Toxicity of silver nanoparticles in fish: a critical review

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May 18, 2015 - and as a broad spectrum antimicrobial agent (Kim et al., 2007; Kim et .... are coated with different organic compounds in the synthesis process ...
J. Bio. & Env. Sci. 2015 Journal of Biodiversity and Environmental Sciences (JBES) ISSN: 2220-6663 (Print) 2222-3045 (Online) Vol. 6, No. 5, p. 211-227, 2015 http://www.innspub.net REVIEW PAPER

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Toxicity of silver nanoparticles in fish: a critical review Muhammad Saleem Khan1, Farhat Jabeen1*, Naureen Aziz Qureshi2, Muhammad Saleem Asghar1, Muhammad Shakeel1 and Aasma Noureen 1

Department of Zoology, GC University Faisalabad, Pakistan

2

GC Women University Faisalabad, Pakistan Article published on May 18, 2015

Key words: Silver, Nanoparticles, Uses, Toxicity, Fish model.

Abstract The variable spectrum of applications largely depends upon silver physicochemical and biological properties which changes as the particles are decreased to nano-scale. This unique behavior is responsible for the larger use of silver in consumer product and industry. Since little information is available about toxicity to the organisms practically in the aquatic environment, the predication of possible environmental hazards and remedy are the hot topics of current research studies. Researchers are drawing more and more data from appropriate model organisms. Fish being aquatic organism is badly affected by Ag-NPs, so concern of potential risk to aquatic organism increases. The toxicity endpoints include growth and reproduction impairment, mortality and biochemical changes in both adult fish and embryos. Being a healthy food for human, the researchers try to know how Ag-NPs can affect the fish and its body when sizes decrease to nano-scale. Therefore, fish is extensively studied model in the toxicological studies. It examined some of these studies which address the adverse effects of Ag-NPs on biological systems of different fish group predicting the dose dependent toxicity. The organisms more acutely sensitive have lower LC50 values. All the studies also indicated that silver ions released from Ag-NPs surface contributes to toxicity. Therefore, it is suggested that emphasis should be placed on upcoming investigations for the evaluation of environmental impact of nano-silver in both in vitro and in vivo studies. The effect of long term exposure and bioaccumulation of silver through food web should be unmasked and discussed in detail. *Corresponding

Author: Dr Farhat Jabeen  [email protected]

211 | Khan et al.

J. Bio. & Env. Sci. 2015 Introduction

including; size, surface area, surface chemistry and

The commercial applications of the nanomaterial

chemical composition (coatings and purity). The

research are maximum in the present era. It is

other factors like water and lipid solubility, vapor

estimated

pressure and aggregation

that

approximately

60,000

tons

of

nanomaterial is produced annually (Jovanovic et al.,

or

coagulation

state

(Wijnhoven et al., 2009).

2011) with 1628 nano based products in 30 countries (Woodrow Wilson Database, 2015). Among the nano

In the aquatic environment, Ag-NPs most likely enter

industry, silver nanoparticles is the most rapidly

the ecosystems produce a physiological response in

growing class with 320 tons of production per year

many animals, altering their fitness and population

(Nowack et al., 2011). Its importance is due to unique

densities (Luoma and Rainbow, 2008). On the other

properties and consumers demands. About 30% of all

hand, the detailed studies on the effect of these

the currently registered nanoproducts are claiming to

particles

contain

environment

the

nano-silver

(Project

on

emerging

on

the

target

have

just

organisms begun.

and

Numbers

their of

nanotechnologies, 2013). It is estimated that 383

toxicological studies have been performed but it

nanoproducts are available in the market (Woodrow

showed huge variations due to lack of proper particles

Wilson Database, 2015).

characterization (Gliga et al., 2014). The researchers focus on toxicity of Ag-NPs in aquatic environment

The extensive use of Ag nanoproducts might increase

including fish in the recent studies (Asharani et al.,

the

aquatic

2008; Yeo and Kang 2008; Bar-Ilan et al., 2009;

environment (Benn and Westerhoff, 2008; Taju et al.,

Chae et al., 2009; Choi et al., 2009; Griffitt et al.,

2014). It may be released into water and air through

2009; Bilberg et al., 2010; Powers et al., 2010; Wu et

different sources including weathering of rocks,

al., 2010). Toxicity induced by Ag-NPs to vertebrate

processing of ores, cement manufacturing and

cell line include generation of the reactive oxygen

burning of fossil fuel. Rain is responsible to release

species (Hussain et al., 2005; Schrand et al., 2008),

the silver in the ground and water reservoirs

apoptosis (Braydich-Stolle et al., 2005; Park et al.,

(Wijnhoven et al., 2009). About 68% of nano silver

2007), reduced mitochondrial function (Braydich-

load will be increased in the waste water due to

Stolle et al., 2005; Hussain et al., 2005; Schrand et

biocidal products from 2010 to 2015 (Blaser et al,

al., 2008), increase lipid peroxidation (Arora et al.,

2008). In the aquatic environment, it exits in four

2008) and depletion of the oxidative stress markers

discharge

Ag+2

of

and

these

Ag+3)

particles

into

(Ag,

Ag+,

oxidation states. But Ag and

(Hussain et al., 2005; Arora et al., 2008). Further a

Ag+

exist more commonly (Smith and Carson, 1997).

study by Larese et al. (2009) demonstrated that Ag-

Metallic silver is insoluble whereas salts (AgCl,

NPs can pass through stratum corneum and the outer

AgNO3) are soluble in water (WHO, 2002). Silver

layer of epidermis and even blood-brain barriers

nanomaterial is found in the form of colloidal

causing damage to human skin, liver, lungs and

particles in the aquatic medium.

olfactory blabs (Braydich-Stolle et al., 2005; Hussain et al., 2005; Arora et al. 2008; Sung et al., 2008). So

In spite of existence in the aquatic environment,

the current review will present the toxicity caused by

limited information regarding the toxicity of Ag-NPs

Ag-NPs on some groups of fish.

is available (Wijnhoven et al., 2009). Depending upon the existing literature, it can be hypothesized

Silver uses

that Ag-NPs are more toxic than other forms because

Silver is among basic elements that formed our

of it’s more readily absorbance than metallic silver

planet. Its size ranges 5-50 nm in many commercial

(Drake and Hazelwood, 2005). The fate and behavior

products so refers as nanosilver (Panyala et al.,

of silver nanomaterial is influenced by many factors

2008). It has a long history of use. Ancient Egypt,

212 | Khan et al.

J. Bio. & Env. Sci. 2015 Rome, Italy and Greece were aware about the use of

current time. The silver containing biocidal products

silver (Reidy et al., 2013). They use silver for the

has reached to 110 to 230 tons in the European

preparation of storage vessels that keep the water

market and significant portion is consists of Ag-NPs

fresh (Russell and Hugo 1994). It was used in the

(Blaser et al., 2008).

form of colloidal silver more than 150 years ago and first time registered as biocidal material in 1954 (Nowack et al., 2011). In the present time, it is mostly used in the fields of chemistry, material science and physics (Syrvatka et al., 2014). It is used worldwide in photography, batteries as coatings of solar energy absorption, water treatment filters (Li et al., 2008), washing machines (Jung et al., 2007), fabrics (Perelshtein et al., 2008), Heat sink, sensors (Schrand et al., 2008), catalysts (Kumar et al., 2008), superconductors, cloud seeding, shampoo, food packing, Electroplating, kitchen utensils, and odor resistant textiles (Sondi and Sondi, 2004; Cohen et

Fig. 1. Uses of silver in different sectors (SOURCE: World Silver Survey 2014, The Silver institute, 2014).

al., 2007; Yon and Lead, 2008). Furthermore silver is also combined with other substance to develop

The demand of silver use and production increases every year. It is because of silver used in industrial,

combined functions.

medical and photography. More attention is devoted towards silver due to its medical importance. It has been used in the fields of biotechnology, medicine, environmental technology and as a broad spectrum antimicrobial agent (Kim et al., 2007; Kim et al., 2013). Table 1 provides the comprehensive medical uses of naonosilver in the

The humans, animals and microorganisms are exposed to nanosilver through three major products. These products are food, medical and consumer’s products. Some common medical uses of Ag-NPs are provided in the table-1.

Table 1. Some common uses of Ag-NPs in the medical fields. Medical applications of silver A.

