Veterinary Parasitology 244 (2017) 102–110

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Veterinary Parasitology
journal homepage: www.elsevier.com/locate/vetpar

Review article

Exploitation of chemical, herbal and nanoformulated acaricides to control MARK

the cattle tick, Rhipicephalus (Boophilus) microplus – A review
Balan Banumathia, Baskaralingam Vaseeharana,⁎, Periyannan Rajasekarb,
Narayanan Marimuthu Prabhub, Palaniappan Ramasamyc, Kadarkarai Murugand,
Angelo Canalee, Giovanni Benellie,f,⁎⁎
a
Biomaterials and Biotechnology in Animal Health Lab, Department of Animal Health and Management, Alagappa University, Science Campus 6th Floor, Karaikudi 630
003, Tamil Nadu, India
b
Disease Control, Prevention and Alternative Medicine Lab, Department of Animal Health and Management, Alagappa University, Science Campus 6th Floor, Karaikudi
630 004, Tamil Nadu, India
c
R & D Wing, Sree Balaji Medical College and Hospital, BIHER (Bharath University), Chromepet, Chennai 600044, Tamil Nadu, India
d
Department of Biotechnology, Thiruvalluvar University, Serkkadu, Vellore, 632 115, Tamil Nadu, India
e
Department of Agriculture, Food and Environment, University of Pisa, via del Borghetto 80, 56124 Pisa, Italy
f
The Bio Robotics Institute, Scuola Superiore Sant’Anna, Viale Rinaldo Piaggio 34, 56025 Pontedera, Pisa, Italy

A R T I C L E I N F O A B S T R A C T

Keywords: The tick Rhipicephalus (Boophilus) microplus is a key vector of bacterial and protozoan diseases causing heavy
Babesia economic losses directly and indirectly in animal husbandry. In the past decades, the control of ticks faced some
Ixodidae major issues, such as the rapid development of resistance in targeted vectors and non-target effects on human
Medicinal plant health and the environment, due to the employ of synthetic acaricides and repellents. Eco-friendly pesticides for
Ethno-veterinary
treating and controlling animal parasites such as ticks were mainly from medicinal plants and thus they form the
Tick control
richest entity for manufacturing resources for drugs. Even though there are efforts made to discover reliable
plant-based acaricides to control ectoparasites in animal husbandry, the effective control of R. (B.) microplus
ticks still represent a major challenge in current veterinary entomology. Recently, a wide number of promising
attempts have been conducted to use herbal preparations and green-fabricated nanoparticles for the control of R.
(B.) microplus. The aim of this review is to critically summarize and discuss the use of herbal preparations used in
ethno-veterinary as well as green-fabricated nanoparticles as novel acaricides for the control of the cattle tick R.
(B.) microplus.

1. Introduction borne diseases (Benelli, 2016c).

Ticks are hematophagous ectoparasites of vertebrate animals that
transmit bacterial, viral, and protozoan diseases (De La Fuente et al.,
2008). The cattle tick, Rhipicephalus microplus is the most important tick
parasite of livestock in the world. This species can transmit babesiosis
caused by protozoan parasites, i.e. Babesia bigemina and Babesia bovis, as
well as anaplasmosis, caused by Anaplasma marginale. Ticks are asso-
ciated with loses in milk and meat production, as well as mortality in
animals, thus they led to economical loses of several million dollars
worldwide (Ram et al., 2004; Polar et al., 2005; Jonsson, 2006; Grisi
et al., 2014). Therefore, there is an urgent need to assess and develop
immediate cost-effective treatments for the control of ticks and tick-
Chemical acaricides have been used extensively to control ticks.
However, these chemicals led to the development of resistance in tar-
geted vectors and residues in the environment. Moreover, these acar-
icides are harmful to animals and humans (Nonga et al., 2011; Balbus
et al., 2013). However, the use of non-chemical control methods in-
cluding the use of plant-borne products containing acaricidal com-
pounds have also been proposed by Castrejon (2003) and Pavela et al.
(2016) to curtail the environmental and economic impact of synthetic
acaricides. The search of natural tools (Habeeb, 2010) using plant-
based bioacaricides are attractive to control tick populations. The so-
called “green pesticides” are currently claimed as one of the useful tools
for controlling ectoparasites (Cruz et al., 2013; Benelli, 2015a, 2015b,

⁎
Corresponding author at: Biomaterials and Biotechnology in Animal Health Lab, Department of Animal Health and Management, Alagappa University, Science Campus 6th Floor,
Karaikudi 630 003, Tamil Nadu, India.
⁎⁎
Corresponding author at: Department of Agriculture, Food and Environment, University of Pisa, via del Borghetto 80, 56124 Pisa, Italy.
E-mail addresses: vaseeharanb@gmail.com, bvaseeharan@yahoo.co.in (B. Vaseeharan), benelli.giovanni@gmail.com (G. Benelli).

