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The Toxicity of Nanoparticles to Algae

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J Nanopart Res (2018) 20:92
https://doi.org/10.1007/s11051-018-4196-4

REVIEW

A historical review and bibliometric analysis of nanoparticles

toxicity on algae
Yulin Tang & Huaijia Xin & Feng Yang & Xin Long

Received: 29 August 2017 / Accepted: 19 March 2018

# Springer Science+Business Media B.V., part of Springer Nature 2018

Abstract With growing concerns about the toxicity of
nanoparticles (NPs) to aquatic systems, a number of
toxicity studies about different NPs to algae have been
reported. Based on Science Citation Index Expanded
(SCI-Expanded), a bibliometric and network analysis
of research outputs was carried out to analyze the global
research situation and trends of NP toxicity to algae
from 2006 to 2017. The results indicate that annual
publication outputs increased rapidly over the past de-
cade. China was the most high-publishing country ac-
counting for 19.8% of the total publications, followed
by the USA (17.1%). The USA and most European
countries like England, Norway, Denmark, and Switzer-
land played major roles in the collaboration network.
Swiss Federal Institute of Aquatic Science and Technol-
ogy contributed the most publications (19) and total
citations (1708). Furthermore, Ag NPs and TiO2 NPs
and Pseudokirchneriella subcapitata and Desmodesmus
subspicatus were the most common studied NPs and
algae, respectively. In addition, the overview of current
Y. Tang (*) : H. Xin : X. Long
State Key Laboratory of Pollution Control and Resource Reuse,
College of Environmental Science and Engineering, Tongji
University, Shanghai 200092, People’s Republic of China
e-mail: tangyulin@tongji.edu.cn
Y. Tang
Shanghai Institute of Pollution Control and Ecological Security,
Shanghai 200092, People’s Republic of China
F. Yang
Tongji University Library, Tongji University, Shanghai 200092,
People’s Republic of China
research and the research tendency about the toxicity of
single NPs and interactions between NPs and environ-
mental contaminants to algae were analyzed and sum-
marized with a timeline. The historical review about NP
toxicity on algae and a bibliometric analysis of the
publications give a global view on future research and
identify potential opportunities and challenges.
Keywords Nanoparticles . Toxicity . Algae . SCI-
Expanded . Bibliometric
Introduction
Nanoparticles (NPs) with sizes smaller than 100 nm in at
least one dimension have received lots of attention
owing to their rapidly growing application (Navarro
et al. 2008a). Since large amounts of NPs may reach
the environment, the environmental impact, especially
the potential aquatic environmental effects, should be
considered. Respective studies were performed on the
toxic impact of NPs on a variety of aquatic organisms
including decomposers (bacteria), primary producers
(algae), and secondary consumers (micro-invertebrates
and fish) (Blaise et al. 2008; Bouldin et al. 2008; Handy
et al. 2008; Navarro et al. 2008a).
Algae are the primary producers at the base of aquatic
food chain and are widely used for the characterization
of chemicals in the (Organization for Economic Co-
operation and Development, OECD) algal growth inhi-
bition test (Petit et al. 2010). Algae are one of the typical
model organisms used for the toxicity examination of
92 Page 2 of 17
NPs (Ji et al. 2011). Diverse physicochemical factors
and morphology, including the size, shape, and aspect
ratio of NPs, can influence the effects of NPs on algae. A
number of toxicity studies reported the effect of different
NPs on algae, including TiO2 (Hund-Rinke and Simon
2006), ZnO (Franklin et al. 2007), Ag (Navarro
et al. 2008b), C60 (Baun et al. 2008), and quantum
dots (Bouldin et al. 2008). Many kinds of fresh-
water algae and marine algae were used for NP
toxicity studies on algae (Sadiq et al. 2011; Zhang
et al. 2008). However, there has been no study to
systematically summarize the findings of NP tox-
icity on algae. To better understand NP toxicity on
the aquatic environment, especially algae, a quan-
titative analysis that provides usable and relevant
information is required for scientific guidelines.
Bibliometric analysis is a useful tool to provide a
potential guide for current and future studies and has
been used in many recent studies globally (Fu et al.
2013). Bibliometric reviews utilize quantitative anal-
ysis and statistics to describe distribution patterns of
articles through a given topic, field, institution, and
country. They can provide more elaborate analyses
to indicate the development trends or future orienta-
tion of research fields (Zhang et al. 2017a). Science
Citation Index Expanded (SCI-Expanded) is the
most important database for an overview of scien-
tific production (Zheng et al. 2017). Analysis of the
top-cited articles in a field provides a historical
perspective in the scientific advancement of re-
search, evolution, and areas of intensive research
activities. To date, only a few bibliometric studies
have been conducted to evaluate the risk of engi-
neering NPs (Ostrowski et al. 2009; Wang et al.
2014). To our best knowledge, no previous studies
have focused on the worldwide research status of
NP toxicity on algae.
In this paper, the toxicity of NPs to algae was
quantitatively and qualitatively analyzed to provide
a better understanding of the global research situa-
tion and trends in this field. The annual publication
outputs, mainstream journals, leading countries and
institutions, funding agencies, and highly cited arti-
cles in NP toxicity on algae were analyzed. Further,
research tendencies and hotspots including the over-
all use of NPs and algae, the historical review and
future trends, were also considered. The findings
will be valuable for research landscape mapping
and technology forecasting.
J Nanopart Res (2018) 20:92
Methodology
A historical review contributes to the summary of a
specific subject and the identification of some research
questions. There are three stages including defining
proper search keywords, retrieving the literature, and
conducting the analysis that are used to complete struc-
tured literature reviews (Rowley and Slack 2004). Sim-
ilarly, we performed a three-step methodology for data
collection and comprehensive assessment.
Data sources and retrieval strategies
The data for NP toxicity on algae was obtained on 8
June 2017. It is based on the SCI-Expanded analysis of
the Web of Science, which is the most efficient database
for backtracking citations. In the whole article, the sta-
tistics in 2017 are only for reference and does not have
statistical significance. A comprehensive search was
conducted under the subject terms Balga*,^ Btoxic*,^
Becotoxic*,^ Bcytotoxic*,^ Bbiotoxic*,^ Bnano,^
Bnanoparticle*,^ and Bnanomaterial*.^
Refinement of the search results
In order to improve the accuracy of bibliometric analysis
and provide a reliable historical review, further refine-
ment of the search results was conducted to eliminate
irrelevant articles (Fahimnia et al. 2015). Titles and
abstracts of the original articles were screened carefully,
and those articles irrelevant to the subject were
discarded. After that, the records including all essential
information such as paper title, abstract, keywords, au-
thors’ names, affiliations, and references were compiled
for further analysis.
Data analysis
Data extraction and analysis were performed using
Microsoft Excel 2016 (Microsoft Corporation, USA)
and InCites (Thomson Reuters, USA). In addition,
VOSviewer (Leiden University, Netherlands), a soft-
ware tool for constructing and visualizing bibliometric
networks (van Eck and Waltman 2010), was used to
construct a knowledge map of co-authorship relations
with nations. Impact factors (IFs) of each journal were
obtained according to the Journal Citation Reports
(JCR) published in 14 June 2017. The h-index intro-
duced in 2005 indicates the h values of Np papers that
J Nanopart Res (2018) 20:92 Page 3 of 17 92

have at least h citations each, while the other (Np − h) Table 1 Characteristics by year of publication outputs from 2006
to 2017
papers were cited less than h times (Hirsch 2005). This
is a comprehensive measurement of quantity and Year TP AU AU/TP PG PG/TP NR NR/TP
impact.
In analysis, several criteria were used for consistency 2006 1 2 2.00 8 8.00 30 30.00
as follows: (i) articles originating from England, Scot- 2007 2 12 6.00 19 9.50 61 30.50
land, Northern Ireland, and Wales were uniformly 2008 15 76 5.07 140 9.33 718 47.87
grouped as the UK; (ii) the Bprint^ author designated 2009 10 57 5.70 125 12.50 594 59.40
by SCI-Expanded was the same as Bcorresponding 2010 11 56 5.09 89 8.09 454 41.27
author^ that we used in this article; (iii) the addresses 2011 19 87 4.58 179 9.42 870 45.79
of authors were used to determine the cooperative rela- 2012 32 149 4.66 302 9.44 1503 46.97
tionships. The term Bsingle country or institute article^ 2013 38 192 5.05 368 9.68 2141 56.34
referred to those articles with all researchers from the 2014 45 236 5.24 512 11.38 3033 67.40
same country or institute, and the term Binternationally 2015 81 411 5.07 825 10.19 4230 52.22
collaborative article^ was assigned to those articles with 2016 79 435 5.51 792 10.03 4021 50.90
co-authors from multiple countries. 2017* 41 222 5.41 437 10.66 2624 64.00
Average 4.95 9.85 49.39

TP total articles, AU author number, AU/TP author number per

Performance of publication article, PG page count, NR cited reference count, PG/TP page
count per article, NR/TP cited reference count per article, * the data
Publication outputs for 2017 only to June, 2017