Treatment and repair

1.

Treatment of ulcerative colitis and acne (Bhol and Schechter, 2007)

2.

Treatment of dermatitis (Bhol et al., 2004)

3.

Allergy prophylaxis (Gulbranson et al., 2000; Silver, 2003)

4.

Inhibition of HIV-1 replication (Elechiguerra et al., 2005; Sun et al., 2005)

5.

Bone cement additive (Alt et al., 2004)

6.

Orthopedic stockings (Pohle et al., 2007)

7.

Rheumatoid arthritis-associated leg ulcers (Coelho et al., 2004)

8.

Coating of implant for joint replacement (Chen et al., 2006)

9.

Coating of catheter for cerebrospinal fluid drainage (Bayston et al., 2007)

10.

Coating of surgical mesh for pelvic reconstruction (Cohen et al., 2007)

11.

Coating of intramedullary nail for long bone fractures (Alt et al., 2006)

12.

In the form of silver proteinate for treatment of conjunctivitis in newborn babies (NCCAM, 2012)

13.

In the form of lunar caustic for treatment of corns and warts (NCCAM, 2012)

213 | Khan et al.

J. Bio. & Env. Sci. 2015 Medical applications of silver 14.

Anti-inflammatory medicine (Kirsner et al., 2001)

15.

Modulate cytokines in wound healing (Tian et al., 2007)

16.

Treatment of burns (Tredget et al.,1998)

17.

Silver diamine fluoride to reduce tooth decay (Rosenblatt et al., 2009; Deery, 2009)

18.

Silver acetate antismoking agent (Lancaster Stead, 2012)

B.

Laboratory diagnosis

1.

Detection of viral strain (SERS and silver nanorods) (Zhao et al., 2006)

2.

Dendrimer nanocomposite for cell labeling (Lesniak et al., 2005)

3.

Ag pyramids enhance bio-detection (Walt, 2005)

4.

Sensitive diagnosis of myocardial infarction (Aslan and Geddes, 2006)

5.

Fluorescence-based RNA sensing (Aslan et al., 2006)

6.

Molecular imaging of cancer cells (Tai et al., 2007)

7.

Protein biosensor any protein or any antibody (Ananth et al., 2011)

8.

Clinical diagnosis of myocardial infraction (Aslan and Geddes, 2006)

9.

Genosensors silver (I) and hydroquinone (He et al., 2009)

C.

Antiseptic uses

1.

Antimicrobial agent against infectious organisms (Yves and Philippe, 2012)

2.

Hydrogel for wound dressing (silver-containing hydrocolloid) (Yu et al., 2007)

3.

Antifungal uses (Wright et al., 1999)

4.

Effective against yeast isolated from bovine mastitis (Kim et al., 2007)

D.

Medical utensils

1.

Coating of driveline for ventricular assist devices (Drake and Hazelwood, 2005)

2.

Coating of endotracheal tube ventilatory support (Bouadma et al., 2012)

3.

Coating of hospital textile (e.g., surgical gowns and face mask) (Lee et al., 2003)

4.

Remote laser light-induced opening of microcapsules Skirtach et al., (2006)

5.

Coating of breathing mask patent (Drake and Hazelwood, 2005)

6.

Needles, catheters, dental amalgams (Drake and Hazelwood, 2005)

7.

Surgical instruments production (Chen and Schluesener, 2008)

8.

Coating of contact lens (Weisbarth et al., 2007)

9.

Drug carrier in the medical products (Chen et al., 2015)

Causes of toxicity

the nano-sized particles show variations of optical,

According to the Thomson Reuters, the number of

electrical and magnetic properties from large particles

papers on the toxicological aspects of Ag-NPs has

of the same compounds (Dowling et al., 2009).

been increased since 1990. Currently more than 3500

Further the toxicity may also affects due to particles

research articles are published on this theme

size (Nowack and Bucheli, 2007; Carlson et al., 2008;

annually. These research articles suggest that the

Inoue et al., 2010). However, the relationship

toxicity of Ag-NPs depends upon many factors such as

between the biological effects and particle size of Ag-

shape, size, surface area, chemical composition and

NPs is still unclear (Ivask et al., 2014). One proposed

surface charges (Hedayati et al., 2012). In most of the

argument is that the smaller size of particles might

studies, it is observed that physical and chemical

allow the Ag-NPs to enter an organism more readily

properties change when we decrease the particle size

than larger particles (Hedayati et al., 2012; Ivask et

to nonoscale (Hedayati et al., 2012). This concluded

al., 2014). To prove this, Lvask et al. (2014) used four

214 | Khan et al.

J. Bio. & Env. Sci. 2015 different sizes of Ag-NPs (10, 20, 60, and 80 nm) on

gills are the primary site for Ag-NPs entrance in the

different organisms. The analysis showed that 10nm

fish body and histological alterations occur very soon

particles were more toxic than all the types. Ag-NPs

(Hawkins et al., 2015). The possible effects of Ag-NPs

are coated with different organic compounds in the

in different groups of fish are discussed in details.

synthesis process which can change fate, toxicity and stability of the particles in the aqueous and biological

Zebra fish (Danio rerio)

mediums. Several organic coated particles may

Zebra fish is extensively studied model in the Ag-NPs

damage cell membrane directly, interfare in DNA

toxicological studies (Asharani et al., 2008; Kanan et

replication and ATP synthesis, cause alteration in the

al., 2011). The toxicity indicators may include, drop in

expression of genes and produce reactive oxygen

heart rate, hatching delay and higher mortality rate

species (Sherma et al., 2014).

(Asharani et al., 2008). The LC50 value is 250 mg L-1 in case of embryo (Choi et al., 2010). Bar-llan et al.

Ag-NPs

enter

organism’s

oral

(2009) calculated the LC50 values of 3nm to 100nm of

absorption, inhalation, through damage skin (ATSDR,

Ag-NPs. The calculated values were 93.31 µM for 3nm

1990; Drake and Hazelwood, 2005) even through

particle size and 137.26 µM for 100 nm. The higher

barrier of retina (Soderstjerna et al., 2014) in adult

value of LC50 for lager particles suggest that the

and diffusion or endocytosis through the skin of

toxicity increases as the particle size decreases. In

embryos (Asharani et al., 2008). Colloidal silver

some studies free Ag+ also demonstrated the almost

nanoparticles

in

same cytotoxicity as Ag-NPs with almost same LC50

organism s body through ingestion from food

values in zebra fish model (Kim et al., 2009). The Ag-

containing silver preservatives, water and children s

NPs also accumulated in the different organs like

toys. Inhalation of the dust or fumes having silver

intestine, gills, blood, liver and brain upon exposing

occurs in the industrial and jewelry processing (Drake

fish

and Hazelwood, 2005). It also enters in the body

concentration of accumulated Ag in the liver tissues

through damage skin from the application of silver

was found 0.29 and 2.4ng/mg liver when treated with

containing burn creams (Wan et al., 1991) or through

30 and 120mgL-1 (Choi et al., 2010). The accumulated

cosmetics and textiles (Jones et al., 2010). It can also

Ag-NPs cause number of cellular alterations in the

enter through female genital tract as most of the

liver. These alterations are haptic cell cords, apoptotic

female use various hygienic products containing Ag-

changes, condensation of chromatin and pyknosis in

NPs (West and Halas, 2003; Chen and Schluesener,

adult (Gonzalez et al., 2006) and circulatory and

2008; Schrand et al., 2008). Other routes may

morphological abnormalities in embryo (Asharani et

include

al., 2008; Bar-Ilan et al., 2009). 2 to 4 mgL-1

and

through

silver

body

through

compounds

acupuncture

enter

needles,

dental

to

particles

Absorption of soluble silver compound is greater than

erythrocytes acetylcholinestrase activity (Katuli et al.,

insoluble or metallic silver in this way causing adverse

2014). The Ag-NPs treatment also causes oxidative

health effects (Drake and, Hazelwood 2005). Is has

damage in the hepatic cells. The DNA damage

been reported that after the administration Ag-NPs

includes double strand breaks cause lesions in cells

accumulate

(Rothkamm and Lobrich, 2003).

organs

and

cause

in

decrease

The

Na(+)/K(+)ATPase

activity

causes

2008).

of jewelry with body (Catsakis and Sulica, 1978).

some

days

al.,

exposure

the

14

et

amalgams (Drake and Hazelwood, 2005) and contact

in

for

(Handy

the

gills

the and

hepatotoxicity or renal toxicity after administration (Sung et al., 2009; Kim et al., 2010).

