Research in Veterinary Science 123 (2019) 159–170

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Research in Veterinary Science

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Prevalence of Anaplasma species in India and the World in dairy animals: A T

systematic review and meta-analysis
⁎
Krishnamoorthy Paramanandham , Ashwini Mohankumar,
Kuralayanapalya Puttahonnappa Suresh, Siju Susan Jacob, Parimal Roy
ICAR-National Institute of Veterinary Epidemiology and Disease Informatics (NIVEDI), Post Box No.6450, Ramagondanahalli, Yelahanka, Bengaluru 560064, Karnataka,
India

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

Keywords: In the present study, the prevalence of Anaplasma species in diary animals from India and World was estimated
Anaplasma species using meta-analysis. Based on systematic review of studies on Anaplasma species from India [35] and World [66]
Prevalence from 1988 to 2017 and 1978–2017, respectively, using online databases and offline literatures, meta-analysis
India using meta package in R-Software was done. Prevalence of Anaplasma species in India and World were 11%
World
[95% level, Confidence Interval[CI] 7–16%, Prediction Interval[PI] 1–69%] and 39% [95% level, CI 30–49%, PI
Meta-analysis
2–95%], and these were obtained using 31,117 and 46,365 samples, respectively. Period-wise analysis revealed
high Anaplasma species prevalence before 2011 for India and the World than from 2011 through 2017. Zone-
wise prevalence indicated high prevalence in Central zone [61%] and low in West and South zones [6%] in
India, and continent-wise, it was high in South America [82%]. The studies used methods including blood smear
examination, serology and nucleic acid-based techniques and revealed high prevalence in serology for India
[34%] and World [46%], low prevalence by blood smear for India [7%] and World [21%], but higher sensitivity
using nucleic acid-based techniques. Species-wise indicated higher prevalence in cattle [12%] than buffaloes
[2%] in India. Prevalence was lower in India compared to the World and higher in South America. Overall,
anaplasmosis causes low productivity in dairy animals and economic loss to dairy farmers. Hence, there is a need
to control Anaplasma infections in high risk areas by adopting effective therapeutic and preventive measures so
as to improve the economic benefits in dairy farming.

1. Introduction
Anaplasmosis is a common disease of cattle and buffaloes in India
and the World. The main cause of bovine anaplasmosis is Anaplasma
marginale, which is an intra-erythrocytic rickettsial organism, trans-
mitted biologically by infected ticks or mechanically by biting flies or
blood-contaminated fomites (Dumler et al., 2001). The Anaplasma or-
ganism has some similarity to protozoa due to the lack of a traditional
cell wall and is not capable of synthesizing lipopolysaccharide and
peptidoglycan (Brayton et al., 2006). Other species that cause ana-
plasmosis in dairy animals in India and the World are A. centrale, A.
bovis, A. phagocytophilum and A. caudatum (Radostits et al., 2000).
Among the five species, A. marginale is the most prevalent, highly pa-
thogenic and distributed Worldwide (Kuttler, 1984). Since A. centrale
causes mild anaplasmosis in cattle, it has been widely used as an im-
munizing agent for cattle (Theiler, 1912). A. bovis is responsible for
acute anaplasmosis which is often related to stress most commonly
reported from South America, West, Central and Southern Africa, and
the Indian subcontinent (Park et al., 2018). A. phagocytophilum (for-
merly known as Ehrlichia phagocytophila, E. equi and human granulo-
cytic ehrlichiosis agent), was identified in cattle and is capable of in-
fecting human and is mainly distributed in Europe, Asia and USA
(Bakken et al., 1994) with few reports from Africa and South America
(Stuen et al., 2013). A. caudatum is a strain of A. marginale with ap-
pendages that also causes bovine anaplasmosis (Kreier and Ristic, 1963)
and is common in mixed infections which has not studied in detail.
Transmission of Anaplasma marginale is by at least 20 species of ticks of
the genera Hyalomma spp., Rhipicephalus spp., Ixodes spp., Demacentor
spp., in the World (Kocan et al., 2010). In India, A. marginale, A. centrale
and A. bovis are the prevalent species in cattle (Nair et al., 2013) and
they are principally transmitted by Rhipicephalus (Boophilus) microplus
(Kolte et al., 2017). A. bovis is transmitted by Rhipicephalus appendicu-
latus, Amblyomma variegatum and Hyalomma truncatum and occur in
India and Africa (Radostits et al., 2000). The clinical signs of the

⁎
Corresponding author.
E-mail address: P.Krishnamoorthy@icar.gov.in (K. Paramanandham).

