The American Journal of Surgery (2013) 205, 691-696

Clinical Surgery

The significance of neutrophil/lymphocyte ratio as a

possible marker of underlying papillary microcarcinomas
in thyroidal goiters: a pilot study
Charalampos Seretis, M.D., M.Sc.a,*, Stavros Gourgiotis, M.D., Ph.D.a,
George Gemenetzis, M.D.a, Fotios Seretisb, Emmanuel Lagoudianakis, M.D., Ph.D.a,
George Dimitrakopoulos, M.D.a

a
2nd Department of Surgery, 401 General Army Hospital of Athens, 95 Lykourgou Street, Kallithea, 17676 Athens,
Greece; bMedical School, University of Patras, Patras, Greece

KEYWORDS: Abstract
Thyroid; BACKGROUND: Preoperatively elevated neutrophil/lymphocyte ratio (NLR) is a negative prognostic
Cancer; factor of survival in various types of cancers. A retrospective study was conducted to examine if pre-
Goiter; operative elevation of NLR is associated with higher risk for incidental papillary thyroid microcarcino-
Papillary thyroid ma (PTMC).
microcarcinoma; METHODS: The study sample consisted of 26 patients with benign goiters, 31 patients with inciden-
Neutrophil-to- tal PTMC, 26 patients preoperatively diagnosed with thyroid cancer, and 26 healthy controls. NLRs
lymphocyte ratio; were compared regarding thyroidal pathology.
Biomarker RESULTS: The mean preoperative NLR was significantly elevated in patients with PTMC and thy-
roid cancer. In addition, the third and fourth quartiles of NLR included only patients with either PTMC
or thyroid cancer. No significant differences in NLR occurred between patients with multifocal and uni-
focal PTMC.
CONCLUSIONS: NLRs were significantly elevated in patients with incidental PTMC and thyroid
cancer. The findings of this pilot study indicate that NLR should be considered an easily accessible bio-
marker for detecting incidental PTCM; nevertheless, further studies are required to confirm these pre-
liminary results.
Ó 2013 Elsevier Inc. All rights reserved.

Papillary thyroid microcarcinomas (PTMCs) are defined
as thyroid carcinomas measuring %1 cm.1 In the vast ma-
jority of patients, the presence of PTMC is an incidental
finding, detected during histopathologic examination of
thyroid gland specimens that are surgically removed be-
cause of concomitant benign thyroid goiters.2 Despite the
The authors declare no conflicts of interest.
* Corresponding author. Tel.: 130-6937236655; fax: 130-2634029443.
E-mail address: babismed@gmail.com
Manuscript received April 9, 2012; revised manuscript August 7, 2012
fact that PTMCs are generally considered to be rather be-
nign entities with excellent prognosis, recent studies have
found mortality of up to .5% in patients with PTMC, as a
result of thyroid cancer progression, suggesting that a
more aggressive approach should be adopted in confronting
PTMCs.3 Thus, the need to assess biomarkers to enhance
the capability of detecting PTMCs is evident, because early
diagnosis of these nascent malignancies can guarantee ex-
cellent outcomes for these patients.
In general, the process of the development of malig-
nancy has been firmly associated with impaired function of

