10.14639/0392-100X-N0790
Introduction. Deep neck space infections (DNSIs) are a group of infective suppurative diseases involving deep neck spaces and cervical fascia. Necrotising and septic evolutions are rare, but severe complications can dramatically affect the prognosis and should be promptly managed. Clinical examination often has low sensitivity, although instrumental diagnosis may delay te treatment. We investigated two laboratory tools, LRINEC (Laboratory Risk Indicator for the Necrotizing fasciitis) and NLR (neutrophil to lymphocyte ratio), in the expectation to find a rapidly available predictive indicator that may help in distinguishing necrotising complications and/or systemic septic involvement.
Methods. A retrospective observational cohort study was performed on 118 patients who had underwent surgical treatment for DNSIs at our Surgical Unit. LRINEC, NLR and the product LRINEC x NLR were calculated. Results. Statistical analysis showed that these scores may have utility in rapidly predicting the risk of necrotising fasciitis and systemic involvement at an early diagnostic stage.
Conclusions. Further studies with a larger cohort may be necessary in order to increase the sensitivity and specificity.
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1827-675X
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Nicola Quaranta
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ACTA Otorhinolaryngologica Italica
neck
New laboratory predictive tools in deep neck space infections
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1
Nicola Quaranta
2020/12/03
10.14639/0392-100X-N0790
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Unit of Otorhinolaryngology, Department of Biomedical Sciences, Neurosciences and Sense Organs, University of Bari, Italy
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New laboratory predictive tools in deep neck space infections
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ACTA OTORHINOLARYNGOLOGICA ITALICA 2020;40:332-337; doi: 10.14639/0392-100X-N0790




Review


New laboratory predictive tools in deep neck space
infections
Nuovi indicatori biochimici predittivi di infezioni suppurative cervicali
Maria Luisa Fiorella1, Paolo Greco1, Luigi Maria Madami1, Orazio Valerio Giannico2, Vito Pontillo1, Nicola Quaranta1
1
    Unit of Otorhinolaryngology, Department of Biomedical Sciences, Neurosciences and Sense Organs, University of Bari, Italy;
2
    Section of Hygiene, Department of Biomedical Sciences and Human Oncology, University of Bari “Aldo Moro”, Bari, Italy


