American Journal of Emergency Medicine 34 (2016) 403406

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American Journal of Emergency Medicine

journal homepage: www.elsevier.com/locate/ajem

Original Contribution

Is the neutrophil-to-lymphocyte ratio a potential diagnostic marker for

peptic ulcer perforation? A retrospective cohort study
Yusuf Tanrikulu, MD a,, Ceren Sen Tanrikulu, MD b, Mehmet Zafer Sabuncuoglu, MD c, Furuzan Kokturk, PhD d,
Volkan Temi, MD a, Ercan Bicakci, MD e
a
Department of General Surgery, Zonguldak Ataturk State Hospital, Zonguldak, Turkey
b
Department of Emergency Medicine, Bulent Ecevit University Faculty of Medicine, Zonguldak, Turkey
c
Department of General Surgery, Sleyman Demirel University Faculty of Medicine, Isparta, Turkey
d
Department of Biostatistics, Bulent Ecevit University Faculty of Medicine, Zonguldak, Turkey
e
Department of Gastroenterology, Zonguldak Ataturk State Hospital, Zonguldak, Turkey

a r t i c l e i n f o a b s t r a c t

Article history: Objectives: Peptic ulcer perforation (PUP) accounts for 5% of all abdominal emergencies and is recognized as a
Received 28 September 2015 gastrointestinal emergency requiring rapid and efcient clinical evaluation and treatment. The mortality rate
Received in revised form 17 October 2015 ranges from 10% to 40% among patients with perforation. In the present retrospective study, we examined the
Accepted 6 November 2015 potential utility of the neutrophil-to-lymphocyte ratio (NLR) in early diagnosis of PUP; we asked whether this
ratio allowed PUP and peptic ulcer disease to be distinguished.
Methods: We enrolled the following patients: 58 with PUP, 62 with noncomplicated peptic ulcer diseases (NCPU),
and 62 controls, between May 2010 and 2015. Patients who underwent surgical repair to treat PUP were included
in the study group. Another group consisted of NCPU patients who had a noncomplicated peptic ulcer. The con-
trol group consisted of patients presenting with nonspecic abdominal pain to the emergency department.
Results: The mortality rate was 5.2% in the PUP group. The white blood cell count, C-reactive protein, and NLRs
were higher in the PUP compared to the other groups (P b .001 for all). The white blood cell count and NLR
did not differ between the NCPU and control groups. The sensitivities, specicities, positive predictive values,
and negative predictive values of the NLRs were 68.0%, 88.0%, 82.9%, and 72.9%, respectively.
Conclusions: We suggest that preoperative NLR aids in the diagnosis of PUP and can be used to distinguish this
condition from peptic ulcer disease. Thus, the NLR should be calculated in addition to the clinical examination.
2015 Elsevier Inc. All rights reserved.

1. Introduction
Peptic ulcer disease (PUD), one of the most common gastrointestinal
disorders, affects 4 million people annually worldwide [1]. Despite our
advanced understanding of the multifactorial etiology of PUD, life-
threatening complications, including hemorrhage or perforation, occur
in a signicant proportion of patients [2]. Peptic ulcer perforation
(PUP) is the most serious complication associated with PUD, accounting
for 5% of all abdominal emergencies [3]. The mortality rate ranges from
10% to 40% among patients with perforation, which is 10-fold higher
compared to other abdominal emergencies such as acute appendicitis
and acute cholecystitis [4,5].
Currently, there is no criterion standard for the diagnosis of PUP, and
patient history is the most important contributor to determining this di-
agnosis. Indeed, diagnosing the condition is very difcult in patients
with no previous history of PUD. However, the sudden onset of severe
abdominal pain, vomiting, shock, and classical signs of peritonitis,
Corresponding author at: Zonguldak Atatrk Devlet Hastanesi, Genel Cerrahi Klinii,
67100 Zonguldak, Turkey. Tel.: +90 505 657 9709; fax: +90 372 259 1900.
E-mail address: drtanrikulu@hotmail.com (Y. Tanrikulu).
such as the presence of defense and rebound in a patient with a previous
history of PUD, suggests a diagnosis of perforation [6].
The optimal treatment of PUP is surgery. Delay in diagnosis and sur-
gical treatment is associated with high morbidity and mortality, and
early recognition accompanied by aggressive resuscitation and early
surgical intervention will clearly help to maintain low morbidity and
mortality [6,7].
Gastric colonization with Helicobacter pylori results in peptic ulcers,
and the outcome of infection is dependent on reciprocal interactions be-
tween bacterial pathogenic factors and the host response [8]. Several
studies have indicated a positive association between coronary heart
disease and H pylori and have demonstrated that the mechanisms of
this relationship are an induction of dyslipidemic alterations; brinogen
elevation; induction of inammatory parameters, such as C-reactive
protein (CRP), and white blood cells (WBCs); and an induction of hyper-
coagulability [9,10]. In addition, an acute inammatory response and
consequent mucosal damage occur in many cases of perforation [11,12].
To predict the prognosis of inammatory diseases, several
inammation-based scoring systems have been suggested, including
the platelet-to-lymphocyte ratio, prognostic nutritional index, and
neutrophil-to-lymphocyte ratio (NLR) [13]. The NLR, derived from