Using the Btopic^ search in the SCI-Expanded database,
the initial search resulted in a total of 515 articles. For
the purpose of this study, a further refinement was
carried out and irrelevant articles were eliminated. The
final number of articles was 374 published during an 11-
year period, between 2006 and 2017. Among these
papers, there were 345 articles, 27 reviews, and 2 meet-
ing abstracts. They were all published in English except
one Czech article. For an overview of the included
articles, the numbers and characteristics of annual arti-
cles are displayed in Table 1. Data indicates that the total
number of annual articles has increased year by year.
Although research about NP toxicity to algae is still in
an early growth and expansion period, the result shows
that a rapid growth in publications is occurring. It is
worth mentioning that after the 2007 publication of two
research articles on ZnO NPs and TiO2 NPs (Franklin
et al. 2007; Warheit et al. 2007), both of which are
highly cited, the amount of research dramatically in-
creased. Over the period from 2006 to 2016, the average
cited references increased from 30 to 50.9 with fluctua-
tion sometimes, in part due to more free online avail-
ability of scientific articles. In addition, other research
indexes of the publication output showed a rising trend
as well. For example, the number of authors in this area
exploded from 2 in 2006 to 436 in 2016 and the average
co-authors per article got a more than twofold increase
over the 11 years, demonstrating a growing interest in
the research of the NP toxicity on algae.
Subject categories and journals
In total, the publication output of NP toxicity on algae was
distributed in 26 Web of Science subject categories. A
total of 203 articles were published by Benvironmental
science,^ followed by Btoxicology^ with 107 articles.
The initial statistics showed that 112 journals con-
tributed to the publication of 374 papers. Among these
journals, 81 (72.3%) published less than 3 articles, while
10 journals contained 186 articles representing approx-
imately half of all articles published. Table 2 shows the
top 10 most productive journals. Aquatic Toxicology
was the most high-publishing journal in NP toxicity on
algae with 30 articles (8.0%), followed by Environmen-
tal Science and Technology and Science of the Total
Environment with 27 articles (7.2%) and 26 articles
(7.0%), respectively. As for h-index and citations, En-
vironmental Science and Technology was outstanding
with the highest h-index (17), citation number (2255),
and average citations per article (83.5). Environmental
Pollution and Environmental Toxicology and Chemistry
had 52.9 and 68.9 citations per article, respectively,
showing good performance in average citations per
article as well. In addition, although Aquatic Toxicology
92 Page 4 of 17 J Nanopart Res (2018) 20:92

Table 2 The top 10 most productive journals

Journals TP (%) IF2016 h-index TC TC/TP

Aquatic Toxicology 30 (8.0) 4.129 14 752 25.1

Environmental Science & Technology 27 (7.2) 6.198 17 2255 83.5
Science of the Total Environment 26 (7.0) 4.900 10 749 28.8
Nanotoxicology 20 (5.4) 6.428 9 285 14.3
Environmental Science and Pollution Research 19 (5.1) 2.741 4 322 17.0
Chemosphere 15 (4.0) 4.208 9 436 29.1
Environmental Pollution 14 (3.7) 5.099 8 741 52.9
Environmental Toxicology and Chemistry 13 (3.5) 2.951 10 896 68.9
Ecotoxicology and Environmental Safety 12 (3.2) 3.743 8 268 22.3
Plos One 10 (2.7) 2.806 8 255 25.5

TP total articles, % the percentage of articles of journals in total articles, TC total citations, TC/TP average citations per article

ranked second in h-index, it ranked sixth in average
citations per article with a number of 25.1.
Countries and institutions
Overall, a total of 56 countries have carried out research
on the toxicity of NPs to algae. The visualized relation
network of co-authorship and collaborations between
countries was made using VOSviewer and is shown in
Fig. 1. Based on the size of the circles, it is easy to
identify that China was the most high-publishing coun-
try, followed by the USA, India, Canada, Switzerland,
and France. For the red-green-blue color scheme, red
corresponds to the highest item density while blue cor-
responds to the lowest item density. It means that the
redder, the higher the number of citations per article and
the more blue, the lower the number of citations per
article. The color of China is light blue which shows the
average citations per article was no more than 30, de-
spite the highest quantity of articles. Similarly, India,
Italy, and South Korea had a poor performance in papers
cited. A noticeable difference is that Spain, Denmark,
Switzerland, and Estonia, which were not high-publish-
ing, were highly cited with more than 70 citations per
article. Furthermore, the USA had a general perfor-
mance with a yellow color. Lines connecting the circles
show the cooperative relationship between countries.
The USA and most European countries like England,
Norway, Denmark, and Switzerland had a high number
of international collaborations. On the contrary, most
Asian countries such as China, India, and Japan were
deficient in international collaborations. Table 3 lists
more research characteristics of the top 10 most
productive countries in detail. The top 10 most produc-
tive countries involved in the research of NP toxicity on
algae included two Asian countries, two American
countries, and six European countries. According to
independent articles (SP) and international collaborative
articles (CP), it is obvious that the SP of China and India
were far more than their CP. Instead, Germany and the
UK only had 5 and 3 SP, respectively, and most of their
research outputs in this field were CP. As for first-author
articles (FP) and corresponding-author articles (RP),
China, the USA, and India took the first three positions
with FP of 65, 42, and 33, respectively, and RP of 64,
46, and 33, respectively. However, Germany was the
only country whose FP and RP were fewer than half of
its total articles. Furthermore, based on h-index, the
USA was outstanding with the highest h-index of 25,
while Germany, Italy, and Spain showed only h-index of
8. Besides, other indicators of the top 10 countries like
total articles, the percentage of international collabora-
tive articles, average citations, and so on, which were in
accordance with Fig. 1, are also shown in Table 3 for
reference; thus, they were not put into details here.
Among the top 10 institutions ranked by the number
of articles (Table 4), the total articles and the h-index of
each were not obviously outstanding. However, the total
citations and the average citations per article of the
National Institute of Chemical Physics and Biophysics
(1389, 92.6), Technical University of Denmark (1006,
91.5), and Swiss Federal Institute of Aquatic Science
and Technology (1708, 89.9) went far beyond the
others. In addition, it is noticeable that both of the two
high-publishing Chinese institutions, Zhejiang Univer-
sity and Chinese Academy of Sciences, had poor
J Nanopart Res (2018) 20:92 Page 5 of 17 92

Fig. 1 Density view of co-authorship and collaborations between color scheme in the bottom right corner. A line connecting two
countries. Each circle represents a country/territory, and the size of circles illustrates the cooperative relationship between two
the circle represents the number of articles. The color in the circle countries
depends in the number of citations referring to the red-green-blue

performance in international collaboration with only 1 illustrates why China and India performed poorly in
and 2 internationally collaborative papers, respectively, international collaboration as discussed above. Further-
as did Vellore Institute of Technology in India. This more, the top 9 most prolific authors all belong to the top

Table 3 The top 10 most productive countries

Country TP (%) SP CP FP RP C% h-index TC TC/TP

China 74 (19.8) 52 22 65 64 29.7 18 1643 22.2

USA 64 (17.1) 34 30 42 46 46.9 25 3268 51.1
India 37 (9.9) 29 8 33 33 21.6 11 397 10.7
Canada 29 (7.8) 11 18 21 21 62.1 15 789 27.2
Switzerland 29 (7.8) 17 12 23 23 41.4 14 2137 73.7
France 28 (7.5) 12 16 16 17 57.1 11 562 20.1
Germany 19 (5.1) 5 14 9 9 73.7 8 1050 55.3
Italy 19 (5.1) 12 7 17 18 36.8 8 281 14.8
Spain 19 (5.1) 10 9 11 11 47.4 8 1514 79.7
United Kingdom 19 (5.1) 3 16 10 11 84.2 11 1076 56.6

TP: total articles, % the percentage of articles of countries in total articles, SP numbers of independent articles, CP numbers of internationally
collaborative articles, FP numbers of first-author articles, RP numbers of corresponding-author articles, C% the percentage of internationally
collaborative articles in the total articles of each country, TC total citations, TC/TP average citations per article
92 Page 6 of 17 J Nanopart Res (2018) 20:92

Table 4 The top 10 most productive institutions

Institutions Country TP CP h-index TC TC/TP Prolific authors

(numbers of articles)

Swiss Federal Institute of Aquatic Science Switzerland 19 9 10 1708 89.9 Sigg, Laura (13); Behra,
and Technology Renata (13)
Centre National de la Recherche Scientifique France 19 9 6 300 15.8
National Institute of Chemical Physics & Estonia 15 10 11 1389 92.6 Kahru, Anne (14); Ivask,
Biophysics Angela (8);
Aruoja, Villem (8)
Vellore Institute of Technology India 13 1 8 214 16.5 Chandrasekaran, N. (13);
Mukherjee, Amitava (13)
University of California System USA 13 6 11 435 33.5
Zhejiang University China 12 1 7 313 26.1 Lin, Daohui (9)
University of Quebec Canada 11 5 7 311 28.3
Technical University of Denmark Denmark 11 8 8 1006 91.5 Baun, Anders (8)
Ecole Polytechnique Federale de Lausanne Switzerland 11 2 7 234 21.3
Chinese Academy of Sciences China 10 2 3 55 5.5

TP total articles, CP numbers of internationally collaborative articles, TC total citations, TC/TP average citations per article

10 institutions and are shown in Table 4. Among them,
Anne Kahru was the most high-publishing author in this
field having published the first article in 2008, and a
total of 14 articles to date. Moreover, five of her articles
were highly cited papers (Aruoja et al. 2009;
Bondarenko et al. 2013; Ivask et al. 2014; Jemec et al.
2016; Kahru and Dubourguier 2010) that promoted the
development of this field. Likewise, Laura Sigg and
Renata Benate from Swiss Federal Institute of Aquatic
Science and Technology were the authors with the sec-
ond most articles contributed and 2 highly cited papers
published in 2008 (Navarro et al. 2008a; Navarro et al.
2008b). To sum up, the top 9 prolific authors were the
major contributors in respective institutions for their
publication outputs and contributed more than half of
the total articles published by their institutions.
Funding agency
Environmental Protection Agency were the trend spot-
ters funding the research of NP toxicity on algae since
2008. Next are the National Science Foundation and
Swiss National Science Foundation from the USA and
Switzerland. What is surprising is that the National
Natural Science Foundation of China started funding
this area of research in 2010, and the number of Web
of Science articles is far more than any of the other
agencies. The number of articles increased year by year
with the development of financial aid, especially in 2016
with a total of 18 articles. Starting in 2011, another three
Chinese funding agencies including National Basic Re-
search Program of China, Fundamental Research Funds
for the Central Universities, and Natural Science Foun-
dation of Zhejiang Province began to support this kind
of research making China the most high-publishing
country, which is in agreement with the contribution of
countries described above (Fig. 1).