http://dx.doi.org/10.1016/j.vetpar.2017.07.021
Received 25 March 2017; Received in revised form 18 July 2017; Accepted 19 July 2017
0304-4017/ © 2017 Elsevier B.V. All rights reserved.
B. Banumathi et al.
2016a; Benelli et al., 2016), but showed several flaws, highlighting
their often-unreliable potential for the control of tick populations
(Pavela and Benelli, 2016). However, they can also be potentially
combined with other control tools, in agreement to the criteria of In-
tegrated Vector Management (WHO, 2017a, 2017b; Benelli and Beier,
2017).
Nanotechnology is a branch of science that currently plays a key
role in several different fields due to its numerous applications in bio-
medicine, food engineering, pharmacology, parasitology, and en-
tomology (Benelli, 2016b, 2016c; Benelli et al., 2017a). Nanomaterials
fabricated using green reducing agents play a major role in the field of
drug delivery, antimicrobials, bio labelling, and pesticide science
(Salam et al., 2012; Benelli et al., 2017). The aim of this review is to
critically summarize and discuss the use of herbal preparations used in
ethno-veterinary and nanoparticles as novel acaricides for the control of
the cattle tick R. (B.) microplus.
2. Current control strategies against the cattle tick R. (B.)
microplus
2.1. Chemical acaricides
Chemical acaricides such as arsenic, chlorinated hydrocarbons, or-
ganophosphates, carbamates, and pyrethroids have played a major role
in tick control programs. However, the use of chemical acaricides has
been reported as only partially effective to control tick populations and
is linked to several disadvantages such as residues occurred in the milk
and meat. Moreover, it can also lead to the development of resistant tick
strains (Nolan, 1990; Clark et al., 1995; Chen et al., 2007; Reck et al.,
2014). Arsenic was the first effective chemical acaricides widely used to
control tick and tick borne diseases, it was cheap and effective. How-
ever, it is very toxic to humans and livestock, and showed the resistance
in R. (B.) microplus in many part of the world (Drummond, 1983).
Subsequently, chlorinated hydrocarbons have been used to control
against ticks replacing arsenic-based products. The usage of chlorinated
hydrocarbon compounds has been considerably condensed due to the
constant presence of residues in animal tissues and related chronic
toxicity. Later, organophosphates have been then utilized to replace
chlorinated hydrocarbons. Their residual efficiency is smaller over
chlorinated hydrocarbons, on the other hand the hazard of causing
acute toxicity in livestock is greater (Drummond, 1983). Carbamates
have been used alternatively to control ticks they are more expensive
and little more toxic than the organophosphates for cattle (Rajput et al.,
2006). Since more than twenty years, other chemical acaricides have
been used, including amitraz, fenilpirazoles and fluazuron; in the last
years, isoxasolinas has been also employed (Miller et al., 2002). Com-
monly used tick acaricides lindane and dieldrin (organochlorides),
carbaryl (carbamates), amitraz (formamidines), coumaphos and dia-
zinon (organophosphates), avermectin and milbemycins (macrocyclic
lactones), cypermethrin and permethrin (pyrethrins/pyrethroids) acted
on nervous system of ticks, with different mode of action GABA
(gamma-aminobutyric acid)-gated chloride channel antagonists, choli-
nesterase inhibitors, octopamine agonists, acetylcholine esterase in-
hibitors, chloride channel activator, and sodium channel modulators,
respectively (Lawrence and Casida, 1983; Li et al., 2005; Chen et al.,
2007; Li et al., 2003; Clark et al., 1995; Narahashi, 1971). However,
different indirect effects of synthetic acaricides, due to their usage of
large scale, have been noted, including the fast-growing development of
resistance (Castro-Janer et al., 2010; Reck et al., 2014).This can lead to
a little impact of these acaricides on the survival and reproduction of
ticks (Mondal et al., 2013).
2.2. Vaccines
The employ of vaccines against ticks have been carried out fol-
lowing two difference ways: (i) development of vaccines of variable
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Veterinary Parasitology 244 (2017) 102–110
