicted early outcome in STEMI patients treated with p < 0.001) was significantly high in the group who had preopera-
primary PCI [29] . tive NLR >3.36 (p < 0.001) [41] . In a prospective cohort study in
the patients undergoing nonemergency CABG who developed
NLR & cardiac arrythmias AF lasting >30 s, preoperative NLR was greater (median: 3.0 vs
The association between inflammation and atrial fibrillation (AF) 2.4, p < 0.001) and postoperative NLR was also significantly high
is well known [2] , and has been studied extensively. Even though (day 2, median: 9.2 vs 7.2; p < 0.001) [42] .
various inflammatory markers have been associated with inci-
dence, recurrence and outcome in AF, association of NLR has Expert commentary
not been much looked into in this group of patients. Despite multiple loopholes and weaknesses in the evidence
Association of inflammation and inflammatory markers in described in this review, the relationship between NLR and the
other arrythmias, especially ventricular arrythmia, is not well various cardiovascular diseases and their outcomes is strengthened
elucidated or understood, and the minimal available evidence is by the fact that most of the results are uniform and consistent. This
conflicting [30–33] . consistent correlation between various cardiovascular disease and
Chatterjee et al. in a retrospective study in patients undergoing NLR is of more significance because of the potential application of
PCI, reported that preprocedural elevated WBC count, neutro- this inexpensive and easily available marker for risk stratification of
philia and elevated NLR were significant predictors of ventricular these patients. The predictive superiority of NLR over WBC and
arrythmias [34] . For all the patients developing ventricular arryth- other individual cell types due to being less likely influenced by
mia during PCI compared with a random group, significantly various physiological conditions and its integrated reflection of two
higher preprocedural total WBC count (means: 14,344 vs 6852; important and opposite immune pathways; may elevate its role as a
p = 0.0004), N count (mean: 75.79 vs 58.06%, p < 0.0001) and risk stratification marker. More robust prospective and randomized
NLR (mean: 3.79 vs 1.56, p < 0.0001) were found in this study. studies may help in finding a clear position for NLR among various
Thus, it is evident that the evidence is not enough to make any markers of risk stratification in cardiovascular diseases.
conclusion on association of NLR and various cardic arrythmias.
Five-year view
NLR & heart failure The science of biomarkers is a highly promising aspect of medi-
Previous studies have shown that inflammatory markers such as cine that is, and will, redefine the whole process of disease man-
increased WBC counts can be associated with increased incidence agement in the near future. Biomarkers are being utilized in
of heart failure hospitalization and mortality [35,36] . Relative, neu- diagnosing various diseases and they can also prognosticate both
trophilia has been associated with increased incidence of acute long- and short-term outcomes. They will soon help us in identi-
decompensated heart failure (ADHF) in patients admitted with fying at-risk populations early, leading to primary prevention of
acute MIs [37] . In a retrospective study of patients who developed many of these disorders. The role of the available new biomark-
congestive heart failure (CHF) within the first 4 days after acute ers in our clinical practice is expected to grow tremendously in
MI, 92.5% had relative neutrophilia on admission (N percent- coming years. The exponentially growing burden of health cost
age >65%) compared with 45% of those in whom CHF did not will have a greater influence in the coming years on develop-
develop [38] . In addition, relative lymphocytopenia has shown ment and application of these markers in daily clinical practice.
to be an independent predictor of mortality in heart failure [39] . The inexpensive and readily available markers like NLR have a
The role of elevated NLR in heart failure incidence and its out- greater potential in the coming years given the circumstance to
come has not been dwelled on much. In a recent large prospective surface as useful maker of cardiovascular disease.
www.expert-reviews.com 57
Review Bhat, Teli, Rijal et al.
Financial & competing interests disclosure This includes employment, consultancies, honoraria, stock ownership
The authors have no relevant affiliations or financial involvement with or options, expert testimony, grants or patents received or pending, or
any organization or entity with a financial interest in or financial con- royalties.
flict with the subject matter or materials discussed in the manuscript. No writing assistance was utilized in the production of this manuscript.