Funding agencies play a motivational role in the devel-
opment of nanoparticle toxicity on algae. In order to
provide an overview of the impetus of funding agencies
to this field and have a better understanding of the
historical research on this topic, we analyzed the
funding agencies that were extracted from each article.
A total of 92 agencies supported this topic, and the top
10 most high-publishing funding agencies are listed in
Table 5. Both the European Union and US
Highly cited articles
Findings on highly cited articles are of particular signif-
icance because that reveals the recognition of scientific
advancement, provides interesting and valuable in-
sights, and shows a historic perspective on scientific
advancement (Baltussen and Kindler 2004; Ohba et al.
2007; Smith 2008). In all included articles, there are 23
highly cited papers including 14 articles and 9 reviews
J Nanopart Res (2018) 20:92 Page 7 of 17 92

Table 5 The top 10 most pro-

ductive funding agencies Funding agency Country Start time TP

National Natural Science Foundation of China China 2010 50

National Science Foundation (NSF) USA 2009 24
European Union (EU) EU 2008 23
Natural Sciences and Engineering Research Council of Canada Canada 2011 13
United States Environmental Protection Agency USA 2008 11
Swiss National Science Foundation Switzerland 2009 10
National Basic Research Program of China China 2011 9
Portuguese Foundation for Science and Technology Portuguese 2011 8
Fundamental Research Funds for the Central Universities China 2011 8
Natural Science Foundation of Zhejiang Province China 2011 8
TP total articles

shown in Table 6. The most productive journal was
Environmental Science and Technology contributing
three highly cited articles, two of which were the most
cited articles with 721 and 616 citations, respectively.
From the titles of those highly cited articles, the most
frequent NPs were TiO2 and Ag appearing five times,
followed by ZnO NPs (four), CuO NPs (two), nano-C-
60 (one), and graphene (one). It can be observed that
articles about the toxicity of TiO2 NPs to algae were
consistently published from 2007 to 2015 and have long
been a hot topic. Although the first highly cited article
was about the toxicity of Ag NPs to Chlamydomonas
reinhardtii published in 2008, Ag NPs appeared to be of
increasing concern in the last 5 years. As for ZnO NPs, it
was also the main hot spot while the highly cited articles
about it did not appear after 2013.
Nanoparticles and algae
With respect to NPs, the first article named
Bnanoparticles—new colloidal drug delivery system^
was published in 1978 (Marty et al. 1978). The toxicity
of NPs is not a new science appearing at the beginning
of 1980s (Fig. 2) and environmental concern of NPs
appeared later. As an indicator, a bibliometric search in
SCI-Expanded made on 7 July 7, 2017 using the term
Bnanoparticle + toxicity^ yielded 41,685 records and
Bnanoparticle + toxicity + algae^ gave 498 records. Fig-
ure 2 shows the trend in quantity of publications. The
result shows that research on the toxicity of NPs is
booming in the twenty-first century showing a geomet-
ric growth in publications. Meanwhile, the field of NP
toxicity on algae is receiving increasing attention even
though it is still in the early growth and expansion
period.
Some articles have reviewed the toxic mechanism of
various NPs to algae, while currently there are no pub-
lications about the overall research tendency of NP
toxicity on algae. In this part, research trend of the
variation of nanoparticles and algae studied between
2006 and 2017 was analyzed.
Nanoparticles
Table 7 shows the number of publications about the
top 10 most popular NPs for each year to reflect the
research trend of nanoparticles. In general, publica-
tions of the top 10 NPs showed an increasing trend
over time. TiO 2 NPs were the first NPs which
caught the attention of researchers to explore the
toxicity of NPs to algae in 2006, followed by ZnO
NPs in 2007. After that, more and more researches
about various NPs were studied rapidly. Ag NPs and
TiO2 NPs were the top 2 most popular NPs with 101
and 96 articles, respectively. Due to the bactericidal
effects of Ag NPs (Navarro et al. 2008b) and the
protection against ultraviolet ray exposure of TiO2
NPs (Manzo et al. 2015), they are the most com-
monly used NPs in numerous industries and are
added to consumer products (Maynard et al. 2006).
Therefore, they are inevitably introduced to the
aquatic environment where they exert toxic effects
(Botta et al. 2011; Huang et al. 2016). This is the
reason for increasing attention and research on the
potential toxic effects to algae. In addition, a turning
point can be observed in Table 7 where the number
of publications about Ag NPs increased sharply in
2012 while there was little research in previous
years. It was found that a major breakthrough was
made by Navarro et al. (2008b), who pointed out
 92

Table 6 The highly cited articles

Year Author Title Journal TC DT

2008 Navarro, Enrique Toxicity of silver nanoparticles to Chlamydomonas reinhardtii Environmental Science and Technology 721 Article
2007 Franklin, Natasha M. Comparative toxicity of nanoparticulate ZnO, bulk ZnO, and ZnCl2 Environmental Science and Technology 616 Article
Page 8 of 17

to a freshwater microalga (Pseudokirchneriella subcapitata): the

importance of particle solubility
2008 Navarro, Enrique Environmental behavior and ecotoxicity of engineered nanoparticles Ecotoxicology 603 Review
to algae, plants, and fungi
2009 Aruoja, Villem Toxicity of nanoparticles of CuO, ZnO and TiO2 to microalgae Science of The Total Environment 474 Article
Pseudokirchneriella subcapitata
2008 Handy, Richard D. The ecotoxicology of nanoparticles and nanomaterials: current status, Ecotoxicology 392 Article
knowledge gaps, challenges, and future needs
2008 Griffitt, Robert J. Effects of particle composition and species on toxicity of metallic Environmental Toxicology and Chemistry 387 Article
nanomaterials in aquatic organisms
2010 Kahru, Anne From ecotoxicology to nanoecotoxicology Toxicology 320 Review
2007 Warheit, David B. Development of a base set of toxicity tests using ultrafine TiO2 particles Toxicology Letters 296 Article
as a component of nanoparticle risk management
2013 Bondarenko, Olesja Toxicity of Ag, CuO, and ZnO nanoparticles to selected environmentally Archives of Toxicology 249 Review
relevant test organisms and mammalian cells in vitro: a critical review
2013 Ma, Hongbo Ecotoxicity of manufactured ZnO nanoparticles—a review Environmental Pollution 230 Review
2008 Baun, A. Toxicity and bioaccumulation of xenobiotic organic compounds in the Aquatic Toxicology 193 Article
presence of aqueous suspensions of aggregates of nano-C-60
2011 Menard, Anja Ecotoxicity of nanosized TiO2. Review of in vivo data Environmental Pollution 170 Review
2012 Handy, Richard D. Ecotoxicity test methods for engineered nanomaterials: practical experiences Environmental Toxicology and Chemistry 135 Review
and recommendations from the bench
2013 Batley, Graeme E. Fate and risks of nanomaterials in aquatic and terrestrial environments Accounts of Chemical Research 112 Review
2011 Ji, Jing Toxicity of oxide nanoparticles to the green algae Chlorella sp. Chemical Engineering Journal 100 Article
2014 Zhao, Jian Graphene in the aquatic environment: adsorption, dispersion, toxicity Environmental Science & Technology 99 Review
and transformation
2013 Clement, Laura Toxicity of TiO2 nanoparticles to cladocerans, algae, rotifers and Chemosphere 84 Article
plants—effects of size and crystalline structure
2014 von Moos, Nadia Oxidative stress induced by inorganic nanoparticles in bacteria and aquatic Nanotoxicology 83 Article
microalgae—state of the art and knowledge gaps
2014 Ivask, Angela Size-dependent toxicity of silver nanoparticles to bacteria, yeast, algae, Plos One 80 Article
crustaceans, and mammalian cells in vitro
2014 Ribeiro, Fabianne Silver nanoparticles and silver nitrate induce high toxicity to Science of The Total Environment 58 Article
Pseudokirchneriella subcapitata, Daphnia magna, and Danio rerio
2015 Bour, Agathe Environmentally relevant approaches to assess nanoparticles Journal of Hazardous Materials 37 Review
ecotoxicity: a review
J Nanopart Res (2018) 20:92

2015 Li, Fengmin Toxicity of nano-TiO2 on algae and the site of reactive oxygen Aquatic Toxicology 30 Article
species production
2016 Jemec, Anita An interlaboratory comparison of nanosilver characterization and hazard Environment International 11 Article
identification: harmonizing techniques for high quality data

TC total citations, DT document type

J Nanopart Res (2018) 20:92 Page 9 of 17 92

8000
120
7000
nanoparticle+toxicity+algae

(nanoparticle+toxicity+algae)
Numbers of publications
(nanoparticle+toxicity)
100