efficacy against tick-borne diseases, (ii) development of vaccines
against tick gut glycoproteins, which have become commercially
available, resulting in a reduced the need of acaricidal applications
(Mondal et al., 2013; De la Fuente, 2015; De La Fuente et al., 2007,
2008, 2016; Schetters et al., 2016).The production of vaccines re-
presents a promising tool to control the cattle tick R. (B.) microplus. Tick
extracts have been used to immunize cattle from ticks (Willadsen et al.,
1988). In the past decades, Theileria parva has been used to formulate
and stabilize a vaccine, mild Boleni strain has been used to isolate
components for vaccine production (FAO, 1998). However, this vaccine
is highly expensive and has several side effects (CRC-VT, 2001). Later,
the recombinant Bm86 based vaccines has been developed to fight R.
(B.) microplus (Garcia-Garcia et al., 2000; Willadsen, 2001). Re-
combinant vaccines like Gavac® (Heber Biotec; Havana, Cuba), TickG-
ARD (Hoechst Animal Health; Australia), and TickGARDPLUS (Intervet
Australia; Australia) are commercially available against R. (B.) micro-
plus, and they were approved for use outside of the United States
(Willadsen, 2008; Freeman et al., 2010). However, Pereira et al. (2008)
reported the Tick-GARD vaccine used in field trials at some areas of
Brazil showed a not complete control of the target tick (Pereira et al.,
2008). Repeated inoculations of Bm86 (concealed antigen) is required
to provide continuing immunity because the presence of feeding ticks
does not boost the immune response of cattle. Subsequently, vitelline
and protein GP 80 have been used to reduce oviposition of B. microplus
feeding on sheep. However, their efficiency is not high. Alternatively,
advanced subunit vaccines are being developed (Jenkins, 2001). Al-
though their development and production is currently delayed and
complicated by several factors such as antigen variation and strain di-
versity. Abbas et al. (2014b) reported that the vaccine efficacy was
screened initially before launching in new geographical area and
combination of vaccine with chemotherapy is essential to reduce the
requirement of the acaricides.
2.3. Herbal preparations
According to Ahmad et al. (2012), and Muhammad et al. (2012),
Abbas et al. (2014a) reported that the development of new drugs and
vaccines against ticks was costly and showed some limits in effective-
ness. On the other hand, the overuse of synthetic acaricides led to re-
levant concerns associated to the presence of drug residues in the en-
vironments and food, as well as to the fast development of resistance in
targeted tick populations. Alternatively, medicinal plants are effective
and cheap for the control of cattle ticks (Babar et al., 2012). Many
ethnoveterinary plant extracts and essential oils have been tested with
success for their antiparasitic activity (Athanasiadou et al., 2007;
Masood et al., 2013; Abbas et al., 2014b). More than 60species of plants
belonging to 26 families have been evaluated against R. (B.) microplus
worldwide (Borges et al., 2011; Benelli et al., 2016).
2.3.1. In-vitro and in-vivo studies
Here, we reviewed current knowledge about the in-vitro and in-vivo
efficacy of plant products used to control R. (B.) microplus larvae and
adults. Different solvent extracts from 67 plants, i.e. ethanol, methanol,
hexane, ethyl acetate, aqueous, acetone, chloroform extracts, as well as
other plant extraction products, including essential oils and oleor-
esinous materials, have been tested at various concentrations against
this tick species (Table 1). These findings show that ethanol extracts are
the most commonly tested (in-vitro 62%, in-vivo 37%) to control R. (B.)
microplus, followed by methanol (in-vitro 10%), lyophilized (in-vitro 7%)
and hexane (in-vitro 6%) extracts. Ethyl acetate, aqueous and essential
oils showed lower percentages (3%) in in-vitro studies. On the other
hand, ethanol and aqueous extracts are equally tested in in-vivo studies
(50%) (Fig. 1).
In in-vitro study on R. (B.) microplus, 100% of lyophilized and
oleoresinous plant extracts were tested for larvicidal activity, while
acetone, chloroform extracts and essential oils were tested on adults;
B. Banumathi et al. Veterinary Parasitology 244 (2017) 102–110