Toxicity to silver carp (Hypophthalmicthys molitrix) Hedayati et al. (2012a) suggested Ag-NPs are very

Fish being aquatic organisms is more venerable to

toxic to the silver carp than the metallic silver. The

xenobiotic exposure containing the silver waste. Fish

recorded LC50 value was 0.34 ppm in case of nanocid

215 | Khan et al.

J. Bio. & Env. Sci. 2015 (Hedayati et al., 2012a) and 66.4 ppm in case of

of 100 µgL-1 of Ag-NPs for a period of 48 h. But after

nanosil (Jahanbakhsi et al., 2012). The mortality also

the 96 h the lipid peroxidation levels in the gills were

increases as the time of exposure and concentration

declined at the same concentration. This is due to the

increases. There was 100% mortality seen in case of

gills endogenous antioxidant system mitigating the

1ppm and 96 hours of exposure (Hedayati et al.,

free radical generation (Diehl, 2000). Taju et al.

2012). In different studies difference in toxicity was

(2014) also found lipid peroxidation level, decrease in

also seen due to change in the size time, age and

level of antioxidant enzymatic level due to Ag-NPs

condition of test organisms (Rathore and Khangarot,

explore.

2002). Shalui et al. (2013) found 0.810 mg L-1 LC50 value for 24h explore and 0.64, 0.383, 0.202 mg L-1

Rohu (Labeo rohita)

for 48, 72 and 96h respectively. The Ag-NPs also

Chemically synthesized Ag-NPs show dose dependent

decrease the RBC, hemoglobin and hematocrit level

toxicity in the Labeo rohita. 500 mg kg-1 causes 100%

in the silver carp (Shalui et al., 2013).

mortality and 50% mortality was observed at 100 mg kg-1 in the studies of Rajkumar et al. (2015). The Ag-

Common Carp (Cyprinus carpio)

NPs

creates

stressful

The results of the comparative toxicities of Ag-NPs

alteration in the WBC, RBC and total protein level in

and Ag ions suggested that Ag-NPs are slightly more

the serum. Acid phosphate (ACP) and alkaline

toxic than Ag ions (Hedayati et al., 2012b). Ag-NPs

phosphate (ALP) level increases in the Ag-NPs treated

alter the metabolic enzymes in the organs like gills,

tissues. Orally administrated Ag-NPs also cause the

kidney, brain and liver (Reddy et al., 2013). The liver

reduction of GST (glutathione-S-transferase), SOD

was found most susceptible to change in Ag-NPs

(superoxide

concentration among all the examined tissues (Lee et

(Rajkumar et al., 2015).

dismutase)

condition

and

which

catalase

causes

activities

al., 2012). Jung et al. (2014) found mean concentration of 5.61 mg kg-1 in the liver when exposed to 0.06±0.12

mgL-1

for 7 days. The other organs were

found to have concentration of 3.32 mg

Exposure

of

nanosilver

causes

impairment

of

in gills,

tolerance to hypoxia in crucian carp. It affects gills

2.93 mg kg-1 in gastrointestinal tract, 0.48 mg kg-1 in

and causes reduction in diffusion of oxygen through

the skeletal muscle 0.48 mg kg-1 in skeletal muscle,

gills epithelium leading to hypoxia (Bilberg et al.,

0.14 mg

kg-1

in brain and 0.02 mg

kg-1

kg-1

Crucian carp (Perca fluviatilis)

in blood. The

2010). The exposure of 45mgL-1 also suppresses

localized Ag-NPs badly reduce the activities of the

olfactory responses. It hyperpolarized the olfactory

metabolic enzymes (SOD, CAT and GST) in brain and

epithelium membrane interfere the odor detection

other tissues (Lee et al., 2012). Silver salts (AgNO3),

mechanism. The free Ag ions release from the surface

Nanocid and Nanosil are mostly used in the

of Ag-NPs form complex with receptors and prevent

toxicological studies of Ag-NPs in the case of the

the odor to combine with olfactory receptors (Klaprat

juvenile common carp (Hedayati et al., 2012b). The

et al., 1992).

recorded values of LC50 for 96 hours exposure are 0.49±0.90 ppm (Nanocid), 73.8±0.38 (Nanosil) and

Rainbow trout (Oncorhynchus mykiss)

0.33± 0.3 ppm (AgNO3) (Hedayati et al., 2012b).

In different studies, the sized effect of Ag-NPs on rainbow trout has been studied. Scown et al. (2010)

Thala (Catla catla)

for example, treated the rainbow trout with 10 nm, 35

Little work has been done for Ag-NPs toxicity in the

nm and 600 to 1600 nm through water medium for

case of catla catla. Reddy et al. (2013) found a

ten days. The uptake level was found very low. 10nm

significant change in the lipid peroxidation level in

Ag-NPs were found highest among all the other size

the gills when fish was exposed to

1/5th

concentration

and concentrated more in the gills than liver and

216 | Khan et al.

J. Bio. & Env. Sci. 2015 kidney. Fish liver also showed significant decrease in

al., 2013). Glucose level was also increases (Webb and

weight (p< 0.05). In hepatic parenchyma, local

Wood, 1998). These changes were dose-dependent

congestion was decrease in size when exposed to Ag-

(Johari et al., 2013). Ag-NPs increase the lipid

NPs (Monfared et al., 2013). The Ag-NPs coated with

peroxidation where Ag+ increase the DNA damage

PVP

(Massarsky et al., 2014) and inhibits the Na(+),K(+)-

(Polyvinylpyrrolidone)

and

citrate

also

accumulate in the gills transport through gill

ATPase activity (Schultz et al., 2013).

epithelium and cause cytotoxicity (Farkas et al., 2010).

Medaka (Oryzias latipes) Kim et al. (2013) demonstrated aged (old) Ag-NPs are

The calculated LC50 values were 0.25 and 28.25 mgL-1

more toxic than fresh one as aged particles release

for colloidal and suspended powder respectively in

more Ag ions. They performed toxicity assay in

alevins for 96 hours exposure and 2.16

for

medaka (Japanese rice fish) and found lower LC50

colloidal in juveniles. No mortality was seen in case of

value (1.44mgL-1) in case of aged Ag-NPs than (3.53

powder Ag-NPs (Kalbassi et al., 2013). Johari et al.

mgL-1) fresh Ag-NPs. Wu et al. (2010) found 100%

(2013) also calculated the LC50 values for the colloidal

mortality at 2.0 mgL-1 in 48h toxicity test and no

particles. Their calculated values were 0.25 mgL-1,

mortality at 0.5 mgL-1.

0.71 and 2.16

mgL-1

mgL-1

for eleutheroembryo, larvae and

juveniles, respectively. According to the European

In

embryo

development

retardation,

reduce

Union Directive (EC, 1999) number 67/548/EEC

pigmentation and reduction of width of optic tectum

dated 27 June 1967 and European legislation (EC,

were seen at 400 µgL-1 concentration (Wu et al.,

2008), any substance that has less than 1 mgL-1 LC50

2010). Other malfunctions include spinal card

value for 96 hours must be classified as very toxic. It

abnormalities, heart deformation, edema and defects

must have long term adverse effect on the aquatic

in eyes development at different concentrations (Wu

organisms. So according to the findings of Johari et

et al., 2010). 0.8 mgL-1 concentration causes heart

al. (2013), the colloidal Ag-NPs should be classified

beat retardation, where lower concentration also

very toxic for eleutheroembryo and larvae and toxic to

causes dose dependent decrease in hatching rate and

juveniles in rainbow trout.

body length posing same toxicity to embryo and adult (Cho et al., 2013). Histological analysis found that Ag-

The serum level of total protein decreases by

NPs can also penetrate through chorion of egg

elevation of Ag-NPs concentration (Monfared et al.,

(embryo) and skin membrane and then distributed to

2013). Reduction of potassium and chloride ions and

the other tissues (Lee et al., 2014). The principal sites

increase of cortisol and cholinsterse present in blood

of uptake are gills in Japanese medaka (Kwok et al.,

plasma were seen when exposed to Ag-NPs (Johari et

2012).