Numbers of publications
6000
nanoparticle+toxicity
5000 80

4000
60
3000
40
2000
20
1000

0 0
1982 1987 1992 1997 2002 2007 2012 2017
Year
Fig. 2 Numbers by year of records in SCI-Expanded. The term algae^ was searched in topic with (nanoparticle* OR
Bnanoparticle + toxicity^ was searched in topic with (nanoparti- nanomaterial*) AND (toxic* OR ecotoxic* OR cytotoxic* OR
cle* OR nanomaterial*) AND (toxic* OR ecotoxic* OR cytotox- biotoxic*) AND alga*. BAND^ means the combination of the
ic* OR biotoxic*). Likewise, the term Bnanoparticle + toxicity + respective keywords

that free Ag+ was the determinant in toxicity of Ag
NPs and caused significant interactions between NPs
and algae. Subsequently, in-depth studies on cell
morphology (Dash et al. 2012), algal photosynthesis
(Li et al. 2015), reactive oxygen species formation
and lipid peroxidation (Oukarroum et al. 2012),
intracellular accumulation (Piccapietra et al. 2012),
various environmental conditions (Das et al. 2014;
Oukarroum et al. 2014), and other research on Ag
NP toxicity on algae were conducted. As for ZnO
NPs, carbon nanotubes (CNTs) and CuO NPs with
the number of articles from 25 to 50, their
publications increased gradually year by year and
these are considered the second most popular NP
groups. Publications about quantum dots (QDs)
were intermittent and only the National Research
Council-Institute of Biophysics from Italy persisted
in working at the toxicity of QDs to algae for several
years. Graphene-family materials (GFMs) are a new
carbon material, with high production and applica-
tion (120 t/year in 2015) (Zurutuza and Marinelli
2014) resulting in discharge to the aquatic environ-
ment (Hazeem et al. 2017). Their toxicity to algae
was noticed and investigated in recent years (Du

Table 7 The top 10 most popular nanomaterials used to test the toxicity to algae

Year 2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017* TP
NPs

Ag 2 1 4 0 10 9 17 22 25 11 101
TiO2 1 1 6 3 2 6 9 12 9 20 16 11 96
ZnO 1 2 1 2 3 2 9 9 9 8 4 50
CNTs 4 2 3 3 4 1 8 5 30
CuO 1 2 1 2 4 2 4 5 4 25
CeO2 1 1 1 2 1 1 3 5 3 1 19
SiO2 3 1 2 2 2 3 4 17
QDs 2 2 2 5 2 3 16
Au 1 1 3 2 3 4 1 15
GFMs 3 3 3 4 13

TP total articles, * the data for 2017 was only to June, 2017
92 Page 10 of 17 J Nanopart Res (2018) 20:92

Table 8 The popular freshwater algae and marine algae used in 2010), since the higher pH and ionic strength of seawa-
the toxicity test of nanomaterials
ter compared to freshwater will alter the physicochem-
Freshwater algae TP Marine algae TP ical property of NPs (Klaine et al. 2008). In 2009,
marine algae were first used in the NP toxicity test.
Pseudokirchneriella 72 Phaeodactylum 15 The adsorption of CdSe/ZnS QDs and its effects on
subcapitata tricornutum
Raphidocelis subcapitata 42 Dunaliella tertiolecta 13
Chlamydomonas sp. photosynthesis were explored
(Lin et al. 2009), and the toxicity of Ag+ dissolved from
Chlorella vulgaris 39 Skeletonema costatum 6
the Ag NPs to the marine diatom Thalassiosira
Scenedesmus obliquus 15 Thalassiosira 5
pseudonana weissflogii (Miao et al. 2009). As shown in Table 8,
Chlorella pyrenoidosa 11 Dunaliella salina 4 Phaeodactylum tricornutum and Dunaliella tertiolecta
Microcystis aeruginosa 11 were the top two major marine algae used with a total of
Desmodesmus 10 28 articles, followed by Skeletonema costatum,
subspicatus Thalassiosira pseudonana, and Dunaliella salina.
TP the number of articles that use corresponding algae for the
toxicity test
Historical review and research tendency
et al. 2016; Hazeem et al. 2017; Nogueira et al.
2015; Zhao et al. 2017; Zhao et al. 2014). Overview of the current research

Researches of NP toxicity on algae can be classified as

Algae
The most popular freshwater algae and marine algae
used in the toxicity test of NPs are summarized in
Table 8. Evidently, freshwater algae contributed the vast
majority of publications. The green algae
Pseudokirchneriella subcapitata (formerly known as
Selenastrum capricornutum and Raphidocelis
subcapitata) (Fu et al. 2013; Zhang et al. 2016b) and
Desmodesmus subspicatus were the most widely used
algae shown to be suitable for the growth inhibition test
and were recommended by OECD test guideline 201
(OECD 2011). Besides, Chlorella vulgaris,
Scenedesmus obliquus, Chlorella pyrenoidosa,
Microcystis aeruginosa, and Desmodesmus subspicatus
were all common freshwater algae used in NP toxicity
tests as well. In the early stage, much of data on the NP
ecotoxicity was limited to species used in regulatory
testing and freshwater algae, while data on marine algae
was particularly lacking (Handy et al. 2008). NPs will
reach the marine environment and the coastal ecosys-
tems as well. Marine algae, which are highly dispersed
in coastal ecosystems (Behrenfeld et al. 2006), can be
considered as a suitable indicator for marine water pol-
luted by NPs due to their being particularly vulnerable to
contaminants related to anthropogenic pollution (Manzo
et al. 2015). Some scholars realized that it is significant
to understand the effects of NPs on marine organisms
(Morelli et al. 2012; Schiavo et al. 2016; Wong et al.
short-term toxicity test and long-term toxicity test ac-
cording to the exposure time. There is no clear definition
between short term and long term. According to OECD
test guideline 201 for algae, test duration is normally
72 h; however, shorter or longer test durations may be
used provided that all validity criteria can be met
(OECD 2011). Ninety-six and 48 h are the other two
common test durations. Thus, in this study, toxicity test
durations less than a week were considered as short-
term toxicity test, whereas toxicity test durations of a
few weeks or months were considered as long-term
toxicity test. With regard to the current articles obtained,
most of the research has focused on the short-term and
acute toxicity test of NPs to algae, only a few studies
conducted the chronic effects from long-term and low-
concentration exposure (Pakrashi et al. 2012; Vincent
et al. 2017). Considering the more representative expo-
sure concentrations and time expected in real environ-
ment, it should pay more attention on the long-term and
chronic effects of NPs at low concentration in the future,
which will promote the value of research enormously.
Overall, of particular concern to researchers is the
environmental behavior and ecotoxicity of NPs to algae.
Particle size (Iswarya et al. 2016; Lei et al. 2016;
Polonini et al. 2015), crystalline form (Clement et al.
2013), exposure concentration (Deng et al. 2017), sur-
face properties, solubility of particles (Aruoja et al.
2009; Zhang et al. 2016a), and irradiation condition
(Chen et al. 2017; Hu et al. 2015) are of essential
J Nanopart Res (2018) 20:92
importance for the environmental behavior of NPs. The
major focus of NP toxicity researched can be divided
into two aspects. The first aspect is the indirect effects of
NPs to algae depending on their physical and chemical
properties, including shading effects (Nogueira et al.
2015; Zhao et al. 2017), aggregation behavior (Sharma
2009; Zamani et al. 2014), solubility of toxic com-
pounds (Sendra et al. 2017), and so on. While, the
second aspect is that NPs provoke alterations of cell
membranes, structures, and molecules directly (Chen
et al. 2017; Navarro et al. 2008a; Sendra et al. 2017).
ECx (e.g., EC10, EC20, and EC50) refers to the con-
centration bringing about a specified x % inhibition of
growth rate (e.g., 10, 20, and 50%) within a stated
exposure period (OECD 2011). Some studies used
LCx (e.g., LC10, LC20, and LC50), which means lethal
concentration after 10, 20, and 50% population response
occurred. ECx (or LCx) is the most common test end-
point for assessing NP ecotoxicity and algal growth
inhibition. In addition, the toxicity of NPs to algae was
also evaluated by measuring the culture yield, chloro-
phyll fluorescence parameter, reactive oxygen species
induced, and so on. Quantification methods and tech-
niques should be further developed to thoroughly ex-
plain the mechanism of the toxicity of nanoparticles to
algae.
Research trends
Since the first paper about the toxicity of NPs to algae
was published in 2006, there has been uninterrupted
development up to now. The extensive use of NPs
indicates that compounds associated with NPs are eco-
logically available (Bessar et al. 2016; Chen et al. 2016;
Dilnawaz et al. 2010; Han and Ghosh 2007; Jiang et al.
2012; Tang et al. 2012; Wilczewska et al. 2012). There-
fore, the interaction of NPs and associated contaminants
has evolved into an emerging research field and gained
particular interest beyond the initial research focusing
only on the inherent toxicity of NPs. The first time that
different NPs and their interaction with other environ-
mental contaminants was used in the toxicity test of
algae is displayed in the timeline (Fig. 3) demonstrating
historical events and trends. It is clear that not only the
single NP but also the interaction effects between NPs
and environmental contaminants (e.g., organic pollut-
ants and heavy metals) were explored extensively, par-
ticularly in the last few years. Besides, researches about
the toxicity of NP-based products or NPs upon release
Page 11 of 17 92
from products to algae were considered as well. There-
fore, narrative literature review was made to highlight
the research trend about the risk of interactions and NP-
based products to algae based on Fig. 3. Further details
are reviewed in the following section.
Organic pollutants
Zhang et al. (2008) first studied the interactive effect of
SiO2 NPs and γ-picoline and recognized them as a
marine pollutant to marine algae. The high adsorption
capacity of SiO2 NPs makes it a toxic carrier of γ-
picoline, which passes through the membrane and enters
into Caulerpa taxifolia resulting in serious toxicity
(Zhang et al. 2008). Some studies also explored the
effects of interaction between NPs and common xeno-
biotic compounds (Baun et al. 2008; Grillo et al. 2015;
Schwab et al. 2013; Wen et al. 2011). The concomitant
exposure of four xenobiotic compounds (phenanthrene,
pentachlorophenol, atrazine, and methyl parathion) and
C60 indicated that the toxicity to Pseudokirchneriella
subcapitata was altered only for the two compounds
phenanthrene and pentachlorophenol with evident sorp-
tion to C60-aggregates. It was observed for pentachloro-
phenol that the toxicity was reduced by absorbing to
C60-aggregates, Conversely, the overall toxicity of
phenanthrene was enhanced (Baun et al. 2008). Also,
the bioavailability of Diuron sorbed to CNTs was in-
creased and exhibited stronger toxicity to Chlorella
vulgaris (Schwab et al. 2013).
Natural organic matter
With respect to natural organic matter (NOM), it is a
ubiquitous component and plays a vital role in aquatic
systems. Therefore, to determine the fate and toxicity of
NPs in aquatic environment, it is significant to explore
the interactions between NPs and NOM. The existing
studies about the toxicity of CeO2, Ag, and TiO2 in the
presence of NOM all found that NOM alleviated the
adverse effects of NPs to algae and increased their
stability by adsorbing to the surface of NPs (Booth
et al. 2015; Cerrillo et al. 2016; Van Hoecke et al.
2011). Humic substances especially humic acid (HA),
which are a kind of NOM, were also used extensively to
test the interactive effects with NPs (Akhil and Khan
2017; Lin et al. 2012; Slaveykova and Startchev 2009;
Tang et al. 2015a). In addition, studies on dissolved
organic matter (DOM) including low-molecular-weight
92 Page 12 of 17 J Nanopart Res (2018) 20:92

