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Nonylphenol NP is a widespread contaminant in the ecosystem Zinc is Paper

Words: 2542, Paragraphs: 230, Pages: 9

Paper type: Essay , Subject: Stem Cells

Nonylphenol (NP) is a widespread contaminant in the ecosystem. Zinc is an essential trace element with many

physiological activities. The existing study aimed to examine the possible favorable role of zinc sulfate against

the immunosuppressive, hepatotoxic and nephrotoxic effects of NP in Oreochromis niloticus (O. niloticus). Two

hundred and twenty-five tilapia fish were categorized into control, vehicle control, zinc sulfate (0.5 mg/L water),

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NP (50 ?g/L water), and zinc sulfate+NP groups with 3 weeks period of exposure. Selective liver and kidney

damaging byproducts, immunological, oxidative stress, lipid peroxidation, hematological, and inflammatory

biomarkers were monitored as well as histopathological examinations were performed. The results revealed that

NP induced hemolytic anemia, leukocytosis, hyperbilirubinemia, hyponatremia, hyperkalemia, azotemia, hyperproteinemia,

hypoalbuminemia, hyper alpha1-globulinemia, hyper alpha2- and beta-globulinemia, and hypo

gammaglobulinemia. Also, significantly elevated levels of ALT, AST, LDH, ammonia, cholesterol, creatinine,

MDA, MPO, and TNF-alpha were recorded. Meanwhile, ALP, IgM, complement3, and NO levels together with

lysozyme activity were significantly declined. Additionally, damage of hepatic and renal structural with splenic

lymphoid depletion was also noted. On the contrast, Addition of zinc sulfate into the water restored the disturbances

in most of those indicators elicited by NP. It is concluded that zinc sulfate has ameliorative action

against hematotoxic, hepatotoxic, nephrotoxic, and immunosuppressive impacts of NP in Nile tilapia fish.

1. Introduction

Tilapia is possibly the most important freshwater aquaculture species

worldwide. The increasing scale of production requires new accurate

and efficient tools to screen and monitor the health status of these

fish (El-Houseiny et al., 2015). Nonylphenol (NP) is the main biodegradation

product of nonylphenol polyethoxylate and has been known

as one of the most common environmental endocrine-disrupting compounds

(EDCs). Currently, NP has been used as modifiers and emulsifiers

in pesticides, paints, plasticizers, textiles and various personal care

products, and antioxidants in resins and plastics (Liu et al., 2015). Because

of its extensive usage, a huge quantity of NP was released into

ecosystem compartments including soil, river water, sediments, atmosphere

and biosphere (Liu et al., 2017; Soares et al., 2008; Vazquez-

Duhalt et al., 2005). For instance, the NP levels were in the range of

2–336 ?g/L in British rivers (Blackburn et al., 1999), 0.3–45 ?g/L in

Swiss rivers (Ahel et al., 1994a,b), and 3–300 ?g/L in Canadian rivers

(O’halloran et al., 1999). Also, in the USA, levels of NP found in sewage

effluent were up to 12 mg/L (Hale et al., 2000).

In the water policy field, NP has been recognized as priority hazardous

materials by the European Community Water Framework

(Todo and Sato, 2002). The non-biodegradable nature, long persistence

in the environment, and its biomagnification over the food chain leads

to considerable attention towards NP as a main worldwide hazardous

aquatic contaminant (Rivero et al., 2008).

Many adverse impacts were documented on fishes exposed to NP

like genotoxicity (Al-Sharif, 2012), neurotoxicity (Jones et al., 1998;

Ton et al., 2006), altered social behavior (Xia et al., 2010), thyrotoxicosis

(Naderi et al., 2014, 2015), immunosuppression (Sharma, 2015),

hemotoxicity (Madhu and Pooja, 2015), hepatotoxicity (Abd-Elkareem

et al., 2018; Midhila and Chitra, 2015; Naderi et al., 2012), testicular

damage (Sayed and Ismail, 2017), nephrotoxicity (Kotb et al., 2018),

altered respiration and embryonic development (Sayed et al., 2012a;

Sharma et al., 2018). Also, NP has been found to induce overstimulation

of reactive oxygen species (ROS) production and antioxidant enzymatic

system depletion, apoptosis, and DNA fragmentation (Sayed and

Received 15 September 2018; Received in revised form 27 January 2019; Accepted 3 February 2019

? Corresponding author.