Table 3. Values of 96h LC50 of different forms of Nano-silver in different fish groups. Sr#

Form of Ag-NPs

Fish Group

LC50 values

Reference

1

Nanocid

Silver carp

0.34ppm

Hedayati et al., 2012a

2

Nanocil

Silver carp

66.4ppm

Jahanbakhsi et al., 2012

3

Nanpcid (61nm)

Silver carp

0.202

4

Nanocid

Common carp (juvenile)

0.49±0.90ppm

Hedayati et al., 2012b

5

Nanosil

Common carp (juvenile)

73.8±0.38ppm

Hedayati et al., 2012b

6

AgNO3

Common carp (juvenile)

0.33±0.3ppm

Hedayati et al., 2012b

7

Ag-NPs (50-100)

Rohu

100 mg kg-1

Rajkumar et al., 2015

8

Ag-NPs (powder)

Zebra fish (embryo)

217 | Khan et al.

250

mgL-1

mgL-1

Shaluei et al., 2013

Choi et al., 2010

J. Bio. & Env. Sci. 2015 Sr#

Form of Ag-NPs

Fish Group

LC50 values

Reference Bar-llan et al., 2009

9

Ag-NPs (3nm)

Zebra fish (juvenile)

93.11µM

10

Ag-NPs (100nm)

Zebra fish (juvenile)

137.26 µM

Bar-llan et al., 2009

11

Colloidal

Zebra fish (adult)

7.07 mg

12

Colloidal

Rainbow trout (eleutheroembryo)

0.25 mgL-1

Johari et al., 2013

13

Colloidal

Rainbow trout (larvae)

2.16 mgL-1

Johari et al., 2013

14

Colloidal

15

Rainbow trout (alevins)

Colloidal

16

Rainbow trout (juvenile)

Colloidal

Rainbow trout (juvenile)

AgL-1

Griffitt et al., 2008

0.25

mgL-1

Kalbassi et al., 2013

0.25

mgL-1

Kalbassi et al., 2013

2.16

mgL-1

Johari et al., 2013

17

Suspended powder

Rainbow trout (alevins)

28.25

18

Ag-NPs (aged)

Medaka (adult)

1.44 mgL-1

Kim et al., 2013

19

Ag-NPs (fresh)

Medaka (adult)

3.53 mgL-1

Kim et al., 2013

20

Ag-NPs (stirred)

Fathead minnow(embryo

10.6 mgL-1

Laban et al., 2010

mgL-1

Laban et al., 2010

21

Ag (sonicated)

Fathead minnow

1.36

Fathead minnow (Pimephales promelas) The

treatment

of

silver

mgL-1

Kalbassi et al., 2013

Variation in the toxicity due to size, form and

nanoproducts

and

condition of target model, the researchers are

nanoparticles cause pericardial, yolk sac edema and

encouraged to further investigate the different aspects

hemorrhages to head region in the Fathead minnow’ s

of Ag-NPs toxicity.

embryo (Laban et al., 2010) and gills alterations. Disturbance in the blood circulation is the prevalent alteration in the gills (Hawkins et al., 2015). 1.3 µg

References

L-1

Alt V, Bechert T, Steinrucke P, Wagener M,

of AgNO3 increases the total goblet cells in the

Seidel P, Dingeldein E, Domann E, Schnettler

mucous. Both Ag-NO3 and Ag-NPs decreases the

R. 2004. An in vitro assessment of the antibacterial

Na+/K+-ATPase

properties and cytotoxicity of nanoparticulate silver

immune-reactivity

in

the

gills

(Hawkins et al., 2015). The calculated LC50 values were

9.4mgL-1,

10.6mgL-1

for nanoAmor and Ag-NPs

in case of stirred particles and

1.25mgL-1,

bone cement. Biomaterials

25(18), 4383-4391.

doi:10.1016/j.biomaterials.2003.10.078

1.36mgL-1

for sonicated particles. Ag-NPs were less toxic than

Alt

V, Wagener

M,

Salz D, Bechert

T,

silver nitrate in fathead minnow (Laban et al., 2010).

Steinrucke P, Schnettler R. 2006. Plasma polymer high-porosity silver composite coating for

Conclusion Silver

nanoparticles

infection prophylaxis in intramedullary nailing. attract

much

attention

of

researchers not because of its wide applications in the

Practice of Intramedullary Locked Nails pp. 297-303. DOI: 10.1007/3-540-32345-7_30

fields of medicine, catalysts, biotechnology, nano biotechnology, electronics, optics, textile engineering

Ananth AN, Daniel SCG, Sironmani TA,

and water treatment but due to toxicity. It can cause

Umapathi. 2011. PVA and BSA stabilized silver

damage to brain cells, liver cells and even to stem

nanoparticles

cells in the human body. So instead of using human in

resonance probes for protein detection Colloids and

toxicological studies, it is preferable to use animal

Surfaces

models.

doi:10.1016/ j.colsurfb.2011.02.012

Among all the models, fish is most

B:

based

surface–enhanced

Biointerfaces

85(2),

plasmon 138-144.

dominantly use model in the toxicological studies. From the published literature, it is concluded that Ag-

Arora S, Jain J, Rajwade JM, Paknikar KM.

NPs poses toxicity to all the life stages of fish model.

2009. Interactions of silver nanoparticles with

218 | Khan et al.

J. Bio. & Env. Sci. 2015 primary mouse fibroblasts and liver cells. Toxicology

model. Clinical Experimental Dermatology 29(3),

and

282-287. DOI: 10.1111/j.1365-2230.2004.01515.x.

Applied

Pharmacology

236(3),

310–318.

doi:10.1016/j.taap.2009.02.020. Bhol

KC,

Schechter

PJ.

2007.

Effects

of

Asharani PV, Wu YL, Gong Z, Valiyaveetti S.

nanocrystalline silver (NPI 32101) in a rat model of

2008. Toxicity of silver nanoparticles in zebrafish

ulcerative colitis. Digestive Diseases and Sciences 52,

models. Nanotechnology 19(25), 55-102.

2732-2742. DOI: 10.1007/s10620-006-9738-4.

-doi:10.1088/0957-4484/19/25/ 255102 Bilberg K, Doving KB, Beedholm K, Baatrup Aslan K, Geddes CD. 2006. Microwave-accelerated

E. 2011. Silver nanoparticles disrupt olfaction in

and metalenhanced fluorescence myoglobin detection

Crucian carp (Carassius carassius) and Eurasian

on silvered surfaces: Potential application to myo-

perch (Perca fluviatilis). Aquatic Toxicology 104,

cardial infarction diagnosis. Plasmonics 1(1), 53-59.

145–152. doi: 10.1016/j.aquatox.2011. 04.010.

DOI: 10.1007/s11468-006-9006-7 Blaser

SA,

Scheringer

M,

MacLeod

M,

Aslan K, Huang J, Wilson GM, Geddes CD.

Hungerbühler K. 2008. Estimation of cumulative

2006.

RNA

aquatic exposure and risk due to silver: Contribution

sensing. Journal of American Chemical Society 128,

of nano-functionalized plastics and textiles. Science of

4206-4207.

Total Environment 390 (2-3), 396–409.

Metalenhanced

fluorescence-based

DOI: 10.1016/ j.scitotenv. 2007.10.010. ATSDR (Agency for Toxic Substances and Disease Registry). 1990. Toxicological profile for

Bouadma L, Wolff M, Lucet JC. 2012. Ventilator-

Silver.

international

associated pneumonia and its prevention. Current

corporation, under Contract 205-88-0608). U.S.

opinion in infectious diseases 25 (4), 395–404. doi:

public Health Service. ATSDR/TP-90-24.

10.1097/ QCO.0b013e328355a835.

Bar-Ilan O, Albrecht RM, Fako VE, Furgeson

Braydich-Stolle L, Hussain S, Schlager JJ,

DY. 2009. Toxicity assessments of multisized gold

Hofmann MC. 2005. In vitro cytotoxicity of

and silver nanoparticles in Zebrafish embryos. Small

nanoparticles in mammalian germline stem cells.

5(16), 1897-910. DOI: 10.1002/smll.200801716.

Toxicological Science 88(2), 412–419.

Prepared

by

Clement

doi: 10.1093/toxsci/kfi340. Bayston R, Ashraf W, Fisher L. 2007. Prevention of infection in neurosurgery: Role of ‘antimicrobial’

Carlson C, Hussain S, Schrand A, Braydich-

catheters. Journal of Hospital Infection 65(2), 39-42.