SUMMARY
Introduction. Deep neck space infections (DNSIs) are a group of infective suppurative dis-
eases involving deep neck spaces and cervical fascia. Necrotising and septic evolutions are
rare, but severe complications can dramatically affect the prognosis and should be promptly
managed. Clinical examination often has low sensitivity, although instrumental diagnosis
may delay te treatment. We investigated two laboratory tools, LRINEC (Laboratory Risk
Indicator for the Necrotizing fasciitis) and NLR (neutrophil to lymphocyte ratio), in the
expectation to find a rapidly available predictive indicator that may help in distinguishing
necrotising complications and/or systemic septic involvement.
Methods. A retrospective observational cohort study was performed on 118 patients who
had underwent surgical treatment for DNSIs at our Surgical Unit. LRINEC, NLR and the
product LRINEC x NLR were calculated.
Results. Statistical analysis showed that these scores may have utility in rapidly predicting
the risk of necrotising fasciitis and systemic involvement at an early diagnostic stage.            Received: April 9, 2020
                                                                                                    Accepted: May 20, 2020
Conclusions. Further studies with a larger cohort may be necessary in order to increase the
sensitivity and specificity.
                                                                                                    Correspondence
KEY WORDS: LRINEC, NLR, necrotizing fasciitis, sepsis, neck                                         Paolo Greco
                                                                                                    Unit of Otorhinolaryngology, Department of Bio-
                                                                                                    medical Sciences, Neurosciences and Sense Organs,
RIASSUNTO                                                                                           University of Bari, piazza Giulio Cesare 11, 70124
Introduzione. Le infezioni suppurative del collo sono un eterogeneo gruppo di patologie a           Bari, Italy
carico degli spazi profondi del collo e delle fasce cervicali. Al suo interno meritano partico-     Tel. +39 080 5593524
lare attenzione le temibili fasciti necrotizzanti, caratterizzate dall’elevato tasso di mortalità   E-mail: pao3greco@hotmail.it
e di compromissione settica. Risulta pertanto indispensabile una loro pronta diagnosi e
un altrettanto tempestivo trattamento. La semeiologia clinica risulta spesso poco sensibi-          Funding
le, mentre l’esame TC comporta un inevitabile ritardo nella presa in carico terapeutica.            None.
Abbiamo quindi valutato l’applicabilità di due indicatori basati unicamente su parametri
laboratoristici, quindi rapidamente disponibili: LRINEC score e NLR ratio.                          Conflict of interest
Metodi. Abbiamo condotto uno studio retrospettivo su 118 pazienti che erano stati sottopo-          The Authors declare no conflict of interest.
sti a drenaggio chirurgico di ascesso cervicale c/o la nostra U.O., calcolando per ciascuno
di essi LRINEC, NLR e il loro prodotto di moltiplicazione LRINEC x NLR.                               How to cite this article: Fiorella ML, Greco P,
Risultati. L’analisi statistica dimostra un loro possibile ruolo nella diagnosi tempestiva            Madami LM, et al. New laboratory predictive
delle fasciti necrotizzanti e/o delle loro complicanze settiche.                                      tools in deep neck space infections.Acta Otorhi-
Conclusioni. Ulteriori studi con una maggiore numerosità campionaria potrebbero essere                nolaryngol Ital 2020;40:332-337. https://doi.
necessari per rafforzare sensibilità e specificità di tali score.                                     org/10.14639/0392-100X-N0790

PAROLE CHIAVE: LRINEC, NLR, fasciti necrotizzanti, sepsi, cervicali
                                                                                                    © Società Italiana di Otorinolaringoiatria
                                                                                                    e Chirurgia Cervico-Facciale


                                                                                                                   OPEN ACCESS
Introduction                                                                                        This is an open access article distributed in accordance with
                                                                                                    the CC-BY-NC-ND (Creative Commons Attribution-Non-
Deep neck space infections (DNSIs) are a group of infective suppurative dis-                        Commercial-NoDerivatives 4.0 International) license. The
eases involving deep neck spaces. They may occur at any age, although the                           article can be used by giving appropriate credit and mentio-
                                                                                                    ning the license, but only for non-commercial purposes and
mean age of onset is 49.5 years 1.                                                                  only in the original version. For further information: https://
DNSI usually occur in patients affected by multiple comorbidities; in par-                          creativecommons.org/licenses/by-nc-nd/4.0/deed.en




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                                                                                        LRINEC and NRL: a novel laboratory approach