E-mail address: [email protected] (Y.M. Abd-Elhakim).

Aquaculture 504 (2019) 227–238

Available online 04 February 2019

0044-8486/ © 2019 Elsevier B.V. All rights reserved.


Soliman, 2018; Sayed and Hamed, 2017; Sayed and Ismail, 2017; Sayed

et al., 2016, 2018a,b).

Zinc is an essential nutritional trace element which promotes

growth and plays a vital role in numerous cellular functions comprising

cell proliferation, co-factor reproduction, immune function and guard

against free radicals (Powell, 2000; Tammy et al., 1990). It plays a vital

role for both genetic function and stability (Dreosti, 2001). Zinc acts as

cofactors for several metabolic pathways in various enzymatic systems

and is also a chief element of a great number of metalloenzymes like

carboxypeptidase, carbonic anhydrase, glutamic dehydrogenase, D-superoxide

dismutase, and alcohol dehydrogenase (Salgueiro et al.,

2000). Zinc has antioxidant and anti-inflammatory activities (Jarosz

et al., 2017).

Normal zinc levels in freshwater (Spry et al., 1988) and seawater

(Willis and Sunda, 1984) are known to be insufficient to cover the needs

of growing aquatic species. Hence, zinc is regarded as an essential nutrient

in fish feeds (National Research Council, 2011; Wei et al., 1999).

Recently, Kumar et al. (2017) reported that dietary zinc safeguards fish

against numerous stresses. Nevertheless, it may also become hazardous

to aquatic organisms on high levels (Bielmyer et al., 2012). Zinc is one

of the most common contaminants in aquatic systems and is associated

with urban runoff, soil erosion, industrial discharges, pharmaceuticals,

pesticides and a variety of other activities and sources (Bowen et al.,

2006; Schmitt, 2004). Fresh water fish could accumulate high zinc levels

via the skin and gills tissues as the gills play an important role in

metal uptake, storage, and eventually transfer to the internal compartments

via blood transport (Abdel-Tawwab et al., 2016; Murugan

et al., 2008).

On the contrary to the terrestrial environment, organisms present in

the aquatic environment are exposed to more complex mixtures of

chemicals. These mixtures present in aquatic environment may elicit

toxicity due to synergistic effects among the constituents or vice versa,

the adverse outcome may be diminished by antagonistic interactions.

Hence, the water-born NP and zinc exposure regimes have been employed

in the present study to evaluate the outcomes of their co-exposure

on the immunity, liver, and kidney of Nile tilapia. Consequently,

the existing study aimed to test the former hypothesis by biochemically

evaluating indicators of the innate and humoral immune system, liver

Fig. 1. Post-mortem changes of fish exposed to nonylphenol and/or zinc sulfate. NP-exposed fish showed dermal hemorrhage with scales loss (A), slimness, congested

gills (blue arrow), congested liver (red arrow), dermal hemorrhage (black arrow), and inflamed and distended intestine (star) (B). But, fish exposed to zinc sulfate (C

and D) or NP+ zinc sulfate (E and F) showed normal external features of the internal organs. (For interpretation of the references to colour in this figure legend, the

reader is referred to the web version of this article.)

Table 1

Hematological changes of Nile tilapia exposed to nonylphenol (NP) (50 ?g/L) and/or zinc sulfate (ZnSO4) (0.5 mg/L water) for 3 weeks.

Control Vehicle control ZnSO4 NP ZnSO4+ NP

RBCs (?106/?l) 2.79a ± 0.029 2.83a ± 0.023 2.80a ± 0.008 1.22c ± 0.065 1.78b ± 0.072

Hb (g/dl) 9.00a ± 0.11 9.00a ± 0.20 8.76a ± 0.21 3.23c ± 0.14 5.50b ± 0.28

PCV (%) 31.33a ± 0.88 2.33a ± 0.88 31.66a ± 0.33 17.00c ± 0.57 23.00b ± 0.57

MCV (fl) 112.12b ± 1.95 113.95b ± 2.46 112.81b ± 0.86 138.91a ± 3.29 129.30a ± 5.17

