Original Article

Scottish Medical Journal

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The role of neutrophil-lymphocyte ! The Author(s) 2020
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ratio and lymphocyte–monocyte sagepub.com/journals-permissions
DOI: 10.1177/0036933020953516
ratio in the prognosis of type 2 journals.sagepub.com/home/scm

diabetics with COVID-19

Gaoli Liu1 , Shaowen Zhang1, Haifeng Hu1, TingTing Liu2 and

Jie Huang3

Abstract
Objectives: To assess the prognostic value of neutrophil-lymphocyte ratio, lymphocyte–monocyte ratio and red cell
distribution width in type 2 diabetics with COVID-19.
Methods: We collected the data of type 2 diabetics with COVID-19 treated in our hospital from January 28 to March
15, 2020 and performed a retrospective analysis. Using severity, duration of hospital stay, and the time required for
nucleic acid results became negative as prognostic indicators, we explored the relationship between these inflammation-
based markers and prognosis of type 2 diabetics with COVID-19.
Results: A total of 134 type 2 diabetics with COVID-19 were selected for this study. Correlation analysis showed that
NLR, LMR and RDW were correlated with prognosis (P < 0.05). In multivariate regression analysis after controlling for
the relevant confounding factors, COVID-19 diabetes patients with higher NLR had heavier severity, longer duration of
hospital stay, more time required for nucleic acid results became negative, and heavier hospital expenses (P < 0.05).
ROC curve result displayed that higher NLR predicted all prognostic indicators with statistical significance, and lower
LMR predicted severe and extremely severe with statistical significance (P < 0.05).
Conclusions: NLR is a more powerful and practical marker for predicting the prognosis of type 2 diabetic COVID-19
patients that is simple and fast.

Keywords
COVID-19, NLR, diabetes, prognostic marker, time required for nucleic acid to become negative

