European Journal of Radiology 108 (2018) 236–241

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European Journal of Radiology

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

Research article

Optimal threshold for the diagnosis of anemia severity on unenhanced T

thoracic CT: A preliminary study
Qing-Qing Zhoua, Yu-Sheng Yua, Yu-Chen Chenb, Bi-Biao Dinga, Si-Yue Fanga, Xianfeng Yangc,
⁎
Bing Zhangc, Hong Zhanga,
a
Department of Radiology, The Affiliated Jiangning Hospital of Nanjing Medical University, No. 168, Gushan Road, Nanjing, Jiangsu Province, 211100, China
b
Department of Radiology, Nanjing First Hospital, Nanjing Medical University, No. 68, Changle Road, Nanjing, 210006, China
c
Department of Radiology, The Affiliated Drum Tower Hospital of Nanjing University Medical School, No. 321, Zhongshan Road, Nanjing, 210008, China

A R T I C LE I N FO A B S T R A C T

Keywords: Objective: To investigate and evaluate the value as accuracy of diagnosis different degrees of anemia through the
Anemia unenhanced thoracic computed tomography (CT) scan.
Computed tomography Materials and methods: The CT attenuation of right ventricle (RV) cavity, left ventricular (LV) cavity, inter-
Interventricular septum ventricular septum and difference between the interventricular septum and left ventricle cavity (IVS-LV) were
Hemoglobin
retrospectively analyzed and measured in 317 patients with different degrees of anemia and the normal patients.
Thorax
The hemoglobin (Hb) level was estimated within 24 h. Statistical analysis was made to obtain the best diagnostic
threshold of anemia levels by CT scan, measurement repeatability was assessed using the intra-class correlation
coefficient (ICC) values.
Results: An obvious parallel correlation of hemoglobin concentration and CT attenuation of IVS-LV existed (the
determination coefficient was 0.818; P < .001). Based on receiver operating characteristic (ROC) curves, the
conclusion was that when the threshold of CT attenuation of IVS-LV at (5.5–9.5) HU in male and (4.5–8.5) HU in
female, the specificity for diagnosing mild anemia was low, while the sensitivity was very high (87.1%, 100%,
respectively), if the CT value was among (9.5–13.5) HU in male or (8.5–13.5) HU in female, the sensitivity and
specificity for diagnosing moderate anemia were fine (92.9% and 74.8% in male; 93.9% and 60.0% in female),
and once the CT value was more than 13.5 HU the sensitivity and specificity for diagnosing severe anemia in all
gender were greatly good (94.7% and 83.6% in male; 82.4% and 84.6% in female). The intra-and inter-observer
reliability and reproducibility were good (ICC were all more than 0.99).
Conclusion: The CT attenuation of IVS-LV could predict the severity of anemia with good sensitivity and spe-
cificity, which could add value to clinical practice and more importantly facilitating patient care as hematologic
laboratory investigations are lacking.

1. Introduction negative impact on socioeconomic development [2,4], which is one of

Anemia is defined as low blood hemoglobin concentration and is a
public health issue in various countries worldwide. According to the
WHO, the prevalence of anemia increases with age, with a global in-
cidence of 24.8% (1.62 billion) [1,2]. Anemia affects half a billion
women of reproductive age worldwide. In 2011, 29% (496 million) of
non-pregnant women and 38% (32.4 million) of pregnant women aged
15–49 years were anemic [3]. Anemia may adversely affect both motor
and cognitive development of children, productivity in adults and has a
the leading factors contributing to global disease burden and is asso-
ciated with increased risk of overall, maternal and perinatal morbidity
[5]. Given this, early detection and prompt treatment are imperative to
avoid poor clinical outcomes.
Currently, the diagnosis of clinical anemia is mainly determined by
the detection of hemoglobin (Hb) concentration in peripheral blood [6].
Many previous studies have showed that anemia can be indicated on
unenhanced computed tomography (CT) of the thorax and head [7–15].
They claimed that anemia can be diagnosed by observing “aortic ring