QDs C60 CNTs

Polystyrene Fe3 O4 TiO2 +Zn2+
Ag CeO2 CuZnFe4 O
TiO2 +DBPs Co0.2 Zn0.8 Fe2 O4
Cu SiO2 NiZnFe4 O4
ZnO+DBPs Co0.5 Zn0.5 Fe2 O4
Al Al2 O3 Y3 Fe5 O12 Cr2 O3 Ag+NOM
QDs+EPS CNTs+Diuron
Co Sm2 O3 SrFe12 O19 Fe+As TiO2 +NOM
Ni Er2 O3 PMMA nZVI PbS Fe Ag+P Fe2 O3 +As Al2 O3 +Cu2+
Au Ho2 O3 SiO2 +γ-picoline TiO2 +HA CNFs Al2 O3 +Cr3+ Fe3 O4 +As CoFe2 O4 +ACP
TiO2 (In2 O3 )0.9 · (SnO2 )0.1 C60 +XOC PAMAM TiO2 +Cd2+ GFMs TiO2 +Cr3+ CuO+BA GFMs+LOAs

2006 2007 2008 2009 2010 2011 2012 2013 2014 2015 2016 2017

ZnO CuO NiO2 Pb La2 O3 Sb2 O3 NiO TiN+DOM

NIPAM CeO2 +NOM Pt Mn3 O4 GO+Cd2+ TiN ZnO+CuO

NIPAM/BAM CS+DCPP CdS Fe2 O3 TiO2 +Cu2+ TiO2 +N Au+Zn2+

CuO+FA Ag2 S Co3 O4 ZnO+HA Paclitaxel-loaded nanomedicine

WO3 CoFe2 O4 Ag+HS

MgO BaTiO3 ZnO+Wastewater
CS/TPP+HS+Paraquat TiO2 +Wastewater

Fig. 3 The historical review of nanomaterials and their interactive
effects with environmental contaminants. ACP acid phosphatase,
BA benzoic acid, CNFs cellulose nanofibers, CS/TPP polymeric
chitosan/tripolyphosphate, DOM dissolved organic matter, DBPs
disinfection byproducts, DCPP chiral herbicide dichlorprop, EPS
extracellular polymeric substances, FA fulvic acid, GFMs
Graphene-family materials, HA humic acid, HS humic substance,
LOAs low-molecular-weight organic acids, N nitrogen, NOM
natural organic matter, NIPAM poly N-isopropylacrylamide co-
polymer, NIPAM/BAM N-isopropylacrylamide/N-tert-
b ut yl a c r y l a m i de co po l y m e r, P p ho sp ho r u s, PM M A
polymethylmethacrylate, PAMAM poly(amidoamine)
dendrimers, XOC xenobiotic organic compounds. BSiO2+ γ-
picoline^ means the interactive effect of SiO2 and γ-picoline, all
else follows

organic acids, benzoic acid, and fulvic acid were con-
ducted (Wang et al. 2016a; Wang et al. 2016b; Wang
et al. 2011; Zhang et al. 2017b). One publication pointed
out that fulvic acid enhanced the toxicity of CuO NPs to
algae through a higher Cu2+ release and CuO NP inter-
nalization (Wang et al. 2011).
Heavy metals
NP concentrations, while when the TiO2 NPs concen-
tration increased to a certain value, the toxicity would
decrease. Similarly, another paper about the toxicity of
Cd2+/GO system comes to the same result (Tang et al.
2013; Tang et al. 2015b). On the other hand, heavy
metal ions could influence the toxicity of NPs as well.
For instance, Zn2+ minimized the toxicity produced by
Au NPs to Scenedesmus obliquus (Iswarya et al. 2017).