http://dx.doi.org/10.1016/j.ajem.2015.11.009
0735-6757/ 2015 Elsevier Inc. All rights reserved.
404 Y. Tanrikulu et al. / American Journal of Emergency Medicine 34 (2016) 403406
counts of circulating neutrophils and lymphocytes, has received great
interest because it can be measured noninvasively, is easily detected
in peripheral blood, and does not require additional cost.
Recent studies have focused on such materials because early and
accurate detection of inammation is essential to optimizing the treat-
ment and prognosis of patients with medical emergencies [14]. Several
biomarkers, such as CRP, procalcitonin, and mean platelet volume
(MPV), have been used as indicators of inammation. Neutrophilia de-
velops during inammation and is triggered by the release of arachi-
donic acid metabolites and platelet activation. Such stress induces
relative lymphopenia. Thus, NLR accurately reects underlying inam-
matory processes. Although several studies have explored the utility
of the NLR in the diagnosis and prognosis of inammatory and malig-
nant diseases, there has been no study to date that applies the NLR to di-
agnose peptic ulcer [15,16]. In the present study, we evaluated the
diagnostic utility of the NLR compared to traditional parameters in pa-
tients with peptic ulcer perforation.
2. Methods
2.1. Study groups and study design
This was a retrospective, cross-sectional study approved by our local
ethics committee. We enrolled 58 patients with PUP, 62 patients with
noncomplicated peptic ulcer diseases (NCPU), and 62 control patients.
All patients were enrolled between 1 May 2010 and 30 April 2015. Ar-
chived and electronically stored records were accessed. Prestudy
power analysis showed that the chosen sample size afforded a power
of 0.9 for achievement of a 95% condence interval.
Patients were divided into 3 groups: PUP, NCPU, and controls.
1. PUP group: Patients who underwent surgical repair to treat PUP
were included in this group. Diagnosis of patients with suspected
peptic ulcer perforation according to the clinical (presence of defense
and rebound), radiologic (presence of subdiaphragmatic free air),
and laboratory evaluation (presence of high inammatory parame-
ters) were conrmed using abdominal tomography. Intraoperative
assessment was performed for a denitive diagnosis. Intraoperative-
ly, patients without PUP were excluded from the study.
2. NCPU group: Patients who had a noncomplicated peptic ulcer were
included in this group. These patients were recruited from the gas-
troenterology clinic. Endoscopic evaluation was performed in all
patients. Patients who were diagnosed for peptic ulcer in endoscopic
evaluation and histopathologically conrmed were included in
this study.
3. Control group: This group consisted of patients presenting with ab-
dominal pain to the emergency department. These patients had
only nonspecic and colicky abdominal pain, and the laboratory
and radiologic ndings of patients in this group were normal. In ad-
dition, these patients did not have additional comorbid disease.
2.2. Complete blood count and biochemical analysis
All biochemical tests and complete blood counts (CBCs) (on venous
blood) were automated. Complete blood count data obtained from all 3
hospitals were similar to the recognized international norms. White
blood cell counts, MPVs, and red cell distribution widths (RDWs) were
evaluated. Neutrophil-to-lymphocyte ratios were calculated. The nor-
mal values of all parameters were the reference gures accepted by he-
matology laboratories nationwide.
2.3. Statistical analysis
All statistical analyses were performed using SPSS version 19.0 soft-
ware (SPSS, Inc, Chicago, IL). The data distribution was evaluated using