Table 1
List of herbal preparations proposed for the control the cattle tick R. (B.) microplus.

Plants species and parts used Concentration Mortality (%) References

In vitro study
Ethanol extract
c c
Acorus calamus Rhizome 10% 100 Ghosh et al. (2011)
Aeschynomene denticulata Leaf, branch, stem, flower, fruit b
20% b
100 Santos et al. (2013)
b b
Annona squamosa Fruit peel 2000 ppm 100 Madhumitha et al. (2012)
c c
Seed 8% 70.8 Magadum et al. (2009)
Angelonia hirta Leaf, branch, stem, flower, fruit b
40% c40% b
100 c88 Santos et al. (2013)
c c
Allium sativum Garlic bulb 8% 8.3 Magadum et al. (2009)
b
Aspilia latissima Leaf 40% c50% b
97.88 c76 Santos et al. (2013)
c c
Azadirachta indica Seed 8% 80 Srivastava et al. (2008)
c c
Leaf 8% 30
Caperonia castaneifolia Leaf, branch, stem, flower b
40% b
100 Santos et al. (2013)
Centratherum punctatum Leaf, branch, stem, flower b
40% b
100 Santos et al. (2013)
c c
Citrus leminum Leaf 8% 20.8 Magadum et al. (2009)
Crotalaria micans Leaf, branch, stem, flower, fruit b
40% b
100 Santos et al. (2013)
Croton glandulosus Leaf, branch, stem, flower b
40% b
45.97 Santos et al. (2013)
c c
Curcuma longa Rhizome 8% 10 Srivastava et al. (2008)
Diodia kuntzei Root, leaf, thin branch, flower b
40% b
100 Santos et al. (2013)
Echinodorus paniculatus Leaf, branch, stem, flower b
20% b
100 Santos et al. (2013)
c c
Eucalyptus globulus Leaf 8% 29.8 Magadum et al. (2009)
c c
Guarea kunthiana Fruit 0.2% 99 Barbosa et al. (2013)
b b
Hippocratea volubilis Thin branch, leaf 40% 84 Santos et al. (2013)
Hyptis mutabilis Leaf, branch, stem, flower b
40% b
95 Santos et al. (2013)
Lantana canescens Leaf, branch, stem, flower b
40% b
99.63 Santos et al. (2013)
c c
Lobelia leschenaultiana Leaf 0.06 mg/ml 100 Banumathi et al. (2016)
Melanthera latifolia Leaf, branch, stem, flower b
40% c40% b
100 c73 Santos et al. (2013)
c c
Murraya koenigii Leaf Ranges 0.625<10.0% 100 Singh et al. (2015)
c c
Nicotiana tabacum Leaf 8% 45.8 Magadum et al. (2009)
c c
Nymphaea amazonum Trunk 0.2% 52 Barbosa et al. (2013)
b b
Ocotea diospyrifolia Thin branch, leaf 40% 98 Santos et al. (2013)
c c
Ocotea lancifolia Leaf 0.2% 34.5 Barbosa et al. (2013)
b
Piper aduncum Leaf 20 mg/mlc100 mg/ml b
40.47 c10 Silva et al. (2009)
* *
Prunus persica Seed 8% 70 Srivastava et al. (2008)
b b
Randia armata Thin branch, leaf, fruit 40% 75 Santos et al. (2013)
Richardia grandiflora Leaf, branch, stem, flower b
40% c40% b
100 c63 Santos et al. (2013)
b b
Sebastiana hispida Leaf, branch, stem 20% 100 Santos et al. (2013)
b b
Sesbania virgata Thin branch, leaf 40% 96.52 Santos et al. (2013)
b b
Fruit 40% 100
Senna obtusifolia Leaf, branch stem, flower, fruit b
40% b
40 Santos et al. (2013)
c c
Strychnos pseudoquina Trunk 0.2% 48 Barbosa et al. (2013)
c c
Tamarindus indica Seed 8% 41.7 Magadum et al. (2009)
b b
Tocoyena formosa Thin branch, leaf 40% 95 Santos et al. (2013)
b b
Zanthoxylum rigidum Thin branch, leaf 40% 100 Santos et al. (2013)

Methanol extract
b
Allium sativum Clove 100 mg/mlc100 mg/ml b
69.0 c80 Shyma et al. (2014)
b
Azadirachta indica Leaf 100 mg/mlc100 mg/ml b
55.2c33.33 Shyma et al. (2014)
b
Calotropis procera Leaf 100 mg/mlc100 mg/ml b
63.2c66.67 Shyma et al. (2014)
b
Carica papaya Seed 100 mg/mlc100 mg/ml b
82.2c93.33 Shyma et al. (2014)
b
Datura stramonium Leaf 100 mg/mlc100 mg/ml b
71.8c73.33 Shyma et al. (2014)
b
Petiveria alliacea Leaf, stem 20%c20% b20% c20% b
100 c26.6 b100 c86.6 Rosado-Aguilar et al. (2010)

Hexane extract
b b
Calea serrata Aerial parts 50 mg/ml 100 Ribeiro et al. (2008)
c c
Murraya koenigii Leaf Ranges 0.625<10.0% 70 Singh et al. (2015)
b
Piper aduncum Leaf 20 mg/ml c100 mg/ml b
70.42 c16 Silva et al. (2009)

Ethyl acetate extract

b
Palicourea marcgravii Leaf 20 mg/ml c100 mg/ml b
95 c78 Silva et al. (2011)
b
Piper aduncum Leaf 20 mg/mlc100 mg/ml b
17.25 c22 Silva et al. (2009)

Aqueous, acetone, chloroform extract

c c
Murraya koenigii Leaf Ranges 0.625<10.0% 10,40,10 Singh et al. (2015)
e e
aBaccharis trimera Leaf 150 mg/ml 100 Lázaro et al. (2013)

Essential oil
c c
Eucalyptus globulus Leaf (purchased) 5% 37.5 Kheirabadi et al. (2009)
c c
Pelargonium roseum Purchased 5% 98.3 Kheirabadi et al. (2009)