ticular, diabetes may raise the risk of infection as a conse-    of these indicators as predictive factors that may help in de-
quence of immunological alterations or secondary micro-          tecting CNFs or systemic involvement in course of DNSIs.
angiopathy 2.
Dental and oropharyngeal infections are the most common          Materials and methods
source of DNSI 3,4, even if in a fourth of cases a defined
trigger cannot be found 5. Submandibular (36.26%) and            A retrospective observational cohort study was performed
sublingual spaces (13%) are the most frequent localisations      on 118 patients who underwent surgical treatment for DN-
followed by the para-pharyngeal (12%) and retropharyn-           SIs at our Surgical Unit in the period between February
geal spaces (3%) 5.                                              2008 and February 2018. Cases of peritonsillar abscess
The isolated microbes in DNSIs reflect the normal flora          treated by transoral incision without cervical drainage were
of the upper respiratory and digestive tract, with a strong      not included. Informed consent for surgery was obtained
prevalence of Gram+ bacteria (Streptococcus viridans             from all patients before surgery, which was performed
41.5%, Staphylococcus aureus 20.7%) 5. The presence              within 48 hours after admission in all cases. All procedures
of Gram- germs (Pseudomonas aeruginosa 4.07%, Kleb-              were in accordance with the ethical standards of the insti-
siella pneumonia 1.48%) 6 is more frequently related to          tutional research committee and with the 1964 Helsinki
diabetic comorbidity 2. Anaerobic bacteria (Prevotella 4%,       Declaration and its later amendments or comparable ethi-
Fusobacterium 5%) 7 have been demonstrated to play an            cal standards. Our Ethics Committee was informed of the
important role in the development of cervical necrotising        retrospective data collection.
fasciitis (CNF) 7,8 due to the production of specific enzymes    Each patient was submitted at admission to clinical ex-
involved in the necrotising process 8. Bacterial cultures        amination and laboratory tests, including CBC (complete
can be polymicrobial in 20.8% 5 of cases and negative in         blood count), electrolytes, glycaemia, coagulation tests,
10.74% 6 of patients, probably due to the wide use of pre-       liver and kidney functional tests and inflammatory markers
hospitalisation antibiotic therapy or to technical difficulty    (CPR, C-reactive protein and ESR, erythrocyte sedimenta-
in isolating anaerobic pathogens 9,10.                           tion rate). A neck and chest CT was performed in all cases
Especially when involving para- and retro- pharyngeal            with the purpose of finding the potential focus of infection
spaces, DNSI may extend by continuity and contiguity to          and evaluate the extension of the suppurative process.
the mediastinal and thoracic spaces. Some authors have           LRINEC and NLR scores were then calculated; further-
proposed the acronym DNM (descending necrotising me-             more, in order to reinforce the predictive power of our
diastinitis) to define a necrotising mediastinitis arising as    analysis, we proposed an additive indicator, the product be-
result of the secondary spread of a CNF (cervical necrotis-      tween both the aforementioned scores (LRINEC x NLR).
ing fasciitis) 7.                                                LRINEC takes into account 6 laboratory values, assigning
CNF, DNM and systemic septic involvement are potential           a specific score to each of them, as reported in Table I.
life-threatening complications of DNSIs, hence it is impor-      NLR is calculated as the ratio between neutrophil and lym-
tant to have a reliable tool that allows a prompt detection of   phocyte percentages at CBC.
these complications.                                             LRINEC score, and consequently the product between
Clinical examination allows identification of the typical        NLR and LRINEC, was obtained only for a subgroup of 90
clinical signs and symptoms of CNF (e.g. crackling palpa-        patients, since CRP was not routinely tested in our depart-
tion, brownish or hyperaemic skin and cutaneous fistula),        ment pre-operatively.
but has low sensitivity (67%) 11; imaging techniques such        Two outcomes were chosen: occurrence of CNF (n = 12/118)
as CT can be useful, but can delay treatment.                    and sepsis. Detection of gas bubbles detection at CT and in-
The aim of this study was to evaluate the role of two well-      traoperative finding of necrosis in patients affected by CNF.
known laboratory tools as predictive factors of DNSI com-        Septic systemic involvement was defined on the basis of
plications such as CNF and sepsis.                               the “The Third International Consensus Definitions for
The “Laboratory Risk Indicator for NECrotizing fasciitis”        Sepsis and Septic Shock (Sepsis-3)” 14. According to this,
score (LRINEC) 12 was first proposed by Wong et al. 12 in        sepsis can be rapidly identified in non-intensive care set-
order to promptly identify a necrotising complication in         tings using a new bedside clinical score termed quickSOFA
case of suppurative infections, not strictly localised in the    (qSOFA), when at least 2 of the following clinical criteria
cervical region. On the other hand, the neutrophil to lym-       are met:
phocyte ratio (NLR) has been proposed for its diagnostic         • respiratory rate of 22/min or greater;
and prognostic role in the early and late phases of the septic   • altered mentation;
process 13. The present study aims to demonstrate the utility    • systolic blood pressure of 100 mm Hg or less.