Key issues
• The relationship between inflammatory markers and cardiovascular diseases is well established.
• Among these inflammatory markers, neutrophil to lymphocyte ratio (NLR) has been a new addition to a long list of these markers.
• NLR is a cheap, easy to calculate and readily available marker that can aid in the risk stratification of patients with various cardiovascular
diseases.
• Elevated NLR is associated with arterial stiffness, high coronary calcium scores and progression of atherosclerosis.
• High NLR is an independent predictor of mortality in stable coronary artery disease, and various acute coronary syndromes including
non-ST-elevation myocardial infarction and ST-elevation myocardial infarction.
• Elevated NLR is associated with increased risk of ventricular arrhythmias during percutaneous coronary intervention (PCI) and increased
long-term mortality in patients undergoing PCI irrespective of indications for PCI.
• Elevated NLR has been associated with higher inpatient mortality in patients admitted with advanced heart failure and an increased
incidence of new-onset atrial fibrillation in patients after coronary artery bypass grafting.
References 7 Ridker PM, Danielson E, Fonseca FA et al.; 13 Azab B, Zaher M, Weiserbs KF et al.
JUPITER Study Group. Rosuvastatin to Usefulness of neutrophil to lymphocyte
1 Ates AH, Canpolat U, Yorgun H et al.
prevent vascular events in men and women ratio in predicting short- and long-term
Total white blood cell count is associated
with elevated C-reactive protein. N. Engl. J. mortality after non-ST-elevation
with the presence, severity and extent of
Med. 359(21), 2195–2207 (2008). myocardial infarction. Am. J. Cardiol.
coronary atherosclerosis detected by
8 Guasti L, Dentali F, Castiglioni L et al. 106(4), 470–476 (2010).
dual-source multislice computed
tomographic coronary angiography. Neutrophils and clinical outcomes in 14 Kalay N, Dogdu O, Koc F et al.
Cardiol. J. 18(4), 371–377 (2011). patients with acute coronary syndromes Hematologic parameters and angiographic
and/or cardiac revascularisation. A progression of coronary atherosclerosis.
2 Aviles RJ, Martin DO, Apperson-Hansen
systematic review on more than 34,000 Angiology 63(3), 213–217 (2012).
C et al. Inflammation as a risk factor for
subjects. Thromb. Haemost. 106(4), 15 Park BJ, Shim JY, Lee HR et al.
atrial fibrillation. Circulation 108(24),
591–599 (2011). Relationship of neutrophil–lymphocyte
3006–3010 (2003).
9 Pearson TA, Mensah GA, Alexander RW ratio with arterial stiffness and coronary
3 Buckley DI, Fu R, Freeman M, Rogers K,
et al.; Centers for Disease Control and calcium score. Clin. Chim. Acta
Helfand M. C-reactive protein as a risk
Prevention; American Heart Association. 412(11–12), 925–929 (2011).
factor for coronary heart disease:
Markers of inflammation and cardiovascu- 16 Tsai JC, Sheu SH, Chiu HC et al.
a systematic review and meta-analyses for
lar disease: application to clinical and Association of peripheral total and
the U.S. Preventive Services Task Force.
public health practice: A statement for differential leukocyte counts with
Ann. Intern. Med. 151(7), 483–495 (2009).
healthcare professionals from the Centers metabolic syndrome and risk of ischemic
4 Danesh J, Collins R, Appleby P, Peto R. for Disease Control and Prevention and the cardiovascular diseases in patients with
Association of fibrinogen, C-reactive American Heart Association. Circulation Type 2 diabetes mellitus. Diabetes Metab.
protein, albumin, or leukocyte count with 107(3), 499–511 (2003). Res. Rev. 23(2), 111–118 (2007).
coronary heart disease: meta-analyses of
10 Olivares R, Ducimetière P, Claude JR. 17 McCaig LF, Burt CW. National Hospital
prospective studies. JAMA 279(18),
Monocyte count: a risk factor for coronary Ambulatory Medical Care Survey: 1999
1477–1482 (1998).
heart disease? Am. J. Epidemiol. 137(1), emergency department summary. Adv.