0002-9610/$ - see front matter Ó 2013 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.amjsurg.2012.08.006
692
the immune system.4 Neutrophil/lymphocyte ratio (NLR)
has been proposed as a reliable indicator of the host’s in-
flammatory status; elevation of NLR has proved to be an in-
dependent predictor of poor prognosis in patients with
cancer, associated with inefficient endogenous anticancer
defense capability of the immune system.5 Until now, this
index has not been evaluated as a prognostic factor in thy-
roid cancer. Moreover, to the best of our knowledge, NLR
has also never been evaluated as a potential biomarker in
the context of detecting underlying malignancy in theoret-
ically benign neoplasia. The aim of this study was to assess
the significance of NLR with respect to the presence of
PTMC in benign goiters of the thyroid gland in patients
with no preoperative evidence of concurrent thyroidal
malignancy.
Methods
We performed a retrospective analysis, enrolling 109
patients who underwent surgery in our department between
January 2010 and December 2011. More specifically, our
study sample consisted of 57 patients who were submitted
to total thyroidectomy because of the presence of goiters,
without preoperative evidence of underlying PTMC; 26
patients preoperatively diagnosed with thyroid carcinoma,
who were also submitted to total thyroidectomy; and 26
healthy subjects, who were referred to our department for
hernia repair and served as a control group. The exclusion
criteria were positive histologic findings of any kind of
thyroiditis, as well as active infection or other known
malignancy, chronic inflammatory or autoimmune diseases,
presence of hematologic disorders, and current or long-term
steroid treatment, because any of these factors could alter
the NLR. The presence of thyroiditis in the removed
specimens was evaluated by a highly experienced pathol-
ogist (consultant); in the presence of any inflammatory
elements in the final histopathology report, the patient was
excluded from the study sample. Regarding the presence of
thyroiditis in the control group, the exclusion of relative
pathology was made after thorough clinical examination,
basic laboratory screening negative for active inflammation,
and absence of a history of thyroidal disorders. Each
patient’s medical record was reviewed independently by 2
physicians of our department to ensure that exclusion
criteria were accurately met in every candidate for enroll-
ment in our study. NLR was calculated as the ratio of the
total count of neutrophils divided by the total count of
lymphocytes in fasting morning blood samples obtained
from our patients during the process of routine preoperative
general blood testing. The blood samples of all patients
were obtained in the morning before the scheduled oper-
ation (thyroidectomy with or without lymph node dissec-
tion, depending on the presence of preoperative findings
suggestive of thyroid malignancy, and open hernia repair
for the control group), between 7:30 and 9 AM, to
standardize the known impact of circulating hormones
The American Journal of Surgery, Vol 205, No 6, June 2013
(circadian rhythm) on the number and subtype distribution
of the various white blood cell indices. Moreover, the blood
samples obtained were fasting, in accordance with the
department’s protocol for routine preoperative evaluation of
patients scheduled for elective surgery, which is applied for
the standardization of preoperative values of biochemical
tests. Finally, the conditions of the proanalytic phase (from
the moment blood was drawn until the final blood sample
analysis) were standardized in all cases, in accordance with
the relevant protocols for handling blood samples as set by
the Department of Microbiology.
The patients included in the study were initially cate-
gorized in 4 groups. Group 1 consisted of patients with
incidental PTMC, who underwent surgery for goiter; group
2 included patients who underwent surgery for goiters, who
were negative for PTMC and the presence of histologic
examination of the removed gland; group 3 included
patients submitted to thyroidectomy for preoperatively
diagnosed thyroid cancer; and group 4 consisted of the
control patients. In these 4 groups, we assessed the possi-
bility of existing differences regarding the mean NLR.
Sequentially, we calculated the quartile distribution of NLR
in the sample of our study and accordingly divided our
patients into 4 quartiles, with respect to NLR of each
patient. We then performed statistical assessment of any
possible correlation of the recorded demographic data and
histologic findings among the groups corresponding to the
quartile distribution of NLR.
Our statistical analyses were performed using SPSS
version 16.0 (SPSS, Inc, Chicago, IL). All continuous and
categorical variables were assessed for normal distribution.
Comparison of NLR between the initial groups was
performed using 1-way analysis of variance, while statis-
tical correlations after quartile splitting of our sample were
carried out using Kruskal-Wallis tests for testing NLR
quartiles and continuous variables and c2 tests when testing
NLR quartiles and categorical variables. P values ,.05
were considered statistically significant. Patients enrolled
in the control group were sex and age matched with the pa-
tients who underwent thyroidectomy (no statistical signifi-
cant differences in age and sex among groups 1–4).
Results
Briefly, the entire cohort’s demographic characteristics
were as follows: the mean age was 54.1 years (range, 28–72
years); 51 were men and 58 were women; and the mean
NLR among all patients was 2.5 (range, .7–6.9) (Table 1).
The statistical analysis demonstrated that older patients
had significantly higher NLRs (P , .001). Among patients
who were submitted to total thyroidectomy without preop-
erative diagnosis of underlying malignancy (n 5 57), in 26
(46%), the histopathologic examinations of the removed
specimens revealed the presence of PTMCs. Thus, the ini-
tial categorization of our study sample was transformed as
follows: 26 patients with PTMC (group 1), 31 patients with
C. Seretis et al. Elevated NLR as a biomarker of incidental PTMC 693