https://doi.org/10.1016/j.rvsc.2019.01.013
Received 20 March 2018; Received in revised form 9 January 2019; Accepted 13 January 2019
0034-5288/ © 2019 Elsevier Ltd. All rights reserved.
K. Paramanandham et al.
anaplasmosis include fever, anaemia, weakness, constipation, icterus,
anorexia, dehydration, depression, laboured breathing, abortion and
often death (Richey and Palmer, 1990). The economic loss due to in-
fections caused by Babesia and Anaplasma infections in India was esti-
mated to be $57 million (Tick Cost Version 1.0, 1990). The tick in-
festations and tick borne diseases in animals in India cause an estimated
economic loss to the tune of more than US$ 498.7 million per annum
(Minjauw and McLeod, 2003). India has the highest population of
buffaloes (105.1 million; approximately 56.7% of the total World buf-
falo population) and cattle in the World and ranks first in buffalo po-
pulation and milk production. The World buffalo population is esti-
mated at 185.29 million, spread in some 42 countries, of which 179.75
million (97%) are in Asia. Anaplasma species infections in dairy animals
causes production loss and economic loss to dairy farmers. Hence, it is
necessary to focus on the Anaplasma species infections in the dairy
animals in India and the World.
Meta-analysis is a rapidly expanding area of research that has been
relatively underutilized in animal and veterinary science. It is a quan-
titative, formal, epidemiological study design used to systematically
assess previous research studies to derive conclusions about that body
of research. Rigorously conducted meta-analyses are useful tools to
improve animal well-being and productivity. There is a need to in-
tegrate findings from many studies to ensure that meta-analytic re-
search is desirable. Large amount of research findings have been gen-
erated in animal health and production, which makes the conduct of
meta-analysis research feasible (Lean et al., 2009). However, there is no
prevalence estimate available for the Anaplasma species in dairy ani-
mals by using meta-analysis for India and the World. By using meta-
analysis approach, for the first time the prevalence of Anaplasma species
in India and the World in dairy animals may be estimated by combining
all the research studies available for calculating the overall prevalence
by forest plot method. Hence, the present study was conducted to un-
derstand the prevalence of Anaplasma species in India and the World
based on various criteria including year, zones, species and methods for
India and year, continents, period and methods for the World.
2. Materials and methods
2.1. Search strategy
Systematic search was performed on the literature about prevalence
of Anaplasma species in dairy animals in India and the World. The da-
tabases included were Pub med, Springer's, Scopus, Indianjournals.com,
J-Gate@Consortium of e-Resources in Agriculture (CeRA) under Indian
Council of Agricultural Research, research abstracts of conferences,
seminars, symposia and other published literatures. The prevalence of
Anaplasma species included in the studies were of Anaplasma marginale,
A. centrale, A. bovis, A. phagocytophilum and these were collected for the
meta-analysis. More than 100 articles were searched, reviewed and
selected, and the results were subjected to meta-analysis to determine
the prevalence rate with respect to various periods and states in India.
The literatures from study areas based on the states in India was divided
into five zones viz., North, East, West, South and Central zones. The
literature search from different publications were undertaken for the
period up to 2017 for Anaplasma species prevalence. Given a vast
quantity of literature, the type of items that were collected include the
characteristics of the publications [author, year, country, state, number
of samples tested and number of positive samples in dairy animals such
as cattle and buffaloes]. The retrieval period was limited to the period
from 1988 to 2017 for India, 1978–2017 for the World based on the
availability of the literatures and data sources. The retrieval language
was limited to English. Finally, the original articles, peer reviewed ar-
ticles and references cited from the retrieved articles were searched
again to trace back the past years published literatures.
160
Research in Veterinary Science 123 (2019) 159–170
2.2. Study selection
All the search results were limited to cross-sectional and long-
itudinal studies conducted on cattle and water buffaloes in India and
the World. The studies had to meet the following criteria for inclusion:
1) frequency of Anaplasma species or antibodies detected, 2) number of
animals screened or tested, 3) year of surveillance or year of study
conducted and 4) studies which have used the standard confirmatory
test such as blood smear examination with different staining methods,
sero-diagnosis by different ELISA methods and nucleic acid-based
techniques by different PCRs. Studies were excluded, if the frequencies
of Anaplasma species were not reported and also studies such as case
reports, review articles and outbreak investigations.
2.3. Data entry and filtration
Two reviewers independently extracted the characteristics of each
included study onto predesigned Excel forms. These included publica-
tion year, authors, study participant, eligibility criteria, study period,
numbers of animals positive for Anaplasma species, the total number of
animals tested and the methods used. The test used for diagnosis of
prevalence of Anaplasma species were blood smear examination with
different staining methods, serology by using different types of ELISA
and nucleic acid-based techniques using different PCRs. The overall
prevalence estimate of Anaplasma species was estimated by calculating
the average of the results obtained by different methods. Results from
the previous research found in the literature had to be entered in the
database. The coding of the database was done with numerous variables
identifying the experimental objectives of all the experiments selected.
There were at least three steps necessary for effective data filtering.
First, we ensured that the study under consideration was coherent with
the objectives of the meta-analysis. The meta-analysis objectives dic-
tated that some traits must be measured and reported. The second step
consisted of a thorough and critical review of each publication under
consideration, focusing on the detection of errors in the reporting of the
quantitative results. Verification of data entered was essential compo-
nent in this process. In the third step, it was important to ensure that a
selected publication does not appear to be an outlier with respect to the
characteristics and relations under consideration.
2.4. Meta-analysis
In the most general terms, meta-analysis is a method of research
synthesis. It employs specialized techniques for data gathering and
analysis developed specifically for the purposes of research synthesis
(Koricheva et al., 2013). Using a rigorous systematic protocol, sys-
tematic reviews were used to synthesize findings from available re-
search reports as the gold standard for measuring the effectiveness of
preventive and therapeutic interventions for the specified conditions.
The overall effect calculated from a group of sensibly combined and
representative condition or criteria provides an essentially unbiased
estimate of the effect, with an increase in the precision of this estimate.
The meta-analysis of prevalence of Anaplasma species in diary animals
in India and the World was conducted by using the R Open source
scripting software (Comprehensive R Archive Network) version 3.2.5
and the R package used for meta-analysis was meta (Schwarzer, 2007).
The graphical representation of meta-analysis was done by using forest
plots. Forest plot (confidence interval plot) is a method utilized to
present the results of meta-analysis, displaying effect estimate and their
confidence interval (CI) for each study. Each study is represented by a
square at a point estimate of effect and a horizontal line extending ei-
ther side of the block depicts a 95% CI. The area of the block was
proportional to the weight assigned to that study in the meta-analysis.
The dark shaded line given below in the forest plot represents the
prediction interval (PI) at 95% level, which indicates the future pre-
diction of the estimate to be within the range of values. The
K. Paramanandham et al. Research in Veterinary Science 123 (2019) 159–170