Introduction
The new coronavirus, severe acute respiratory syn-
drome coronavirus 2 (SARS-CoV-2), has spread to
many countries around the world, causing a global out-
break of coronavirus disease 2019 (COVID-19). The
case detection rate changes daily, and morbidity in
each country or region can be queried at any time on
the websites provided by Johns Hopkins University
and other forums.1 The world is burdened by high mor-
bidity and mortality. As of April 6, 2020, there were
1,202,714 laboratory-confirmed cases worldwide, with
a mortality rate of 5.6%. Diabetics accounted for
12%–22% of patients with COVID-19,2–4 higher than
the incidence in non-diabetic people, which was 9.3%.5
Patients with type 2 diabetes required more medical
interventions and had a significantly higher mortality
(7.8% versus 2.7%;) and multiple organ injury than the
non-diabetic individuals.6 Therefore, identifying the
prognosis of type 2 diabetic patients with COVID-19
early is of great significance for clinicians’ ability to
1
Attending Physician, Department of Thoracic surgery, Renmin Hospital
of Wuhan University, PR China
2
Attending Physician, Department of Cardiac Function, Renmin Hospital
of Wuhan University, PR China
3
Chief Physician, Department of Thoracic surgery, Renmin Hospital of
Wuhan University, PR China
Corresponding author:
Jie Huang, Department of Thoracic surgery, Renmin Hospital of Wuhan
University, Jiefang Road 238, Wuhan City 430060, Hubei Province, PR
China.
Email: 13392186@qq.com
2 Scottish Medical Journal 0(0)
make early diagnosis and treatment plans, and thus
reduce the risk of conversion to critical illness.
The role of inflammation in the progression of var-
ious viral pneumonitis has received increasing atten-
tion.4 COVID-19 involves inflammatory processes. In
patients with COVID-19, leukocyte count in the
peripheral blood is normal or decreased in the early
stage, and the lymphocyte count is generally reduced.7
When under stress from COVID-19, cell composition
changes in the patient’s blood become more signifi-
cant.8 Therefore, a rise or fall in leukocytes or lympho-
cytes may be related to the prognosis of patients with
COVID-19.9 The early detection of the neutrophil–
lymphocyte ratio (NLR), lymphocyte–monocyte ratio
(LMR), and red cell distribution width (RDW) has
been used to predict the severity of various diseases,
including COVID-19, and these procedures are eco-
nomical.10–13 However, COVID-19 prognosis includes
not only the severity of the disease, but also when the
patient’s nucleic acid results became negative, duration
of hospital stay, and other factors. Whether NLR,
LMR, and RDW have similar predictive effects on
these prognostic results in type 2 diabetics with
COVID-19 has not been reported.
In this study, we retrospectively analysed the data of
type 2 diabetics with COVID-19 who were treated in
our hospital from January 28 to March 15, 2020, and
explored whether NLR, LMR, and RDW could predict
the prognosis of type 2 diabetics with COVID-19.
Patients and methods
Patients
This study continuously selected a series of type 2 dia-
betic patients with COVID-19 who were hospitalised in
the East Campus of Renmin Hospital of Wuhan
University from January 30, 2020 to March 10, 2020.
Inclusion criteria were as follows: (1) type 2 diabetics
with COVID-19, (2) results of blood routine examina-
tion were obtained within 24 hours of admission.
Patients were excluded using the following criteria:
(1) patients with mild COVID-19, (2) patients with
other chronic diseases, (3) patients who died during
treatment, or (4) patients with missing data.
A diagnosis of COVID-19 required the following:
(1) history of epidemiological exposure; (2) clinical
symptoms: fever (axillary temperature >37.3
C) or
cough, sputum symptoms, or gastrointestinal symp-
toms; (3) laboratory test results: leukocyte count in
peripheral blood normal or decreased in the early
stages, and/or reduced lymphocyte count; (4) pulmo-
nary imaging changes: multiple ground glass shadows
or interstitial thickening seen on early chest CT, extra
pulmonary bands found and progressing in both lungs
with infiltration, and pulmonary consolidation as the
disease worsens, with relatively rare pleural effusion;
and (5) real-time polymerase chain reaction (PCR):
positive nucleic acid test for COVID-19 in respiratory
or blood specimens.14
COVID-19 was categorized as mild, moderate,
severe, and extremely severe in accordance with the
Diagnosis and Treatment Protocol for Novel
Coronavirus Pneumonia (Trial Version 6).15
Consequently, mild COVID-19 was considered to be
associated with mild clinical symptoms, with no sign
of pneumonia on imaging. Patients with moderate
COVID-19 had fever (>37.3
C) and respiratory symp-
toms with radiological findings of pneumonia. Severe
COVID-19 was considered to meet any of the following
criteria: (1) respiratory distress (⭌30 breaths/min), (2)
oxygen saturation 93% at rest, or (3) arterial partial
pressure of oxygen (PaO2)/fraction of inspired oxygen
(FiO2) 300 mmHg (l mmHg ¼ 0.133 kPa). Cases with
chest imaging that showed obvious lesion progression
>50% within 24–48 hours were managed as severe
cases. Extremely severe COVID-19 needed to meet
one of the following conditions: (1) respiratory failure
requiring mechanical ventilation, (2) shock, or (3) other
organ failure requiring ICU care.
A confirmed COVID-19 patient required simulta-
neous positive results for both SARS-CoV-2 open
reading frame 1ab (SARS-CoV-2 ORF1ab) and
SARS-CoV-2 nucleocapsid protein gene (SARS-CoV-
2 N gene). The standard for confirming that the
patient’s nucleic acid results had turned negative was
that two consecutive throat swab tests were negative in
a testing interval > 24 hours.
All patients admitted to our hospital were referred
from other hospitals, because our hospital was a
government-designated facility for the diagnosis and
treatment of severe COVID-19. Some patients had
been treated with antiviral drugs at local hospitals,
and patients with diabetes and/or hypertension rou-
tinely received antihypertensive and/or antihypoglyce-
mic treatment before and after admission.
A routine blood test performed within 24 hours after
admission was collected from the medical record fol-
lowing discharge. NLR and LMR were calculated by
the ratio of neutrophils to lymphocytes and lympho-
cytes to monocytes, respectively. Prognostic indicators
included disease severity, time required for negative
nucleic acid results, and duration of hospital stay.
Ethics statement
The treatment of each patient conformed to the ethical
principles outlined in the Declaration of Helsinki. We
also obtained informed consent from the patient or
relatives. The data required for the study, including
Liu et al. 3

