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8th Scientific Congr. of Egypt. Soc. For Anim. Manag. 23-27 August,2016: 1-16
COMPARISON OF TUBERCULIN SKIN TEST AND LATERAL FLOW
RAPID TEST FOR DETECTION OF BOVINE TUBERCULOSIS IN
DAIRY CATTLE
Nasr E.A.*, Marwah M.*, Lilian F.S. **, MelikaAbeer A. Tammam***,
Seham F. Gorge ****
*Department of Bacterial Diagnostic Products (Tuberculosis), Veterinary Serum and
Vaccine Research Institute, Abassia, Cairo, Egypt.
**Parasitological Vaccine Research Department, Veterinary Serum and Vaccine
Research Institute, Abassia, Cairo, Egypt.
***Department of Rinder Pest, Veterinary Serum and Vaccine Research Institute,
Abassia, Cairo, Egypt.
**** Animal Healthy Institute Beheira Branch
Corresponding author Email: essamnasr@yahoo.com Mobile: 0100575061
ABSTRACT
Tuberculosis is the most important zoonotic bacterial disease that
is hazardous to both man and animals. A huge economic loss
which could be direct or indirect is associated with the disease, so
rapid diagnostic tests for tuberculosis are needed to facilitate early
detection and prevention of disease transmission. The aim of this
work is the detection of bovine tuberculosis by application of
different serological tests. Tuberculin skin test applied on 1900
cattle, only 50 (2.6%) showed positive results, and then
slaughtered. Forty five (90%) of slaughtered animals showed
visible lesions on post mortem examination, while the other five
(10%) showed non visible lesions. The bacteriological examination
of the 50 samples reveled Mycobacterium bovis form 40
processed samples (80%). Results of Anigen Rapid Bovine TB Ab
test and ELISA test had detected 42% and 48% of tuberculin
positive cattle respectively. It was concluded that the Anigen
Rapid Bovine TB Ab kit test is rapid, safe, simple and easy to
perform and provide yes or no results within 15 to 20 minutes but
it is not efficient for detection of bovine tuberculosis in cattle and
could be useful as a complementary for tuberculin test.
ــــــــــــــــــــــــــــــــــــــــــــــــــــــ
Key words: Anigen Rapid Bovine TB Kit, bovine tuberculosis,
ELISA, M. bovis
Nasr E.A.et al…..
2
INTRODUCTION
Bovine tuberculosis is a worldwide disease that causes a great harm on
dairy farms and poses health risks to the population that consumes
products of animal origin. It is still a problem with public health and
economic importance in large areas of the world (Ritacco et al.,
1987).The economic losses caused by the disease are not only a
reduction of 10-20% in milk production and weight, but also due to
infertility and condemnation of meat. The loss is estimated to be 10-
25% of the reproductive efficiency, excluding the losses from mortality
(Lilenbaum et al., 2001). The disease has been difficult to control in
livestock because of the lack of an effective vaccine and the presence
of wildlife reservoirs. Currently, the primary methods used for the
detection of TB in humans and ruminants include the measurement of a
delayed type hypersensitivity (skin test) to purified protein derivative
(PPD) and an indirect in vitro assay that measures the concentration of
gamma interferon (IFN-γ) produced in response to stimulation with PPD
(Monaghan et al., 1994, Wood et al., 1992, Wood and Jones 2001).
Some infected animals may have antibody response in absence of cell
– mediated response, particularly when the bacterial load is high. A
number of Enzyme Linked Immunosorbent Assays (ELISA) have been
described based on complex M. bovis antigens, such as Purified
Protein Derivatives (PPD) and phosphatide antigens. All of these
assays were successful in detecting circulating antibodies to
mycobacteria but have been considered to lack specificity (Mcnair et al.,
2001).