Another research trend was the interactive effects be-
tween NPs and heavy metals discharged into aquatic
systems from various industries. Zinc, copper, cadmi-
um, and chromium all exist in the environment. Their
toxic forms Zn2+, Cu2+, Cd2+, and Cr3+ can exert severe
toxicity on algae and have been widely used to explore
the interactions with NPs (Chen et al. 2015; Dalai et al.
2014; Iswarya et al. 2017; Li et al. 2016; Tang et al.
2013; Tang et al. 2015b; Yang et al. 2012). The toxicity
of those heavy metal ions to algae was either alleviated
or enhanced in the presence of different NPs. One
notable phenomenon is that the toxicity impacts were
not absolute. Several studies indicated that it could
depend on the concentration of NPs. For example, the
toxicity of Zn2+/TiO2 system could increase at low TiO2
Nanoparticle-based products
To ensure the safely use of NPs when incorporated into
products or processes, it is significant to further explore
the toxicity of NP-based products to algae in different
models and systems. Five different commercial CNTs
representing three different common manufacturing
processes were selected to assess their toxicity to fresh-
water algae by Bennett et al. (2013). Results showed
that the stability, photoactivity, metal leachate, and
toxicity of the tested CNTs to freshwater algae
depended on the type of CNTs and environmental
conditions. In addition, Galletti et al. (2016) focused
on the toxicity effects and release behavior of industrial
TiO2 NPs and sunscreen- and toothpaste-derived TiO2
J Nanopart Res (2018) 20:92
NPs on marine organisms. It revealed that a significant
release, enhanced aggregation, and more time-
dependent toxicity of the two model product-derived
TiO2 NPs compared to industrial TiO2 NPs. So far, data
for the potential toxicity of NPs derived from consumer
NP-based products on algae is far from enough. Further
research is encouraged for the toxicity assessment of
NP-based products to algae in realistic scenarios.
Conclusion
This paper reveals that the literature on the toxicity of
NPs to algae has more extensive and global over the
past 11 years. The total number of articles published
annually and the citations per article have increased
since 2006. First, 112 journals contributed to the
publication of 374 papers. The top 10 journals
accounted for 186 articles, among which Aquatic
Toxicology contributed the most, followed by Envi-
ronmental Science and Technology and Science of the
Total Environment. Second, there were 23 highly
cited papers and the most productive journal was
Environmental Science and Technology. Third, 56
countries carried out research in the toxicity of NPs
to algae. China was the most high-publishing country,
followed by the USA and India. However, the average
citations per article from China was no more than 30
and most Asian countries such as China, India, and
Japan were deficient in international collaborations
compared with USA and most European countries.
From the funding agency analysis, the European
Union and US Environmental Protection Agency
were the trend spotters funding the research of NP
toxicity on algae since 2008. Finally, Ag NPs and
TiO2 NPs were the top two NPs used in the algae
toxicity tests due to their bactericidal effects and
ultraviolet ray exposure characteristics. The green
a l g a e P s e u d o k i rc h n e r i e l l a s u b c a p i t a t a a n d
Phaeodactylum tricornutum were the most widely
used freshwater and marine algae for the growth in-
hibition test, respectively. A current research trend is
the increasing concern about interactive toxic effects
of NPs and environmental contaminants, such as xe-
nobiotic compounds, natural organic matter, dis-
solved organic maters, and heavy metal ions that are
frequently found in aquatic systems. Further research
is encouraged for the toxicity assessment of NP-based
products to algae in realistic scenarios.
Page 13 of 17 92
Acknowledgements This work was supported by Natural Sci-
ence Foundation of China (21776224) and National Water Pollu-
tion Control and Treatment Key Technologies RD Program
(2015ZX07406-001).
Compliance with ethical standards
Conflict of interest The authors declare that they have no con-
flict of interest.
References
Akhil K, Khan SS (2017) Effect of humic acid on the toxicity of
bare and capped ZnO nanoparticles on bacteria, algal and
crustacean systems. J Photochem Photobiol B Biol 167:136–
149. https://doi.org/10.1016/j.jphotobiol.2016.12.010
Aruoja V, Dubourguier HC, Kasemets K, Kahru A (2009) Toxicity
of nanoparticles of CuO, ZnO and TiO2 to microalgae
Pseudokirchneriella subcapitata. Sci Total Environ 407:
1461–1468. https://doi.org/10.1016/j.scitotenv.2008.10.053
Baltussen A, Kindler CH (2004) Citation classics in anesthetic
journals. Anesth Analg 98:443–451. https://doi.org/10.1213
/01.ane.0000096185.13474.0a
Baun A, Sorensen SN, Rasmussen RF, Hartmann NB, Koch CB
(2008) Toxicity and bioaccumulation of xenobiotic organic
compounds in the presence of aqueous suspensions of aggre-
gates of nano-C-60. Aquat Toxicol 86:379–387. https://doi.
org/10.1016/j.aquatox.2007.11.019
Behrenfeld MJ, O’Malley RT, Siegel DA, McClain CR, Sarmiento
JL, Feldman GC, Milligan AJ, Falkowski PG, Letelier RM,
Boss ES (2006) Climate-driven trends in contemporary
ocean productivity. Nature 444:752–755. https://doi.
org/10.1038/nature05317
Bennett SW, Adeleye A, Ji ZX, Keller AA (2013) Stability, metal
leaching, photoactivity and toxicity in freshwater systems of
commercial single wall carbon nanotubes. Water Res 47:
4074–4085. https://doi.org/10.1016/j.watres.2012.12.039
Bessar H, Venditti I, Benassi L, Vaschieri C, Azzoni P, Pellacani G,
Magnoni C, Botti E, Casagrande V, Federici M, Costanzo A,
Fontana L, Testa G, Mostafa FF, Ibrahim SA, Russo MV,
Fratoddi I (2016) Functionalized gold nanoparticles for top-
ical delivery of methotrexate for the possible treatment of
psoriasis. Colloid Surf B 141:141–147. https://doi.
org/10.1016/j.colsurfb.2016.01.021
Blaise C, Gagne F, Ferard JF, Eullaffroy P (2008) Ecotoxicity of
selected nano-materials to aquatic organisms. Environ
Toxicol 23:591–598. https://doi.org/10.1002/tox.20402
Bondarenko O, Juganson K, Ivask A, Kasemets K, Mortimer M,
Kahru A (2013) Toxicity of Ag, CuO and ZnO nanoparticles
to selected environmentally relevant test organisms and
mammalian cells in vitro: a critical review. Arch Toxicol
87:1181–1200. https://doi.org/10.1007/s00204-013-1079-4
Booth A, Størseth T, Altin D, Fornara A, Ahniyaz A, Jungnickel
H, Laux P, Luch A, Sørensen L (2015) Freshwater dispersion
92 Page 14 of 17
stability of PAA-stabilised-cerium-oxide nanoparticles and
toxicity towards Pseudokirchneriella subcapitata. Sci Total
Environ 505:596–605. https://doi.org/10.1016/j.
scitotenv.2014.10.010
Botta C, Labille J, Auffan M, Borschneck D, Miche H, Cabié M,
Masion A, Rose J, Bottero JY (2011) TiO2-based nanoparti-
cles released in water from commercialized sunscreens in a
life-cycle perspective: structures and quantities. Environ
Pollut 159:1543–1548. https://doi.org/10.1016/j.
envpol.2011.03.003
Bouldin JL, Ingle TM, Sengupta A, Alexander R, Hannigan RE,
Buchanan RA (2008) Aqueous toxicity and food chain trans-
fer of quantum dots (TM) in freshwater algae and
Ceriodaphnia dubia. Environ Toxicol Chem 27:1958–1963.
https://doi.org/10.1897/07-637.1
Cerrillo C, Barandika G, Igartua A, Areitioaurtena O, Mendoza G
(2016) Towards the standardization of nanoecotoxicity test-
ing: natural organic matter ‘camouflages’ the adverse effects
of TiO2 and CeO2 nanoparticles on green microalgae. Sci
Total Environ 543:95–104. https://doi.org/10.1016/j.
scitotenv.2015.10.137
Chen JY, Qian Y, Li HR, Cheng YH, Zhao MR (2015) The reduced
bioavailability of copper by nano-TiO2 attenuates the toxicity
to Microcystis aeruginosa. Environ Sci Pollut Res 22:12422–
12429. https://doi.org/10.1007/s11356-015-4492-9
Chen SZ, Hao X, Liang X, Zhang Q, Zhang C, Zhou G, Shen S,
Jia G, Zhang J (2016) Inorganic nanomaterials as carriers for
drug delivery. J Biomed Nanotechnol 12:1–27. https://doi.
org/10.1166/jbn.2016.2122
Chen XJ, Lu RR, Liu P, Li X (2017) Effects of Nano-TiO2 on
Chlamydomonas reinhardtii cell surface under UV, natural
light conditions. J Wuhan Univ Technol Mat Sci Ed 32:217–
222. https://doi.org/10.1007/s11595-017-1583-0
Clement L, Hurel C, Marmier N (2013) Toxicity of TiO2 nano-
particles to cladocerans, algae, rotifers and plants—effects of
size and crystalline structure. Chemosphere 90:1083–1090.
https://doi.org/10.1016/j.chemosphere.2012.09.013
Dalai S, Pakrashi S, Bhuvaneshwari M, Iswarya V,
Chandrasekaran N, Mukherjee A (2014) Toxic effect of
Cr(VI) in presence of n-TiO2 and n-Al2O3 particles towards
freshwater microalgae. Aquat Toxicol 146:28–37. https://doi.
org/10.1016/j.aquatox.2013.10.029
Das P, Metcalfe CD, Xenopoulos MA (2014) Interactive effects of
silver nanoparticles and phosphorus on phytoplankton
growth in natural waters. Environ Sci Technol 48:4573–
4580. https://doi.org/10.1021/es405039w
Dash A, Singh AP, Chaudhary BR, Singh SK, Dash D (2012)
Effect of silver nanoparticles on growth of eukaryotic green
algae. Nano-Micro Lett 4:158–165. https://doi.org/10.3786
/nml.v4i3.p158-165
Deng XY, Cheng J, Hu XL, Wang L, Li D, Gao K (2017)
Biological effects of TiO2 and CeO2 nanoparticles on the