the Kolmogorov-Smirnov test. Continuous variables are expressed as
the mean SDs, and categorical variables are expressed as frequencies
(percentages). The signicance of each difference between continuous
variables was examined using the independent-samples t test or the
Mann-Whitney U test. The signicance of each difference between cat-
egorical variables was compared using Pearson 2 test. Receiver operat-
ing characteristic (ROC) curve analysis was used to dene the optimal
cutoffs of the NLR and RDW, for which specicities, sensitivities, positive
and negative predictive values, and overall accuracies were calculated.
Youden index was used to optimize the accuracies of all calculations. P
b .05 was considered to reect statistical signicance.
3. Results
We enrolled 58 PUP, 62 NCPU, and 62 control patients. The mean pa-
tient age did not differ signicantly among groups, which were 48.06,
52.04, and 55.28 years, respectively. Of the PUP patients, 13 (26.0%)
were female and 37 (74.0%) were male; 28 (56.0%) NCPU patients
were female and 22 (44.0%) were male; and 32 (64.0%) control patients
were female and 18 (36%) were male. The mortality rate was 5.17% (3
patients) in the PUP group.
The WBC counts, CRP levels, RDWs, MPVs, and NLRs are shown in
Table 1. The WBC count, CRP level, and NLRs were signicantly higher
in the PUP compared to other groups (P b .001 for all). Although
the WBC and NLR did not differ between the NCPU and the control
groups, the CRP in the NCPU was signicantly higher in the control
group (P = .022).
The sensitivities and specicities of the CRP levels and CBC data used
to distinguish control and PUP patients and ROC data on WBC counts,
CRP, and NLRs are shown in Table 2 and Fig. 1. The sensitivities, specic-
ities, positive predictive values (PPVs), and negative predictive values
(NPVs) of the NLRs were 68.0%, 88.0%, 82.9%, and 72.9%, respectively.
Receiver operating characteristic curve analysis showed that the cutoff
values for the WBC count, CRP level, MPV, and NLR yielded the best sen-
sitivities and specicities, which were 11.22 109/L (56%-96%), 1.10
mg/dL (66%-98%), 9.10 f. (46%-70%), and 5.45 (68%-88%), respectively.
The areas under the curves for the WBC count, CRP, and NLR were
78.8%, 85.1%, and 82.8%, respectively.
The sensitivities and specicities of the CRP levels and CBC data used
to distinguish the NCPU and PUP patients and ROC data on WBC counts,
CRP, and NLRs are shown in Table 3 and Fig. 2. The sensitivities, specic-
ities, PPVs, and NPVs of the NLRs were 68.0%, 86.0%, 82.9%, and 72.9%, re-
spectively. Receiver operating characteristic curve analysis showed that
the cutoff values for the WBC count, CRP level, MPV, and NLR yielded the
best sensitivities and specicities, which were 9.03 109/L (80%-80%),
3.20 mg/dL (52%-94%), 8.8 f. (52%-70%), and 4.72 (68%-86%), respective-
ly. The areas under the curves for the WBC count, MPV, and NLR, were
81.3%, 75.6%, and 82.2, respectively.
4. Discussion
We found that the NLR was highly sensitive and specic when used
to identify patients with PUP. Because delaying the diagnosis and treat-
ment of patients with PUP is life threatening, the differential diagnosis
of PUP must be rapid.
Table 1
Laboratory data from all groups
PUP, n = 58 NCPU, n = 62 Control, n = 62
WBC (109/L) 12.70 (2.28-28.34)a 7.43 (3.68-13.55) 8.12 (4.15-12.20)
CRP (mg/dL) 3.40 (0-32.60)a 0.55 (0-4.80)b 0.20 (0-2.11)
RDW (%) 13.10 (11.10-45.60) 13.30 (6.70-33.10) 13.20 (11.60-34.60)
MPV (fL) 8.95 1.08 9.39 0.96c 8.72 0.96
NLR 8.99 (1.14-43.05)a 2.39 (0.87-13.11) 2.75 (1.12-12.28)
a
P b .001 vs noncomplicated peptic ulcer and control.
b
P = .022 vs control.
c
P = .001 vs control.
 Y. Tanrikulu et al. / American Journal of Emergency Medicine 34 (2016) 403406 405