Fig. 1. Schematic diagram showing the studies from India and the World on Anaplasma species prevalence included for meta-analysis.

transformation used in analysis was Logit transformation for propor- Table 1

tion, i.e., ‘sm = PLOGIT’. This method of analysis used in the present Details of the Anaplasma species prevalence studies from India included in the
study was similar to our previous study on determining the prevalence systematic review and meta-analysis.
estimate for subclinical and clinical mastitis in dairy animals in India S. no. Study [author and year] Study locations in India Zones
(Krishnamoorthy et al., 2017). Moreover, forest plots may include the
results if the overall effect from a meta-analysis, normally at the bottom 1. Misraulia et al. (1988) Madhya Pradesh Central
2. Jithendran (1997) Himachal Pradesh North
of the graph, and often using a diamond to distinguish from the in-
3. Chitravel et al. (1998) Tamil Nadu South
dividual studies (Higgins et al., 2013). The Q statistics for the meta- 4. Muraleedharan et al. (2005) Karnataka South
analysis data generated was calculated as reported earlier 5. Kumar and Sangwan (2010) Haryana North
(Krishnamoorthy et al., 2017). The forest plots were prepared for the 6. Reetha et al. (2012) Tamil Nadu South
Anaplasma species prevalence for period-wise, species-wise, zone-wise, 7. Singh et al. (2012a) Punjab North
8. Singh et al. (2012b) Punjab North
method-wise and continent-wise separately. The prevalence estimates 9. Vahora et al. (2012) Gujarat West
for Anaplasma species in dairy animals was expressed as percentage and 10. Ashuma et al. (2013) Punjab North
along with CI and PI at 95% level. 11. Arunkumar and Nagarajan Tamil Nadu South
(2013)
12. Chaudhri et al. (2013) Haryana North
3. Results 13. Nair et al. (2013) Kerala South
14. Jaswal et al. (2014) Punjab North
15. Jeyathilakan et al. (2014) Tamil nadu South
3.1. Details of prevalence studies
16. Krishnamurthy et al. (2014) Karnataka South
17. Murthy et al. (2014) Karnataka South
The details of study selection criteria followed for the meta-analysis 18. Velusamy et al. (2014) Tamil Nadu South
of Anaplasma species prevalence are given in Fig. 1. The present study 19. Bhatnagar et al. (2015) Rajasthan West
was carried out based on systematic review of prevalence of Anaplasma 20. Filia et al. (2015) Punjab North
21. Kakati et al. (2015) Assam East
species in dairy animals of India [1988–2017] and the World 22. Kumar et al. (2015) Haryana North
[1978–2017]. The details of the studies on Anaplasma species pre- 23. Maharana et al. (2016) Gujarat West
valence with location and zones for India, and location and continents 24. Maria et al. (2015) Rajasthan West
of the World are presented in Tables 1 and 2, respectively. The studies 25. Rather et al. (2015) Jammu and Kashmir North
26. Sharma et al. (2015a) Punjab North
used for Asia continent excludes the studies from India and was used for
27. Sharma et al. (2015b) Punjab North
analysis purpose for better comparison. The forest plot analysis was 28. Debbarma (2016) West Bengal East
carried out to show the meta-analysis results for better understanding 29. Dharanesha et al. (2017) Karnataka South
and to determine the heterogeneity between the various studies. 30. George et al. (2016) Andhra Pradesh and South
Telangana
31. Harikrishnan et al. (2016) Tamil Nadu South
3.2. Meta-analysis of Anaplasma species prevalence from India 32. Kumar et al. (2016) Gujarat West
33. Kolte et al. (2017) Maharashtra West
34. Maurya et al. (2017) Uttar Pradesh North
The detailed results of meta-analysis of prevalence studies of 35. Sudhakar et al. (2017) Uttar Pradesh North
Anaplasma species in India are presented in Table 3. The forest plot for
Anaplasma species prevalence studies from different states in India are
depicted in Fig. 2. The number of prevalence studies were 35 for the
period 1988–2017 with a total of 31,117 samples from the dairy ani-
mals in India. The pooled estimates for prevalence of Anaplasma species

161
K. Paramanandham et al. Research in Veterinary Science 123 (2019) 159–170

Table 2

Q statistics
Details of the Anaplasma species prevalence studies from World included in the

72.73b
3300b

2800b

1000b

3200b

2600b
6.45a
500b

350b
systematic review and meta-analysis.