past history, age, sex, BMI, and laboratory results,
were collected after discharge.
Statistics
Continuous variables were expressed as the mean 
standard deviation (SD), and categorical variables
were expressed as cases or percentages. Student’s t
test and Mann-Whitney U test were used for compar-
ative analysis of continuous variables, and v2 test was
used for categorical data as appropriate. The associa-
tions between inflammatory markers and clinical out-
comes were analysed using correlation analysis and
multivariate regression analysis adjusted for age, sex,
the presence of hypertension, and BMI. We used a
receiver operating characteristic (ROC) curve to
assess the accuracy of each indicator in predicting
prognosis of type 2 diabetics with COVID-19. The
parameters of the ROC analyses were defined as
severe and extremely severe COVID-19, hospital
stay > 26 (median) days, time required for nucleic
acid results became negative >19 (median) days, and
hospital expenses incurred over 33474.455 (median)
yuan CNY. Data analyses were performed using
SPSS 25.0 and MedCalc 18.5. P values < 0.05 were con-
sidered statistically significant.
Results
Patient characteristics
There were 134 type 2 diabetic COVID-19 patients
(52 moderate COVID-19, 72 severe COVID-19, 10
extremely severe COVID-19) selected in this study.
Of the patients, 36 were male and 58 were female,
and the average age was 65.54  11.28 years, with a
minimum age of 41 years and a maximum age of
92 years. Five patients used ACE2-stimulating drugs
before admission. Sixteen patients were excluded for
the following reasons: two patients had a history of
tumours, two patients were undergoing dialysis for
renal failure, eight patients were accompanied by liver
and kidney dysfunction, and two patients died.
We used case-control matching to extract the same
number of non-diabetic patients, and compared the
baseline characteristics and prognosis in diabetics and
non-diabetics. The matching conditions were sex: 0,
age: 8, hypertension: 0, and BMI: 8. The results
showed that sex, age, BMI, the presence of hyperten-
sion, neutrophil count, lymphocyte count, monocyte
count, RDW, severity, time required for nucleic acid
results to become negative, and hospital expenses did
not show significant difference (P > 0.05). However,
type 2 diabetics had higher a NLR, a lower LMR,
and longer hospital stays than non-diabetics, and
these differences were statistically significant
(P < 0.05) (Table 1).
The relationship between inflammatory markers and
prognosis of diabetic COVID-19 patients
Correlation analysis between inflammatory markers
and prognosis revealed that age, NLR, and LMR
were correlated with COVID-19 severity in type 2 dia-
betics. NLR was correlated with duration of hospital
stay and the time required for nucleic acid results to
become negative, and NLR, LMR, and RDW were
correlated with hospital expenses (P < 0.05) (Table 2).

Table 1. Comparison of baseline characteristics between the diabetics and non-diabetics.