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Table I. LRINEC score calculating model.                       Results
 Variable, Unit                                     Score
                                                               118 patients underwent a surgical intervention for DNSIs
 C-reactive protein (CRP), mg/L
                                                               between February 2008 and February 2018 in our Unit: 73
 < 150                                                0
                                                               males (61.86%) and 45 females (38.13%) with a mean age
 ≥ 150                                                4
                                                               of 48.39 years (range 2-83 years).
 Haemoglobin, g/dL
                                                               Table II reports the suspected foci of infection in our co-
 > 13.5                                               0
                                                               hort. In 43.22% of cases the source was unknown as re-
 11-13.5                                              1
                                                               ported by other authors 15. Dental infection was the most
 < 11                                                 2
                                                               common cause occurring in a third of cases.
 Total white cell count, per mm³
                                                               In Table II, the anatomical localisations of DNSIs in our
 < 15                                                 0
                                                               series are reported. The submandibular region and the
 15-25                                                1
                                                               parapharyngeal space were involved in almost 50% of all
 > 25                                                 2
                                                               cases, while multiple localisations occurred in 24 cases
 Sodium, mmol/L
                                                               (20%). In 4 cases (3.4%), a mediastinal extension was
 ≥ 135                                                0
                                                               evident.
 <135                                                 2
                                                               Seventy patients (59.32%) presented at least one major
 Creatinine, µmol/L
                                                               comorbidity (Tab. II), mostly hypertension (21.19%) and
 ≤ 141                                                0
 > 141                                                2
 Glucose, mg/dL                                                Table II. Clinical findings in our series.
 ≤ 180                                                0         Sources of infection                           N     %
 > 180                                                1         Unknown                                        51   43.2
                                                                Odontogenic                                    33   27.9
                                                                Recurrent tonsillitis                          11   9.3
Septic shock is defined as a subset of sepsis in which a va-    Sialolithiasis                                 8    6.8
sopressor is required to maintain a mean arterial pressure      Previous neck procedures (FNAB/surgery)        4    3.4
of 65 mm Hg or greater and serum lactate level greater          Neck cysts                                     3    2.5
than 2 mmol/L (> 18 mg/dL) in the absence of hypovol-           Lymphadenopathy                                3    2.5
aemia 14.                                                       Mastoiditis                                    2    1.7
In accordance with these criteria, we identified 53 patients    Other                                          3    2.5
without sepsis, 52 with sepsis and 13 with septic shock.        Sites of infection                             N     %
                                                                Submandibular                                  34   28.81
Statistical analysis                                            Parapharyngeal                                 24   20.34
Statistical analysis was performed using R 3.5.1. Statis-       Parotid space                                  13   11.02
tical significance was reached with a P < 0.05. Categori-       Oral pelvis/base of tongue                      5   4.237
cal variables were reported as absolute and relative fre-       Retropharyngeal                                 3   2.542
quencies. Numerical variables were reported as median           Multiple localisations                         24   20.34
and IQR and compared through Wilcoxon and Kruskall              Other                                          15   12.71
Wallis rank sum test in order to account for non-nor-           Comorbidities                                  N     %
mality (evaluated through Shapiro-Wilk test) and hetero-
                                                                Hypertension                                   25   21.19
scedasticity (evaluated through Bartlett test). Post-hoc
                                                                Diabetes                                       16   13.56
analysis was performed through pairwise Wilcoxon rank
                                                                Cardiopathy                                    10   8.475
sum test with Benjamini-Hochberg correction (false dis-
                                                                Autoimmune diseases                             5   4.237
covery rate).
                                                                Endocrinopathy (except diabetes)                4   3.39
Six ROC curves were then fitted for the three scores (LRI-
                                                                Nephropathy                                     4   3.39
NEC, NLR e LRINEC×NLR) and for the two outcomes
(CNF and Sepsis Score), with the estimation of AUC (area        Neoplasia                                       3   2.542
under the curve), optimal cut-off, sensibility, specificity,    Chronic obstructive pulmonary disease (COPD)    3   2.542
positive and negative predictive value.                         None                                           48   40.68