Table 2 Table 3
Overall accuracies afforded by laboratory parameters used to distinguish patients with Overall accuracies provided by laboratory parameters used to distinguish patients with
PUP from controls (%) PUP from noncomplicated peptic ulcer (%)

Sensitivity Specicity PPV NPV Cutoff Youden index Sensitivity Specicity PPV NPV Cutoff Youden index

WBC 56 96 93.30 68.60 11.22 0.520 WBC 80 80 80 80 9.03 0.600

CRP 66 98 97.10 74.20 1.10 0.640 CRP 52 94 89.70 66.20 3.20 0.460
RDW 18 90 64.30 52.30 14.70 0.080 RDW 16 98 88.90 53.80 11.90 0.140
MPV 46 70 60.50 56.50 9.10 0.160 MPV 52 70 63.40 59.30 8.80 0.220
NLR 68 88 82.90 72.90 5.45 0.560 NLR 68 86 82.90 72.90 4.72 0.540

Peptic ulcer disease is one of the most common gastrointestinal dis-
orders. The frequency of PUD is estimated to be 1500 to 3000 per
100 000 people. The chance of an individual developing PUD is approx-
imately 5% [17]. Peptic ulcer perforation is predisposed in individuals in
their 40s and 50s, and the male/female ratio of this condition is in the
range of 2 to 8:1. Age older than 60 years directly affects the prognosis
of PUP, and the risk increases in this age group [18]. In their retrospec-
tive study, Ta et al [19] found that the mean patient age is 51.7 years.
Ugochukwu et al [6] found that adults in their 40s were most likely to
be affected, with a mean of 39.5 years. In our study, the mean patient
age was 51.8 years, which was consistent with other reports.
Peptic ulcer disease has life-threatening complications, such as hem-
orrhage and perforation. Peptic ulcer perforation is the most serious
complication associated with PUD, accounting for 5% of all abdominal
emergencies [3]. Because emergency PUP operations are associated
with high morbidity and mortality rates, identication of the diagnostic
markers and risk factors affecting perforation is very important. These
risk factors and diagnostic parameters include male sex, age 60 years
or older, coexisting illnesses, a history of PUD, patient habits (including
smoking or alcohol consumption), use of nonsteroidal anti-inammatory
drugs, symptoms of an acute abdomen, time to presentation longer than
24 hours, presence of shock at the time of presentation, blood urea nitro-
gen (BUN)/creatinine ratio greater than or equal to 12-fold, x-ray with
subdiaphragmatic free air, and referral from another hospital [3,19,20].
Some of these parameters are associated with postoperative mortality
and morbidity, but other parameters are related to the diagnostic protocol.
Peptic ulcer perforation is generally diagnosed clinically [6]. The clin-
ical diagnostic indicators of PUP include intense abdominal pain, ten-
derness, and guarding. Gastroduodenal perforation by the ulcer often
results in spillage of gastrointestinal contents into the abdominal cavity.
Although perforations at the anterior surface of the stomach usually re-
sult in intense abdominal pain, perforations at the posterior surface
often manifest as back pain [21].
Laboratory and radiologic diagnostic indicators include increased in-
ammatory parameters, increased BUN/creatinine ratio, and x-ray with
subdiaphragmatic free air. It has been reported that subdiaphragmatic
free air has been identied in the abdominal x-ray images of 47.2% to
80% of patients with PUP [18]. However, several case series have
shown that the x-ray may be negative for free air, particularly in elderly
patients [22]. Suriya et al [3] found that a BUN/creatinine ratio greater
than or equal to 12-fold is associated with PUP.
In addition to these diagnostic and prognostic markers, the most im-
portant parameter affecting the morbidity and mortality of patients
with PUP is the time that elapses between perforation and surgical
treatment. Perforation time is generally regarded as the beginning of
pain. Boey et al [23] found that a longstanding perforation ( 24
hours) was an important prognostic risk factor. Although Suriya et al
[3] found a similar result, Ta et al [19] did not identify any correlation
between the time to presentation and increased morbidity.
High morbidity and mortality rates caused by a delay in the diagno-
sis and surgical treatment of PUP have encouraged researchers to devise
new laboratory tests and imaging methods. In a 2009 study, Jafarzadeh
et al [24] found higher concentrations of CRP in H pyloriinfected sub-
jects. After these results, they published another study in 2013 in
which they found higher total WBC counts and NLR among H pylori
infected patients with PUD and asymptomatic subjects compared with
controls [12]. Another study from Japan found that H pylori eradication
reduces blood neutrophil and monocyte counts [25]. Similarly, Romero-
Adrin et al [26] found increased production of tumor necrosis factor,
interleukin (IL) 1, IL-6, and IL-8 among H pyloriinfected individuals. In-
terestingly, it has also been shown that H pyloriderived neutrophil-
activating protein increases the lifespan of neutrophils [27].
In clinical practice, the NLR is increasingly used to predict the surviv-
al of patients with malignancies, coronary artery disease, acute appendi-
citis, acute cholecystitis, acute pancreatitis, and community-acquired
infections [14]. Lee et al [28] found that preoperative NLR accurately
predicted the development of severe cholecystitis. Suppiah et al [29]