Variables Type 2 diabetics Non-diabetics P value Statistic

Sex (male) 76 (56.7%) 76 (56.7%) 1.0000 v2 ¼ 0.000

Age (year) 65.54  11.28 64.82  10.98 0.710 Z ¼ –0.372
BMI (kg/m2) 23.97  3.39 24.14  3.03 0.570 Z ¼ –0.567
Hypertension 54 (40.3%) 54 (40.3%) 1.000 v2 ¼ 0.000
Neutrophil count (109/L) 4.62  2.89 4.11  2.54 0.138 Z ¼ –1.482
Lymphocyte count (109/L) 1.15  0.62 1.28  0.63 0.204 Z ¼ –1.271
Monocyte count (109/L) 0.52  0.19 0.47  0.20 0.165 t ¼ 1.395
NLR 6.88  8.21 4.82  6.56 0.018 Z ¼ –2.372
LMR 2.05  1.20 3.05  1.61 0.000 Z ¼ –4.530
RDW% 12.37  0.88 12.55  1.13 0.224 Z ¼ –1.217
Severity (1/2/3)% 52 (38.8%)/72 (53.7%)/ 31 (26.9%)/82 (61.2%)/ 0.311 v2 ¼ 2.472
10 (7.5%) 16 (11.9%)
Duration of hospital stay (day) 29.60  14.36 24.52  12.83 0.031 Z ¼ –2.159
Time required for nucleic 21.99  13.07 18.24  10.69 0.094 Z ¼ –1.672
acid results became
negative (days)
Hospital expenses (yuan, ¥) 48032.55  54517.60 47044.55  57191.54 0.342 Z ¼ –.950
Note: Severity (1/2/3) %: 1, 2 and 3 represent moderate, severe, extremely severe.
4 Scottish Medical Journal 0(0)

Table 2. Correlation analysis between inflammatory markers and prognosis.

Time required for nucleic

Severity Duration of hospital stay acid results became negative Hospital expenses

correlation Correlation Correlation Correlation

P value coefficient P value coefficient P value coefficient P value coefficient

Sex (male) 0.021 –0.282 0.242 –0.145 0.083 –0.214 0.312 –0.125
Age (year) 0.401 0.104 0.817 –0.029 0.477 –0.088 0.692 0.067
BMI (kg/m2) 0.837 0.026 0.955 –0.007 0.836 –0.026 0.843 –0.025
Hypertension 0.065 –0.227 0.825 –0.028 0.539 0.076 0.960 –0.006
NLR 0.000 0.436 0.010 0.313 0.008 0.321 0.011 0.311
LMR 0.002 –0.371 0.070 –0.223 0.061 –0.230 0.007 –0.326
RDW% 0.401 0.104 0.425 0.009 0.895 0.016 0.018 0.287

Table 3. ORs of inflammatory markers for prognosis in patients with COVID-19 accompanied.

Time required for nucleic Hospital expenses

Duration of hospital acid results became <33474.455 yuan
Common or not stay <26 days or not negative <19 days or not ¥ or not

OR (95% CI) P Value OR (95% CI) P Value OR (95% CI) P Value OR (95% CI) P Value

NLR 2.548 (1.225–5.297) 0.012a 1.972 (1.061–3.666) 0.032 2.411 (1.229–4.733) 0.011b 2.915 (1.444–5.886) 0.003
LMR 0.548 (0.282–1.064) 0.076a 0.843 (0.479–1.482) 0.553 0.612 (0.335–1.119) 0.111 0.619 (0.342–1.120) 0.113
RDW% 1.521 (0.749–3.091) 0.246a b
1.420 (0.758–2.661) 0.273 1.166 (0.629–2.161) 0.625 1.716 (0.894–3.293) 0.105
Note: Adjusted for age, sex, BMI and hypertension.
a
The OR of hypertension was statistically significant, P < 0.05.
b
The OR of age was statistically significant, P < 0.05.