Other materialsd,f
d b b
Acacia pennatula Lyophilized, leaf 4800 >g/ml 54.8 Fernández-Salas et al. (2011)
d b b
Leucaena leucocephala Leaf 4800 >g/ml 66.79 Fernández-Salas et al. (2011)
d b b
Lysiloma latisiliquum Leaf 4800 >g/ml 52 Fernández-Salas et al. (2011)
d b b
Piscidia piscipula Leaf 4800 >g/ml 84 Fernández-Salas et al. (2011)
f b b
Copaifera reticulata Trunk 4500 ppm 100 Fernandes & Freitas (2007)

In-Vivo Study
(continued on next page)

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B. Banumathi et al. Veterinary Parasitology 244 (2017) 102–110

Table 1 (continued)

Plants species and parts used Concentration Mortality (%) References

Ethanol extract
c c
Acorus calamus Rhizome 10% 21.2 Ghosh et al. (2011)
c c
Annona squamosa Seed 8% 65.9 Magadum et al. (2009)
c c
Azadirachta indica Seed 8% 70.5 Srivastava et al. (2008)
c c
Dahlstedtia pentaphylla Root 1:10 mL 76.10 Pereira and Famadas (2006)

Aqueous extract
c,a c
Aloe ferox Leaf 40% 0 Moyo and Masika (2009)
c,a c
Lantana camara Leaf 40% 61.7 Moyo and Masika (2009)
c,a c
Ptaeroxylon obliquum Bark 40% 11 Moyo and Masika (2009)
c,a c
Tagetes minuta Leaf 40% 8.5 Moyo and Masika (2009)

a
Aqueous.
b
Larvae.
c
Adult.
d
Lyophilized.
e
Inhibition of egg hatching.
f
Oleoresinous.

ethyl acetate and methanol plant extracts were tested both on larvae
and adults of R. (B.) microplus. In addition, 44.7% of ethanol plant
extracts and 33% of hexane plant extract showed larvicidal activity.
50% of aqueous extracts and 39.47% of ethanol extracts showed
adulticidal activity. 33% of hexane extract (Piper aduncum) and 15.78%
of ethanol extracts of five plants i.e. Angelonia hirta, Aspilia latissima,
Melanthera latifolia, P. aduncum and Richardia grandiflora had larvicidal
and adulticidal activity against R. (B.) microplus (Fig. 2A). The ethanol
extracts from Angelonia hirta, Caperonia castaneifolia, Centratherum
punctatum, Crotalaria micans, Diodia kuntzei, Melanthera latifolia, Ri-
chardia grandiflora, Sesbania virgata and Zanthoxylum rigidum showed
complete larvicidal mortality (100%) when tested at 40% concentra-
tion. Similarly, the ethanol extracts of Aeschynomene denticulata, Echi-
nodorus paniculatus and Sebastiana hispida showed complete mortality
(100%) when tested at 20% concentration (Santos et al., 2013).
Madhumitha et al. (2012) also reported 100% mortality of tested ticks
at 2000 ppm. Moreover, the methanol extracts of all the plants were
reported to control both larvae and adults of R. (B.) microplus (Shyma
et al., 2014).The methanol extract of Petiveria alliacea (Rosado-Aguilar
et al., 2010), hexane extract of Calea serrata (Ribeiro et al., 2008) and
oleoresinous extract from Copaifera reticulata (Fernandes and Freitas,
2007) showed complete mortality at the concentrations of 20%, 50 mg/
ml and 4500 ppm respectively, in tests focused on larval stages. Hexane
(Palicourea marcgravii, Piper aduncum) and ethyl acetate (P. marcgravii,
P. aduncum) extracts possess both larvicidal and adulticidal activity
(Silva et al., 2009, 2011). The highest adulticidal mortality (100%) was
recorded testing ethanol extract of Lobelia leschenaultiana and Murraya
koenigii at 10%, 0.06 mg/ml and 10%, respectively (Banumathi et al.,
2016; Singh et al., 2015), followed by the ethanol fruit extract of Guarea
kunthiana (99%), the essential oil of Pelargonium roseum (98.3%) and
the methanol seed extract of Carica papaya (93.33%), tested at the
concentration of 0.2%, 5% and 100 mg/ml, respectively (Barbosa et al.,
2013; Kheirabadi et al., 2009; Shyma et al., 2014).
There are very few in-vivo studies about the control of R. (B.) mi-
croplus. Overall, two ethanol and aqueous extracts showed 100% used
against R. (B.) microplus (Fig. 2B). All the in-vivo studies focused on
adulticidal activity. The highest adulticidal mortality (76.10%) was
reported testing the ethanol root extract of Dahlstedtia pentaphylla at the
concentration of 1:10 mL (Pereira and Famadas, 2006). The extracts of
Acorus calamus, Annona squamosa and Azadirachta indica can control R.
(B.) microplus population in both in-vitro and in-vivo studies (Ghosh
et al., 2011; Magadum et al., 2009; Srivastava et al., 2008). The ethanol

Fig. 1. In-vitro and in-vivo studies aimed to control R.