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                                                                                                     LRINEC and NRL: a novel laboratory approach




Table III. Kruskal-Wallis and Wilcoxon Tests.
                                                                     LRINEC                       NLR                      NLR x LINREC
                                                                   median (IQR)                median (IQR)                median (IQR)
 Sepsis                No sepsis                                     4.5 (3.3)                    7.0 (6.9)                 29.4 (43.7)
                        Sepsis                                       5.0 (3.0)                   10.3 (11.3)                59.2 (71.7)
                      Septic shock                                   8.0 (2.0)                    13.4 (8.2)                107.3 (82.6)
                                           (Kruskal-Wallis Test)    P = 0.003                    P = 0.001                   P < 0.001
 CNF                       Yes                                       8.0 (3.5)                   15.0 (17.5)                86.3 (113.9)
                           No                                        5.0 (3.5)                     9.2 (9.5)                 39.2 (72.5)
                                                (Wilcoxon Test)     P = 0.020                    P = 0.041                   P = 0.010



diabetes (13.56%). In 11 cases (9.32%), multiple comor-                  Table IV. Pairwise comparison for Sepsis Score.
bidities were found.                                                      Wilcoxon rank sum test                                    P-value
Surgical treatment, consisting in cervical incision with ab-              LRINEC
scess drainage and cervical fascia/spaces debridement and                 No Sepsis / Sepsis                                         0.039
rinsing, was performed in all cases. In 42 cases (35.59%)                 No Sepsis / Septic shock                                   0.004
the submandibular gland was removed; 4 patients (3.39%)                   Sepsis / Septic shock                                      0.039
presented suppurative mediastinitis, thus necessitating tho-              NLR
racic drainage; tracheotomy was performed in 21 patients
                                                                          No Sepsis / Sepsis                                         0.011
(17.79%). Twenty-four patients (20.33%) needed intensive
                                                                          No Sepsis / Septic shock                                   0.005
care. The survival rate in our series was 98.3%: 2 patients
                                                                          Sepsis / Septic shock                                      0.203
died for severe respiratory and systemic complications.
                                                                          NLRxLRINEC
In Table III, LRINEC, NLR and LRINEC x NLR values are
                                                                          No Sepsis / Sepsis                                         0.011
reported in relation to sepsis and occurrence of CNF. Sta-
tistical analysis showed significantly higher values of LRI-              No Sepsis / Septic shock                                  < 0.001
NEC, NLR and NLR x LRINEC in case of severe septic                        Sepsis / Septic shock                                      0.034
involvement (septic shock > sepsis > no sepsis) and CNF.
Pairwise comparison (Tab. IV) demonstrated a potential
utility of LRINEC and NLR x LRINEC in discriminating                     dictors of mortality and morbidity for DNSIs 8, particularly
sepsis from septic shock.                                                in case of CNF.
ROC curves (Tab. V) show for both the considered out-                    CNF represent only 3.5% 15 of total DNSIs, but they dra-
comes (sepsis and CNF) the performances of the three                     matically affect the prognosis of these patients, with a mor-
scores, with acceptable values of AUC (between 0.6 and                   tality rate of 7-22%, increasing to 41% in case of thoracic
0.8).                                                                    involvement and up to 64% if associated with DNM and sep-
                                                                         tic complications 17. This wide range is probably explained
                                                                         by the fact that early diagnosis requires relevant diagnostic
Discussion                                                               instruments, not always available in poor resource countries,
Neck spaces are bordered by cervical fascia which repre-                 where the prognosis is obviously worse 10. Hence, it has been
sent, rather than an obstacle, a possible route of spreading             stated that prompt diagnosis and surgical treatment within 12
for suppurative processes. For this reason, it is important              hours 8,18 from admission are strongly advisable in order to
to consider the possible dissemination of DNSIs, espe-                   lower the mortality rate. Clinical signs of necrosis alone have
cially when evolving to CNF, to regions such as the me-                  been demonstrated to have a low sensitivity (67%) in detect-
diastinum and thorax. In addition, the significant risk of               ing CNF 11. On the contrary, CT scan is a sensitive (79%)
systemic inflammatory involvement should not be ignored.                 and specific (94%) tool 15,19, but not always available in short
Septic presentation in case of DNSIs has been frequently                 time frames, especially in poorer countries. For this reason,
described by several authors 4,16, especially in case of CNF.            the use of short-term laboratory predictors must be investi-
Thus, this condition must be considered as a challenging                 gated in order to allow prompt diagnosis.
race against time, since only early diagnosis allows well-               According to Wong et al. 12, the risk of developing necrotis-
timed and adequate medical and surgical treatment. In fact,              ing fasciitis is distinguishable on the basis of LRINEC in:
delayed diagnosis is considered to be one of the main pre-               • low risk (probability less than 50%) for LRINEC-score 5;



