A Survey on Hemorrhage Detection in Diabetic

Retinopathy Retinal Images

Parisut Jitpakdee, Pakinee Aimmanee, Bunyarit Uyyanonvara
Sirindhom International Institute of Technology
Thammasat University,
Bangkok, Tha

Abstract-Diabetic Retinopathy is a medical condition where the

The objectives of this paper are to review the relevant

retina is damaged because fluid leaks from blood vessels into the

literatures in the field of hemorrhage detection, to provide

researchers with a detailed resource of retinal images, to

retina. The presence of hemorrhages in the retina is the earliest

symptom of diabetic retinopathy. The number and shape of
hemorrhages is used to indicate the severity of the disease. Early
automated hemorrhage detection can help reduce the incidence
of blindness. In this paper we review techniques, algorithms, and
methodologies

used

for

the

detection

of

hemorrhage

from

diabetic retinopathy retinal images.

Keywords- Hemorrhage; Red Lesion; Diabetic Retinopathy;

Retinal Image; Image Processing; Medical Imaging
I.

INTRODUCTION

Diabetic retinopathy (DR) is the leading cause of blindness.

The World Health Organization estimates that 135 million
people have diabetes mellitus worldwide and that the number
of people with diabetes will increase to 300 million by the year
2025 [1]. Usually, ophthalmologists recognize diabetic
retinopathy based on features, such as blood vessel areas,
exudates, hemorrhages, microaneurysms, and texture. Diabetic
retinopathy is classified into 3 stages of non-proliferative
retinopathy: mild, moderate, and severe, and 1 stage of
proliferative
Retinopathy
[2].
Hemorrhages
and
microaneurysms are the first clinically observable lesions
indicating diabetic retinopathy. Therefore, their detection is
very important for a diabetic retinopathy screening system.
and

conclude the available methodologies used for detection of

hemorrhage and to comparing the results.
II.

METHODOLlES USED IN HEMORRHAGE DETECTION

Most of the existing methods of hemorrhage detection can

be divided into 2 consequent stages: red lesion candidate
extraction and classification. First stage requires image
preprocessing to reduce noise and improve contrast. After that
the red area of the picture are extracted and segmented to be
the candidate of red lesion. The vessel segmentation algorithms
are applied to extract the blood vessel from the candidates to
reduce false detection. Then the feature analysis which
involves feature extraction and feature selection is used to
detect hemorrhage. The classification algorithm is applied to
categorize these features into the hemorrhage group (abnormal)
and not hemorrhage group (normal). Overall processes for
detection of hemorrhages are concluded in Figure 1.

Pre-processing

Retinal
Images

In automated grading of diabetic retinopathy, hemorrhage

microaneurysm detection are very important. In [3]

detected microaneurysms, hemorrhages and exudates for

grading of diabetic retinopathy using the Scottish Diabetic
Retinopathy Grading Scheme. Another criterion for grading
diabetic retinopathy presented in [4] use numbers of
microaneurysm and hemorrhages to grade the diabetic
retinopathy stage. With a large number of patients, the number
of ophthalmologists is not sufficient to cope with all patients,
especially in rural areas. Therefore, automated early detection
could limit the severity of the disease and assist
ophthalmologists in investigating and treating the disease more
efficiently.
Automated analysis of retinal images has become interested
for ophthalmologists and researcher in digital image
processing. Some paper on hemorrhage detection has mainly
grouped hemorrhages and microaneurysm into a single
category, often referred to as red lesions [5- 10]. In this paper,
we focus only on the detection of hemorrhages or red lesions.

978-1-4673-2025-2/12/$31.00 2012 IEEE

Hemorrhage Classification

Figure I.

Performance Measure

The processes of hemorrhage detection

The following subsections review the researches based on

their main methodologies.

A. Morphological Processing
The commonly method used for detection of hemorrhages
is morphological method, a collection of techniques used for
extracting image components.
Shivaram

et

al.

[11]

used

image

arithmetic

and

mathematical
morphology
methods
for
detection
the
hemorrhages and suppressing the blood vessels. The method

and/or

hemorrhages/microaneurysms

was

95.10%

and

result is compared with ophthalmologists' hand-drawn ground

truth images pixel by pixel. The results obtained for sensitivity,
specificity and predictive value were 89.49, 99.89 and 98.34

specificity is 46. 30%. In [8], color and shape based features

extracted by morphological and region growing method and

respectively. A morphological reconstruction method [12] for

segmentation retina lesion was proposed by Karnowski et al.

selected by logistic regression. Neural network classification:

multilayer perceptron, radial basis fimction, support vector

The segmentation is performed at a variety of scales determine

using ground-truth data to separate nuisance blobs from true

machine, and majority voting were used to detect red lesions.