MCHC (%) 28.74a ± 0.44 27.83a ± 0.12 27.70a ± 0.98 19.03c ± 0.82 23.91b ± 1.09

WBCs (?103/?l) 4.29c ± 0.17 4.29c ± 0.15 4.36c ± 0.08 8.41a ± 0.37 6.03b ± 0.36

Lymphocytes (?103/?l) 2.11c ± 0.066 2.14c ± 0.028 2.12c ± 0.043 4.19a ± 0.020 2.80b ± 0.091

Heterophils (?103/?l) 1.18c ± 0.118 1.13c ± 0.158 1.26c ± 0.061 2.72a ± 0.276 2.00b ± 0.000

Eosinophils (?103/?l) 0.34a ± 0.020 0.35a ± 0.012 0.32a ± 0.014 0.34a ± 0.037 0.35a ± 0.032

Monocytes (?103/?l) 0.65b ± 0.026 0.66b ± 0.014 0.65b ± 0.028 1.14a ± 0.078 0.86ab ± 0.260

RBCs: red blood cells; Hb: hemoglobin; PCV: packed cell volume; MCV: Mean corpuscular volume; MCH: mean corpuscular hemoglobin; MCHC: mean corpuscular

hemoglobin concentration; WBC: white blood cells. A one-way analysis of variance (ANOVA) followed by Duncan’s Multiple Range test was used for statistical

analysis. Means within the same row carrying different superscripts (a,b,c) are significantly different at p < .05. The values shown are means ± SE. n=10.

W.A.M. Mohamed et al. Aquaculture 504 (2019) 227–238


and kidney functions, oxidative stress, lipid peroxidation, and inflammation.

Additionally, a histopathological and histochemical evaluation

has been performed to assess probable antagonistic actions of

zinc on NP-induced liver, kidney, and spleen dysfunctions.

2. Material and methods

2.1. Test compounds, reagents, and chemicals

Nonylphenol (NP) was purchased from Sigma-Aldrich Co. (St. Louis,

MO, USA). A stock solution was prepared by dissolving NP in acetone,

diluted to concentrations of 50 ?g/L, and stored in the dark at 4 °C. Zinc

sulfate (ZnSO4·7H2O, Merck) dissolved in distilled water was used. In

each aquarium, the total of zinc sulfate to be added was calculated after

the volume of each aquarium was exactly determined. All other reagents,

chemicals, and stains used were purchased from (Sigma, St.

Louis, MO) and were of analytical grade.

2.2. Fish and experimental design

Two hundred and twenty-five (25 ± 0.05 g average body weight

and 1.67 ± 0.13 average condition factor) apparently healthy

Oreochromis niloticus fish were obtained from Abbassa fish hatchery,

Sharkia, Egypt. The fish were acclimated for 2 weeks before the

beginning of the experiment. Fish were allocated into five groups, each

group had three replicate (15 fish/replicate). Group1 was kept as a

control without any treatment in water, group2 was kept as solvent

control (acetone), group3 was exposed to zinc sulfate at dose 0.5 mg/L

water, group 4 was exposed to NP at a dose level of 50 ?g/L water

(equal to 1/28 of LC50–96 h of NP) (Naylor, 1995), group 5 was exposed

to both NP and Zinc sulfate at the previously mentioned doses. The

exposure continued for 3 weeks. The dose of zinc sulfate was chosen

based on a pilot study of different doses ranging from 3 to 0.5 mg/L

(data not shown). The water parameters were within the recommended

ranges during the experiment (pH=7.2 ± 0.5; ammonia=0.02 ±

0.001 mg/L, nitrite=0.017 ± 0.001 mg/L; dissolved oxygen

6.55 mg/L; water temperature 24 °C; photoperiod 12:12 light: dark).

The water was completely changed every 48 h. by transferring the fish

to freshly prepared both NP and ZnSO4 solutions. Fish were fed at the

rate of 3% of fish live body weight two times daily at 9:00 and 16:00 h.

The amount of feed was readjusted every week according to the biomass

of each replicate. Throughout the experiment, the uneaten feed

was collected by siphoning. The proximate analysis of basal diet indicated

38.9% crude protein, 10.5% crude lipid, and 3.68% fiber according

to NRC (2011). This protocol was approved by the Ethics of

Animal Use in Research Committee of Zagazig University, and experimental

procedures were done in accordance with the NIH general

guidelines for the Care and Use of Laboratory Animals in scientific

Table 2

Immunological response as well as liver and kidney function tests of the serum of Nile tilapia exposed to nonylphenol (NP) (50 ?g/ L) and/or zinc sulfate (ZnSO4)

(0.5 mg/L water) for 3 weeks.