second quartile (group B) included patients with

Table 1 Demographic characteristics of the study sample
NLRs .1.65 to 2.5, the third quartile (group C) included
Patients Age (y), patients with NLRs .2.5 to 3, and the fourth quartile
Characteristic (men/women) mean 6 SD (group D, with the highest values of the ratio) included
PTMC 26 (12/14) 53.6 6 14.2 patients with NLRs .3 to 6.9. After this categorization,
Benign goiters 31 (12/19) 51.8 6 13.6 group A numbered 50 patients, while groups B, C, and D
Thyroid cancer 26 (13/13) 55.4 6 12.6 numbered 45, 11, and 3 patients, respectively. Groups C
Controls 26 (14/12) 55.4 6 12.0 and D (14 patients) included only patients with incidental
Total 109 (51/58) 53.9 6 13.0
PTMC and thyroid cancer, meaning that only patients with
PTMC 5 papillary thyroid microcarcinoma. thyroidal malignancy had preoperative NLRs .2.5. Statis-
tical significance (P , .001) was reached when assessing
the existence of potential differences in the distribution of
benign goiters (group 2), 26 patients preoperatively groups 1 to 4 according to NLR quartiles (groups A–D);
diagnosed with thyroid cancer (group 3), and 26 controls in other words, elevated NLR was significantly associated
(group 4). The mean NLRs in each of these groups were with the presence of thyroidal malignancy, either cancer
3, 1.9, 3.4, and 1.8 respectively, with the differences being or PTMC (Table 2). Moreover, no statistical significance
statistically significant between groups 1 and 2 (P , .001), was obtained when assessing age in NLR quartiles, as
groups 1 and 4 (P , .001), groups 2 and 3 (P , .001), and well as when comparing NLRs between patients with mul-
groups 3 and 4 (P , .001), indicating a clear elevation of tifocal and unifocal PTMC.
NLR in thyroid malignancy compared with benign thyroid Considering these results, it is clearly demonstrated that
disorders and controls (Fig. 1). No statistical significance patients with elevated NLRs had greater risk for concurrent
was attained when comparing mean NLRs among the thyroidal malignancy. Nevertheless, although it would be of
groups with incidental PTMC and preoperatively diagnosed great interest to propose an NLR cutoff value above which
thyroid cancer. Regarding the group with incidental PTMC, patients with thyroidal goiters may be at higher risk for
local lymphatic spread in the harvested local minor lymph concurrent PTMC, such an attempt would be ill advised
nodes was detected in none of the patients (0%) (1 or 2 in because of the relatively small sample size of our pilot
all cases, situated around the isthmus). No significant corre- study. Nevertheless, as demonstrated above, only patients
lation was found between elevated NLR and the size of the with thyroidal malignancy, either preoperatively diagnosed
incidental PTMC (mean PTMC size, 6 6 2.9 mm). cancer or incidental PTMC, had NLRs .2.5.
Sequentially, we separated our patients into quartiles
with respect to NLR and assessed the existence of statis-
tically significant differences regarding the distribution of Comments
groups 1 to 4, according to the categorization of our
patients into quartiles NLR. The first quartile (group A) Impaired function of the immune system represents a
included patients with NLRs ranging from .7 to 1.65, the turning point concerning the endogenous capability of
intercepting carcinogenesis, with inflammation and cancer
pathogenesis being strongly associated.6 Moreover, apart
from the negative impact of chronic inflammation in cancer
progression, various studies have demonstrated that carci-
nogenesis itself enhances chronic inflammation, which
has led to the evaluation of inflammation markers as possi-
ble predictors of survival and cancer-related complica-
tions.7 The 2 most frequently used markers of active
inflammatory status in patients with cancer are C-reactive
protein and NLR, because they are reliable and widely
available in daily clinical practice, and their sensitivity in
predicting survival rates has been supported by a large
number of studies in various types of cancer.8 With respect
to the pathophysiologic interpretation of preoperatively el-
evated NLR, it appears that there are many possible expla-
nations regarding its wide application in predicting survival
in patients with cancer. More specifically, low lymphocyte
counts have been associated with generalized suppression
Figure 1 Mean NLR in groups 1 to 4. Statistical significance of the immune systems of patients with cancer.9 Moreover,
was obtained when comparing groups 1 and 2 (P , .001), groups coexisting neutrophilia is believed to occur because of
1 and 4 (P , .001), groups 2 and 3 (P , .001), and groups 3 and 4 either paraneoplastic activity of the primary tumor10 or
(P , .001). the production of granulocyte colony–stimulating factor,
694 The American Journal of Surgery, Vol 205, No 6, June 2013