The multivariate logistic regression models, adjusted
for age, sex, the presence of hypertension, and BMI,
revealed that COVID-19 patients with type 2 diabetes
who had a higher NLR had heavier disease severity, a
longer hospital stay, more hospital expenses, and
needed more time required for nucleic acid results to
become negative (P < 0.05). LMR and RDW had no
correlation with prognosis (P > 0.05). Hypertension
was correlated with COVID-19 severity, and age was
correlated with time required for nucleic acid results to
become negative (P < 0.05) (Table 3).
Predictive value of inflammatory markers for
prognosis
We analysed the area under the curve (AUC) of ROC
curves of NLR, LMR, and RDW for predicting the
prognosis of type 2 diabetic COVID-19 patients.
Higher NLR predicted severe & extremely severe
COVID-19, hospital stay >26 days, time required for
nucleic acid results to become negative >19 days, and
hospital expenses >33474.455 yuan, with statistical sig-
nificance (P < 0.05) (Table 4). NLR þ hypertension
(AUC: 0.736, 95% CI: 0.618–0.855, P ¼ 0.001) and
age þ hypertension (AUC: 0.688, 95% CI: 0.563–
0.795, P ¼ 0.004) and also predicted severe and
extremely severe COVID-19 with statistical significance
(P < 0.05). NLR þ age (AUC: 0.730, 95% CI: 0.608–
0.831, P ¼ 0.000) predicted the time required for nucleic
acid results to become negative >19 days with statisti-
cal significance (P < 0.05). The AUCs of NLR,
NLR þ hypertension, and age þ hypertension were
not significantly different in predicting severe and
extremely severe COVID-19, and the AUCs of NLR
and NLR þ age were also not significantly different in
predicting time required for nucleic acid results to
become negative > 19 days (P > 0.05). A lower LMR
predicted severe and extremely severe COVID-19 with
statistical significance (P < 0.05) (Table 4).
We also verified the ability of inflammatory markers
to predict prognosis. The results showed that NLR and
LMR, when bound by the cut-off value, were statisti-
cally significant predictors of different prognoses
(P < 0.05) (Table 5).
Discussion
The results of the this study showed that NLR had
predictive effects not only for the severity of COVID-
19 in type 2 diabetics, but also for when patient’s nucle-
ic acid results turned negative, duration of hospital
stay, and hospital expenses. In multivariate regression
Liu et al. 5

Table 4. ROC curves in predicting poor prognosis of inflammatory markers.

Time required for

Severe & extremely Duration of hospital nucleic acid results Hospital expenses
severe or not stay >26 days became negative >19 day >33474.455 yuan

AUC (95% CI) P Value AUC (95% CI) P Value AUC (95% CI) P Value AUC (95% CI) P Value

NLR 0.730 (0.607–0.854) 0.002 0.661 (0.528–0.794) 0.024 0.672 (0.543–0.801) 0.016 0.725 (0.601–0.850) 0.002
LMR 0.322 (0.190–0.455) 0.015 0.435 (0.296–0.575) 0.365 0.380 (0.244–0.515) 0.090 0.385 (0.249–0.520) 0.104
RDW% 0.542 (0.404–0.680) 0.563 0.550 (0.411–0.689) 0.485 0.487 (0.348–0.626) 0.856 0.589 (0.452–0.726) 0.210

Table 5. ORs of NLR and LMR bounded by the cut-off value in different prognosis of diabetics with COVID-19.

NLR > cut-off or not LMR> cut-off or not

Cut-off OR (95% CI) P value Cut-off OR (95% CI) P value

Severe & extremely severe 3.91 6.429 (2.103–19.655) 0.001 2.21 0.190 (0.063–0.575) 0.002
COVID-19 or not
Duration of hospital stay >26 3.74 4.889 (1.728–13.832) 0.002 – – –
day or not
Time required for nucleic acid 3.25 4.308 (1.535–12.092) 0.005 – – –
results became negative >19
day or not
Hospital expenses >33474.455 4.02 6.534 (2.236–19.096) 0.000 – – –
yuan or not