                                                                                                                                             335
M.L. Fiorella et al.




• medium risk (probability of 50-75%) for LRINEC-score               95.4%). In our study, we tried to find an application of this
   between 6 and 7;                                                  score as a predictor of the risk of CNF and sepsis, simi-
• high risk (probability more than 75%) for LRINEC-                  larly to what was explained above for the LRINEC score.
   score ≥ 8.                                                        We found sensitivity and specificity values, respectively, of
The Wong et al. 12 model considers necrotising soft tissue           50% and 84.9% (cut-off 17.5) in discriminating the risk of
infections in general and CNF was only minimally repre-              CNF and of 74.2% and 61.5% (cut-off 8.2) in predicting
sented in their cohort. In their publication, Wong et al. dem-       systemic septic involvement (Tab. V).
onstrated LRINEC score to be significantly associated with           Based on the these first disappointing results, in accordance
the risk of necrotising fasciitis.                                   with other authors25, we proposed a new score, LRINEC
Thomas et al. 15 were the first to propose the application of        x NLR (multiplication of the above-mentioned scores),
LRINEC score to CNF, still achieving discouraging results.           which was demonstrated to have acceptable sensitivity
Sensitivity and specificity were, respectively, of 56% and           (90.9% with a cut-off of 43.5) in discriminating the risk of
60% in case of value ≥ 6 (medium risk according to Wong’s            CNF (Tab. V).
model), 22% and 90% in case of value ≥ 8 (high risk ac-              Nevertheless, LRINEC, NLR and LRINEC x NLR signifi-
cording to Wong). Sandner et al. 19 found 94% sensitivity            cantly differed depending on sepsis and the presence of ne-
and 94% specificity in case of LRINEC score ≥ 6, with a              crotising phenomena, as demonstrated by our analysis. The
positive predictive value of 0.29. They concluded that LRI-          research of new optimal cut-offs or the implementation by
NEC score is a useful method to identify CNF cases early,            the mean of correction factors may represent a line of de-
especially in consideration of the easy availability of its pa-      velopment for future perspectives, with the aim of increas-
rameters, even at an early stage.                                    ing the sensitivity and specificity of these scores.
In our analysis, we proposed another optimal cut-off, with
a sensitivity of 54.5% and a specificity of 84.8% in detect-
                                                                     Conclusions
ing CNF for LRINEC score ≥ 7 (Tab. V). Additionally, we
have investigated the utility of this score in predicting the        Septic and necrotising complications rarely occur in pa-
severity of systemic involvement. A cut-off of 6 was set to          tients suffering from a head-neck suppurative infection,
detect sepsis, but low sensitivity and specificity were found        but enormously affect prognosis. Correct diagnosis is un-
(respectively 42.6% and 86.1%) (Tab. V).                             doubtedly based on clinical presentation and instrumental
Another indicator with proven clinical value in case of in-          techniques (CT), but laboratory markers must be taken into
fection is NLR. It has been used as inflammation marker in           consideration as a prompt and valid aid. For this reason,
several diseases, such as myocardial infarction 20, psoria-          we propose the use of LRINEC, NLR and LRINEC x NLR
sis 21, gastritis 22 and gangrenous appendicitis 23. Baglam 24       scores as predictive tools to early evaluate septic complica-
was the first to apply NLR as predictive factor for DNSIs,           tions and the risk of CNF in the course of DNSIs. As con-
especially when occurring as a complication of acute bac-            firmed by our analysis, even though with a sensitivity and
terial tonsillitis in pediatric patients. An NLR cut-off of          specificity values that were not encouraging, perhaps due to
5.4 was set to predict the risk of DNSI in these patients,           the poor number of our cohort, these scores may have util-
with a sensitivity of 96% and a specificity of 83% (positive         ity in discriminating these potential life-threatening condi-
predictive value of 85% and negative predictive value of             tions. Further studies on a larger cohort may be helpful in