The result with a lesion-based criterion a mean sensitivity of

lesions. They created a "lesion population" feature vector from

each image to classify normal or abnormal classes. Kande et al.

86.01%, and positive predictive value of 51.99% were

achieved. Garcia et al. [10] detected red lesions using

[5, 13] proposed a detection method of Microaneurysms and

hemorrhage based on pixel classification and mathematical

multilayer perceptron neural network.

The algorithm was
tested on 50 images with a set of 29 features that describe the

morphology. Red lesion candidates are detected by using the

matched filter and the morphological top-hat transformation

shape and color of image regions. Using a lesion based

criterion, they reached a mean sensitivity of 86. 1% and a mean

method. Support Vector Machine (SVM) is applied to classify

red lesion areas and non-red lesion areas with 89 retinal images

positive predictive value of 71.4%.

selected
randomly
from
3
databases
STARE
[14],
DIARETDBO, and DIARETDBI [15]. This approach achieved

C.

a sensitivity of 100% and specificity of 91%.

Zhang and Fan [16] presented a spot lesion detection
algorithm using multiscale morphological processing. Blood
vessels and over-detection were removed by scale-based lesion
validation. An algorithm was tested on 30 retinal images and it
achieved the sensitivity and predictive value of 84.10% and
89.20% respectively.
Matei and Matei [17] and Langroudi and Sadjedi [18] used
morphological operations and thresholding to detect blood
vessels and hemorrhages. In [19] they improved Maximum of
Multiple linear Top Hats (MML TH) by using multi-scale
method to detect candidate hemorrhages and region growing
around these candidates. Local vessel detection performed by
thresholding and skeletonizing method. Blot hemorrhages were
classified by SVM classifier. The method archived a maximum
sensitivity, specificity of 98.60 and 95.50 respectively.
Acharya et al. [35] detected hemorrhages by subtracting the
blood vessel from hemorrhage candidates using morphological
method and ' Ball'-shaped structuring elements. In [21]
mathematic morphological and fuzzy clustering methods were
used in vessel extraction. Hemorrhages and microaneurysm
were detected by suppressing vessels and fovea. Hybrid
approach to detection of red lesions presented by Niemeijer et
al. [9]. Red candidates were extracted by mathematical
morphology method. The kNN classifier was used to
classification of red lesion candidates. The system achieves a
sensitivity of 100% at a specificity of 87%.

Mahalanobis distance classifiers. They obtained sensitivity and

specificity of 80% and 80% respectively. Gray level grouping
based contrast enhancement was applied to improve the
contrast of the green channel [26]. Then candidate red lesions
were extracted by employing automatic seed generation. The k
Nearest Neighbor (kNN) and Gaussian mixture models (GMM)
classifiers were combined together and called Hybrid classifier
was used to classify true red lesions from non-red lesions. The
best sensitivity obtained was 87% with 95.53% specificity.
Tang et al. [27] used watershed algorithm for segmentation
of splats, a collection of pixels with similar color and spatial
location. The connected vasculatures were removed by
automated vessels segmentation method. The kNN classifier
was applied with 42 features in training and reduced to 7
features using forward feature selection method in testing
stage. A set of 20 images from DRIVE database [28] was used
for training and then 1200 images from MESSIDOR database
[29] are used in testing.
Zhang and Chutatape [30] proposed the bottom-up strategy
to detection of bright lesions and the top-down strategy in dark
lesions detection. In hemorrhage detection, hemorrhages are
located in the ROI firstly by calculating the evidence value of
every pixel using SVM. The kernel PCA and PCA are used to
selection features. SVM Classifier with kernel yields 90.6%
true positive while PCA is 89. 1%.
D.

B.

Neural Network Approach

An early approach proposed by Gardner et al. [22] used a

back propagation neural network to detect diabetic features.