50b
0b

0b

–
No. Study [author and year] Study locations in Continents
World

1. Obi, 1978 Nigeria Africa

Degrees of
2. Knowles et al. (1982) Saint Lucia North America

freedom
3. Verhulst et al. (1983) Morocco Africa
4. Verhulst et al. (1983) Cameroon Africa

34

29

11

11

33

27
4

3
5

2
8
–
5. Verhulst et al. (1983) Congo Africa
6. Ajayi and Dipeolu (1986) Nigeria Africa
7. Teclaw et al. (1985) Mexico North America

Tau square
8. Hugh-Jones et al. (1988) USA North America
9. Goff et al. (1990) USA North America

2.001

4.111
1.746

1.615
0.047
2.956
1.712

1.930
3.638

1.462
0.917
0.456
value
10. Payne and Osorio (1990) Paraguay South America

–
11. Baumgartner (1992) Austria Europe
12. Ssenyonga et al. (1992) Uganda Africa

I2 value (%)
13. Perez et al. (1994) Costa Rica North America
14. Cossio-Bayugar et al. (1997) Mexico North America

100.0

100.0
99.0

99.0

98.0
69.0

99.0

99.0
89.0

99.0
98.0
98.0
15. Hungerford and Smith (1997) Illinois, USA North America

–
16. Dreyer et al. (1998) South Africa Africa
17. Shaibi et al. (1998) Morocco Africa

Prediction interval (%) at 95%

18. Torioni de Echaide et al. (1998) Oregon, USA North America
19. Magona and Mayende, 2002 Uganda Africa
20. Khan et al. (2004) Pakistan Asia
21. Mtshali et al. (2004) South Africa Africa
22. Rodríguez-Vivas et al. (2004) Mexico North America
23. Alfredo et al. (2005) Mozambique Africa
24. Barros et al. (2005) Brazil South America
25. Dreher et al. (2005) Switzerland Europe

0–100
26. Fuente et al. (2005) Italy Europe

1–69

0–99
1–65

1–80
6–36
0–92
0–60

1–70
0–65

1–47

8–71
27. Rajput et al. (2005) Pakistan Asia level

–
28. Swai et al. (2005) Tanzania Africa
Pooled prevalence (%) [confidence interval at 95%

29. Chowdhury et al. (2006) Bangladesh Asia

30. Carelli et al. (2007) Italy Europe
31. Hornok et al. (2007) Hungary Europe
32. Mtshali et al. (2007) South Africa Africa
33. Torina and Caracappa (2007) Italy Europe
34. Coetzee et al. (2010) Iowa, USA North America
35. Kamani et al. (2010) Nigeria Africa
36. Noaman and Shayan (2010) Iran Asia
37. Oliveira et al. (2011) Costa Rica North America
38. Alim et al. (2012) Bangladesh Asia
39. Awad et al. (2011) Sudan Africa
40. Atif et al. (2012) Pakistan Asia
41. Hamou et al. (2012) Morocco Africa
16 [12−20]

61 [55–66]

34 [15–61]
32 [23–42]
42. Hornok et al. (2012) Hungary Europe
11 [7–16]

13 [2–48]
10 [7–16]

17 [9–30]

12 [8–18]
6 [1−20]
6 [3−13]

7 [4–10]
Meta-analysis of prevalence studies on Anaplasma species in dairy animals of India.

43. Kubelova et al. (2012) Portugal Europe 2 [0–6]

level]

44. Malak et al. (2012) Sudan Africa

45. Rahman et al. (2012) Malaysia Asia
46. Ashraf et al. (2013) Pakistan Asia
31,117

25,612

10,413
11,961

29,378

27,848
Total

5505

5943
2495

5936

47. Barbosa da Silva et al. (2014) Brazil South America 3529

305

673

48. Belal et al. (2014) Bangladesh Asia

49. Hairgrove et al. (2014) Texas, USA North America
Number of studies

50. Hosseini-Vasoukolaei et al. Iran Asia

(2014)
51. Tay et al. (2014) Malaysian Asia
52. Aktas and Ozubek (2015) Turkey Europe
53. Barbosa da Silva et al. (2015) Brazil South America
35