Control Vehicle control ZnSO4 NP ZnSO4+ NP

IgM (?g/ml) 236.33a ± 1.20 235.00a ± 2.30 236.00a ± 1.73 189.66c ± 2.40 213.00b ± 6.42

Lysozyme (?g/ml) 18.66a ± 1.20 20.33a ± 0.88 18.33a ± 1.20 7.00c ± 1.15 13.33b ± 0.88

NO (?mol/l) 49.00a ± 2.08 50.33a ± 0.88 48.66a ± 3.28 21.33c ± 0.88 37.66b ± 1.45

Complement3 (?g/ml) 107.00a ± 2.64 106.66a ± 1.45 106.66a ± 3.48 62.00c ± 1.52 85.33b ± 2.72

ALT (U/L) 13.00c ± 0.57 14.00c ± 2.64 12.33c ± 1.85 63.33a ± 2.33 35.66b ± 2.40

AST (U/L) 28.66c ± 1.85 28.33c ± 1.85 30.33c ± 1.85 50.33a ± 0.88 39.66b ± 1.45

LDH (U/L) 1489.33c ± 4.97 1488.33c ± 0.88 1482.33c ± 8.81 1818.66a ± 39.63 1605.33b ± 6.33

ALP (IU/L) 23.00a ± 1.15 22.66a ± 3.48 23.33a ± 1.76 17.00c ± 1.52 25.00b ± 2.51

Ammonia (?g/dl) 228.00c ± 3.78 228.00c ± 1.52 228.00c ± 1.52 312.66a ± 4.05 272.00b ± 3.21

Total bilirubin (mg/dl) 0.30c ± 0.02 0.30c ± 0.05 0.29c ± 0.02 0.98a ± 0.01 0.61b ± 0.01

Cholesterol (mg/dl) 196.00c ± 3.21 198.33c ± 1.20 198.33c ± 2.60 285.33a ± 2.72 244.33b ± 2.33

Urea (mg/dl) 2.80c ± 0.23 2.83c ± 0.11 2.90c ± 0.12 9.46a ± 0.18 5.20b ± 0.11

Creatinine (mg/dl) 0.44c ± 0.02 0.46c ± 0.02 0.46c ± 0.03 0.93a ± 0.02 0.59b ± 0.03

Sodium (mEq/L) 152.66a ± 1.45 152.00a ± 2.08 155.00a ± 5.03 103.66c ± 2.33 127.33b ± 2.33

Potassium (mEq/L) 3.13c ± 0.20 3.20c ± 0.25 3.16c ± 0.26 8.40a ± 0.26 5.16b ± 0.12

IgM: immunoglobin M; ALT: alanine aminotransferase; AST: aspartate transaminase; LDH: lactate dehydrogenase; ALP: Alkaline phosphatase. A one-way analysis of

variance (ANOVA) followed by Duncan’s Multiple Range test was used for statistical analysis. Means within the same row carrying different superscripts (a, b, c) are

significantly different at p < .05. The values shown are means±SE. n=10.

Table 3

Oxidative, inflammatory biomarkers and electrophoretic pattern of serum proteins of Nile tilapia exposed to nonylphenol (NP) (50 ?g/ L) and/or zinc sulfate (ZnSO4)

(0.5 mg/L water) for 3 weeks.

Control Vehicle control ZnSO4 NP ZnSO4+ NP

MDA (nmol/ml) 11.03c ± 0.43 10.90c ± 0.37 11.10c ± 0.36 32.73a ± 1.09 20.70b ± 0.52

SOD (U/ml) 4.16a ± 0.42 4.10a ± 0.47 3.96a ± 0.59 0.92b ± 0.02 2.10b ± 0.15

GPX (U/L) 155.33a ± 4.17 158.66a ± 3.52 158.33a ± 2.40 107.00c ± 2.88 136.66b ± 2.60

CAT (U/L) 74.00a ± 0.57 73.66a ± 0.88 73.00a ± 1.15 50.33c ± 0.33 63.33b ± 0.33

TNF-? (pg/ml) 16.36c ± 0.49 16.56c ± 0.33 16.40c ± 0.60 43.83a ± 1.49 24.73b ± 2.29