Serological assays are generally simple, rapid and inexpensive, but
the development of improved serodiagnostic assays also require
understanding the bovine tuberculosis humeral immune mechanisms
which is characterized by heterogeneous antigen recognition
(Lyashchenko et al., 1998). Advances in humeral based responses
tests have led to the recently development of two membrane-based
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8th Scientific Congr. of Egypt. Soc. For Anim. Manag. 23-27 August,2016
3
antibody detection methods, Multi Antigen Print Immuno Assay
(MAPIA) and a lateral-flow test. Ab Test Kit is a solid phase
chromatographic immunoassay for the qualitative detection of
Mycobacterium bovis antibody in serum or plasma (Greenwood et
al., 2003).The purpose for conducting this study was to compare
between the sensitivity of recent lateral flow rapid test and ELISA for
diagnosis of bovine tuberculosis of tuberculin skin test reactor cattle.
MATERIAL AND METHODS
I - Tuberculin skin test: A total number of (1900) cross- breed dairy
cattle from different farms were tested by Single Intradermal Cervical
(SIC) tuberculin test as performed by OIE (2009).
II- Serum samples: From the positive tuberculin reactors cattle, blood
samples were collected and serum samples were separated and stored
at- 20°C till used in serological test
.
III- Post–mortem examination: After slaughtering of tuberculin
positive reactors, Post – mortem examination was done to detect the
presence of any suspected tuberculous lesions such as caseation,
calcification, or congestion that might be present in any lymph node
(head, bronchial, hepatic, mesenteric, prescapular, popliteal and
internal iliac lymph nodes). Moreover, specimens were collected from
the lung, liver, kidney, diaphragm and peritoneum which showed
congestion or suspected tuberculous lesions.
IV – Tissue samples: The internal organs (livers, spleens, and lungs
lymph nodes) and lymph nodes showing tuberculous-like lesions were
collected using aseptic techniques, placed in an ice pox and submitted
as soon as possible to the laboratory where they were processed for
isolation and identification of the organism.
Nasr E.A.et al…..
4
V- Bacteriological examination: The organs, lymph nodes and/or
tissues showing gross lesions were prepared for bacteriological
examination. Prepared sections were stained with Ziehl – Neelsen’s
stain. Samples were cultured on four tubes of Lowenstein-Jensen
slants after being decontaminated with 4% H2So4. Obtained isolates
were identified by conventional methods (rate of growth, colonial
morphology, pigmentation, and biochemical properties) according to
Brasil (1994).
VI - Enzyme Linked Immunosorbent Assay (ELISA): The Enzyme
Linked Immunosorbent Assay (ELISA) was applied in sera of tuberculin
positive cattle according to Collee et al. (1996) using Bovine Purified
Protein Derivatives (B – PPD). The optical density was measured at
405 nm using spectra III ELISA reader. Sample was considered
positive if it yield a mean OD of each group equal to / or greater than
the cut off value {Cut off value was calculated according to Nassau et
al. (1976) which equal to the mean OD of negative serum plus 2
standard deviation}.
VII- Lateral flow test Kit: The testing of sera was carried out according
to the manufacturer's instructions using the Anigen Rapid Bovine TB
Ab test kit as follows:
1. The foil pouch of test kit was removed and placed on a flat, dry
surface.
2. Test units were labeled with samples names.
3. Four drops of serum were added slowly to sample well with the
specimen dropper (if the migration has not appeared after one
minute, one more drop of the specimen was added to the
sample well).
4. A test result will be seen as a band in the result window of the
kit.
5. The test results were interpreted within 20 minutes (no
interpretation after 20 minutes).
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8th Scientific Congr. of Egypt. Soc. For Anim. Manag. 23-27 August,2016
5
Interpretation of the test:
- Negative result: The presence of only one color band within the
result window.
- Positive result: The presence of tow color bands (T band and C
band) within the result window. (Even if the intensity of the band
color is faint it should be consider as positive).
- Invalid: If the color band was not visible within the result window
after performing the test, the result was considered invalid and
the specimen was re-tested.