Abbreviations: CT, computed tomography; HU, hounsfield unit; RV, right ventricle; LV, left ventricular; IVS-LV, difference between the interventricular septum and
left ventricular cavity; Hb, hemoglobin; DVS, dural venous sinuses; ROIs, regions of interest; ICC, intra-class correlation coefficient; ROC, receiver operating
characteristic; NC, normal control
⁎
Corresponding author.
E-mail address: jnyyfsk@126.com (H. Zhang).

https://doi.org/10.1016/j.ejrad.2018.10.007
Received 14 June 2018; Received in revised form 16 September 2018; Accepted 8 October 2018
0720-048X/ © 2018 Published by Elsevier B.V.
Q.-Q. Zhou et al. European Journal of Radiology 108 (2018) 236–241

Fig. 1. A. One 27-year-old woman with mild anemia (Hb level 99 g/L). LV CT value was 29 HU, RV CT value was 31 HU, septum mean CT value was 376 HU, IVS-LV
CT value was 7 HU. B. One 43-year-old man with moderate anemia (Hb level 88 g/L). LV CT value was 20 HU, RV CT value was 21 HU, septum mean CT value was 32
HU, IVS-LV CT value was 12 HU. C. One 38-year-old woman with severe anemia (Hb level 49.2 g/L). LV CT value was 20 HU, RV CT value was 21 HU, septum mean
CT value was 41 HU, IVS-LV CT value was 21 HU. D. One 29-year-old woman who was normal participant (Hb level 128 g/L), and a long strip was drawn connecting
the depressed areas on the heart near the sternum (top arrow) and the depressed point near the spine (bottom arrow).
LV: left ventricular; RV: right ventricle; IVS-LV: difference between the interventricular septum and left ventricular cavity; Hb: hemoglobin; CT: computed tomo-
graphy.

sign” or “interventricular septum sign”, or they can deduce anemia by information to patient care.
measuring the CT value of dural venous sinuses (DVS). However, none
of the previous studies have demonstrated predictability of severity of
2. Materials and methods
anemia on unenhanced thoracic CT by measuring CT attenuation of
difference between the interventricular septum and left ventricular
2.1. Study population
cavity (IVS-LV), nor have established statistically significant data re-
garding sensitivity and specificity. Even more, they failed to propose
This retrospective single-center study was approved by the local
effective methods when distinguished mild anemic patients from the
medical ethics review boards. A total of 317 consecutive patients (mean
normal. Although Chaudhry et al. [14] had assessed CT attenuation of
age ± standard deviation, 57.66 ± 16.50; 164 females) who pre-
DVS to evaluate the severity of anemia, nevertheless, the consistency of
sented at hospital from January 2016 to March 2017 were enrolled, in
measurement was not so well and the clinical popularizing rate was
addition, all participants performed an unenhanced CT scan and per-
low.
ipheral blood examination within 24 h. Most of them suffered with
As anemic patients are more likely to be hospitalized, have in-
hematological diseases such as iron deficiency anemia, myelodysplastic
creased lengths of hospital stays, have increased disability resulting in
syndrome, leukemia and lymphoma, and chronic kidney disease in-
greater health care costs, furthermore, the level of hemoglobin has a
cluding chronic nephritis, renal failure, and others were malignant tu-
significant influence of patient's life quality and the prognosis of the
mors, multiple fractures and coronary heart disease, cardiac in-
disease [16–25]. The primary purpose of this study was to evaluate the
sufficiency. According to the hemoglobin level, four subgroups have
strength of correlation between CT attenuation of IVS-LV and patients’
been formed: mild anemia group (n = 60), moderate anemia group
Hb level. We hypothesized that the optimal threshold for diagnosing
(n = 91), severe anemia group (n = 53) and the normal control (NC)
severity of anemia was obtained which will be beneficial to clinical
group (n = 113). Anemia is classified according to the WHO [6] and
treatment and disease prognosis for the patients who cannot tolerate
Chinese criteria of diagnostic anemia [26]: hemoglobin concentration
blood drawing (such as severe coagulopathy) or in emergency thor-
(g/L) at sea level is (90–120) g/L in male defined as mild anemia (fe-
acoabdominal CT examination, such information could add serviceable
male: [90–110] g/L); (60–90) g/L defined as moderate anemia; less