Table V. ROC indicators.
                                        Discriminating septic involvement (sepsis/septic shock)
 Test                       AUC              Cut-off              Sens.                Spec.         PV+               PV-
 LRINEC                     0.672               7.0                42.6                86.1          82.1              50.0
 NLR                        0.679               8.2                74.2                61.5          71.0              65.3
 NLRxLRINEC                 0.716              30.4                81.5                52.8          72.1              65.5
                                                          Discriminating CNF
 Test                       AUC              Cut-off              Sens.                Spec.         PV+               PV-
 LRINEC                     0.716               7.0                54.5                84.8           6.9              66.7
 NLR                        0.681              17.5                50.0                84.9           6.2              72.7
 NLRxLRINEC                 0.742              43.5                90.9                59.5           2.1              76.2




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                                                                                                              LRINEC and NRL: a novel laboratory approach




finding other implementations with the purpose of increas-                      12
                                                                                     Wong CH, Khin LW, Heng KS, et al. The LRINEC (Labora-
                                                                                     tory Risk Indicator for Necrotizing Fasciitis) score: A tool for
ing the clinical use of these scores.                                                distinguishing necrotizing fasciitis from other soft tissue infec-
                                                                                     tions. Crit Care Med 2004;32:1535-41. https://doi.org/10.1097/01.
                                                                                     ccm.0000129486.35458.7d
Acknowledgements                                                                13
                                                                                     Kaushik R, Gupta M, Sharma M, et al. Diagnostic and prognostic role
We thank the Medical Laboratory of our Hospital for per-                             of neutrophil-to-lymphocyte ratio in early and late phase of sepsis.
                                                                                     Indian J Crit Care Med 2018;22:660-3. https://doi.org/10.4103/ijccm.
forming blood tests. We are also immensely grateful to                               IJCCM_59_18.
the ‘Istituto di Igiene’ of University of Bari for statistical                  14
                                                                                     Singer M, Deutschman CS, Seymour CW, et al. The Sepsis Defini-
analysis. We would also like to show our gratitude to the                            tions Task Force Members. The third international consensus defini-
University of Bari for the support and for providing all sci-                        tion for sepsis and septic shock (Sepsis-3). JAMA 2016;315:801-10.
                                                                                     https://doi.org/10.1001/jama.2016.0287
entific material for the research.
                                                                                15
                                                                                     Thomas AJ, Meyer TK. Retrospective evaluation of laboratory-based
                                                                                     diagnostic tools for cervical necrotizing fasciitis. Laryngoscope
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     https://doi.org/10.1086/511638                                                  westjem.2017.3.33607




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