30

12

12

34
10

28
5

4
6

3
9

54. Hairgrove et al. (2015) Texas, USA North America

55. Moumouni et al. (2015) Kenya Africa
1988–2017

1988–2010
2011–2017

1997–2017
2015–2017
2012–2017
1998–2016

1988–2017
2012–2017

1988–2017
1988–2015
2013–2016

56. Fereig et al. (2016) Egypt Africa

Period

57. Kispotta et al. (2016) Bangladesh Asia

1988

58. M'Ghirbi et al. (2016) Tunisia Africa

59. Machado et al. (2016) Mozambique Africa
Anaplasmosis in Central Zone

Anaplasmosis by Blood smear

60. Pothmann et al. (2016) Madagascar Africa

Anaplasmosis in North Zone

Anaplasmosis in South Zone

Anaplasmosis in West Zone

Anaplasmosis by Molecular
Anaplasmosis in East Zone

Anaplasmosis by Serology

61. Tucker et al. (2016) Northern California, North America

Anaplasmosis in India-II

Anaplasmosis in Buffalo
Anaplasmosis in India-I

Anaplasmosis in Cattle

USA
Anaplasmosis in India

62. Zhou et al. (2016) Turkey Europe

63. Aktas and Ozubek (2017) Turkey Europe
Highly significant.

64. Belkahia et al. (2017) Tunisia Africa

Parameters

65. Cui et al. (2017) China Asia

66. Sisson et al. (2017) South Africa Africa
Significant.
wise
Species wise
Zone wise
Year wise

Method
Table 3

Sl. no.

1.

1.
2.

1.
2.
3.
4.
5.

1.
2.

1.
2.
3.

b
a

162
K. Paramanandham et al.
Fig. 2. Forest plot showing the details of the studies from India and their prevalence estimates.
was 11% [95% CI 7–16%, PI 1–69%]. The Anaplasma species pre-
valence was high during 1988–2010 [13%] from five studies than
2011–17 period [10%] with thirty studies and endorses the decreasing
prevalence of Anaplasma species in the recent years. The studies from
India covered sixteen states, which includes Punjab (Bakken et al.,
1994), Tamilnadu (Park et al., 2018), Karnataka (Kuttler, 1984), Gu-
jarat (Radostits et al., 2000), Haryana (Radostits et al., 2000), Ra-
jasthan (Brayton et al., 2006), Uttar Pradesh (Brayton et al., 2006) and
one study each from Andhra Pradesh, Assam, Himachal Pradesh,
Jammu and Kashmir, Kerala, Madhya Pradesh, Maharashtra, Telangana
and West Bengal states. The zone-wise prevalence of Anaplasma species
in India are depicted in Fig. 4. The zone-wise analysis revealed in-
creased prevalence of Anaplasma species in Central zone [61%] and less
in South and West zones [6%]. The Anaplasma species prevalence stu-
dies was limited from Central (Dumler et al., 2001) and East zones
(Kuttler, 1984) in India. The species-wise analysis indicated that the
Anaplasma species pooled prevalence was high in cattle with 12% [95%
CI 8–18%, PI 1–70%] when compared to buffalo with 2% [95% CI
0–6%, PI 0–65%]. Based on the methods of detection of the Anaplasma
species, it was observed that the prevalence was high in using serology
[34%], followed by nucleic acid-based techniques [32%] and blood
smear examination method [7%]. The Q statistics showed highly sig-
nificant [P < 0.01] difference between the studies except for the East
zone was significant [P < 0.01] and Central zone which was having
one study only.
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Research in Veterinary Science 123 (2019) 159–170
3.3. Meta-analysis of Anaplasma prevalence from the world
The results of meta-analysis of prevalence studies of Anaplasma
species from the World are presented in Table 4. The forest plot for
prevalence of Anaplasma species in the World are depicted in Fig. 3. The
number of studies on prevalence of Anaplasma species was 66 studies
from the World obtained from 46,365 samples. The pooled estimate of
prevalence of Anaplasma species was 39% [95% CI 30–49%, PI 2–95%]
with the studies obtained from five continents and thirty countries in
the World. The year-wise analysis showed larger prevalence during
1978–2010 [46%] when compared to 2011–17 years [31%]. The Ana-
plasma species prevalence in different continents of the World are de-
picted in Fig. 5. The continent-wise analysis revealed high Anaplasma
species prevalence in South America [82%] followed by Europe [42%],
North America [36%], Africa [35%] and Asia [33%]. The country
which reported highest number of studies were from United States of
America (Stuen et al., 2013) followed by Bangladesh (Kuttler, 1984),
Pakistan (Kuttler, 1984) and South Africa (Kuttler, 1984) compared to
other countries. The period-wise analysis of prevalence of Anaplasma
species revealed decreasing trend in all the five continents during
2011–17 period when compared to the past years studies. The Ana-
plasma species prevalence based on method-wise indicated high pre-
valence by serology [46%] followed by nucleic acid-based techniques
[42%] and blood smear examination method [21%]. The Q statistics
revealed highly significant difference, indicating the heterogeneity be-
tween the studies for Anaplasma species prevalence in the World based
on year-wise, continent-wise, period-wise and method-wise.
 K. Paramanandham et al.