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Q.-Q. Zhou et al. European Journal of Radiology 108 (2018) 236–241

Table 1
Descriptive analysis of baseline characteristics of the study population and the CT value.
Index NC group Mild anemia group Moderate anemia group Severe anemia group P
n = 113 n = 60 n = 91 n = 53 value

Age (years) 57.00 ± 14.67 57.40 ± 17.72 59.88 ± 15.77 55.55 ± 19.73 .439
No. of women 52/113 (46.0 %) 29/60 (48.3%) 49/91 (53.8%) 34/53(64.2%) .159
Hb level (g/L) 133.49 ± 12.06 101.63 ± 7.20 73.03 ± 8.05 53.56 ± 5.60 .000*
RV CT value 36.27 ± 4.76 29.13 ± 4.10 24.08 ± 5.10 21.25 ± 4.10 .000*
LV CT value 35.20 ± 4.65 28.97 ± 4.50 23.08 ± 5.12 19.96 ± 4.20 .000*
Septum CT value 38.47 ± 4.46 37.00 ± 4.17 36.76 ± 5.06 36.23 ± 3.84 .007
IVS-LV CT value 3.27 ± 2.75 8.03 ± 2.72 13.56 ± 2.94 16.26 ± 2.46 .000*

Note—Unless otherwise indicated, data are means ± standard deviations, and numbers in parentheses are percentages.
LV: left ventricular; RV: right ventricle; IVS-LV: difference between the interventricular septum and left ventricular cavity; Hb: hemoglobin; CT: computed tomo-
graphy; NC: normal control.
* P < .001 The difference was statistically significant in comparison with all subgroups.