(B.) microplus using plant products obtained using
solvents with different polarity or other extraction
methods.

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B. Banumathi et al. Veterinary Parasitology 244 (2017) 102–110

Fig. 2. Abundance (%) of in-vitro and in-vivo studies testing

different plant products against the life stages of cattle tick R.
(B.) microplus.

extract of A. calamus rhizomes showed 100% mortality at 10% in-vitro, resistant tick strains (Sarda et al., 2007; Pavela and Benelli, 2016).
while the mortality strongly decreased in in-vivo study (21.2% at Major shortcomings to face when preparing effective herbal formula-
10%).The great differences noted between in-vitro and in-vivo studies tions deal with important differences in the chemical composition of
can be due to the variations of experimental conditions from the la- plants of the same species due to extrinsic and intrinsic factors, as well
boratory to the field, where higher temperature, differences in R.H. and as complexity of transposing the efficacy obtained from the laboratory
UV radiations can lead to the degradation of some herbal components to the field (Borges et al., 2011). The combination of ethnoveterinary
in the tested preparations (see also Pavela and Benelli, 2016). In other products with synthetic acaricides may be expected to produce better
cases the efficacy of a given product is comparable; for example, the effects in terms of controlling ticks and delaying the resistance than the
ethanol extract of A. squamosa seeds led to mortality of 70.8% in-vitro use of acaricides alone (Abbas et al., 2014b)
and 65.9% in-vivo, when tested at 8%. The ethanol seed extract of A.
indica showed 80% mortality when tested at 8%. However, the mor-
2.4. Nanoparticle toxicity
tality decreased to 70.5% in-vivo, when testing the same concentration.
The R. (B.) microplus mortality varied among different solvents (e.g.,
2.4.1. In-vitro studies
ethanol, methanol, hexane, ethyl acetate, acetone and chloroform) and
Several applications of nanotechnology in veterinary medicine have
among in-vitro and in-vivo researches. Finally, the above reported herbal
been reported using nanomaterial scale devices for diagnosis, treat-
preparations may be enhanced with addition of other bioactive com-
ment, monitoring and traceability of agropecuary supplies (Kumar,
pounds. Another issue to face is that worldwide, researchers used dif-
2010). Furthermore, the advantages of nanoparticles used in drug de-
ferent plant material concentration units, including %, mg/ml, >g/ml,
livery system are mainly represented by decreased toxicity and site-
and ppm, in their studies. Based on the reports, it is very difficult to
specific targeting, which can be achieved by attaching targeted ligands
compare the various concentrations for the control of tick infection on
on the surface of the particles, through various routes of administration
cattle. Therefore, uniformity of concentration units is essential to cal-
including oral, nasal, parenteral, and intraocular. In addition, limita-
culate with accuracy tick mortality, this is also important in in-vivo
tions of antiparasitic drugs have been also recognized including drug
experimental analysis. For example, >g/ml can be followed uniformly
toxicity, and development of resistance. Currently, nanobiotechnology
to estimate the mortality in future research. This can be also helpful for
represents a novel approach in livestock science, with special reference
young researchers to easily review and understand the tick mortality
to the treatment of parasitic infections and arthropod vectors (Irache
concentrations for application works in the field.
et al., 2011; Rai and Ingle, 2012; Underwood and van Eps, 2012; Benelli
Many researchers have documented them as potential acaricides to
and Lukehart, 2017). Nanoparticles such as silver, gold, zinc oxide,
control all stages of tick species (Ghosh et al., 2011). There are many
selenium oxide, and chitosan ones have high efficacy of inhibition
advantages of using plant extracts to control R. (B.) microplus, indeed
against vectors of parasitic infections (Elmi et al., 2013; Sujitha et al.,
they can be used in organic cattle farming and are also associated with
2015). Particle aggregation is difficult in liquid nanoparticle formula-
lower environmental and food contamination to animals (Borges et al.,
tions, which are characterized by smaller size and large surface area
2011). In addition, herbal preparations used in ethno-parasitology are
(Jawahar and Meyyanathan, 2012). Currently, a limited number of
usually scarcely toxic to mammals and rarely allow the development of
attempts has been made by researchers to study the toxicity of various

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B. Banumathi et al. Veterinary Parasitology 244 (2017) 102–110

Table 2
Metal and metal oxide nanoparticles used to control the cattle tick R. (B.) microplus.