Table 4
Meta-analysis of prevalence studies on Anaplasma species in dairy animals of World.
Sl. no. Parameters Period Number of Total events Pooled prevalence (%) [confidence interval at Prediction interval (%) at 95% I2 value (%) Tau square Degrees of Q statistics
studies 95% level] level value freedom

1. Anaplasmosis in World 1978–2017 66 46,365 39 (30–49) 2–95 99 2.892 65 6400a

Year wise
1. Anaplasmosis in World-I 1978–2010 37 31,874 46 (31–62) 2–98 100 3.728 36 0a
2. Anaplasmosis in World-II 2011–2017 29 14,491 31 (21–42) 3–87 99 1.737 28 2700a

Continent wise
1. Anaplasmosis in Africa 1978–2017 24 10,690 35 (21–52) 1–96 99 3.131 23 2200a
2. Anaplasmosis in Asia 2004–2017 13 3302 33 (19–51) 2–92 98 1.845 12 550a
3. Anaplasmosis in Europe 1992–2017 11 7670 42 (23–65) 2–96 99 2.331 10 900a
4. Anaplasmosis in North America 1982–2016 14 17,836 36 (19–57) 1–96 100 2.657 13 0a
5. Anaplasmosis in South America 1990–2015 4 6867 82 (29–98) 0–100 99 6.141 3 200a

Period wise
1. Anaplasmosis in Africa-I 1978–2010 14 6284 39 (18–65) 1–98 99 4.152 13 1200a
2. Anaplasmosis in Africa-II 2011–2017 10 4406 30 (15–51) 1–93 98 2.065 9 400a

164
3. Anaplasmosis in Asia-I 2004–2010 4 1172 38 (18–63) 0–99 97 1.015 3 66.7a
4. Anaplasmosis in Asia-II 2011–2017 9 2130 30 (13–55) 1–95 98 2.360 8 350a
5. Anaplasmosis in Europe-I 1992–2010 6 6943 46 (15–79) 0–100 100 3.562 5 0a
6. Anaplasmosis in Europe-II 2012–2017 5 727 39 (18–64) 1–97 96 1.335 4 75a
7. Anaplasmosis in North 1982–2010 11 15,424 43 (21–68) 1–98 100 2.956 10 0a
America-I
8. Anaplasmosis in North 2011–2017 3 2412 18 (7–37) 0–100 98 0.793 2 33.3a
America-II
9. Anaplasmosis in South 1990–2010 2 2051 97 (81–100) – 97 2.059 1 0a
America-I
10. Anaplasmosis in South 2011–2017 2 4816 41 (10–82) – 91 1.642 1 0a
America-II

Method wise
1. Anaplasmosis by Blood smear 2002–2017 15 4422 21 (11–35) 1–85 98 1.935 14 700a
2. Anaplasmosis by Serology 1978–2016 37 37,973 46 (32–61) 2–97 100 3.349 36 0a
3. Anaplasmosis by Molecular 1990–2017 24 6476 42 (28–57) 3–95 98 2.306 23 1100a

a
Highly significant.
Research in Veterinary Science 123 (2019) 159–170
K. Paramanandham et al. Research in Veterinary Science 123 (2019) 159–170

Fig. 3. Forest plot showing the details of the studies from the World and their prevalence estimates.

4. Discussion production. It is also considered as one of the top ten economically

important livestock diseases affecting ruminants in India as per the
Anaplasmosis, caused by the intracellular rickettsia and endemic in PD_ADMAS Annual report, 2005–06. The results of meta-analysis pro-
several parts of the World and has continued to impact the dairy vides a quantitative level of Anaplasma species prevalence by