Stolle L, Hess K, Jones R, Schlager J. 2008.

DOI: http://dx.doi.org/10.1016/S0195-6701(07)60013-9.

Unique cellular interaction of silver nanoparticles: Size-dependent generation of reactive oxygen species.

Benn TM, Westerhoff P. 2008. Nanoparticle silver

The Journal of Physical Chemistry 112(43), 13608-

released into water from commercially available sock

13619. DOI: 10.1021/jp712087m.

fabrics. Environmental Science and Technology 42(11), 4133–4139. DOI: 10.1021/es7032718.

Catsakis LH, Sulica VI. 1978. Allergy to silver amalgams. Oral Surgery Medicine Oral Pathology

Bhol KC, Alroy J, Schechter PJ. 2004. Anti-

Oral Radiology 46(3), 371-375.

inflammatory effect of topical nanocrystalline silver

DOI: http://dx.doi.org/ 10.1016/0030-4220(78)90402-4.

cream on allergic contact dermatitis in a guinea pig

219 | Khan et al.

J. Bio. & Env. Sci. 2015 Chae YJ, Pham CH, Lee J, Bae E, Yi J, Gu MB.

Cohen MS, Stern JM, Vanni AJ, Kelley RS,

2009. Evaluation of the toxic impact of silver

Baumgart E, Field D, Libertino JA, Summer-

nanoparticles on Japanese medaka (Oryzias latipes).

hayes IC. 2007. In vitro analysis of a nanocrystalline

Aquatic Toxicology 94(4), 320–327.

silver-coated

doi:10.1016/j.aquatox.2009.07.019

(Larchmt.)

surgical 8(3),

mesh. 397-403.

Surgical

Infections

DOI: 10.1089/sur.

2006.032 Chen LQ, Fang L, Ling J, Ding CZ, Kang B, Huang CZ. 2015. Nanotoxicity of silver nanoparticles to red

Deery C. 2009. Silver lining for caries cloud?

blood cells: size dependent adsorption, uptake, and

Evidence-Based Dentistry 10(3), 68. doi:10.1038/ sj.

hemolytic activity. Chemical Research in Toxicology

ebd.6400661

28(3), 501-9. doi: 10.1021/tx 500479m. Diehl AM. 2000. Cytokine regulation of liver injury Chen W, Liu Y, Courtney HS, Bettenga M,

and repair. Immunological Reviews 174(1), 160-171.

Agrawal CM, Bumgardner JD, Ong JL. 2006. In

DOI: 10.1034/j.1600-0528.2002.017411.x

vitro anti-bacterial and biological properties of magnetron co-sputtered silver-containing hydroxyapatite

Dowling A, Clift R, Grobert N, Hutton D,

coating. Biomaterials 27(32), 5512-5517.

Oliver R, Neill O, Pethica J, Inoue KI, Takano

doi:10.1016/j.biomaterials.2006.07.003.

H, Yanagisawa R, Koike E, Shimada A. 2009. Size

effects

of

latex

nanomaterials

on

lung

Chen X, Schluesener HJ. 2008. Nanosilver: A

inflammation in mice. Toxicology and Applied

nanoproduct in medical application. Toxicological

Pharmacology 234(1), 68-76.

Letters 176(1), 1–12.

doi:10.1016/j.taap.2008.09.012

doi:10.1016/j.toxlet.2007.10.004. Drake PL, Hazelwood KJ. 2005. Exposure-related Cho JG, Kim KT, Ryu TK, Lee JW, Kim JE,

health effects of silver and silver compounds: A

Kim J, Lee BC, Jo EH, Yoon J, Eom IC, Choi

review. The Annals of Occupational Hygiene 49(7),

K, Kim P. 2013. Stepwise Embryonic Toxicity of

575-585. doi: 10.1093/annhyg/mei019

Silver Nanoparticles on Oryzias latipes. BioMed Research International, Article ID 494671, 7 pages.

EC. 1999. Annex VI of Directive 1999/45/EC to

http:// dx. doi.org/10.1155/2013/494671.

consolidated

version

of

directive

67/548/EEC.

General classification and labeling requirements for Choi JE, Kim S, Ahn JH, Youn P, Kang JS,

dangerous substances and preparations.

Park K, Yi J, Ryu D. 2009. Induction of oxidative

ec.europa.eu/environment/archives/dansub/pdfs/an

stress and apoptosis by silver nanoparticles in the

nex6_ en.pdf

liver of adult Zebrafish. Aquatic Toxicology 100(2), 151-159. doi: 10.1016/j.aquatox. 2009.12.012.

EC. 2008. Regulation (EC) No 1272/2008 of the European Parliament and Council of 16 December

Coelho S, Amarelo M, Ryan S, Reddy M,

2008 on classification, labeling and packaging of

Sibbald RG. 2004. Rheumatoid arthritis-associated

substances and mixtures, Official Journal of the

inflammatory leg ulcers: A new treatment for

European Union, 31.12.2008.

recalcitrant wounds. International Wound Journal

http://eur-lex.europa.eu/legal-content/en/TXT/?uri

1(1), 81-84. DOI: 10.1111/j.1742-481x.2004. 0002.x.

=CELEX:32008R1272.

220 | Khan et al.

J. Bio. & Env. Sci. 2015 Elechiguerra JL, Morones JR, Camacho A,

Handy RH, Owen R, Valsami-Jones E. 2008.

Holt K, Kouri JB, Ramirez JT, Yacaman MJ.

The ecotoxicology of nanoparticles and nanomaterials:

2005. Interaction of silver nanoparticles with HIV-1.

current status, knowledge gaps, challenges, and

Journal of Nanotechnology 16, 23-46.

future needs. Ecotoxicology 17(5), 315-325. doi:

DOI: 10.1186/1477-3155-3-6

10.1007/s10646-008-0206-0.

Farkas J, Christian P, Gallego JA, Urrea N,

Hawkins AD, Thornton C, Kennedy AJ, Bu

Roos, Hassellöv M, Tollefsen KE, Thomas KV.

K, Cizdziel J, Jones BW, Steevens JA, Willett

2010. Effects of silver and gold nanoparticles on

KL. 2015. Gill histopathologies following exposure to

rainbow trout (Oncorhynchus mykiss) hepatocytes.

nanosilver or silver nitrate. Journal of Toxicology and

Aquatic Toxicology 96(1), 44-52. doi:10.1016/j.

Environmental Health A 78(5), 301-15.

aquatox.2009.09. 016

doi: 10.1080/15287394.2014.971386.

Gliga AR, Skoglund S, Wallinder IO, Fadeel B,

He J, Lin L, Liu H, Zhang P, Lee M, Sankey OF,

Karlsson HL. 2014. Size-dependent cytotoxicity of

Lindsay SM. 2009. A hydrogen-bounded electron-

silver nanoparticles in human lung cells: the role of

tunneling circuit reads the base composition of

cellular uptake, agglomeration and Ag release.

unmodified DNA. Nanotechnology 20(7), 075102.

Particle and Fibre Toxicology 11(11), 1-17 doi:

doi: 10.1088/0957-4484/20/7/075102

10.1186/1743-8977-11-11 Hedayati A, Kolangi H, Jahanbakhshi A, Gonzalez

P,

Baudrimont

M,

Boudou

A,

Shaluei F. 2012a. Evaluation of Silver nanoparticles

Bourdineaud JP. 2006. Comparative effects of

Ecotoxicity in Silver carp (Hypophthalmicthys molitrix)

direct cadmium contamination on gene expression in

and Goldfish (Carassius auratus). Bulgarian Journal

gills, liver, skeletal muscles and brain of the zebrafish

of Veterinary Medicine 15(3), 172−177. Article id:

(Danio rerio). Biometals 19(3), 225–235. DOI:

80158939

10.1007/s10534-005-5670-x. Hedayati A, Shaluei F, Jahanbakhshi A. 2012b. Griffitt RJ, Hyndman K, Denslow ND, Barber

Comparison of Toxicity Responses by Water Exposure to

DS. 2009. Comparison of molecular and histological

Silver Nanoparticles and Silver Salt in Common Carp

changes in zebrafish gills exposed to metallic

(Cyprinus carpio). Global Veterinaria 8(2), 179-184.

nanoparticles. Toxicological Science 107(2), 404-415. doi: 10.1093/toxsci/kfn256

Hussain SM, Hess KL, Gearhart JM, Geiss KT, Schlager JJ. 2005. In vitro toxicity of nanoparticles

Griffitt RJ, Luo J, Gao J, Bonzongo JC, Barber

in BRL 3A rat liver cells. Toxicology in Vitro 19(7),

DS. 2008. Effects of particle composition and species

975–983. doi:10.1016/j.tiv.2005.06.034.

on toxicity of metallic nanomaterials in aquatic organisms. Environmental Toxicology and Chemistry

Inoue Y, Uota M, Torikai T, Watari T, Noda I,

27(9), 1972–1978. DOI: 10.1897/08-002.1

Hotokebuchi T. 2010. Antibacterial properties of nanostructured silver titanate thin films formed on a

Gulbranson SH, Hud JA, Hansen RC. 2000.

titanium plate. Journal of Biomedical Materials

Argyria following the use of dietary supplements

Research Part A 92A(3), 1171-1180.

containing colloidal silver protein. Cutis 66, 373-376.

doi: 10.1002/jbm.a.32456.