Nanoparticles Mode of synthesis Material used Concentration and mortality (%) References

a a
Zinc oxide (ZnO) Chemical synthesis Zinc nitrate and sodium hydroxide 10 mg/L 100 Kirthi et al. (2011)
b b
Green synthesis Aqueous leaf extract of Lobelia leschenaultiana 0.008 mg/ml 100 Banumathi et al. (2016)
a a
Silver (Ag) Green synthesis Aqueous leaf extract of Mimosa pudica 20 mg/L 89 Marimuthu et al. (2011)
a a
Green synthesis Aqueous leaf extract of Manilkara zapota 20 mg/L 100 Rajakumar and Rahuman (2012)
a a
Green synthesis stem aqueous extract of Cissus quadrangularis 5 mg/L 100 Santhoshkumar et al. (2012)
a a
Copper (Cu) Chemical synthesis Copper acetate 8 mg/L 100 Ramyadevi et al. (2011)
a a
Nickel (Ni) Chemical synthesis Nickel hydrazine 25 mg/L 100 Rajakumar et al. (2013)
Titanium dioxide (Ti) Green synthesis Aqueous flower extract of Calotropis gigantea a
20 mg/L a
100 Marimuthu et al. (2013)
a a
Green synthesis Aqueous leaf extract of Mangifera indica 25 mg/L 100 Rajakumar et al. (2015)

a
Larvae.
b
Adult.

metallic nanoparticles against R. (B.) microplus (Table 2).
2.4.1.1. Zinc oxide nanoparticles. The efficacy of zinc oxide
nanoparticles synthesized with wet chemical method, using zinc
nitrate and sodium hydroxide, has been reported, showing high
acaricidal activity. The mortality of R. (B.) microplus was 43% at 1 h,
64% at 3 h, 78% at 6 h, and 100% at 12 h post-treatment with ZnO
nanoparticles. The chemically synthesized ZnO nanoparticles produced
100% mortality on R. (B.) microplus when tested at 10 mg/L, and
showed a LC50 of 13.41 mg/L (Kirthi et al., 2011). Later, it was reported
that zinc oxide nanoparticles synthesized with the leaf extract of Lobelia
leschenaultiana (Ll-ZnO NPs) were effective against R. (B.) microplus.
The adult R. (B.) microplus were treated with different concentrations of
L. leschenaultiana leaf extract, zinc acetate and Ll-ZnO NPs 24 h post-
treatment. R. (B.) microplus exposed to 40, 40, 8 mg/L of L.
leschenaultiana leaf extract, zinc acetate and Ll-ZnO NPs showed
93.33, 70, 100% mortality with LC50 of 5, 19.2, and 1.7 mg/L,
respectively. The calculated percentage mortality and LC50 of Ll-ZnO
NPs were really lower if compared to that of zinc acetate and L.
leschenaultiana leaf extract (Banumathi et al., 2016).
2.4.1.2. Silver nanoparticles. A study conducted by Marimuthu et al.
(2011) evaluated the antiparasitic activity efficacy of silver
nanoparticles synthesized using the aqueous leaf extract of Mimosa
pudica against the larvae of R. (B.) microplus. The highest percentage of
mortality, i.e. 89%, was reported testing 20 mg/L and the LC50 was
8.98 mg/L. The antiparasitic activity of aqueous leaf extract of
Manilkara zapota and M. zapota-synthesized silver nanoparticles on R.
(B.) microplus have also been reported. The percentage mortalities
testing the aqueous leaf extract of M. zapota were 13, 25, 48, 56 and
75% at the doses of 3.125, 6.25, 12.5, 25 and 50 mg/L, respectively.
However, the highest mortality was recorded with silver nanoparticles
synthesized using the aqueous leaf extract of M. zapota (18% at
1.25 mg/L, 34% at 2.5 mg/L, 67% at 5 mg/L, 86% at 10 mg/L and
100% at 20 mg/L). Silver nanoparticles from aqueous leaf extract of M.
zapota exhibited an LC50 of 3.44 mg/L (Rajakumar and Rahuman,
2012).
The acaricidal activity of aqueous extract of Cissus quadrangularis
and silver nanoparticles synthesized from stem aqueous extract of C.
quadrangularis against the larvae of cattle tick R. (B.) microplus have
been studied (Santhoshkumar et al., 2012). The mortality rates
achieved testing the aqueous extract of C. quadrangularis were 08, 25,
33, 40 and 59% at the concentrations of 10, 20, 30, 40 and 50 mg/L,
respectively. However, the highest mortality was recorded testing silver
nanoparticles synthesized using the stem aqueous extract of C. quad-
rangularis (42% at 5 mg/L, 55% at 10 mg/L, 68% at 15 mg/L, 85% at
20 mg/L and 100% at 5 mg/L). Overall, the Ag nanoparticles fabricated
using the stem aqueous extract of C. quadrangularis achieved LC50 and
LC90 values of 7.61 and 22.68 mg/L, respectively (Santhoshkumar
et al., 2012).
2.4.1.3. Copper nanoparticles. Metallic copper nanoparticles were
synthesized using a polyol process and tested against the larvae of R.
(B.) microplus. The larval mortality rates were 36, 47, 69, 88 and 100%
at 0.5, 1.0, 2.0, 4.0 and 8.0 mg/L, with LC50 of 1.06 mg/L (Ramyadevi
et al., 2011).
2.4.1.4. Nickel nanoparticles. The larvicidal activity against R. (B.)
microplus was studied testing nanoparticles synthesized using a
chemical route based on the employ of nickel hydrazine complexes
solution. The larval mortality rates were 25, 45, 69, 80 and 100% at 5,
10, 15, 20 and 25 mg/L. LC50 values of Ni<hydrazine complex solution
and synthesized Ni nanoparticles were 20.35 and 10.17 mg/L,
respectively (Rajakumar et al., 2013).
2.4.1.5. Titanium dioxide nanoparticles. Titanium dioxide nanoparticles
are considered promising photocatalytic materials due to their long-
term thermodynamic stability, strong oxidizing power, and relative
non-toxicity (Rajakumar et al., 2015; Murugan et al., 2016). The
acaricidal activity of TiO2 nanoparticles synthesized from flower
aqueous extract of Calotropis gigantea was assessed on the larvae of R.
(B.) microplus. The mortality rates post-treatment with the flower
extract and TiO (OH)2 solution at the concentration of 50 mg/L were
94% and 88%, respectively. The green synthesized TiO2 nanoparticles
showed 100% mortality at the concentration of 20 mg/L. The LC50 of
TiO2 nanoparticles was 5.43 mg/L (Marimuthu et al., 2013). The
mortality rates of R. (B.) microplus post-treatment with the TiO2
nanoparticles synthesized from the aqueous extract of Mangifera
indica were 19, 32, 54, 74 and 100% at 5, 10, 15, 20 and 25 mg/L.
The LC50 of TiO2 nanoparticles was 13.21 mg/L (Rajakumar et al.,
2015).
As a final remark, it should be noted that the smaller size of nano-
particles improved biocompatibility, with relevant advantages in the
fields of biomedicine and parasitology (Kim et al., 2007; Benelli,
2016b). In this framework, metal and metal oxide nanoparticles should
be studied further as new potential acaricides against R. (B.) microplus.,
with special reference to further research efforts aimed to shed light on
their mechanism of action. Very little is known on this. The small size of
nanoparticles can allow them to penetrate the nuclear membrane, in-
teracting with nucleic acids and protein synthesis (Benelli et al.,
2017b). In addition, it has been proposed that the adhesion of green
capped nanoparticles on the exoskeleton of ectoparasites may reduce
their physical movements (Baun et al., 2008). Besides, the phyto-
chemical capping nanoparticles may also deliver more efficiently their
toxicity on ticks, exploiting the large surface: volume ratio of the na-
nocarriers.
3. Conclusions
This review summarized different approaches for the control of
cattle tick R. (B.) microplus. The overuse of chemical acaricides is often