5 Ensrud K, Grimm RH Jr. The white blood 49–53 (1993). Data 320, 1–34 (2001).
cell count and risk for coronary heart
11 Horne BD, Anderson JL, John JM et al.; 18 Takakuwa KM, Halpern EJ. Evaluation of
disease. Am. Heart J. 124(1), 207–213
Intermountain Heart Collaborative Study a ‘triple rule-out’ coronary CT a ngiography
(1992).
Group. Which white blood cell subtypes protocol: use of 64-Section CT in
6 Lee CD, Folsom AR, Nieto FJ, Chambless predict increased cardiovascular risk? low-to-moderate risk emergency depart-
LE, Shahar E, Wolfe DA. White blood cell J. Am. Coll. Cardiol. 45(10), 1638–1643 ment patients suspected of having acute
count and incidence of coronary heart (2005). coronary syndrome. Radiology 248(2),
disease and ischemic stroke and mortality
12 Papa A, Emdin M, Passino C, Michelassi 438–446 (2008).
from cardiovascular disease in African–
C, Battaglia D, Cocci F. Predictive value of 19 Romagnoli A, Martuscelli E, Sperandio M
American and White men and women:
elevated neutrophil–lymphocyte ratio on et al. Role of 64-slice cardiac computed
atherosclerosis risk in communities study.
cardiac mortality in patients with stable tomography in the evaluation of patients
Am. J. Epidemiol. 154(8), 758–764 (2001).
coronary artery disease. Clin. Chim. Acta with non-ST-elevation acute coronary
395(1–2), 27–31 (2008).
syndrome. Radiol. Med. 115(3), 341–353 segment elevation myocardial infarction. Cardiovasc. Hematol. Disord. Drug Targets
(2010). Am. J. Cardiol. 101(6), 747–752 (2008). 11(2), 58–60 (2011).
20 Mingels AM, Joosen IA, Versteylen MO 28 Cho KH, Jeong MH, Ahmed K et al. Value 35 Cooper HA, Exner DV, Waclawiw MA,
et al. High-sensitivity cardiac troponin T: of early risk stratification using hemoglobin Domanski MJ. White blood cell count and
risk stratification tool in patients with level and neutrophil-to-lymphocyte ratio in mortality in patients with ischemic and
symptoms of chest discomfort. PLoS ONE patients with ST-elevation myocardial nonischemic left ventricular systolic
7(4), e35059 (2012). infarction undergoing primary dysfunction (an analysis of the Studies Of
21 Zazula AD, Précoma-Neto D, Gomes AM percutaneous coronary intervention. Am. J. Left Ventricular Dysfunction [SOLVD]).
et al. An assessment of neutrophils/ Cardiol. 107(6), 849–856 (2011). Am. J. Cardiol. 84(3), 252–257 (1999).
lymphocytes ratio in patients suspected of 29 Kruk M, Przyluski J, Kalinczuk L et al.; 36 Engström G, Melander O, Hedblad B.
acute coronary syndrome. Arq. Bras. ANIN Myocardial Infarction Registry Leukocyte count and incidence of
Cardiol. 90(1), 31–36 (2008). Group. Association of non-specific hospitalizations due to heart failure. Circ.
22 Li DB, Hua Q, Liu Z et al. Association inflammatory activation with early Heart Fail. 2(3), 217–222 (2009).
between inflammatory mediators and mortality in patients with ST-elevation 37 Arruda-Olson AM, Reeder GS, Bell MR,
angiographic morphologic features acute coronary syndrome treated with Weston SA, Roger VL. Neutrophilia
indicating thrombus formation in patients primary angioplasty. Circ. J. 72(2), predicts death and heart failure after
with acute myocardial infarction. Chin. 205–211 (2008). myocardial infarction: a community-based
Med. J. 122(15), 1738–1742 (2009). 30 Blangy H, Sadoul N, Dousset B et al. study. Circ. Cardiovasc. Qual. Outcomes