RESULTS
3.1. Results of tuberculin skin test and post mortem finding of
slaughtered tuberculin positive cattle
The results in table (1) illustrated the prevalence of tuberculin reactors
in dairy cattle from different farms and PM findings of slaughtered
tuberculin reactor cattle. From total 1900 tuberculin tested cattle, 50
were found to be reactors with a prevalence rate of 2.6%. On other
hand, the number of non – visible lesion (NVL) reactors amounted to 5
animals (10%), while the number of visible lesions found to be 45
animals with an overall percentage of 90% as shown in the same table.
3.2. Results of postmortem finding in slaughtered tuberculin
reactor cattle according to the site of lesion.
Out of 50 tuberculin reactor animals, 45(90%) showed visible and
5(10%) had non visible lesions, on the same time the visible lesions
showing 6(12%) head, 24(48%) pulmonary, 10(20%) digestive and
5(10%) generalized as shown in the same table (Table-2).
3.3. Results of Anigen Rapid Bovine TB Ab test kit from tuberculin
reactor cattle in comparison to the type of lesions.
It is cleared from table (3) that 21(42%) of tuberculin reactor cattle were
positive with Ani- gen Rapid Bovine TB kit. While, 29 (58%) were
negative with Ani- gen Rapid Bovine TB kit.
Nasr E.A.et al…..
6
3.4. Comparison between the results of bacteriological isolation,
ELISA and Anigen Rapid Bovine TB Ab test kit on samples
obtained from tuberculin positive animals.
The obtained results in table (4) showed that, from 50 carcasses, 40
cultures positive for M. bovis were recovered with an isolation rate of
80 %. While, Anigen Rapid Bovine TB AB Test Kit has detected 42% of
tuberculin positive cattle and the ELISA with B-PPD antigen has
detected 48 % of tuberculin positive reactor cattle as shown in the
table.
Table (1): Results of tuberculin skin test and post mortem finding of
slaughtered tuberculin positive cattle.
No. of
tested
cattle
Reactor
cattle
PM finding
Visible Lesion
Non Visible Lesion
No.
%
No.
%
No.
%
1900
50
2.6
45
90
5
10
PM: Postmortem. No.: Number.
Table (2) Results of postmortem finding in 50 slaughtered tuberculin
reactor cattle according to the site of lesion.
VL: Visible Lesion NVL: Non Visible Lesion PM: Postmortem.
Reactor
cattle
PM finding
VL (45)
NVL(5)
Head
Pulmonary
Digestive
Generalized
No
%
No.
%
No.
%
No.
%
No.
%
No.
%
50
2.6
6
12
24
48
10
20
5
10
5
10
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8th Scientific Congr. of Egypt. Soc. For Anim. Manag. 23-27 August,2016
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Table (3): Results of Anigen Rapid Bovine TB Ab test kit from tuberculin
reactor cattle in comparison to the type of lesions.
PM: Postmortem. TB: Tuberculosis.
Table (4) Comparison between the results of bacteriological isolation,
ELISA and Anigen Rapid Bovine TB Ab test kit on samples obtained
from tuberculin positive animals.
PM finding
Sites of lesions
N0
M. bovis
isolates
ELISA
Ani gen Rapid
Bovine TB kit
No.
%
No.
%
No.
%
I. Visible
lesions
1. Local
a. Head
6
4
66.7
2
33.3
2
33.3
b. Pulmonary
24
22
91.7
12
50
10
41.7
c. Digestive
10
7
70
4
40
3
30
2. Generalized
5
5
100
5
100
5
100
Sub total
45
38
84.4
23
51.1
20
44.4
II. Non
visible lesions
Congestion in
L.N.
5
2
40
1
20
1
20
Total
50
40
80
24
48
21
42
B-PPD: Bovine Protein Purified Derivatives. TB: Tuberculosis.
PM finding
Number of positive
tuberculin reactor
Anigen Rapid Bovine TB kit
Positive
Negative
No.
%
No.