221 | Khan et al.

J. Bio. & Env. Sci. 2015 Ivask A, Kurvet I, Kasemets K, Blinova I,

Kalbassi MR, Johari SA, Soltani M, Yu LJ.

Aruoja V. 2014. Size-Dependent Toxicity of Silver

2013. Particle Size and Agglomeration Affect the

Nanoparticles to Bacteria, Yeast, Algae, Crustaceans

Toxicity Levels of Silver Nanoparticle Types in

and Mammalian Cells In Vitro. PLoS ONE 9(7),

Aquatic Environment. ECOPERSIA 1(3), 273-290.

e102108. doi:10.1371/journal.pone.0102108 Kannan R, Jerley A, Ranjani M, Prakash V. Jahanbakhshi A, Shaluei F, Hedayati A. 2012b.

2011. Antimicrobial silver nanoparticle induces organ

Detection of Silver Nanoparticles (Nanosil®) LC50 in

deformities in the developing Zebra fish (Danio rerio)

Silver Carp (Hypophthalmichthys molitrix) and

embryos.

Goldfish (Carassius auratus). World Journal of

Engineering 4, 248-254.

Zoology

doi: 10.4236/ jbise.2011.44034.

7(2),

126-130.

DOI:

10.5829/idosi.

Journal

of

Biomedical

Science

and

wjz.2012.7.2.62129. Katuli KK, Massarsky A Hadadi A, Pourmehran Jang MH, Kim WK, Lee SK, Henry TB, Park

Z. 2014. Silver nanoparticles inhibit the gill Na⁺/K⁺-

JW.

and

ATPase and erythrocyte AChE activities and induce

depuration of total silver in common carp (Cyprinus

the stress response in adult zebrafish (Danio rerio).

carpio) after aqueous exposure to silver nanoparticles.

Ecotoxicology and Environmental Safety 106, 173-80

Environmental Science and Technology 48(19),

doi: 10.1016/j.ecoenv.2014.04.001.

2014.

Uptake,

tissue

distribution,

11568-74. doi: 10.1021/es5022813. Kim J, Kuk E, Yu K, Park S, Lee H, Kim S, Johari SA, Kalbassi MR, Soltani M, Yu IJ.

Park Y, Hwang C, Kim Y, Lee Y, Jeong D, Cho

2013.

silver

M. 2007. Antimicrobial effects of silver nanoparticles.

nanoparticles in various life stages of rainbow trout

Nanomedicine: Nanotechnology, Biology and Medicine

(Oncorhynchus mykiss). Iranian Journal of Fisheries

3(1), 95-101. doi:10.1016/j.nano. 2006.12.001

Toxicity

comparison

of

colloidal

Science 12(1), 76 -95. Kim J, Lee J, Kwon S, Jeong S. 2009. Jones CM, Hoek EM. 2010. A review of the

Preparation of biodegradable polymer/silver nano-

antibacterial effects of silver nanomaterials and

particles composite and its antibacterial efficacy.

potential implications for human health and the

Journal of Nanoscience and Nanotechnology 9(2),

environment. Journal of Nanoparticle Research 12,

1098–1102. doi:10.1166/jnn.2009.C096

1531–1551. Kim JY, Kim KT, Lee BG, Lim BJ, Kim SD. Jovanovic B, Anastasova L, Rowe EW, Zhang Y,

2013. Developmental toxicity of Japanese medaka

Clapp AR, Palic D. 2011. Effects of nanosized titanium

embryos by silver nanoparticles and released ions in

dioxide on innate immune system of fathead minnow

the presence of humic acid. Ecotoxicology and

(Pimephales promelas Rafinesque, 1820). Ecotoxicology

Environmental Safety 92(1), 57-63. doi: 10.1016/j.

and

ecoenv.2013.02.004.

Environmental

Safety

74(7),

675-683.

DOI: 10.1016/j.ecoenv.2010.10.017 Kirsner RS, Orstead H, Wright JB. 2001. Matrix Jung WK, Kim SH, Koo HC, Shin S, Kim JM,

metalloproteinases in normal and impaired wound

Park YK, Hwang SY, Yang H, Park YH. 2007.

healing: a potential role for nanocrystalline silver.

Antifungal

Wounds 13(3), 5-12.

activity

of

the

silver

ion

against

contaminated fabric. Mycoses 50(4), 265–269. DOI: 10.1111/j.1439-0507.2007.01372.x

222 | Khan et al.

J. Bio. & Env. Sci. 2015 Klaprat

DA,

Evans

RE,

Hara

TJ.

1992.

Lee B, Duong C, Cho J, Lee J, Kim K, Seo Y,

Environmental contaminants and chemoreception in

Kim P, Choi K, Yoon J. 2012. Toxicity of Citrate-

fishes. In Fish Chemoreception Fish and Fisheries

Capped Silver Nanoparticles in Common Carp

Series 6, 321-341. DOI: 10.1007/978-94-011-2332-

(Cyprinus carpio). Journal of Biomedicine and

7_15.

Biotechnology 2012, 262670. doi: 10.1155/2012/262670.

Kumar

PS,

Sivakumar

R,

Anandan

S,

Madhavan J, Maruthamuthu P, Ashokkumar

Lee BC, Kim J, Cho JG, Lee JW, Duong CN, Bae

M. 2008. Photocatalytic degradation of Acid Red 88

E, Yi J, Eom IC, Choi K, Kim P, Yoon J. 2014.

using Au TiO2 nanoparticles in aqueous solutions.

Effects of ionization on the toxicity of silver

Water Research 42(19), 4878–4884. doi:10.1016/j.

nanoparticles to Japanese medaka (Oryzias latipes)

watres.2008.09.027

embryos. Toxic/Hazardous Substances and Environmental Engineering 49(3), 287-93.

Kwok KW, Auffan M, Badireddy AR, Nelson

doi: 10.1080/10934529.2014. 846614.

CM, Wiesner MR, Chilkoti A, Liu J, Marinakos SM, Hinton DE. 2012. Uptake of silver nanoparticles

Lee HJ, Yeo SY, Jeong SH. 2003. Antibacterial

and toxicity to early life stages of Japanese medaka

effect of nanosized silver colloidal solution on textile

(Oryzias latipes): effect of coating materials. Aquatic

fabrics. Journal of Materials Science 38(10), 2199-

Toxicology 120(121), 59-66.

2204. DOI: 10.1023/A: 1023736416361.

doi: 10.1016/j.aquatox.2012.04.012. Lesniak W, Bielinska AU, Sun K, Janczak KW, Laban G, Nies LF, Turco RF, Bickham JW,

Shi X, Baker JR, Balogh LP, 2005. Silver

Sepulveda

/dendrimer

nanoparticles

MS.

2010.

The

on

fathead

effects

silver

nanocomposites

as

biomarkers:

(Pimephales

Fabrication, characterization, in vitro toxicity, and

promelas) embryos. Ecotoxicology 19(1), 185-195.

intracellular detection. Nano Letters 5(11), 2123-

DOI: 10.1007/s10646-009-0404-4

2130. DOI: 10.1021/nl051077u.

Lancaster T, Stead LF. 2012. Silver acetate for

Li Q, Mahendra S, Lyon, DY, Brunet L, Liga

smoking

MV, Li D, Alvarez PJJ. 2008. Antimicrobial

cessation. The

minnow

of

Cochrane

Collaboration.