than 60 g/L defined as severe anemia. The exclusion criteria were as
follows: (1) the subjects were aged under 15 years; (2) had diseases that
affect cardiac density such as vasculitis lesions, glycogen accumulation,
or hepatic hemochromatosis; (3) had a history of iodine allergy test or
transfusion high protein recently; (4) performed enhanced scan with
contrast medium before the CT scan; (5) images have motion or metal
(calcification) streak artifacts.
2.2. CT scan and data measurement
All non-contrast thoracoabdominal CT studies were volume scans
performed on a 16-detector row CT scanner (Brilliance,Philips,
Eindhoven, the Netherlands) with a chest scan from the thoracic inlet to
the diaphragm, and abdomen scan from the top of the diaphragm to the
anterior superior iliac spine level. The scans were performed after
breath-hold. Scan parameters for this protocol were tube voltage
120 kV, automatic tube current setting (30–500 mA), rotation time of
0.4 s, and axial slice thickness of 0.5 mm with reconstruction interval of
1.25 mm. Unenhanced CT images were evaluated on a preset standard
mediastinum window (window width, 350 HU; window level, 40 HU).
Two experienced pectoral radiologists (Y.S.Y. and B.B.D.; pectoral
radiologist with 12 and 10 years' experience, respectively) who were
blinded to the subjects’ characteristics independently read and mea-
sured the CT value (unit HU) of patient's left ventricle (LV), right
ventricle (RV), and the ventricular septal [10] on a Picture Archiving
and Communication System (PACS) (ZLsoft, Chongqing, China). The
average of two measurements was considered as the result, and the CT
attenuation difference between the interventricular septum and left
ventricle (IVS-LV) was calculated.
Regions of interest (ROIs) were placed on the LV cavity, RV cavity,
and interventricular septum. The sizes of the ROIs differed from each
other based on the difference in size of the underlying, irregularly long
strips was measured on interventricular septum and small rounds were
taken on ventricular cavity approximately 100 mm2 for the areas
(Fig. 1). We choose the level avoiding artifacts from the spine as the
heart measurement levels. In cases where difficulty was encountered
during delineation of the interventricular septum, a long strip con-
necting the depressed area on the heart margin near the sternum (top
arrow) and the depressed point near the spine or descending aorta
(bottom arrow) was drawn, and the possible CT value of the inter-
ventricular septum was measured along this line (Fig. 1D)
2.3. Statistical analysis
parameters and the least significant difference (LSD) multiple com-
parison method was employed to compare differences among variables.
Categorical variables were assessed by the Pearson’s χ2 test, with the
Fisher exact test used when n < 40 or T < 1. To identify the optimal
diagnostic parameter, scatter plot and simple linear regression analysis
were performed in the study groups. Receiver operating characteristic
(ROC) curve analysis was performed to determine the threshold CT
value for diagnosing the severity of anemia, and Medcalc Statistical
software version 15.6.1 (Medcalc Software bvba, Ostend, Belgium) was
used to compare the statistical significance of the ROC areas among
these groups. Measurement repeatability was assessed using intraclass
correlation coefficient (ICC) values. A P value less than 0.05 was con-
sidered to represent the significance threshold. All statistical analyses
were performed with SPSS software version 21.0 (International
Business Machines Corporation, Chicago Illinois, United States). All
graphics were created using GraphPad Prism version 5.00 for Windows
(GraphPad Software, San Diego California, United States).
3. Results
The study cohort contained 164 (51.74%) female and 153(48.26%)
male participants aged 57.66 ± 16.49 years (mean ± standard de-
viation; range, 16–90 years). The NC group (n = 113; age,
57.00 ± 14.67 years; 52 females), mild anemia group (n = 60; age,
57.40 ± 17.72 years; 29 females), moderate anemia group (n = 91;
age, 59.88 ± 15.77 years; 49 females), and severe anemia group
(n = 53; age, 55.55 ± 19.73 years; 34 females) were matched for age
and gender (P > .05). After ANOVA analysis and LSD multiple com-
parison, Hb level, the CT value of RV, LV and IVS-LV showed significant
difference in comparison with all subgroups (all P < .001) (Table 1).
A pectoral radiologist (Y.S.Y.) measured all the parameters using the
PACS once and repeated the measurement a week later, while another
pectoral radiologist (B.B.D.) obtained another measurement. The intra-
and inter-observer ICC values were close to 1 (Table 2), showing the
high reliability and good repeatability of CT measurements obtained
using the PACS.
In all subjects, the scatter points of Hb level, RV CT value, LV CT
value and IVS-LV CT value were all linearly distributed around the
diagonal. There was a positive linear correlation between Hb level and
RV/LV CT value (R2 = 0.646 and 0.664 respectively; P < .001). Hb
Table 2
Comparison of intra- and inter-observer measurement reliability and repeat-
ability.

Demographic information, measurement data and clinical char- ICC 95%CI P value
acteristics (age, gender and Hb level) were reported as mean ±
intra-observer 0.997 0.996–0.997 .573
standard deviation and compared between the four groups. The per- inter-observer 0.993 0.991–0.995 .577
formance of the Kolmogorov-Smirnov test to detect normal distribution.
One-way analysis of variance (ANOVA) was used for continuous ICC: intraclass correlation coefficient.