analysis, after controlling for the relevant confounding
factors, type 2 diabetics with COVID-19 with higher
NLRs had higher disease severity, longer hospital
stays, more hospital expenses, and more time required
for nucleic acid results to become negative. ROC curve
results showed that a higher NLR predicted all prog-
nostic indicators with statistical significance, and a
lower LMR predicted severe and extremely severe
COVID-19 with statistical significance. Therefore, our
findings suggest that NLR and LMR are useful and
practical markers for identifying type 2 diabetics with
COVID-19 who have poor prognoses.
The possible mechanism that increased diabetic sus-
ceptibility to COVID-19 may be that the use of thiazo-
lidinedione in diabetics increased the expression of
ACE2, and thus, human pathogen coronavirus may
bind to target cells via ACE2. Expression of ACE2 is
more concentrated in epithelial cells of the lung, intes-
tine, kidney, and blood vessels.15 In this study, five type
2 diabetics used ACE2-stimulating drugs before admis-
sion, and diabetics with COVID-19 had heavier inflam-
mation (higher NLR and lower LMR) and longer
hospital stays than non-diabetics.
In the progression of viral pneumonia, the balance
of T cells, CD4þ T cells, and CD8þ T cells was very
important in the fight against pathogens and the devel-
opment of autoimmunity.16 T helper cells induce the
production of cytokines, such as IL-17, through
the NF-kB signalling pathway,17 which can increase
the aggregation of monocytes and neutrophils.18
SARS-CoV-2 infects circulating immune cells and
increases apoptosis of lymphocytes, leading to lympho-
cytopenia.19 Therefore, NLR and LMR changed with
the severity of COVID-19. In this study, NLR and
LMR predicted the severity well, and NLR was also
a strong predictor of hospital stay duration and hospi-
tal expenses. This may have occurred because hospital
stay, hospital expenses, and COVID-19 severity were
correlated. As mentioned before, SARS-CoV-2 infec-
tion leads to lymphopenia and a corresponding
decrease in CD4þ T cells, which delays clearance of
the virus.20 In our study, a higher NLR was correlated
with more time required for nucleic acid results to
become negative.
RDW is a parameter reflecting the heterogeneity of
red blood cell volume, which is expressed by the coef-
ficient of variation of red blood cell volume.21 RDW
can be used as an important parameter in the differen-
tial diagnosis of thalassemia and iron deficiency
anemia.22 There was a positive correlation between
RDW and inflammatory markers such as erythrocyte
sedimentation rate and C-reactive protein.23 This asso-
ciation may be a sign of abnormal ferritin levels and/or
anemia,24 and elevated levels of inflammatory
6 Scottish Medical Journal 0(0)
cytokines could play an important role in SARS-CoV-
2-induced lung damage.9,25 Previous studies have
shown that RDW could be used as a prognostic
factor in patients with diabetes.26,27 However, in this
study, RDW showed no prognostic effect. The reasons
for this require further study.
Conclusion
In conclusion, NLR is a more powerful and practical
marker for predicting the prognosis of type 2 diabetic
COVID-19 patients that is simple and fast.
Limitations
The study had several limitations. First, we collected
fewer cases, it was not a prospective study, and the level
of evidence was low. Second, we did not stratify
patients by the type of drug they used, and we did
not explore more correlations. Third, we did not com-
pare the role of these markers in diabetic patients with
their role in non-diabetic patients. Although these lim-
itations existed, this study also had its strengths. This is
the first study to comprehensively investigate the prog-
nostic value of NLR, LMR, and RDW in diabetic
COVID-19 patients.
Authors’ contribution
Jie Huang designed the conception for this study。
Gaoli Liu, and Jie Huang made important contributions
to the analysis and preparation of manuscripts.
Gaoli Liu, Shaowen Zhang, TingTing Liu collected and
analyzed the data and wrote the manuscript.
Gaoli Liu and Haifeng Hu helped the analysis through
reasonable discussion
Declaration of Conflicting Interests
The author(s) declared no potential conflicts of interest with
respect to the research, authorship, and/or publication of this
article.
Funding
The author(s) received no financial support for the research,
authorship, and/or publication of this article.
ORCID iD
Gaoli Liu https://orcid.org/0000-0001-6675-2422
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