bioaccumulation and distribution

Bioaccumulation and distribution of trace elementsin tissues of giant river prawn Macrobrachium rosenbergii Decapoda: Palaemonidae from South Vietnam Nguyen Phuc Cam TU,1Nguyen Ngoc HA,2

Bioaccumulation and distribution of trace elements

in tissues of giant river prawn Macrobrachium

rosenbergii (Decapoda: Palaemonidae) from

South Vietnam

Nguyen Phuc Cam TU,1Nguyen Ngoc HA,2Tokutaka IKEMOTO,2Bui Cach TUYEN,3

Shinsuke TANABE2AND Ichiro TAKEUCHI1*

1Department of Life Environment Conservation, Faculty of Agriculture, Ehime University,

Matsuyama, Ehime 790-8566,2Center for Marine Environmental Studies, Ehime University, Matsuyama, Ehime 790-8577, Japan; and3Nong Lam University, Thu Duc District, Ho Chi Minh City, Vietnam

ABSTRACT: Accumulation profiles of 22 trace elements in abdominal muscle, abdominal

exoskel-eton and the hepatopancreas of the giant river prawn Macrobrachium rosenbergii were analyzed The

giant river prawn is an indigenous freshwater species from South Vietnam, and is cultured commer-cially and fished in the wild Samples were collected from Ho Chi Minh City and the surrounding area (SKEZ, South Key Economic Zone), and from the Mekong River Delta between 2003 and 2005 Highest accumulations of essential (Cu, Se and Mo) and toxic (As, Ag, Cd and Hg) elements were observed in hepatopancreatic tissue, except for Mn, Sr, Sn, Ba and V in the exoskeleton and Rb and

Cs in muscle tissue Spatial differences showed concentrations of Cs and Pb in muscle and Sr in exoskeletons from the SKEZ were higher than those from the Mekong River Delta The opposite trend was observed for Cr, Se and Sb in muscle, Mo, Sb and Tl in exoskeleton, and Se, Hg, Mo, Cd, Sb,

Tl and Bi in the hepatopancreas These differences in trace element concentrations in prawns likely reflect differences in industrialization and human activities between the two regions of South Vietnam

KEY WORDS: exoskeleton, hepatopancreas, Macrobrachium rosenbergii, Mekong River

Delta, muscle, trace elements, Vietnam.

INTRODUCTION

Since the early 1990s, aquaculture in Vietnam has

greatly expanded in total area of production and

the number of target species cultured The level of

management intensity has also increased Of the

shrimp/prawn species cultured in South-East Asia,

the black tiger shrimp Penaeus monodon is

well-known and has become commercially important

to the region In Vietnam and throughout South

and South-East Asia, the giant river prawn

Macro-brachium rosenbergii is gaining importance as a

target species in brackish and freshwater areas

Macrobrachium rosenbergii is indigenous to South

Vietnam, including the South Key Economic Zone

(SKEZ) and the Mekong River Delta.1

The SKEZ, including Ho Chi Minh City and seven surrounding provinces, is the most industrialized area of Vietnam, contributing up to one-third of Vietnam’s gross national product and approxi-mately 40% of gross domestic product (GDP), of which Ho Chi Minh City accounted for 60–65% The GDP per capita of the SKEZ is double that of the Mekong River Delta The Mekong River Delta is

a major agricultural production region of Vietnam contributing over 50 and 60% of the total national rice production and fishery exports, respectively.2,3 However, the rapid growth of urbanization, agri-culture and industry in the southern region has also resulted in increased production and use of harmful substances such as certain trace ele-ments.2,4,5There is a possibility that elevated levels

of trace elements could be harmful to exposed prawns, and that the elements may be transferred

to higher trophic levels in the food web, including humans who consume the prawns

*Corresponding author: Tel: 81-89-946-9899.

Fax: 81-89-946-9899 Email: takeuchi@agr.ehime-u.ac.jp

Received 9 April 2007 Accepted 23 July 2007.

The species M rosenbergii can be used to

monitor the trace element pollution in the aquatic

environment because they are omnivorous

benthic animals6that maintain their body in direct

contact with the water and substrate of their

envi-ronment, and they tend to accumulate metals in

their tissues Previous studies have examined the

accumulation of contaminants in tissues of a

number of freshwater prawn species, and under

different concentrations and times of exposure in

the field (Cd, Cr, Cu, Hg, Ni, Pb and Zn in M

nip-ponensis)7and the laboratory (Cd and Pb in M

ros-enbergii;8Cu, Cr and Zn in M malcolmsonii;9Cd

and Zn in M malcolmsonii;10and Cu in M

rosen-bergii11) It has been shown that elements passively

adsorbed onto the exoskeleton of a crustacean will

contribute to the total body concentration of an

element in the crustacean, and crustaceans can

accumulate trace elements in hepatopancreatic

and edible tissue (muscle).12The present study was

conducted to measure the specific accumulation

of 22 trace elements in tissues of giant river prawns

and to explore geographic variation of the

ele-ments in this commercially important species

MATERIALS AND METHODS

Sampling

Wild-caught giant river prawns Macrobrachium

rosenbergii were purchased directly from local

fishers or from local small markets at the SKEZ (Ho

Chi Minh City and Dong Nai) and the Mekong

River Delta region (Can Tho, Dong Thap, Hau

Giang and Tra Vinh) between September 2003 and

April 2005 The locality of the prawns was verified

prior to the purchases, and the fishers and stall-holders were not informed that purchases would