Fig. 1. Receiver operating characteristic curve used to distinguish PUP patients

from controls. Fig. 2. Receiver operating characteristic curve used to distinguish PUP from NCPU patients.
406 Y. Tanrikulu et al. / American Journal of Emergency Medicine 34 (2016) 403406
found that NLR elevation during the rst 48 hours of admission was sig-
nicantly associated with severe acute pancreatitis and was an indepen-
dent (negative) prognostic factor. Kahramanca et al [30] found that
preoperative NLR is useful in the diagnosis of acute appendicitis and to
differentiate patients with simple and complicated appendicitis.
In our present study, the NLRs were higher in the PUP than NCPU
and control groups (P b .001). However, the NCPU and control groups
did not differ in this respect (P = 1.000). In addition, the sensitivities,
specicities, PPVs, and NPVs for the WBC count, the CRP, and the NLR
were 56.0%, 96.0%, 93.3%, and 68.6%; 66%, 98%, 97.10%, and 74.2%; and
68.0%, 88.0%, 82.9%, and 72.9%, respectively. Receiver operating charac-
teristic curve analysis yielded cutoffs for the WBC count, CRP, and NLR
and optimal sensitivities and specicities. These were 11.22 10 9/L
(56%-96%), 1.10% (66%-98%), and 5.45 (68%-88%), respectively.
5. Conclusion
The results of the present study showed higher total WBC and CRP
counts and NLR in the PUP group compared to the control group. Thus,
preoperative NLR aids in the diagnosis of PUP, differentiating the condi-
tion from PUD, and can be used as an adjunct to clinical examination.
References
[1] Zelickson MS, Bronder CM, Johnson BL, Camunas JA, Smith DE, Rawlinson D, et al.
Helicobacter pylori is not the predominant etiology for peptic ulcers requiring oper-
ation. Am Surg 2011;77:105460.
[2] Thorsen K, Glomsaker TB, von Meer A, Sreide K, Sreide JA. Trends in diagnosis and
surgical management of patients with perforated peptic ulcer. J Gastrointest Surg
2011;15:132935.
[3] Suriya C, Kasatpibal N, Kunaviktikul W, Kayee T. Diagnostic indicators for peptic
ulcer perforation at a tertiary care hospital in Thailand. Clin Exp Gastroenterol
2011;4:2839.
[4] Sreide K, Thorsen K, Sreide JA. Strategies to improve the outcome of emergency
surgery for perforated peptic ulcer. Br J Surg 2014;101:e5164.
[5] Thorsen K, Sreide JA, Kvaly JT, Glomsaker T, Sreide K. Epidemiology of perforated
peptic ulcer: age- and gender-adjusted analysis of incidence and mortality. World J
Gastroenterol 2013;19:34754.
[6] Ugochukwu AI, Amu OC, Nzegwu MA, Dilibe UC. Acute perforated peptic ulcer: on
clinical experience in an urban tertiary hospital in south east Nigeria. Int J Surg
2013;11:2237.
[7] Hermansson M, Stal von Holstein C, Zilling T. Surgical approach and prognostic fac-
tors after peptic ulcer perforation. Eur J Surg 1999;165:56672.
[8] Snaith A, El-Omar EM. Helicobacter pylori: host genetics and disease outcomes. Ex-
pert Rev Gastroenterol Hepatol 2008;2:57785.
[9] Jha HC, Prasad J, Mittal A. High immunoglobulin A seropositivity for combined Chla-
mydia pneumoniae, Helicobacter pylori infection, and high-sensitivity C-reactive pro-
tein in coronary artery disease patients in India can serve as atherosclerotic marker.
Heart Vessels 2008;23:3906.
[10] Manolakis A, Kapsoritakis AN, Potamianos SP. A review of the postulated mecha-
nisms concerning the association of Helicobacter pylori with ischemic heart disease.
Helicobacter 2007;12:28797.
[11] Ramakrishnan K, Salinas RC. Peptic ulcer disease. Am Fam Physician 2007;76:
100512.
[12] Jafarzadeh A, Akbarpoor V, Nabizadeh M, Nemati M, Rezayati MT. Total leukocyte
counts and neutrophil-lymphocyte count ratios among Helicobacter pyloriinfected