Classification

Yuji et al. [24, 25] proposed a methodology to detect

hemorrhage using density analysis, rule-based method and 3

Region growing
Sinthanayothin et al. [20 and 31] used adaptive intensity

thresholding and a ''moat operator" increasing the contrast of

the lesions by enhancing the edges. Red lesions were

The images were divided into squares of 30x30 and 20x20

segmented

pixels used as training data and test data. The features from
each square are used to classify them into "normal", or

algorithm and then a neural network was used to extract the

"vessel", or "exudate", or ''hemorrhage''. The authors reported

detection rates for the hemorrhage is 73.80%.
Usher et al. [23] also employed a neural network. After
preprocessing, hemorrhages/microaneurysms were extracted
using recursive region growing and adaptive intensity
thresholding in conjunction with a "moat operator", edge
enhancement operator. Sensitivity for detection of any exudates

by

recursive

region-growing

segmentation

retinal blood vessels from Hemorrhages. They used the

matched filter based on three properties to detected blood
vessels and then used tracking method to detect hemorrhages.
Bae et al. [32] proposed hybrid method of hemorrhage
detection. Hemorrhage candidates were extracted using a
circular shaped template matching with normalized cross
correlation (NCC). Then hemorrhages were segmented by two
methods of region growing: region growing segmentation

using the local threshold and adaptive seed region growing

hemorrhages.

segmentation. The method achieved a sensitivity of 85% at 4.0

FPs per image. Red lesions detection proposed by Marino et

methodology is needed.

al. had three stages [6]. First, red lesions candidates were
obtained by using a correlation filter set. Then region growing
method and feature based filtering were applied to remove
false positives.
E.

So

the

effective

detection

of

hemorrhages

This paper reviews all existing methods to give a complete

view of the field. Based on this work, researchers can get a
head start of the problem and can develop better and more
effective algorithms.
ACKNOWLEDGMENT

Inverse Method

Unlike previous studies based on segmentation of

unhealthy regions, Kose et al. [36] proposed inverse method
utilizing the background image of healthy areas for detection of

This

research

is

funded

by

the

National

Research

University Project of Thailand Office of Higher Education

Commission (Thammasat University).

diabetic retinopathy lesions. Dark lesions were segmented from

low intensity region after eliminating vessels.
III.

REFERENCES
[1]

S. Wild, G. Roglic, A Green et aI., "Global prevalence of diabetes:

estimates for the year 2000 and projections for 2030", Diabetes Care,
27,pp.l047-1053,2004.

[2]

National Eye Institute, National Institutes of Health, "Diabetic

Retinopathy: What you should know", Booklet, NIH Publication, No:
06-2171,2003.

[3]

Fleming, AD., Goatman, KA, et aI., JA & Scottish Diabetic

Retinopathy Clinical Research Network (2010), "The role of
haemorrhage and exudate detection in automated grading of diabetic
retinopathy", British Journal of Ophthalmology, vol 94, no. 6, pp. 706711.

[4]

Dupas B, Walter T,Erginay A, et aI., "Evaluation of automated fundus

photograph analysis algorithms for detecting microaneurysms,
haemorrhages and exudates, and of a computer-assisted diagnostic
system for grading diabetic retinopathy", Diabetes Metab, Jun;36(3),
pp.213-20.,Epub 2010.

[5]

G.B. Kande, S.S. Tirumala, P.V. Subbaiah, and M.R. Tagore,

"Detection of Red Lesions in Digital Fundus Images", in Proc. ISBI,
pp.558-561,2009.

[6]

C.Marino, E. Ares , M.G.Penedo, M. Ortega, N. Barreira, F. Gomez

U1Ia, "Automated Three Stage Red Lesions Detection In Digital Color
Fundus Images", WSEAS Transactions on Computers, vol. 7, pp. 207215,2008.

[7]

M. Esmaeili, H. Rabbani, AM. Dehnavi, and A Dehghani, "A new

curvelet transform based method for extraction of red lesions in digital
color retinal images", in Proc. ICIP" pp.4093-4096, 2010.

[8]

Garcia M, Lopez MI, Alvarez D, Hornero R., "Assessment of four

neural network based classifiers to automatically detect red lesions in
retinal images",Med Eng Phys. 2010 Dec;32(1O):1085-93. Epub 2010.

[9]

Niemeijer M, van Ginneken B,Staal J,Suttorp-SchuItenMSA,Abrmoff

MD., "Automatic detection of red lesions in digital color fundus
photograph". IEEE Trans Med lmag 24(5):584592,2005.

[10]

Garcia M, Sanchez CI, Lopez Ml, Diez A, Hornero R., "Automatic

Detection of Red Lesions in Retinal Images Using a Multilayer
Perceptron Neural Network", Conf Proc IEEE Eng Med BioI Soc.,
2008:5425-8,2008.