Table 2 Statistical significance (P , .001) was obtained when assessing the existence of potential differences in the distribution of
groups 1 to 4 according to NLR quartile (groups A–D)
PTMC Benign goiter Thyroid cancer Controls Total
Group A (first quartile) 6 20 5 19 50
NLR .7–1.65 23.1% 64.5% 19.2% 73.1% 45.9%
Group B (second quartile) 15 11 12 7 45
NLR . 1.65–2.5 57.7% 33.5% 46.2% 26.9% 41.3%
Group C (third quartile) 5 0 6 0 11
NLR . 2.5–3 19.2% 0% 23.1% 0% 10.1%
Group D (fourth quartile) 0 0 3 0 3
NLR . 3–6.9 0% 0% 11.5% 0% 2.8%
Total 26 (100.0%) 31 (100.0%) 26 (100.0%) 26 (100.0%) 109 (100.0%)
NLR 5 neutrophil/lymphocyte ratio; PTMC 5 papillary thyroid microcarcinoma.

through an interaction between malignant cells and bone
marrow granulocytic cells.11–14 As a result, elevation of
NLR seems justified in patients with cancer with limited
immune anticancer capability. Nevertheless, the underlying
mechanisms of neutrophilia and lymphopenia in patients
with cancer remain a matter of intensive scientific research.
These findings have led to further examination of the
significance of preoperative NLR in terms of the prediction
of overall survival, disease-free survival, and response to
chemotherapy in various types of cancers.15–20 As far as
thyroid malignancy is concerned, NLR until now has not
been examined in any study as a potential prognostic factor
of survival. In addition, no studies have assessed NLR ele-
vation as a possible indicator of underlying malignancy in
benign neoplastic tumors.
The aim of our pilot study was to investigate the possible
application of preoperative NLR elevation as an indirect
marker of incidental PTMC in patients submitted to
thyroidectomy because of the presence of thyroidal goiters.
The findings of our study clearly support that the evaluation
of preoperative NLR may be a useful means of assessing
risk for the presence of PTMC in thyroidal goiters.
Although further studies with larger samples are required
to examine this association in patients with thyroid neo-
plasia, our preliminary results suggest that elevated NLR
could be used as a potential biomarker of the necessity
of close monitoring in patients with presumably benign
goiters. From a more clinical point of view, elevation of
NLR could stratify the group of patients with goiters who
could possibly be candidates for thyroidectomy or for a
more intensive protocol of monitoring the progression of
the thyroidal pathology. Moreover, NLR could possibly
serve as a marker of closer follow-up after thyroidectomy,
to increase the possibility of early detection of recurrence
and lymphatic or even distant metastases, because this ratio
has been associated with higher risk for recurrence and
metastatic spread in previous studies.21 The significance of
our findings increases considering that, to the present time,
confrontation of PTMC remains a matter of scientific de-
bate,22,23 while the incidence of PTMC is explosively in-
creasing24,25 and NLR stands as an emerging biomarker
of cancer activity in an increasing number of types of solid
malignancies (Table 326–28,30–33).
Taking into account the relatively small sample of
patients enrolled in our study, it would be ill advised to
propose a cutoff NLR that would be more safely associated
with underlying malignancy. Because there are no previous
data on the evaluation of NLR concerning both thyroid
malignancies and lesions that share characteristics similar
to the microcarcinomas (extent, progression, and biologic
behavior), we decided to include an analysis based on the
quartile distribution of NLR, following the excellent study
by Azab et al,17 who were the first group to assess NLR in
breast cancer and thus had no previous relevant data on