107
B. Banumathi et al.
Fig. 3. Abundance (%) of in-vitro and in-vivo studies using plant products and nano-
particles to control the cattle tick R. (B.) microplus.
responsible for the development of fast-growing drug resistance and
wide presence of toxic residues in food and the environment. The
availability of vaccines is still limited, and the currently available ones
showed major limitations in their effectiveness. Therefore, this review
focused on the current knowledge about herbal preparations and na-
noparticles used to control R. (B.) microplus populations. Currently
available researches are mostly focused (59%) on in-vitro studies when
testing herbal preparations, while only the 8% of the studies reported
on in-vivo data (Fig. 3). Notably, for nanoparticles, only in-vitro re-
searches have been done, while no reports are available on in-vivo re-
search. Several researchers pointed out that the nanotechnological ad-
vancement would be a modernizing aspect in the field of animal health
and veterinary medicine (Benelli and Lukehart, 2017; Benelli et al.,
2017b). Various studies documented that the metal nanoparticles
(copper, zinc, silver, nickel, and titanium dioxide ones) synthesized by
chemical and biological methods showed broad spectrum of action
against parasites and vectors of medical and veterinary importance.
Besides, chemically synthesized nanoparticles can be highly toxic to
non-target animals due to the presence of hazardous chemicals and
related side-effects. On the other hand, green synthesized nanoparticles
using plant extracts are easy to prepare, eco-friendly, cost-effective and
promising in the control of cattle tick, R. (B.) microplus. Nanoparticles
may provide a novel route for effective drug formulations to control R.
(B.) microplus. However, the mechanisms of action of the nanoparticle
action in R. (B.) microplus still need to be investigated. The current
review would attract researchers to explore deeply the use of medicinal
plants and green synthesized nanoparticles for the effective control of
veterinary ectoparasites, including ticks.
Acknowledgements
The author Mrs. B.Banumathi gratefully acknowledge the Rajiv
Gandhi National Fellowship (F1-17.1/RGNF-2012-13-SC-TAM-23853)
by UGC, New Delhi.
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