238
Q.-Q. Zhou et al.
Fig. 2. Scatter plot and simple linear regression analysis between the difference
in CT attenuation between the left ventricle and interventricular septum (IVS-
LV CT value) and hemoglobin level. The correlation coefficient was 0.818
(P < .001).
IVS-LV: difference between the interventricular septum and left ventricular
cavity; CT: computed tomography.
level was significantly negatively correlated with IVS-LV CT value
(R2 = 0.818; P < .001) (Fig. 2). Therefore, IVS-LV CT value was se-
lected as diagnostic indicator of the severity of anemia.
The results of ROC analysis in male groups (n = 153) were shown in
Fig. 3(A). The area under the curve (AUC) was 0.908 (95% CI: 0.862,
0.955; P < .001) for IVS-LV CT value in diagnosing severe anemia,
0.859 (95%CI: 0.802, 0.916; P < .001) for diagnosing moderate an-
emia, and 0.471 (95%CI: 0.384, 0.558; P > .05) for diagnosing mild
anemia. Therefore, the diagnostic value of IVS-LV CT value in diag-
nosing mild anemia was limited, while in diagnosing moderate and
severe anemia were high. According to the Youden index, when the
IVS-LV CT value threshold was set at 5.5 HU in diagnosing mild anemia,
the sensitivity can reach to 87.1%, however, the specificity is low.
When the CT value was (5.5–9.5) HU, the sensitivity and specificity for
diagnosing moderate anemia was 92.9% and 74.8%, and when greater
than 13.5 HU, the sensitivity and specificity for diagnosing severe an-
emia was 94.7% and 83.86%.
ROC analysis in female groups (n = 164) were shown in Fig. 3(B).
The AUC was 0.923 (95%CI: 0.881, 0.966; P < .001) for IVS-LV CT
value in diagnosing severe anemia, 0.731 (95%CI: 0.656, 0.806;
P < .001) for the moderate anemia group, and0.40 (95%CI, 0.317,
0.482; P > .005) for the mild anemia group. In a similar way, the di-
agnostic value in diagnosing mild anemia was limited, while in diag-
nosing moderate and severe anemia were high. Set the IVS-LV CT value
threshold at 4.5 HU, the sensitivity of diagnosing mild anemia can
reach to 100.0%, nevertheless the specificity was low. Set the IVS-LV
CT value at (4.5–8.5) HU in diagnosing moderate anemia, the
Fig. 3. Comparison of receiver operating characteristic (ROC) curves of IVS-LV CT value diagnosing various degrees of anemia in male patients (A) and female
patients (B).
IVS-LV: difference between the interventricular septum and left ventricular cavity; CT: computed tomography.
239
European Journal of Radiology 108 (2018) 236–241
sensitivity and specificity were 93.9% and 60.0%, and when the CT
value was greater than 13.5 HU in diagnosing severe anemia, the di-
agnostic sensitivity was 82.4% and the specificity was 84.6%.
4. Discussion
Anemia has a variety of harmfulness to human health, and the se-
verity of anemia has a major impact on disease progression and prog-
nosis, especially to patients with moderate or severe anemia.
Additionally, this hazard is even more pronounced if the patients were
the elderly or children [16–18,22,24]. The radiologist makes a sea-
sonable and accurate diagnosis of anemia (especially anemia severity)
in patients who cannot tolerate blood draws (such as severe coagulo-
pathy) or performed emergency thoracoabdominal CT examination
could provide assistance to clinicians’ treatment programs.
The X-ray attenuation of the material produces different CT values
[27]. The attenuation coefficient for whole blood is related linearly to
the hemoglobin [28]. This theoretical analysis was also consistent with
our study. However, the interventricular septum is composed of myo-
cardial tissue, the density was less changed in the exclusion of en-
docardial disease. Corcoran et al [8] have pronounced that when the
hemoglobin level was 105–128 g/L, the interventricular septum could
be discerned on CT plain scan images; when the hemoglobin level was
105–128 g/L, approximate 50% of the interventricular septum could be
distinguish; when the hemoglobin level was 129–160 g/L, the inter-
ventricular septum couldn't be distinguished. It is confirmed that there
is a correlation between the degree of anemia and CT attenuation dif-
ference between the LV cavity and interventricular septum. As the
concentration of hemoglobin in the blood was decrease, the inter-
ventricular septum becomes more obvious, the bigger of IVS-LV CT
value.
For the first time, Doppman et al. [15] proposed that patients with
severe anemia with a low density blood pool on CT scan, and the
morphology of ventricular and ventricular wall could be discerned by
naked eyes. He also recommended that if the interventricular septum
could be discerned on CT scan, it indicated the presence of severe an-
emia. As our study revealed, when people suffered from severe anemia,