165
K. Paramanandham et al.
Fig. 4. India map showing the zone -wise prevalence estimates of Anaplasma
species based on meta-analysis.
considering differences in the results and approaches followed by var-
ious researchers in different studies from various states of India and
different countries of the World. The present study revealed pooled
prevalence estimate of Anaplasma species in dairy animals from India
and various countries of the World over the years up to 2017 and found
high prevalence in the World when compared to India. This indicated
the importance of Anaplasma species infections in different countries of
the World. In the present study, the prevalence estimate for Anaplasma
Fig. 5. World map showing the Continent -wise prevalence estimates of Anaplasma species based on meta-analysis.
166
Research in Veterinary Science 123 (2019) 159–170
species was higher in central zone when compared to other zones in
India, which showed ≤17%. This might be due to the differences in
agroclimatic factors, dairy animal rearing systems, management prac-
tices, breeds and presence of wildlife due to more forest cover in central
zone as reported earlier (Misraulia et al., 1988). In a study from South
India, the prevalence of Anaplasma species was found to be 20% as
detected by nucleic acid-based techniques (Nair et al., 2013), and was
high when compared to the present study in south zone of India. It was
reported that the prevalence of Anaplasma species in dairy animals is
highly variable (Kocan et al., 2010; Kocan et al., 2003) and concurred
with the present study. This might be due to the variation in the pre-
valence studies used for meta-analysis and it was the purpose of this
study to determine the prevalence estimate from various studies. Fur-
ther, there was high heterogeneity was observed between various stu-
dies for the estimates of Anaplasma species prevalence and it might be
due to various factors including age (Kolte et al., 2017; Ashuma et al.,
2013; Rather et al., 2015), breed (Kolte et al., 2017), sex (Rather et al.,
2015), parity of cattle, agroclimatic conditions (Arunkumar and
Nagarajan, 2013; Sharma et al., 2015a) and farm managemental prac-
tices. In a study reported that the buffaloes and young animals may act
as persistent carrier, which may act as source of infection for other
animals in the herd (Ashuma et al., 2013). Young crossbred animals are
more likely than native breeds or older age crossbred cattle for har-
bouring infections with two tick borne pathogens, as reported earlier
(Kolte et al., 2017). Higher prevalence of anaplasmosis in clinically
normal crossbreds of northern Kerala of South India indicated sub-
clinical infections or carrier status of these vector borne diseases, as
previously reported (Nair et al., 2013). The abundance of biting flies
(Tabanus spp. and Stomoxys spp.) due to the hot and humid tropical
climatic conditions prevailing in the Tamil Nadu may augment the
mechanical transmission of the disease to naïve animals (Arunkumar
and Nagarajan, 2013). There were large differences in distribution of
tick borne pathogens across different agroclimatic zones of Maharashtra
state in India, as reported earlier (Kolte et al., 2017). In a study from
Mysuru, Karnataka, the anaplasmosis in dairy animals was more pre-
valent during rainy season followed by winter and summer seasons
K. Paramanandham et al.
(Murthy et al., 2014).
The wildlife reservoirs of A. marginale may impact the epidemiology
of anaplasmosis of the World. Concern about the transmission of A.
marginale, between wildlife and domestic livestock is increasing, espe-
cially in areas where free-ranging wildlife and cattle share common
grazing areas (Chomel et al., 1994). Clinical anaplasmosis occurs in
cattle, but other ruminants have been reported to serve as reservoirs of
A. marginale, including American bison (Bison bison), white-tailed deer
(Odocoileus virginianus), mule deer (Odocoileus hemionus hemionus),
black-tailed deer (Odocoileus hemionus columbianus) and rocky moun-
tain elk (Cervus elaphus nelsoni) as reviewed by Kuttler (1984). Wildlife
species may be a factor in the epidemiology and spread of anaplasmosis
because, as reservoir hosts of A. marginale, they could serve as source of
infective blood for mechanical spread by various routes and biological
transmission by ticks. The distribution of anaplasmosis may be expected
to continue to change as a result of cattle movement, but also may be
impacted in the future by climate change which could affect the
movement of the ticks (Jonsson and Reid, 2000). Climate change may
also affect the anaplasmosis prevalence by affecting the range of ru-
minants and tick hosts (Kocan et al., 2010). Ticks in the environment
have adapted to survive extreme cold temperatures and survival is
dependent on vegetation to promote conservation of humidity and
protect them from desiccation. The arthropod population usually in-
crease after periods of extreme weather conditions as reported earlier
(Kocan et al., 2010). The species of animal mostly affected by Ana-
plasma species infection indicated that the high prevalence in cattle
than in buffaloes in India. This may be due to host species preferences
of the disease and also due to more number of Anaplasma species pre-
valence studies available for cattle than buffaloes in India. Further, the
buffaloes may act as reservoirs of Anaplasma species that are re-
sponsible for disease prevalence in cattle (Kocan et al., 2010). The
Anaplasma species prevalence was high in serological method of de-
tection and it might be due to the antibodies was detected in animals for
long time periods. Among the antigen detection methods, nucleic acid-
based techniques are highly sensitive and detected more positive cases
than compared to blood smear examination and concurred with pre-
vious studies (Arunkumar and Nagarajan, 2013; Sharma et al., 2015b).
The period-wise prevalence estimates for Anaplasma species showed
decreasing trend during 2011–17 when compared to before 2011
period for India and in the five continents of the World. This might be
due to better treatment practices, diagnostic facilities available for ac-
curate diagnosis and awareness on tick and tick borne diseases among
the dairy farmers in recent years compared to the past years as per the
previous reports (Kocan et al., 2010; Nair et al., 2013).
In the present study, based on the continent-wise meta-analysis, the
prevalence in South America was higher than other continents, which
concurred with previous reports from countries of South America
continent includes Venezuela [57.7%], Colombia [64–100%], Brazil
[67.3%], Paraguay [92%] and Argentina [7–61%] (Kocan et al., 2003).
This might be due to the practices of vaccine against the anaplasmosis is
being followed in many countries of South America. It also might be
due to the less number of studies reported, more number of endemic
countries present in this continent, more tick population, agroclimatic
conditions favourable for occurrence of disease in South America
(Payne and Osorio, 1990; Alfredo et al., 2005; Belal et al., 2014; Aktas
and Ozubek, 2015). Further, it may be due to the limited number of
studies i.e., four studies (Payne and Osorio, 1990, Alfredo et al., 2005,
Belal et al., 2014, Aktas and Ozubek, 2015), were available from this