%
Visible
45
20
44.4
25
55.6
Non visible
5
1
20
4
80
Total
50
21
42
29
58
Nasr E.A.et al…..
8
DISCUSSION
Bovine tuberculosis is an important zoonotic disease transmitted by
direct contact, respiratory pathway, ingestion of unpasteurized milk
and milk product, raw or uncooked meet. Tuberculosis can be difficult
to diagnose based only on the clinical signs. Tuberculosis is usually
diagnosed in the field with the tuberculin skin test, sputum and other
body fluids may be collected for microbiological examination (Kaya et
al., 2015). The tuberculin skin test was found to be the test of choice.
Although the tuberculin test is a very reliable diagnostic method, yet as
in all biological test, difficulties have been encountered, the greatest
problem is the occurrence of so – called false negative responses,
which sometimes see soon after infection, in the late stages of the
disease (anergic cattle), in animals with poor immune responses and in
those that have recently calved. To obviate this problem, an extensive
effort has been under way to identify and characterized antigens unique
to M. bovis that could be used in diagnostic assay ( El- Mahrouk and
El- Balawy, 2010).The objective of this study was to compare the
sensitivity of two serological test for diagnosis of bovine tuberculosis in
cattle.
The results in table (1) illustrated the prevalence of tuberculin reactors
in dairy cattle from different farms and PM findings of slaughtered
tuberculin reactor cattle. From total 1900 tuberculin tested cattle, 50
were found to be reactors with a prevalence rate of 2.6%. The
prevalence rate recorded in the present study is comparatively lower
than that given by other investigators in Egypt (Lotfy et al., 1960, 6.9%
; Guindi et al., 1965, 26.5% ; El- Sabban et al.,1992, 24% and El
battawy 2008, 4.6 % and in other countries of the world Oliveira et al.
1983, 3.2% in Brazil ; Ameni and Erkihun, 2007 in Ethiopia 11.6 % ;
Borna et al. ,2009, 8% in Chad
In the present study, the low incidence of infection could be attributed
to many factors such as herd size, density of animals, breeding and
Comparison Of Tuberculin Skin Test……
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8th Scientific Congr. of Egypt. Soc. For Anim. Manag. 23-27 August,2016
9
management system, uncontrolled animal movements, unhygienic local
habits and stress factors due to other diseases and mass vaccination
against various diseases (Abuo – Eisha et al., 1995).At the same time,
the prevalence recorded in the present study is comparatively higher
than that given by other investigators (Shirma et al., 2003) and
(Cleaveland et al., 2007) in Tanzania, as it was 1.3 % and 0.9%,
respectively. The high prevalence rate of tuberculin reactors, in
general, is a function of different factors such as the past history of
tuberculosis in the dairy herd (Thornton and Gracey, 1976), method of
breeding and housing besides the susceptibility and age of the animals
(Guinidi et al., 1980; Sharama et al., 1985).
On other hand, the number of non – visible lesion (NVL) reactors as
shown in table (1) amounted to 5 animals (10%), a finding which may
be attributed to the non-specific reaction to the tuberculin test which
may be due to sensitization by other mycobacteria rather than M. bovis
or even closely related microorganisms especially of the genus
Nocardia or a combination of liver fluke infestation with saprophytic
mycobacteria (Karlson, 1962, Cortina and Vera, 1986). Moreover,
O'Reilly (1992) and Huitema (1994) ascribed the cause of non-specific
reaction to the assumption that reactors may be slaughtered at stage of
the disease where the tuberculous lesions are invisible or the lesions
may be found in parts of carcass such as bone or skin.
As shown in table (1) the visible lesions found with an overall
percentage of 90% which are higher than that reported by Oliviera et
al. (1983), 75% ; Zivkovic et al.(1984),75.2% and Nasr (1997),73.4 %.
On the other hand, other authors claimed a much higher percentage
(Kilian, 1982, 96.3% in Germany and El- Sabban, 1992, 100% in
Egypt).