growth, photosynthetic activity, and cellular components of a
marine diatom Phaeodactylum tricornutum. Sci Total
E n v i r o n 5 7 5 : 8 7 – 9 6 . h t t p s : / / d o i . o rg / 1 0 . 1 0 1 6 / j .
scitotenv.2016.10.003
Dilnawaz F, Singh A, Mohanty C, Sahoo SK (2010) Dual drug
loaded superparamagnetic iron oxide nanoparticles for
targeted cancer therapy. Biomaterials 31:3694–3706.
https://doi.org/10.1016/j.biomaterials.2010.01.057
J Nanopart Res (2018) 20:92
Du ST, Zhang P, Zhang RR, Lu Q, Liu L, Bao XW, Liu HJ (2016)
Reduced graphene oxide induces cytotoxicity and inhibits
photosynthetic performance of the green alga Scenedesmus
obliquus. Chemosphere 164:499–507. https://doi.
org/10.1016/j.chemosphere.2016.08.138
Fahimnia B, Sarkis J, Davarzani H (2015) Green supply chain
management: a review and bibliometric analysis. Int J Prod
E c o n 1 6 2 : 1 0 1 – 11 4 . h t t p s : / / d o i . o r g / 1 0 . 1 0 1 6 / j .
ijpe.2015.01.003
Franklin NM, Rogers NJ, Apte SC, Batley GE, Gadd GE, Casey
PS (2007) Comparative toxicity of nanoparticulate ZnO, bulk
ZnO, and ZnCl2 to a freshwater microalga
(Pseudokirchneriella subcapitata): the importance of particle
solubility. Environ Sci Technol 41:8484–8490. https://doi.
org/10.1021/es071445r
Fu HZ, Wang MH, Ho YS (2013) Mapping of drinking water
research: a bibliometric analysis of research output during
1992-2011. Sci Total Environ 443:757–765. https://doi.
org/10.1016/j.scitotenv.2012.11.061
Galletti A, Seo S, Joo SH, Su C, Blackwelder P (2016) Effects of
titanium dioxide nanoparticles derived from consumer prod-
ucts on the marine diatom Thalassiosira pseudonana. Environ
Sci Pollut Res 23:21113–21122. https://doi.org/10.1007
/s11356-016-7556-6
Grillo R, Clemente Z, Oliveira JL, Campos EVR, Chalupe VC,
Jonsson CM, Lima R, Sanches G, Nishisaka CS, Rosa AH,
Oehlke K, Greiner R, Fraceto LF (2015) Chitosan nanopar-
ticles loaded the herbicide paraquat: the influence of the
aquatic humic substances on the colloidal stability and tox-
icity. J Hazard Mater 286:562–572. https://doi.org/10.1016/j.
jhazmat.2014.12.021
Han G, Ghosh P, Rotello VM (2007) Functionalized gold nano-
particles for drug delivery. Nanomedicine 2:113–123.
https://doi.org/10.2217/17435889.2.1.113
Handy RD, Owen R, Valsami-Jones E (2008) The ecotoxicology
of nanoparticles and nanomaterials: current status, knowl-
edge gaps, challenges, and future needs. Ecotoxicology 17:
315–325. https://doi.org/10.1007/s10646-008-0206-0
Hazeem LJ, Bououdina M, Dewailly E, Slomianny C, Barras A,
Coffinier Y, Szunerits S, Boukherroub R (2017) Toxicity
effect of graphene oxide on growth and photosynthetic pig-
ment of the marine alga Picochlorum sp during different
growth stages. Environ Sci Pollut Res 24:4144–4152.
https://doi.org/10.1007/s11356-016-8174-z
Hirsch JE (2005) An index to quantify an individual's scientific
research output. Proc Natl Acad Sci U S A 102:16569–
16572. https://doi.org/10.1073/pnas.0507655102
Hu XG, Zhou M, Zhou QX (2015) Ambient water and visible-
light irradiation drive changes in graphene morphology,
structure, surface chemistry, aggregation, and toxicity.
Environ Sci Technol 49:3410–3418. https://doi.org/10.1021
/es503003y
Huang TD, Sui MH, Yan X, Zhang X, Yuan Z (2016) Anti-algae
efficacy of silver nanoparticles to Microcystis aeruginosa:
influence of NOM, divalent cations, and pH. Colloid Surf
A Physicochem Eng Asp 509:492–503. https://doi.
org/10.1016/j.colsurfa.2016.09.009
Hund-Rinke K, Simon M (2006) Ecotoxic effect of photocatalytic
active nanoparticles TiO2 on algae and daphnids. Environ Sci
Pollut Res 13:225–232. https://doi.org/10.1065
/espr2006.06.311
J Nanopart Res (2018) 20:92
Iswarya V, Manivannan J, De A, Paul S, Roy R, Johnson JB,
Kundu R, Chandrasekaran N, Mukherjee A, Mukherjee A
(2016) Surface capping and size-dependent toxicity of gold
nanoparticles on different trophic levels. Environ Sci Pollut
Res 23:4844–4858. https://doi.org/10.1007/s11356-015-
5683-0
Iswarya V, Johnson JB, Parashar A, Pulimi M, Chandrasekaran N,
Mukherjee A (2017) Modulatory effects of Zn2+ ions on the
toxicity of citrate-and PVP-capped gold nanoparticles to-
wards freshwater algae, Scenedesmus obliquus. Environ Sci
Pollut Res 24:3790–3801. https://doi.org/10.1007/s11356-
016-8131-x
Ivask A, Kurvet I, Kasemets K, Blinova I, Aruoja V, Suppi S, Vija
H, Käkinen A, Titma T, Heinlaan M, Visnapuu M, Koller D,
Kisand V, Kahru A (2014) Size-dependent toxicity of silver
nanoparticles to bacteria, yeast, algae, crustaceans and mam-
malian cells in vitro. PLoS One 9:14. https://doi.org/10.1371
/journal.pone.0102108
Jemec A, Kahru A, Potthoff A, Drobne D, Heinlaan M, Böhme S,
Geppert M, Novak S, Schirmer K, Rekulapally R, Singh S,
Aruoja V, Sihtmäe M, Juganson K, Käkinen A, Kühnel D
(2016) An interlaboratory comparison of nanosilver charac-
terisation and hazard identification: Harmonising techniques
for high quality data. Environ Int 87:20–32. https://doi.
org/10.1016/j.envint.2015.10.014
Ji J, Long ZF, Lin DH (2011) Toxicity of oxide nanoparticles to the
green algae Chlorella sp. Chem Eng J 170:525–530.
https://doi.org/10.1016/j.cej.2010.11.026
Jiang HT, Wang TY, Wang LH, Sun CS, Jiang TY, Cheng G, Wang
SL (2012) Development of an amorphous mesoporous TiO2
nanosphere as a novel carrier for poorly water-soluble drugs:
effect of different crystal forms of TiO2 carriers on drug
loading and release behaviors. Microporous Mesoporous
M a t e r 1 5 3 : 1 2 4 – 1 3 0 . h t t p s : / / d o i . o rg / 1 0 . 1 0 1 6 / j .
micromeso.2011.12.013
Kahru A, Dubourguier HC (2010) From ecotoxicology to
nanoecotoxicology. Toxicology 269:105–119. https://doi.
org/10.1016/j.tox.2009.08.016
Klaine SJ, Alvarez PJJ, Batley GE, Fernandes TF, Handy RD,
Lyon DY, Mahendra S, McLaughlin MJ, Lead JR (2008)
Nanomaterials in the environment: behavior, fate, bioavail-
ability and effects. Environ Toxicol Chem 27:1825–1851.
https://doi.org/10.1897/08-090.1
Lei C, Zhang LQ, Yang K, Zhu LZ, Lin DH (2016) Toxicity of
iron-based nanoparticles to green algae: effects of particle
size, crystal phase, oxidation state and environmental aging.
Environ Pollut 218:505–512. https://doi.org/10.1016/j.
envpol.2016.07.030
Li XM, Schirmer K, Bernard L, Sigg L, Pillai S, Behra R (2015)
Silver nanoparticle toxicity and association with the alga
Euglena gracilis. Environ Sci Nano 2:594–602. https://doi.
org/10.1039/c5en00093a
Li XM, Zhou SY, Fan WH (2016) Effect of Nano-Al2O3 on the
toxicity and oxidative stress of copper towards Scenedesmus
obliquus. Int J Environ Res Public Health 13:15. https://doi.
org/10.3390/ijerph13060575
Lin S, Bhattacharya P, Rajapakse NC, Brune DE, Ke PC (2009)
Effects of quantum dots adsorption on algal photosynthesis. J
Phys Chem C 113:10962–10966. https://doi.org/10.1021
/jp904343s
Page 15 of 17 92
Lin DH, Ji J, Long ZF, Yang K, Wu FC (2012) The influence of
dissolved and surface-bound humic acid on the toxicity of
TiO2 nanoparticles to Chlorella sp. Water Res 46:4477–
4487. https://doi.org/10.1016/j.watres.2012.05.035
Manzo S, Buono S, Rametta G, Miglietta M, Schiavo S, Di
Francia G (2015) The diverse toxic effect of SiO2 and TiO2
nanoparticles toward the marine microalgae Dunaliella
tertiolecta. Environ Sci Pollut Res 22:15941–15951.
https://doi.org/10.1007/s11356-015-4790-2
Marty JJ, Oppenheim RC, Speiser P (1978) Nanoparticles - new
colloidal drug delivery system. Pharm Acta Helv 53:17–23
Maynard AD, Aitken RJ, Butz T, Colvin V, Donaldson K,
Oberdörster G, Philbert MA, Ryan J, Seaton A, Stone V,
Tinkle SS, Tran L, Walker NJ, Warheit DB (2006) Safe
handling of nanotechnology. Nature 444:267–269.
https://doi.org/10.1038/444267a
Miao A-J, Schwehr KA, Xu C, Zhang S-J, Luo Z, Quigg A,
Santschi PH (2009) The algal toxicity of silver engineered
nanoparticles and detoxification by exopolymeric sub-
stances. Environ Pollut 157:3034–3041. https://doi.
org/10.1016/j.envpol.2009.05.047
Morelli E, Cioni P, Posarelli M, Gabellieri E (2012) Chemical
stability of CdSe quantum dots in seawater and their effects
on a marine microalga. Aquat Toxicol 122:153–162.
https://doi.org/10.1016/j.aquatox.2012.06.012
Navarro E, Baun A, Behra R, Hartmann NB, Filser J, Miao AJ,
Quigg A, Santschi PH, Sigg L (2008a) Environmental be-
havior and ecotoxicity of engineered nanoparticles to algae,
plants, and fungi. Ecotoxicology 17:372–386. https://doi.
org/10.1007/s10646-008-0214-0
Navarro E, Piccapietra F, Wagner B, Marconi F, Kaegi R, Odzak
N, Sigg L, Behra R (2008b) Toxicity of silver nanoparticles
to Chlamydomonas reinhardtii. Environ Sci Technol 42:
8959–8964. https://doi.org/10.1021/es801785m
Nogueira PFM, Nakabayashi D, Zucolotto V (2015) The effects of
graphene oxide on green algae Raphidocelis subcapitata.
Aquat Toxicol 166:29–35. https://doi.org/10.1016/j.
aquatox.2015.07.001
OECD (2011) OECD guideline for testing of chemicals. Test No.
201: freshwater alga and cyanobacteria, growth inhibition
test. https://doi.org/10.1787/9789264069923-en
Ohba N, Nakao K, Isashiki Y, Ohba A (2007) The 100 most
frequently cited articles in ophthalmology journals. Arch
Ophthalmol 125:952–960. https://doi.org/10.1001
/archopht.125.7.952
Ostrowski AD, Martin T, Conti J, Hurt I, Harthorn BH (2009)
Nanotoxicology: characterizing the scientific literature,
2000-2007. J Nanopart Res 11:251–257. https://doi.