the CT attenuation between IVS-LV was larger, therefore the inter-
ventricular septum sign was more likely to be found. When people
suffered from mild anemia, the difference was small, so it was difficult
to distinguish the severity of anemia by subjective observation only. It
was necessary to measure the specific CT value to increase discernment.
Wojtowicz et al. [7] further demonstrated that these manifestations
could be presented when the CT attenuation between the ventricular
wall and ventricular cavity was at least 6–8 HU after analyzed 21 cases
of severe anemic patients' CT images. Hai et al. [10] considered a CT
attenuation difference > 10 HU in male patients or > 12 HU in female
patients would be an almost definite sign of severe anemia. The further
analysis of present study was basically consistent with the above
Q.-Q. Zhou et al.
previously reports.
In the current study, DVS, aorta, abdominal aortic, inferior vena
cava or other large vessels were not selected as the measurements in-
dexes, which was consistent with the research of Hai et al. [10]. In their
standpoint, the best quantitative diagnostic of anemia by CT scan was
the attenuation of IVS-LV rather than the blood pool. As the scan
parameters are diverse for different CT scanners, especially the value of
kilovolt have a certain influence to the densities and discrimination
between materials [29], the CT value of blood pool is inconsistent
under different scanners. Therefore, the difference value method was
adopted in this study which can maximum avoid inconsistent mea-
surements from different machines. In normal human arteries [30], the
arterial wall consists of collagen, elastin, fibrillin, glycoproteins and
proteoglycans collagen. Nevertheless, some diseases of the aorta such as
arteriosclerosis could increase the arterial wall density [30], rising the
false positive rate of the aortic ring sign. In addition, abdominal CT
examination were performed in most emergency circumstances, in-
cluding interventricular septal levels generally, which could be used to
measure the compartmental differences. Therefore, measurement of the
IVS-LV CT value has a strong feasibility and practicality. Left ven-
tricular papillary muscles on the ventricular walls appeared the soft
tissue density similar to the ventricular septum, and moved with the
ventricular contraction [31]. Therefore, ROIs were placed on the po-
sition near the interventricular septum in order to avoid the impact of
the papillary muscles.
Several constraints must be acknowledged in the current study.
Firstly, our study is limited in that our scanner’ s rotation time was
0.4 s, which is too long to avoid artifacts owing to cardiac motion.
Cardiac motion may deteriorate the image quality, thus influencing CT
attenuation. Secondly, the tube voltage was 120 kV, as to other scan
parameters, whether the IVS-LV CT value consistent with the results of
this study required further study. Finally, the sample size was too small
especially the severe anemic patients (Hb < 60 g/L), although there
was normal distribution of study sample, the addition of which may
change the CT attenuation cutoff values for anemia severity classifica-
tion. Therefore, various advanced, extremely fast CT scanners and large
number of samples were required in subsequent studies.
5. Conclusion
The present study has further demonstrated that CT attenuation
difference between the left ventricle cavity and interventricular septum
could predict the severity of anemia with good sensitivity and specifi-
city, moreover, the intra- and inter-observer reliability and reproduci-
bility were fairly good (ICC > 0.99). This study is mainly helpful for
radiologists to make a comprehensive and accurate imaging diagnosis,
with the use of these findings, the radiologist can suggest the presence
and severity of anemia to the clinician, thus adding value to clinical
practice and more importantly facilitating patient care as hematologic
laboratory investigations are lacking.
Conflict of interest
None.
Acknowledgements
The authors would like to acknowledge Jianlin Lv, MD, PhD
(Department of Urology, The affiliated Jiangning hospital of Nanjing
medical university) for his support and invaluable assistance with the
statistical analysis. The authors would also like to thank Yong Zhu, PhD
(School of Science, China Pharmaceutical University) for his support in
language editing.
This work was supported by Nanjing Health and Family Planning
Commission (YKK16233) and the social development project of science
and technology in Jiangsu Province (BE2016605).
240
European Journal of Radiology 108 (2018) 236–241
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