Table (2) showed that the higher lesion severity was observed in the
pulmonary lymph nodes (48%), this may be due to the intensive
husbandry systems which make the respiratory excretion the main
Nasr E.A.et al…..
10
route by which animal – to – animal transmission occurs (Smyth et al.,
2001).
The total isolation rates of M. bovis form carcasses of tuberculin
reactors with and without lesions demonstrated in table (4). From a
total of 50 carcasses, 40 positive culture were recovered with an
isolation rate of 80 %. The obtained results were near to that mentioned
by Tammemagi et al. (1973) (89.1 %) and Naglaa (2008) (70.59 %).
Other investigators reported lower M. bovis recovery rate, by Adawy
(1986) (17.5 %) and Zschoc et al. (1990) (1.6 %). These results
depend mainly on the actual disease status present in the tested herd
and to some extend on the experience of the investigators as well as
the technique used for decontamination of tissue specimens.
Additionally the harsh decontamination which was used to destroy
contaminating bacteria other than mycobacteria in a sample may also
have a harmful effect on the M. bovis causative organism (Victor et al.
1992 and Quinn et al., 1994).
It is cleared from table (3) that 21(42%) of tuberculin reactor cattle were
positive with Ani- gen Rapid Bovine TB kit. While, 29 (58%) were
negative with Ani- gen Rapid Bovine TB kit. The obtained results
indicated the difference between the tuberculin test and Anigen Rapid
Bovine TB kit for detection of tuberculosis in cattle. The Negative
Anigen Rapid Bovine TB kit explained by the fact that low titer of
antibodies to mycobacterial antigens which may be associated with
heavy infection and that antigens may be released into the blood
circulation and cause temporary suppression of antibody formation
Krambovitis (1986) and that agree with Thorns and Morris (1983)
who cleared the level of specific anti- bodies in many M. bovis infected
cattle may be low or undetectable. Again this is supported with
Amadori et al. (1998) who pointed that antibodies to mycobacterial
antigens were investigated with various rates of success since the
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8th Scientific Congr. of Egypt. Soc. For Anim. Manag. 23-27 August,2016
11
humeral immune response to M. bovis is late and irregular during the
course of the disease.
Table (4) showed that the Anigen Rapid Bovine TB AB Test Kit has
detected 42% of tuberculin positive cattle. While the ELISA with B-PPD
antigen has detected 48 % of tuberculin positive reactor cattle. The
results agreed with those of Danbirni et al. (2013) who mentioned that
the antigen rapid bovine TB Ab test alone is not efficient in diagnosis of
TB and that the serological tests like ELISA must be used to validate
results and disagreed with Danbirni et al. (2009) who found that (62%)
of cows gave positive in antigen rapid bovine test TB Ab test.
Moreover, Kalaf et al. (2014) showed that out of (28) cows examined
with comparative tuberculin test, (21) cows showed positive tuberculin
reactions (75%) and twenty two cow with a percentage of (78.57%)
showed positive results for antigen rapid bovine TB
.
The differences may be attributed to that the humoral immune test
using the Enzme Linked Immunosorbent Assay (ELISA), immune-
chromatography (lateral flow) assay and other serologic based test may
complement test of cellular immunity in anergic hosts (Awah-Ndukum,
2010).
CONCLUSION
It could be concluded that the Anigen Rapid Bovine TB Ab kit test is
rapid, safe, simple and easy to perform and provide yes or no results
within 15 to 20 minutes but alone it is not efficient for detection of
bovine tuberculosis in cattle and may be useful as a complementary
test for tuberculin test in some cases as in the late stages of the
disease (anergic cattle).
Nasr E.A.et al…..
12
ACKNOWLEDGEMENT
This work was supported by Bovine Tuberculosis Project of Academics
in Egypt with Department of Bacterial Diagnostic Products, Veterinary
Serum and Vaccine Research Institute, Abassia, Cairo, Egypt.
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Anigen Rapid Bovine TB Ab