(Online) 9, CD000191.

nanomaterials for water disinfection and microbial

DOI: 10.1002/14651858.CD000191.

control: potential applications and implications. Water Research 42 (18), 4591–4602.

Lansdown

A.

2006.

Silver

in

health

care:

doi: 10.1016/j.watres.2008.08.015.

antimicrobial effects and safety in use. Current Problems in Dermatology 33, 17-34.

Luoma

SN,

Rainbow

PS.

2008.

Metal

DOI: 10.1159/000093928.

contamination in aquatic environments: science and lateral management. Journal of Fish Biology 75,

Larese FF, Dagostin F, Crosera M, Adami G,

1911–1912.

Renzi N, Bovenzi M, Maina G. 2009. Human

DOI: 10.1111/j.1095-8649.2009.02440_4.x.

skin penetration of silver nanoparticles through intact and damaged skin. Toxicology 255(1-2), 33–37.

Massarsky

A, Abraham

R, Nguyen

KC,

doi:10.1016/j.tox.2008.09.025

Rippstein P, Tayabali AF, Trudeau VL, Moon TW. 2014. Nanosilver cytotoxicity in rainbow trout (Oncorhynchus mykiss) erythrocytes and hepatocytes.

223 | Khan et al.

J. Bio. & Env. Sci. 2015 Comparative Biochemistry and Physiology Part C:

Perelshtein I, Applerot G, Perkas N, Guibert

Pharmacology, Toxicology and Endocrinology; 159,

G, Mikhailov S, Gedanken A. 2008. Sonochemical

0-21. doi: 10.1016/j. cbpc.2013.09.008.

coating of silver nanoparticles on textile fabrics (nylon, polyester and cotton) and their antibacterial

Moaddab

S,

Ahari

Motallebi

A,

H,

Anvar

Shahbazzadeh

D,

activity. Nanotechnology 19, 245705.

Rahman-Nya

J,

doi:10.1088/0957-4484/19/24/245705

A,

Shokrgozar MA. 2011. Toxicity study of nanosilver (Nanocid®)

on

osteoblast

cancer

cell

Line.

International Nano Letters 1(1), 11-16.

Pohle D, Damm C, Neuhof J, Rosch A, Munstedt H. 2007. Antimicrobial properties of orthopaedic textiles after in-situ deposition of silver

Monfared AL, Soltani S. 2013. Effects of silver

nanoparticles. Polymers & Polymer Composites

nanoparticles administration on the liver of rainbow

15(5), 357-363. Accession# 28655926.

trout

(Oncorhynchus

biochemical

studies.

mykiss):

histological

European

Journal

and of

Exponential Biology 3(2), 285-289.

Powers CM, Yen J, Linney EA, Seidler FJ, Slotkin TA. 2010. Silver exposure in developing Zebrafish (Danio rerio): Persistent effects on larval

NCCAM. 2012. Colloidal Silver Products. National

behavior

and

survival.

Center for Complementary and Alternative Medicine.

Teratology 32(3), 391-397.

February 2012.

doi:10.1016/j.ntt.2010.01.009

Neurotoxicology

and

https://nccih.nih.gov/health/providers/digest/topsu pplements

Project on emerging nanotechnologies. 2013. Available online: http://www. nanotechproject. org/

Nowack

B,

Bucheli

behavior

and

effects

TD. of

2007. Occurrence,

nanoparticles

in

inventories/consumer/ (accessed on 3 June 2013).

the

environment. Environmental Pollution 150(1), 5-22.

Rajkumar KS, Kanipandian N, Thirumurugan

doi:10.1016/j. envpol.2007.06.006

R. 2015. Toxicity assessment on haemotology, biochemical and histopathological alterations of silver

Nowack B, Krug HF, Height M. 2011. 120 years of

nanoparticles-exposed freshwater fish Labeo rohita.

nanosilver history: implications for policy makers.

Applied Nanoscience DOI 10.1007/s13204-015-0417-7.

Environmental Science and Technology 45(4), 1177– 1183. DOI: 10.1021/es103316q.

Rathore RS, Khangarot BS. 2002. Effect of temperature on the sensitivity of sludge worm Tubifex

Pal S, Tak YK, Song JM. 2007. Does the

tubifex (Muller) to selected heavy metals. Ecotoxi-

Antibacterial Activity of Silver Nanoparticles Depend

cology and Environmental Safety 53(1), 27–36.

on the Shape of the Nanoparticle? A Study of the

doi:10.1006/eesa.2001.2100

Gram-Negative Bacterium Escherichia coli. Applied and Environmental Microbiology 73(6), 1712-1720.

Reddy TK, Reddy SJ, Prasad TNVKV.

2013.

doi:10.1128/AEM.02218-06.

Effect of Silver Nanoparticles on Energy Metabolism in Selected Tissues of Aeromonas Hydrophila

Panyala NR, Pena-Mendez EM, Havel J. 2008.

Infected Indian Major Carp, Catla Catla. IOSR

Silver or silver nanoparticles: a hazardous threat to

Journal of Pharmacy 3(1), 49-55.

the environment and human health? Journal of Applied Biomedicine 6, 117–129.

Reidy B, Haase A, Luch A, Dawson KA, Lynch A. 2013. Mechanisms of Silver Nanoparticle Release,

224 | Khan et al.

J. Bio. & Env. Sci. 2015 Transformation and Toxicity: A Critical Review of

Schultz AG, Ong KJ, MacCormack T, Ma G,

Current Knowledge and Recommendations for Future

Veinot JG, Goss GG. 2012. Silver nanoparticles

Studies and Applications.

inhibit sodium uptake in juvenile rainbow trout

Materials 6, 2295-2350.

doi: 10.3390/ma6062295.

(Oncorhynchus mykiss). Environmental Science and Technology 46(18), 10295-301.

Rivero P, Urrutia A, Goicoechea J, Zamarreno

doi: 10.1021/es3017717.

C, Arregui F, Matias I. 2011. An antibacterial coating based on a polymer/solgel hybrid matrix

Scown TM, Santos EM, Johnston BD, Gaiser

loaded with silver nanoparticles. Nanoscale Research

B, Baalousha M, Mitov S, Lead JR, Stone V,

Letters 6(305). doi:10.1186/1556-276X-6-305.

Fernandes TF, Jepson M, Van Aerle R, Tyler CR. 2010. Effects of aqueous exposure to silver

Rosenblatt A, Stamford TCM, Niederman R.

nanoparticles of different sizes in rainbow trout.

2009. Silver Diamine Fluoride: A Caries Silver-

Toxicological

Fluoride Bullet. Journal of Dental Research 88 (2),

10.1093/toxsci/ kfq076.

Science

115(2),

521–534.

doi:

116–125. DOI: 10.1177/0022034508329406 Shaluei F, Hedayati A, Jahanbakhshi A, Kolangi Rothkamm K, Lobrich M. 2003. Evidence for a

H, Fotovat M. 2013. Effect of subacute exposure

lack of DNA double-strand break repair in human

to silver nanoparticle on some hematological and

cells exposed to very low X-ray doses. Proceding of

plasma biochemical indices insilver carp (Hypoph-

National and Academy of Sciences U.S.A. 100, 5057-

thalmichthys

5062. doi: 10.1073/pnas.0830918100

Toxicology 32(12), 1270-7.

molitrix).

Human&

Experimental

doi: 10.1177/0960327113485258. Russell AD, Hugo WB. 1994. Antimicrobial activity and action of silver. Progress in Medicinal

Sharma VK, Siskova KM, Zboril R, Gardea-

Chemistry 31, 351-370.

Torresdey nanoparticles

Safaepour M, Shahverdi A, Shahverdi Khorramizadeh M,

Gohari

JL. in

2014.

Organic-coated

biological

and

silver

environmental

H,

conditions: fate, stability and toxicity. Advances in

A. 2009. Green

Colloid and Interface Science 204, 15-34. doi:

synthesis of small silver nanoparticles using geraniol and

10.1016/j. cis.2013.12.002.

its cytotoxicity against Fibro sarcoma-Wehi 164. Avicenna Journal of Medical Biotechnology 1(2), 111-

Silver Institute, 2014. World Silver Survey 2014.