[11]

J. M. Shivaram, R. Patil and Aravind H. S, "Automated Detection and

Quantification of Haemorrhages in Diabetic Retinopathy Images Using
Image Arithmetic and Mathematical Morphology Methods",
International Journal of Recent Trends in Engineering (IJRTE), pp.l741 76,Volume 2,2009.

[12]

Karnowski TP, Govindasamy VP, Tobin K W, Chaum E, Abramoff

MD. "Retina Lesion and Microaneurysm Segmentation using
Morphological Reconstruction Methods with Ground-Truth Data".
ConfProc IEEE Eng Med BioI Soc 1:5433-5436,2008.

[13]

G.B. Kande, S.S. Tirumala, and P.V. Subbaiah, "Automatic Detection

of Microaneurysms and Hemorrhages in Digital Fundus Images",
presented at J. Digital Imaging, pp.430-437,2010.

[14]

STARE: Structured Analysis of the Retina, [Online]. Available:

http://www.ces.c1emson.edul-ahoover/stare/

EVALUATION AND PERFORMANCE MEASURES

The results of hemorrhage detection methodologies

reviewed in previous sections are compared with each other. In
this section, we describe the evaluation approaches and the
performance measuring.
Evaluation methods from all the papers can be classified
into 3 approaches: pixel-based, lesion-based, and image-based.
In pixel based approach, the detected hemorrhages are
comparing with the ground truth image pixel by pixel while in

the lesion based approach, numbers of hemorrhage are used for

comparing. The widely use is image based approach. The
correct classification of normal images and abnormal (diabetic
retinopathy) images including the correct of stage or grade of
disease are used to evaluate the detection method.
The most used measures are Sensitivity and Specificity.
Sensitivity measures the proportion of actual positives which
are correctly identified. Specificity measures the proportion of
negatives which are correctly identified. We classify the papers
based on evaluation approach, and then compare only the
papers that show the number sensitivity, and specificity as
show in Figure 2.
From Figure 2. we can see that image-based and lesion
based approaches give high values of sensitivity but low in
specificity. Many research use this approach in evaluate their
methodologies because the aims is to detection of hemorrhage
for screening the patient. If we want to detect exactly the
position of hemorrhages the testing should be use the pixel
based approach. The good methodologies should be providing
high both sensitivity and specificity.
IV.

CONCLUSION

The automatic detection of

the

hemorrhages

presents

various challenges. The hemorrhages are hard to distinguish

from background variations because it typically low contrast.
Automatic detection of hemorrhage can be confused by other
dark areas in the image such as the blood vessels, fovea, and
microaneurysms. Hemorrhages have a variable size and often
they are so small that can be easily confused with the images
noise or microaneurysyms and no standard database that
classify hemorrhage by shape. The most false detection is the
case when the blood vessels are adjacent

or

overlapping with

[15] DIARETDB: Diabetic Retinopathy Ratabase and Evaluation Protocol,

[Online]. Available: http://www2.it.\ut.fi/projectlimageret/

[16]

X. Zhang and G. Fan, "Retinal Spot Lesion Detection Using Adaptive

Multiscale Morphological Processing", in Proc. ISVC (2), pp.490-501,
2006.

[17]

Matei, Daniela, and Radu Matei. "Detection of diabetic symptoms in

retina images using analog algorithms." International Journal of
Biological and Life Sciences 6.4 (2010): 224+. Health Reference
Center Academic. Web. 25 Mar. 2010.

[18] Langroudi, M.N., Sadjedi, H., "A New Method for Automatic Detection
and Diagnosis of Retinopathy Diseases in Colour Fundus Images Based
on Morphology", Bioinformatics and Biomedical Technology
(ICBBT), pp. 134 - 138,2010.
[19]

[20]

Fleming AD, Philip S, Goatman KA, Olson JA, Sharp PF, "Automated
detection of blot haemorrhages as a sign of referable diabetic
retinopathy", In: Proc. Medical Image Understanding and Analysis,
2008.
Acharya UR, Lim CM, Ng EY, Chee C, Tamura T., "Computer-based
detection of diabetes retinopathy stages using digital fundus images",
Proc Inst Mech Eng H., vol. 223(5),pp. 545-53,2009.

for the Detection of Red Lesions in Digital Fundus Images",

CITWORKSHOPS, IEEE Information Technology Workshops, pp:
462-467,2008.
[27]

L. Tang, M. Niemeijer, and M.D. Abrilmoff, "Splat feature

classification: Detection of the presence of large retinal hemorrhages",
in Proc. ISBI,pp.681-684,201 I.