continent during the period of study and serological methods were used
for prevalence estimations. However, the prevalence estimates was less
in the Asia continent and might be due to different agroclimatic zones
(Arunkumar and Nagarajan, 2013; Sharma et al., 2015a), vector po-
pulation availability (Kocan et al., 2010, Nair et al., 2013) and different
strains of A. marginale from different countries (Dreher et al., 2005). In
a phylogenetic association analysis study of the strains from India
showed close proximity with strains of Mexico and also identified
167
Research in Veterinary Science 123 (2019) 159–170
heterologous population of A. marginale strains causing anaplasmosis in
India (George et al., 2016). Further, in a genetic diversity study from
Brazil, South America indicated that only three strains of A. marginale
was circulating in the study area and in Rio de Janeiro also indicated
animals infected with high quantities of Rhipicephalus microplus and
animals are circulated through different pastures throughout course of
the year, exposed to new infected tick populations (Hairgrove et al.,
2015). The method-wise prevalence estimate was high in serology and
indicated the more number of animals having the antibodies against
Anaplasma species. This might be due to the serological tests detects
both present and past exposure to Anaplasma species when compared to
nucleic acid-based techniques that detect present infections only. Fur-
thermore, Anaplasma species infections may become persistent with low
parasitemia and are unable to detect by nucleic acid-based techniques
but with circulating antibodies, which can be detected by serological
methods. The use of drugs for therapeutic purposes against Anaplasma
species may also lead to clearance of parasites from the blood, but with
circulating antibodies remaining, which may be detected by serological
methods (Rather et al., 2015). Based on antigen-based detection
methods, it indicated high sensitivity for nucleic acid-based techniques
in detection of Anaplasma species than blood smear examination and
corroborated with earlier reports (Arunkumar and Nagarajan, 2013;
Sharma et al., 2015b).
This meta-analytic study shows wide-spread occurrence of
Anaplasma infections in dairy cattle and buffaloes in India and the
World. Dairy animals that are detected as positive by antigen-based
detection methods (e.g., blood smear examination and PCR) should be
treated with therapeutic drugs like tetracycline compounds. Further,
the animals can be prevented from Anaplasma species infection by
avoiding transmission through needles, surgical instruments and also
by use of insecticide sprays and dips to reduce the insects and tick
population. The antibodies positive animals may act as carrier and re-
servoir animals which may be treated with low doses of chlortetracy-
cline and by using insecticides, acaricide sprays at regular intervals may
minimize the biting insect and tick populations. Proper management of
manure with proper disposal may be practiced to reduce the insect
population in the dairy farms and prevent the Anaplasma species in-
fection in dairy animals in India and the World.
The prevalence estimate in the present study may be viewed with
certain limitations, as it does not provide the estimate for the associa-
tion of disease prevalence with risk factors. Further, there are many
other factors which causes variation between the studies are breed, age,
parity of the animal, lactation number, milk yield, managemental
practices, climatic conditions, geographical area and period of study
may also affect the prevalence of Anaplasma species in dairy cattle. The
prevalence estimates in various zones of India and continents in the
World, identifies the high prevalence zones or areas to be concentrated
to overcome the occurrence of Anaplasma species infections in dairy
animals. This prevalence data will help the dairy farmers to modulate
farming practices, and for the policy and decision makers to strategize
the prevention and control measures for Anaplasma species infections in
the dairy animals. The resource allocation for the implementation of
effective control measures for this disease may be diverted to only those
areas where the disease is highly prevalent. Presence of vectors, carrier
and reservoir animals play a significant role for the incidence and
transmission of Anaplasma species. The effective control of the disease
depends on the control of these three elements. Control of ticks and
biting insects may be achieved by the use of insecticide sprays and dips
that can help to reduce the insect population and the potential for the
transmission of anaplasmosis by insect vectors. In order to successfully
prevent Anaplasma species transmission by needles, surgical instru-
ments and other veterinary equipments, a thorough rinse in hot water
or dilute disinfectant may be practiced. Vaccination is practiced for the
control of anaplasmosis Worldwide but not in India presently. Vaccines
for the control of anaplasmosis can be divided into two major types,
namely live and killed vaccines both rely on the use of A. marginale
K. Paramanandham et al.
from infected bovine erythrocytes. These vaccines induce protective
immunity that prevents clinical disease, but these vaccines do not
prevent cattle from becoming persistently infected with A. marginale.
There is need for scientific management practices, early diagnosis and
timely therapeutic interventions by field veterinarians, so as to control
and prevent the occurrence of Anaplasma species in India and the
World, and thereby improving the productivity of dairy animals.
5. Conclusion
In conclusion, the present study estimated the pooled prevalence of
Anaplasma species in India and the World in dairy cattle by using meta-
analysis. There was high prevalence of Anaplasma species in the World
when compared to India and also in South America when compared to
other continents. Hence, there is need for scientific management
methods to be adopted to minimize the prevalence of Anaplasma species
in dairy animals in India and the World. The serological method of
antibody detection and nucleic acid-based techniques for detection of
antigen are highly sensitive when compared to other methods and may
be followed in future studies on Anaplasma species prevalence. The high
prevalence of Anaplasma species in dairy cattle may cause low milk
yield over the years and lead to greater economic loss to the dairy
farmers. Hence, the study advocates, to overcome the occurrence of
Anaplasma species, there is need for scientific management practices,
early diagnosis and timely therapeutic interventions by field veter-
inarians, so as to improve the productivity of dairy animals in India and
the World. Further, to assess the overall prevalence levels of Anaplasma
species in India and across the zones, there is a need for more studies on
Anaplasma species prevalence from Central and East zones of India and
also apart from thirty countries of the World.
Conflict of interest
The authors declare no conflict of interests.
Acknowledgement
The authors thank Indian Council of Agricultural Research spon-
sored National Innovations in Climate Resilient Agriculture (NICRA)
Project for providing funds and necessary support, under which this
research work has been carried out.
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