115.

https://www.silverinstitute.org/ site/supply- demand/

Samuel U, Guggenbichler J. 2004. Prevention of

Silver S. 2003. Bacterial silver resistance: Molecular

catheter-related infections: the potential of a new

biology and uses and misuses of silver compounds.

nano-silver

FEMS

impregnated

catheter.

International

Microbiology

Reviews

27,

341-353.

Journal of Antimicrob Agents 23, 75-78.

DOI: http://dx. doi.org/10.1016/S0168-6445(03) 000

DOI: 10.1016/j.ijantimicag.2003.12.004

47-0

Schrand AM, Braydich-Stolle LK, Schlager JJ,

Skirtach AG, Antipov AA, Shchukin DG,

Dai L, Hussain SM. 2008. Can silver nanoparticles

Sukhorukov GB. 2004. Remote activation of

be useful as potential biological labels? Nanotech-

capsules containing Ag nanoparticles and IR dye by

nology 19(2), 235104.

laser

doi: 10.1088/0957-4484/19/23/235104

DOI: 10.1021/la048873k

225 | Khan et al.

light.

Langmuir

20(17),

6988-6992.

J. Bio. & Env. Sci. 2015 Smith I, Carson B. 1977. Trace metals in the

of silver nanoparticles using heart and gill cell lines of

environment. Trace Metals in the Environment 469

Catla catla and gill cell line of Labeo rohita.

pp. ISBN: 978-0-444-50352-7

Comparative Biochemistry and Physiology Part C: Pharmacology, Toxicology and Endocrinology 161,

Soderstjerna E, Bauer P, Cedervall T, Abdshill H,

Johansson

F.

2014.

Silver

and

41-52. doi: 10.1016/j.cbpc.2014.01.007.

Gold

Nanoparticles Exposure to In Vitro Cultured Retina

Tian J, Wong KK, Ho CM, Lok CN, Yu WY, Che

Studies on Nanoparticle Internalization, Apoptosis,

CM, Chiu JF, Tam PK. 2007. Topical delivery of

Oxidative Stress, Glial- and Microglial Activity. PLoS

silver nanoparticles promotes wound healing. Chem

ONE 9(8), e105359.

Med Chem 2(1), 129-136.

doi:10.1371/journal.pone.0105359.

DOI: 10.1002/cmdc.200600171

Sondi I, Sondi BS. 2004. Silver nanoparticles as

Tredget EE, Shankowsky HA, Groeneveld A,

antimicrobial agent: a case study on E. coli as a model

Burrell R. 1998. A matched-pair randomized study

for Gram-negative bacteria. Journal of Colloid and

evaluating the efficacy and safety of Acticoat silver-

Interface Science 275(1), 177–182.

coated dressing for the treatment of burn wounds.

doi:10.1016/j.jcis.2004.02.012

Journal of Burn Care & Rehabilitation 19, 531-537. DOI: 10.1097/00004630-199811000-00013.

Sung J, Ji J, Yoon J, Kim D, Song M, Jeong J, Han B, Han J, Chung Y, Kim J, Kim T, Chang

Walt DR. 2005. Miniature analytical methods for

H, Lee E, Lee J, Yu I. 2008. Lung function changes

medical diagnostics. Science 308(5719), 217-219.

in Sprague-Dawley rats after prolonged inhalation

DOI: 10.1126/science.1108161

exposure

to

silver

nanoparticles.

Inhalation

Toxicology 20(6), 567–574. doi:10.1080/089583707

Wan AT, Conyers RA, Coombs CJ, Masterton

01874671.

JP. 1991. Determination of silver in blood, urine and tissues of volunteers and burn patients. Clinical

Syrvatka V, Rozgoni I, Slyvchuk Y, Milovanova

Chemistry 37(10), 1683-1687.

G, Hevkan I, Matyukha I. 2014. Effects of Silver nanoparticles in Solution and liposomal form on

Webb NA, Wood CM. 1998. Physiological analysis

some blood Parameters in female rabbits during

of the stress response associated with acute silver

fertilization

nitrate

and

early

embryonic

development.

exposure

in

freshwater

rainbow

trout

Journal of microbiology, biotechnology and food

(Oncorhynchus mykiss). Environmental Toxicology

sciences 3 (4), 274-278. ICID: 1092144

and Chemistry 17(4), 579–588. DOI: 10. 1002/etc.5620170408

Tai SP, Wu Y, Shieh BD, Chen LJ, Lin KJ, Yu CH, Chu SW, Chang CH, Shi XY, Wen YC, Lin

Weisbarth

RE,

Gabriel

MM,

George

M,

KH, Liu TM, Sun CK. 2007. Molecular imaging of

Rappon J, Miller M, Chalmers R, Winterton L.

cancer cells using plasmonresonant- enhanced third-

2007. Creating antimicrobial surfaces and materials

harmonic-generation in silver nanoparticles. Advance

for contact lenses and lens cases. Eye and Contact

Materials 19, 4520-4523.

Lens 33, 426-429.

DOI: 10.1002/adma.200602213. West JL, Halas NJ. 2003. Engineered nanomaterials Taju G, Majeed AS, Nambi KS, Sahul Hameed

for biophotonics applications: Improving sensing,

AS.

imaging,

2014.

In

vitro

assay

for

the

toxicity

226 | Khan et al.

and

therapeutics.

Annual

Review

of

J. Bio. & Env. Sci. 2015 Biomedical Engineering 5, 285–292. doi: 10.1146/

Wu Y, Zhoua Q, Li H, Liua W, Wanga T,

annurev.bioeng.5.011303.120723.

Jianga G. 2010. Effects of silver nanoparticles on the development

Wijnhoven Herberts

SWP, CA,

Peijnenburg

Hagens

WI,

WJGM,

Oomen

AG,

Heugens EHW, Roszek B, Bisschops J, Gösens

and histopathology biomarkers of

Japanese medaka (Oryzias latipes) using the partiallife test. Aquatic Toxicology 100(2), 160-167. doi: 10.1016/j.aquatox.2009.11.014

I, Van de Meent D, Dekkers S, De Jong WH, Van Zijverden M, Sips AJAM, Geertsma RE.

Yeo M, Kang M. 2008. Effects of nanometer sized

2009. Nano-silver - A review of available data and

silver materials on biological toxicity during Zebra

knowledge gaps in human and environmental risk

fish embryogenesis. Bulletin of the Korean Chemical

assessment. Nanotoxicology 3(2), 109-138.

Society 29(6), 1179-1184.

doi:10.1080/17435390902725914. Yon

JN,

Lead

JR.

2008.

Manufactured

Woodrow Wilson Database. 2015. Nanotechnology

nanoparticles: An overview of their chemistry,

consumer product inventory

interactions

http://www.nanotechproject.org/cpi/about/analysis/.

implications. Science of Total Environment 400(1-

and

potential

environmental

3), 396–414. doi:10.1016/j.scitotenv.2008.06.042. World Health Organization. 2002. Silver and silver compounds: Environmental aspects. (Concise

Yu H, Xu X, Chen X, Lu T, Zhang P, Jing X.

international chemical assessment document; 44). 1.

2007. Preparation and antibacterial effects of PVA-

Silver _ adverse effects 2. Water pollutants, Chemical

PVP

3. Risk assessment 4. Environmental exposure I.

Journal of Applied Polymer Science 103, 125-133.

International Programme on Chemical Safety II.

DOI: 10.1002/app.24835

hydrogels

containing

silver

nanoparticles.

Series ISBN 92 4 153044 8 (NLM Classification: QV 297). ISSN 1020 6167.

Yves MJ,

http://www.who.int/ipcs/publications/cicad /en/cicad

antimicrobial: Facts and gaps in knowledge. Critical

44.Pdf

Reviews

in

Philippe

H.

2012. Silver as an

Microbiology 39(4),

373-83.

doi:

10.3109/1040841X.2012. 713323. Wright JB, Lam K, Hansen D, Burrell RE. 1999. Efficacy of topical silver against fungal burn

Zhao Y, Shanmukh S, Liu Y, Jones L, Dluhy

wound pathogens. American Journal of Infection

RA, Tripp RA. 2006. Silver nanorod arrays can

Control

distinguish virus strains. Nanotech SPIE Newsroom

27(4),

6553(99)70055-6

344-350.

doi:10.1016/S0196-

DOI: 10.1117/2. 1200610.0438.

227 | Khan et al.