patients with peptic ulcers: independent of bacterial CagA status. Southeast Asian
J Trop Med Public Health 2013;44:828.
[13] Proctor MJ, Morrison DS, Talwar D, Balmer SM, Fletcher CD, O'Reilly DS, et al. A com-
parison of inammation-based prognostic scores in patients with cancer. A Glasgow
Inammation Outcome Study. Eur J Cancer 2011;47:263341.
[14] de Jager CP, van Wijk PT, Mathoera RB, de Jongh-Leuvenink J, van der Poll T, Wever
PC. Lymphocytopenia and neutrophil-lymphocyte count ratio predict bacteremia
better than conventional infection markers in an emergency care unit. Crit Care
2010;14:R192.
[15] Ishizuka M, Shimizu T, Kubota K. Neutrophil-to-lymphocyte ratio has a close associ-
ation with gangrenous appendicitis in patients undergoing appendectomy. Int Surg
2012;97:299304.
[16] Aktimur R, Cetinkunar S, Yildirim K, Aktimur SH, Ugurlucan M, Ozlem N. Neutrophil-
to-lymphocyte ratio as a diagnostic biomarker for the diagnosis of acute mesenteric
ischemia. Eur J Trauma Emerg Surg 2015 [Epub ahead of print].
[17] Zittel TT, Jehle EC, Becker HD. Surgical management of peptic ulcer disease today-
indication, technique and outcome. Langenbecks Arch Surg 2000;385:8496.
[18] Kocer B, Surmeli S, Solak C, Unal B, Bozkurt B, Yildirim O, et al. Factors affecting mor-
tality and morbidity in patients with peptic ulcer perforation. J Gastroenterol
Hepatol 2007;22:56570.
[19] Ta , lger BV, nder A, Kapan M, Bozda Z. Risk factors inuencing morbidity and
mortality in perforated peptic ulcer disease. Ulus Cerrahi Derg 2014;31:205.
[20] Kim JM, Jeong SH, Lee YJ, Park ST, Choi SK, Hong SC, et al. Analysis of risk factors for
postoperative morbidity in perforated peptic ulcer. J Gastric Cancer 2012;12:2635.
[21] Lange A. Stomach and duodenum. In: Way LW, editor. Current surgical diagnosis
and treatment. Norwalk, CT: Appleton and Lange; 1994. p. 43759.
[22] Wallstabe L, Veitt R, Krner T. Diagnosis of perforated gastric ulcers by ultrasound. Z
Gastroenterol 2002;40:87780.
[23] Boey J, Choi SK, Poon A, Alagaratnam TT. Risk stratication in perforated duodenal
ulcers. A prospective validation of predictive factors. Ann Surg 1987;205:226.
[24] Jafarzadeh A, Hassanshahi GH, Nemati M. Serum levels of high-sensitivity C-reactive
protein (hs-CRP)in Helicobacter pyloriinfected peptic ulcer patients and its associa-
tion with bacterial CagA virulence factor. Dig Dis Sci 2009;54:26126.
[25] Kondo Y, Joh T, Sasaki M, Oshima T, Itoh K, Tanida S, et al. Helicobacter pylori eradi-
cation decreases blood neutrophil and monocyte counts. Aliment Pharmacol Ther
2004;20:749.
[26] Romero-Adrin TB, Leal-Montiel J, Monsalve-Castillo F, Mengual-Moreno E,
McGregor EG, Perini L, et al. Helicobacter pylori: bacterial factors and the role of cy-
tokines in the immune response. Curr Microbiol 2010;60:14355.
[27] Cappon A, Babolin C, Segat D, Cancian L, Amedei A, Calzetti F, et al. Helicobacter py-
loriderived neutrophil-activating protein increases the lifespan of monocytes and
neutrophils. Cell Microbiol 2010;12:75464.
[28] Lee SK, Lee SC, Park JW, Kim SJ. The utility of the preoperative neutrophil-to-
lymphocyte ratio in predicting severe cholecystitis: a retrospective cohort study.
BMC Surg 2014;14:100.
[29] Suppiah A, Malde D, Arab T, Hamed M, Allgar V, Smith AM, et al. The prognostic
value of the neutrophil-lymphocyte ratio (NLR) in acute pancreatitis: identication
of an optimal NLR. J Gastrointest Surg 2013;17:67581.
[30] Kahramanca S, Ozgehan G, Seker D, Gkce EI, Seker G, Tun G, et al. Neutrophil-to-
lymphocyte ratio as a predictor of acute appendicitis. Ulus Travma Acil Cerrahi
Derg 2014;20:1922.
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