Table 3 Presentation of the increasing rate of application of NLR as a prognostic factor of survival in various types of cancer (selected
publications in leading journals in 2012 alone)
Study Type of malignancy Citation details
Gondo et al26 Bladder cancer Urology 2012;79:1085–91
Dutta et al27 Gastric cancer Am J Surg 2012;204:294–9
Kwon et al28 Colorectal cancer Biomarkers 2012;17:216–22
He et al29 Nasopharyngeal carcinoma Head Neck 2012;34:1769–76
Pinato et al30 Malignant pleural mesothelioma J Thorac Oncol 2012;7:587–94
Sato et al31 Advanced esophageal cancer World J Surg 2012;36:617–22
Wang et al32 Gastric cancer Tumour Biol 2012;33:749–56
Ohno et al33 Renal cell carcinoma J Urol 2012;187:411–7
NLR 5 neutrophil/lymphocyte ratio.
C. Seretis et al. Elevated NLR as a biomarker of incidental PTMC
which to base their findings. We adopted their approach
because, in any other case, on the basis of the conventional
cutoff values associated with poor survival, we would in
fact compare the interplay between thyroid malignancy
and the immune system to that between the immune system
and highly immune-regulating types of cancer, such as pan-
creatic, gastric, and colorectal cancer. Nevertheless, accord-
ing to our results, only patients with preoperatively
diagnosed thyroid cancer and incidental PTMC had
NLRs .2.5; after grouping our patients according to
NLR quartiles, we found that the third and fourth quartiles,
corresponding to higher NLR values, included only patients
with thyroidal malignancy, either cancer or incidental mi-
crocarcinomas. Moreover, approximately 20% of all pa-
tients with incidental PTMC and 35% of patients with
thyroid cancer belonged in the top 2 quartiles, with this par-
ticular finding being a primitive indicator of the pool of pa-
tients who could benefit from coevaluation of NLR in the
context of monitoring thyroidal pathology. Finally, with re-
spect to the fact that our study sample did not reflect the 3:1
female preponderance in thyroid operations, the ultimately
equal numbers of male and female patients are a conse-
quence of the nature of the hospital, which is a tertiary mil-
itary hospital; thus, an above-average percentage of patients
are inevitably men.
Although promising in terms of sensitivity, it is obvious
that NLR, at least excluding the highest values, cannot be
regarded as a specific detector of malignancy. As the
exclusion criteria of our study highlight, NLR can be
influenced in many common pathologic conditions. Never-
theless, it should be taken into account that NLR is always
available in routine blood tests and does not increase the
cost of the diagnostic strategy; this particular point repre-
sents a major advantage regarding its easy and cost-effective
application. Also, as mentioned above, clinical suspicion of
underlying malignancy can be increased with relative safety
when a remarkable elevation of NLR is found.
In summary, our pilot study suggests that NLR eleva-
tion may be useful as a serum biomarker in terms of
stratifying patients with thyroidal goiters regarding the
possibility of having concurrent PTMC. Although of
doubtful specificity, NLR appears to be a cost-effective
and rather sensitive indicator of progressing thyroidal
malignancy in patients with goiters. Further studies are
required to confirm our preliminary results and shed light
on the possible association of thyroidal malignancy with
NLR elevation.
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