MPO (U/L) 73.66c ± 1.45 76.66c ± 1.85 74.00c ± 2.08 115.66a ± 2.40 91.66b ± 1.20

Total proteins (g/dl) 6.00c ± 0.11 6.10c ± 0.11 5.96c ± 0.37 8.26a ± 0.17 7.16b ± 0.08

Albumin (g/dl) 2.96a ± 0.08 3.26a ± 0.23 2.70a ± 0.26 0.79c ± 0.02 1.73b ± 0.17

Total globulins (g/dl) 3.03c ± 0.03 3.16c ± 0.12 3.26c ± 0.12 7.47a ± 0.16 5.43b ± 0.08

? 1 globulin (g/dl) 0.45c ± 0.10 0.54c ± 0.02 0.67c ± 0.08 2.72a ± 0.24 1.83b ± 0.01

? 2 globulin (g/dl) 0.52c ± 0.02 0.53c ± 0.02 0.56c ± 0.01 1.89a ± 0.01 1.32b ± 0.10

? globulin (g/dl) 0.71c ± 0.01 0.72c ± 0.02 0.76c ± 0.01 2.16a ± 0.08 1.39b ± 0.13

? globulin (g/dl) 1.33a ± 0.12 1.36a ± 0.12 1.26ab ± 0.21 0.73c ± 0.01 0.88bc ± 0.02

MDA: malondialdehyde; SOD: super oxide dismutase; GPx: glutathione peroxidase; CAT: catalase; TNF-?: tumor necrosis factor-alpha; MPO: myeloperoxidase; NO:

nitric oxide. A one-way analysis of variance (ANOVA) followed by Duncan’s Multiple Range test was used for statistical analysis. Means within the same row carrying

different superscripts (a, b, and c) are significantly different at p < .05. The values shown are means ± SE. n=10.

W.A.M. Mohamed et al. Aquaculture 504 (2019) 227–238



2.3. Sampling

At the end of exposure (3 weeks), blood samples were collected from

fish caudal vein and were divided into two parts. The first part was

collected into plain, clean, and sterile centrifuge tubes without anticoagulant

to separate serum for biochemical analysis to assess the immunological

response, liver, and kidney functions, electrophoretic

pattern of serum proteins as well as oxidative and inflammatory status.

The second part was taken at EDTA tubes for complete blood cells count

picture. Moreover, liver, kidney, and spleen specimens were freshly

collected, post-mortem lesions were recorded, and organs were fixed for

48 h in 10% neutral buffered formalin for histopathological and histochemical


2.4. Blood cells count picture

Red blood cells count, hemoglobin (Hb) concentration, packed cell

volume (PCV), mean corpuscular volume (MCV), mean cell hemoglobin

concentration (MCHC), and white blood cells counts were assessed by

using an automated blood cell analyzer of Sysmex XT-2000iVKobe

(Japan) (Harvey, 2012). Giemsa-stained blood smears were prepared

for differential leukocytic count including lymphocytes, heterophils,

eosinophils, basophils, and monocytes (Dacie and Lewis, 1984).

2.5. Immunological response, liver and kidney function tests

Selective immunological parameters such as IgM and complement3

were measured using fish specific ELISA kits according to the instruction

of the manufacturer. Meanwhile, lysozyme activity in the serum

was measured with spectrophotometry (Ellis, 1990). Nitric oxide (NO)

was measured following the methods of Montgomery and Dymock

(1961). Liver and kidney injury byproducts [alanine (ALT), and aspartate

(AST) aminotransferases, alkaline phosphatase (ALP), lactate

dehydrogenase (LDH), ammonia, total bilirubin, cholesterol, urea,

creatinine, sodium, and potassium] were measured in serum using the

kits of Spinreact (Esteve De Bas,Girona,Spain) according to the methods

of Murray (1984), Burtis and Ashwood (1994), Wenger et al. (1984),

Pesce (1984), Neely and Phillipson (1988), Martinen (1966), Naito

(1984), Kaplan (1984), Fossati et al. (1983),Trinder (1951), and

Hillmann and Beyer (1967) respectively.

About the author

This sample is completed by Emma with Health Care as a major. She is a student at Emory University, Atlanta. All the content of this paper is her own research and point of view on Nonylphenol NP is a widespread contaminant in the ecosystem Zinc is and can be used only as an alternative perspective.

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