org/10.1007/s11051-008-9579-5
Oukarroum A, Bras S, Perreault F, Popovic R (2012) Inhibitory
effects of silver nanoparticles in two green algae, Chlorella
vulgaris and Dunaliella tertiolecta. Ecotoxicol Environ Saf
78:80–85. https://doi.org/10.1016/j.ecoenv.2011.11.012
Oukarroum A, Samadani M, Dewez D (2014) Influence of pH on
the toxicity of silver nanoparticles in the green alga
Chlamydomonas acidophila. Water Air Soil Pollut 225:8.
https://doi.org/10.1007/s11270-014-2038-2
Pakrashi S, Dalai S, Sneha RB, Chandrasekaran N, Mukherjee A
(2012) A temporal study on fate of Al2O3 nanoparticles in a
fresh water microcosm at environmentally relevant low
92 Page 16 of 17
concentrations. Ecotoxicol Environ Saf 84:70–77. https://doi.
org/10.1016/j.ecoenv.2012.06.015
Petit AN, Eullaffroy P, Debenest T, Gagne F (2010) Toxicity of
PAMAM dendrimers to Chlamydomonas reinhardtii. Aquat
Toxicol 100:187–193. https://doi.org/10.1016/j.
aquatox.2010.01.019
Piccapietra F, Allue CG, Sigg L, Behra R (2012) Intracellular
silver accumulation in Chlamydomonas reinhardtii upon ex-
posure to carbonate coated silver nanoparticles and silver
nitrate. Environ Sci Technol 46:7390–7397. https://doi.
org/10.1021/es300734m
Polonini HC, Brandão HM, Raposo NRB, Brandão MAF, Mouton
L, Couté A, Yéprémian C, Sivry Y, Brayner R (2015) Size-
dependent ecotoxicity of barium titanate particles: the case of
Chlorella vulgaris green algae. Ecotoxicology 24:938–948.
https://doi.org/10.1007/s10646-015-1436-6
Rowley J, Slack F (2004) Conducting a literature review. Manag
R e s N e w s 2 7 : 3 1 – 3 9 . h t t p s : / / d o i . o r g / 1 0 . 11 0 8
/01409170410784185
Sadiq IM, Dalai S, Chandrasekaran N, Mukherjee A (2011)
Ecotoxicity study of titania (TiO2) NPs on two microalgae
species: Scenedesmus sp and Chlorella sp. Ecotoxicol
Environ Saf 74:1180–1187. https://doi.org/10.1016/j.
ecoenv.2011.03.006
Schiavo S, Oliviero M, Miglietta M, Rametta G, Manzo S (2016)
Genotoxic and cytotoxic effects of ZnO nanoparticles for
Dunaliella tertiolecta and comparison with SiO2 and TiO2
effects at population growth inhibition levels. Sci Total
Environ 550:619–627. https://doi.org/10.1016/j.
scitotenv.2016.01.135
Schwab F, Bucheli TD, Camenzuli L, Magrez A, Knauer K, Sigg
L, Nowack B (2013) Diuron sorbed to carbon nanotubes
exhibits enhanced toxicity to Chlorella vulgaris. Environ
Sci Technol 47:7012–7019. https://doi.org/10.1021
/es304016u
Sendra M, Yeste MP, Gatica JM, Moreno-Garrido I, Blasco J
(2017) Direct and indirect effects of silver nanoparticles on
freshwater and marine microalgae (Chlamydomonas
reinhardtii and Phaeodactylum tricornutum). Chemosphere
179:279–289. https://doi.org/10.1016/j.
chemosphere.2017.03.123
Sharma VK (2009) Aggregation and toxicity of titanium dioxide
nanoparticles in aquatic environment—a review. J Environ
Sci Health Part A Tox Hazard Subst Environ Eng 44:1485–
1495. https://doi.org/10.1080/10934520903263231
Slaveykova VI, Startchev K (2009) Effect of natural organic
matter and green microalga on carboxyl-polyethylene glycol
coated CdSe/ZnS quantum dots stability and transformations
under freshwater conditions. Environ Pollut 157:3445–3450.
https://doi.org/10.1016/j.envpol.2009.06.017
Smith DR (2008) Citation indexing and highly cited articles in the
Australian Veterinary Journal. Aust Vet J 86:337–339.
https://doi.org/10.1111/j.1751-0813.2008.00330.x
Tang FQ, Li LL, Chen D (2012) Mesoporous silica nanoparticles:
synthesis, biocompatibility and drug delivery. Adv Mater 24:
1504–1534. https://doi.org/10.1002/adma.201104763
Tang YL, Li SY, Qiao JL, Wang HT, Li L (2013) Synergistic
effects of nano-sized titanium dioxide and zinc on the pho-
tosynthetic capacity and survival of anabaena sp. Int J Mol
Sci 14:14395–14407. https://doi.org/10.3390
/ijms140714395
J Nanopart Res (2018) 20:92
Tang YL, Li SY, Lu Y, Li Q, Yu SL (2015a) The influence of
humic acid on the toxicity of nano-ZnO and Zn2+ to the
Anabaena sp. Environ Toxicol 30:895–903. https://doi.
org/10.1002/tox.21964
Tang YL, Tian JL, Li SY, Xue CH, Xue ZH, Yin DQ, Yu SL
(2015b) Combined effects of graphene oxide and Cd on the
photosynthetic capacity and survival of Microcystis
aeruginosa. Sci Total Environ 532:154–161. https://doi.
org/10.1016/j.scitotenv.2015.05.081
van Eck NJ, Waltman L (2010) Software survey: VOSviewer, a
computer program for bibliometric mapping. Scientometrics
84:523–538. https://doi.org/10.1007/s11192-009-0146-3
Van Hoecke K, De Schamphelaere KAC, Van der Meeren P,
Smagghe G, Janssen CR (2011) Aggregation and ecotoxicity
of CeO2 nanoparticles in synthetic and natural waters with
variable pH, organic matter concentration and ionic strength.
Environ Pollut 159:970–976. https://doi.org/10.1016/j.
envpol.2010.12.010
Vincent JL, Paterson MJ, Norman BC, Gray EP, Ranville JF, Scott
AB, Frost PC, Xenopoulos MA (2017) Chronic and pulse
exposure effects of silver nanoparticles on natural lake phy-
toplankton and zooplankton. Ecotoxicology 26:502–515.
https://doi.org/10.1007/s10646-017-1781-8
Wang ZY, Li J, Zhao J, Xing BS (2011) Toxicity and internaliza-
tion of CuO nanoparticles to prokaryotic alga Microcystis
aeruginosa as affected by dissolved organic matter. Environ
Sci Technol 45:6032–6040. https://doi.org/10.1021
/es2010573
Wang Q, Yang ZG, Yang Y, Long CL, Li HP (2014) A
bibliometric analysis of research on the risk of engineering
nanomaterials during 1999-2012. Sci Total Environ 473:
483–489. https://doi.org/10.1016/j.scitotenv.2013.12.066
Wang Z, Fang H, Wang S (2016a) Benzoic acid interactions affect
aquatic properties and toxicity of copper oxide nanoparticles.
Bull Environ Contam Toxicol 97:159–165. https://doi.
org/10.1007/s00128-016-1804-9
Wang Z, Gao YC, Wang S, Fang H, Xu DF, Zhang F (2016b)
Impacts of low-molecular-weight organic acids on aquatic
behavior of graphene nanoplatelets and their induced algal
toxicity and antioxidant capacity. Environ Sci Pollut Res 23:
10938–10945. https://doi.org/10.1007/s11356-016-6290-4
Warheit DB, Hoke RA, Finlay C, Donner EM, Reed KL, Sayes
CM (2007) Development of a base set of toxicity tests using
ultrafine TiO2 particles as a component of nanoparticle risk
management. Toxicol Lett 171:99–110. https://doi.
org/10.1016/j.toxlet.2007.04.008
Wen YZ, Chen H, Yuan YL, Xu DM, Kang XD (2011)
Enantioselective ecotoxicity of the herbicide dichlorprop
and complexes formed with chitosan in two fresh water green
algae. J Environ Monit 13:879–885. https://doi.org/10.1039
/c0em00593b
Wilczewska AZ, Niemirowicz K, Markiewicz KH, Car H (2012)
Nanoparticles as drug delivery systems. Pharmacol Rep 64:
1020–1037
Wong SWY, Leung PTY, Djurisic AB, Leung KMY (2010)
Toxicities of nano zinc oxide to five marine organisms:
influences of aggregate size and ion solubility. Anal
Bioanal Chem 396:609–618. https://doi.org/10.1007
/s00216-009-3249-z
Yang WW, Li Y, Miao AJ, Yang LY (2012) Cd2+ toxicity as
affected by bare TiO2 nanoparticles and their bulk
J Nanopart Res (2018) 20:92
counterpart. Ecotoxicol Environ Saf 85:44–51. https://doi.
org/10.1016/j.ecoenv.2012.08.024
Zamani H, Moradshahi A, Jahromi HD, Sheikhi MH (2014)
Influence of PbS nanoparticle polymer coating on their ag-
gregation behavior and toxicity to the green algae Dunaliella
salina. Aquat Toxicol 154:176–183. https://doi.org/10.1016
/j.aquatox.2014.05.012
Zhang H, Leung Y, Louden D, De Nys R, Lamb R (2008) The
potential intrinsic and extrinsic toxicity of silica nanoparticles
and its impact on marine organisms. Nano 3:271–278
Zhang L, He YL, Goswami N, Xie JP, Zhang B, Tao XJ (2016a)
Uptake and effect of highly fluorescent silver nanoclusters on
Scenedesmus obliquus. Chemosphere 153:322–331.
https://doi.org/10.1016/j.chemosphere.2016.03.076
Zhang YQ, Dringen R, Petters C, Rastedt W, Koser J, Filser J,
Stolte S (2016b) Toxicity of dimercaptosuccinate-coated and
un-functionalized magnetic iron oxide nanoparticles towards
aquatic organisms. Environ Sci Nano 3:754–767. https://doi.
org/10.1039/c5en00222b
Zhang S, Mao GZ, Crittenden J, Liu X, Du HB (2017a)
Groundwater remediation from the past to the future: a
bibliometric analysis. Water Res 119:114–125. https://doi.
org/10.1016/j.watres.2017.01.029
View publication stats
Page 17 of 17 92
Zhang X, Wang Z, Wang S, Fang H, Zhang F, Wang DG (2017b)
Impacts of dissolved organic matter on aqueous behavior of
nano/micron-titanium nitride and their induced enzymatic/
non-enzymatic antioxidant activities in Scenedesmus
obliquus. J Environ Sci Health Part A Tox Hazard Subst
Environ Eng 52:23–29. https://doi.org/10.1080
/10934529.2016.1221219
Zhao J, Wang ZY, White JC, Xing BS (2014) Graphene in the
aquatic environment: adsorption, dispersion, toxicity and
transformation. Environ Sci Technol 48:9995–10009.
https://doi.org/10.1021/es5022679
Zhao J, Cao XS, Wang ZY, Dai YH, Xing BS (2017) Mechanistic
understanding toward the toxicity of graphene-family mate-
rials to freshwater algae. Water Res 111:18–27. https://doi.
org/10.1016/j.watres.2016.12.037
Zheng TL, Wang J, Wang QH, Meng HM, Wang LH (2017)
Research trends in electrochemical technology for water
and wastewater treatment. Appl Water Sci 7:13–30.
https://doi.org/10.1007/s13201-015-0280-4
Zurutuza A, Marinelli C (2014) Challenges and opportunities in
graphene commercialization. Nat Nanotechnol 9:730–734