[28]

J.J. Staal, MD. Abramoff, M. Niemeijer, M.A. Viergever, B. van

Ginneken, "Ridge based vessel segmentation in color images of the
retina", IEEE Transactions on Medical Imaging, vol. 23, pp. 501-509,
2004.

[29]

MESSIDOR: Methods to evaluate segmentation and indexing

techniques in the field of retinal ophthalmology TECHNO-VISION
Project [Online]. Available: http://messidor.crihan.fr/

[30]

X. Zhang and O. Chutatape, "Top-Down and Bottom-Up Strategies in

Lesion Detection of Background Diabetic Retinopathy", in Proc.
CVPR (2), pp.422-428,2005.

[31]

Sinthanayothin C, Boyce JF, Williamson TH, Cook HL, Mensah E,Lal

S,et aI., "Automated detection of diabetic retinopathy on digital fundus
images",Diabet Med.,voI. 19,pp. 105-12,2002.

[21]

Singh N,Tripathi R, "Automated early detection of diabetic retinopathy

using image analysis techniques", Int J Comput App 2010;8:18-23. 85.

[32]

[22]

Gardner G, Keating 0, Williamson TH, Ell AT., "Automatic detection

of diabetic retinopathy using an artificial neural network: a screening
tool",Br J Ophthalmol, vol. 80,pp. 940-4,1996.

J.P. Bae, K.G. Kim, H.C. Kang, C.B. Jeong, K.H. Park, and J. Hwang,
"A Study on Hemorrhage Detection Using Hybrid Method in Fundus
Images", presented at J. Digital Imaging, pp.394-404,2011.

[33]

[23]

Usher 0, DumskyjM,HimagaM,Williamson TH,Nussey S, Boyce J.

"Automated detection of diabetic retinopathy in digital retinal images: a
tool for diabetic retinopathy screening", Diabet Med., vol. 21, pp. 8490,2004.

Patton N, Aslam TM, MacGillivray T, Deary IJ, Dhillon B, Eikelboom

RH, Yogesan K, Constable IJ., Retinal image analysis:
Concepts,applications and potential, Prog Retin Eye Res. 2006
Jan;25(l):99-127. Epub 2005 Sep 9.

[34]

[24]

Hatanaka Y, Nakagawa T, Hayashi Y, Hara T, Fujita H, "Improvement

of automated detection method of hemorrhages in fundus images", In:
30th Annual Inter. IEEE EMBS Con., pp 5429-5432,2008.

Larsen, M, Godt, J, Larsen, N, et aI., "Automated detection of fundus

photographic red lesions in diabetic retinopathy", Invest Ophthalmol
Vis Sci 44,761-766,2003.

[25]

Y. Hatanaka, T. Nakagawa, Y. Hayashi, M. Kakogawa, A. Sawada, K.

Kawase, T. Hara, and H. Fujita, "Improvement of Automatic
Hemorrhages Detection Methods using Brightness Correction on
Fundus Images," in Proc. SPIE Medical Imaging 2008: Computer-aided
Diagnosis,10(2008).

[26]

S. Pradhan, S. Balasubramanian, V. Chandrasekaran, "An Integrated

Approach using Automatic Seed Generation and Hybrid Classification

[35] S A Barman, C Sinthanayothin, A Toniappa, E Corvee, "Classification

of haemorrhage pathologies on digital fundus images using a
combination of neural network and tracking algorithms", The 2nd
International Conference in Electronics,Computer, Telecommunication
and Information (ECTI2005). May 12-13,2005.
[36]

Kose C, Sevik U, Ikiba C, Erdol H., "Simple methods for

segmentation and measurement of diabetic retinopathy lesions in retinal
fundus images",Comput Methods Programs Biomed. , 20II.

1.0
1.0
0.9
0.9
0.8
0.8
0.7
0.7
0.6
0.6
0.5
[04] [06] [08] [09] [ 10] [ 12] [ 18] [20] [22] [23] [24] [25] [34] [36] [05] [10] [ 12] [13] [ 19] [22] [25] [26] [31] [32] [07] [\I] [ 16]
Image based

Lesion based

Figure 2.

sensitivity

til specificity

Performance measures: sensitivity and apecificity based on 3 approaches: image,lesion,and pixel