23 Muhmmed Suliman MA, Bahnacy Juma Serum BNP, hs-C-reactive protein, 2(6), 656–662 (2009).
AA, Ali Almadhani AA, Pathare AV, procollagen to assess the risk of ventricular 38 Kyne L, Hausdorff JM, Knight E, Dukas
Alkindi SS, Uwe Werner F. Predictive value tachycardia in ICD recipients after L, Azhar G, Wei JY. Neutrophilia and
of neutrophil to lymphocyte ratio in myocardial infarction. Europace 9(9), congestive heart failure after acute
outcomes of patients with acute coronary 724–729 (2007). myocardial infarction. Am. Heart J.
syndrome. Arch. Med. Res. 41(8), 618–622 31 Konstantino Y, Kusniec J, Reshef T et al. 139(1 Pt 1), 94–100 (2000).
(2010). Inflammatory biomarkers are not predictive 39 Rudiger A, Burckhardt OA, Harpes P,
24 Tamhane UU, Aneja S, Montgomery D, of intermediate-term risk of ventricular Müller SA, Follath F. The relative
Rogers EK, Eagle KA, Gurm HS. tachyarrhythmias in stable CHF patients. lymphocyte count on hospital admission is
Association between admission neutrophil Clin. Cardiol. 30(8), 408–413 (2007). a risk factor for long-term mortality in
to lymphocyte ratio and outcomes in 32 Volk T, Schmutzler M, Engelhardt L et al. patients with acute heart failure. Am. J.
patients with acute coronary syndrome. Effects of different steroid treatment on Emerg. Med. 24(4), 451–454 (2006).
Am. J. Cardiol. 102(6), 653–657 (2008). reperfusion-associated production of 40 Uthamalingam S, Patvardhan EA,
25 Duffy BK, Gurm HS, Rajagopal V, Gupta reactive oxygen species and arrhythmias Subramanian S et al. Utility of the
R, Ellis SG, Bhatt DL. Usefulness of an during coronary surgery. Acta Anaesthesiol. neutrophil to lymphocyte ratio in
elevated neutrophil to lymphocyte ratio in Scand. 47(6), 667–674 (2003). predicting long-term outcomes in acute
predicting long-term mortality after 33 Wu KC, Gerstenblith G, Guallar E et al. decompensated heart failure. Am. J.
percutaneous coronary intervention. Am. J. Combined cardiac magnetic resonance Cardiol. 107(3), 433–438 (2011).
Cardiol. 97(7), 993–996 (2006). imaging and C-reactive protein levels 41 Gibson PH, Croal BL, Cuthbertson BH
26 Poludasu S, Cavusoglu E, Khan W, identify a cohort at low risk for defibrillator et al. Preoperative neutrophil–lymphocyte
Marmur JD. Neutrophil to lymphocyte firings and death. Circ. Cardiovasc. Imaging ratio and outcome from coronary artery
ratio as a predictor of long-term mortality 5(2), 178–186 (2012). bypass grafting. Am. Heart J. 154(5),
in African Americans undergoing 34 Chatterjee S, Chandra P, Guha G, Kalra V, 995–1002 (2007).
percutaneous coronary intervention. Clin. Chakraborty A, Frankel R. Pre-procedural 42 Gibson PH, Cuthbertson BH, Croal BL
Cardiol. 32(12), E6–E10 (2009). elevated white blood cell count and et al. Usefulness of neutrophil/lymphocyte
27 Núñez J, Núñez E, Bodí V et al. Usefulness neutrophil–lymphocyte (N/L) ratio are ratio as predictor of new-onset atrial
of the neutrophil to lymphocyte ratio in predictors of ventricular arrhythmias fibrillation after coronary artery bypass
predicting long-term mortality in ST during percutaneous coronary intervention. grafting. Am. J. Cardiol. 105(2), 186–191
(2010).
www.expert-reviews.com 59