be made ahead of time At the markets, prawns were sampled from stallholders who bought from the fishers exploiting in river These markets were confirmed to be situated approximately 500–

1000 m from prawn catching areas Prawns were placed in polyethylene bags, transported to Japan, and stored in a deep freezer at-20°C until chemical analysis Sampling locations were noted and indi-vidual body weights of prawns were measured (Table 1 and Fig 1)

Chemical analyses

To analyze tissue-specific concentrations of trace

elements, M rosenbergii were dissected and

tissues of abdominal muscle, the abdominal exosk-eleton and the hepatopancreas were carefully separated from other body organs Trace element concentrations were analyzed based on the

proce-dure described by Kubota et al.13and Nam et al.14 Tissue samples were dried for 12 h at 80°C About 0.2 g of the sample was digested in 5 mL of concen-trated HNO3 in a microwave system for 30 min Levels of 19 trace elements (V, Cr, Mn, Co, Cu, Zn,

Rb, Sr, Mo, Ag, Cd, In, Sn, Sb, Cs, Ba, Tl, Pb and Bi) were analyzed with an inductively coupled plasma–mass spectrometer (ICP-MS) (HP-4500, Hewlett-Packard, Avondale, PA, USA) Matrix effects and instrument drift in the ICP-MS mea-surements were corrected using an internal stan-dard method with yttrium as the internal stanstan-dard Concentrations of Hg and Se were determined using a cold vapor atomic absorption spectrometer (AA680, Shimadzu, Kyoto, Japan; Model HG-3000

Table 1 Sampling locations and biometry of giant river prawn Macrobrachium rosenbergii from South Vietnam

Location Date Latitude Longitude Remarks n Weight†(g) Site 1

Bien Hoa, Dong Nai 16 Apr 2005 10°52.056′ 106°49.894′ River 3 58.7⫾ 31.0 Site 2

District 9, Ho Chi Minh City 17 Apr 2005 10°47.005′ 106°51.578′ Local small market 5 62.5⫾ 44.3 Site 3

District 2, Ho Chi Minh City 17 Apr 2005 10°47.049′ 106°45.288′ Local small market 5 126.8⫾ 76.9 Site 4

Can Tho City, Can Tho 12 Sep 2003 10°01.843′ 105°45.904′ Local small market 3 23.8⫾ 2.1 Site 5

Cao Lanh, Dong Thap 19 Apr 2005 10°24.331′ 105°41.387′ River 3 43.5⫾ 19.3 Site 6

Phung Hiep, Hau Giang 29 Aug 2004 09°48.281′ 105°49.252′ Local small market 3 29.2⫾ 3.4 Site 7

Cau Ngang, Tra Vinh 21 Apr 2005 09°47.510′ 106°27.177′ Local small market 3 55.1⫾ 18.1

cold vapor system, Sanso, Tsukuba, Japan) and a

hydride generation atomic absorption

spectrom-eter (Model HFS-3 hydride system, Hitachi, Tokyo,

Japan), respectively For As analysis, samples were

digested with an acid mixture (HNO3–H2SO4–

HClO4= 1:1:2) and determined by a hydride

gen-eration atomic absorption spectrometer (HVG-1

hydride system, Shimadzu) Accuracies of the

methods were assessed using certified reference

material DORM-2 (National Research Council of

Canada) in triplicate, and recoveries of all the

ele-ments ranged from 87 to 111% of the certified

values All data were expressed on a dry weight

basis (mg/g dry wt)

Statistical analyses

One-half of the value of the respective limit of

detection was substituted for those values below

the limit of detection and used in statistical

analy-sis.15 Data were tested for goodness-of-fit to a

normal distribution with Kolmogorov–Smirnov’s

one-sample test Because concentrations of some

trace elements did not follow a normal

distribu-tion, non-parametric tests were alternatively used

to compare between different groups A Wilcoxon

signed ranks test was used to detect

between-tissue differences in trace element concentrations

Spearman’s rank correlation coefficient was used

to measure the strength of the association between

elements in tissues For testing geographic

differ-ences, log-transformed data were analyzed using

one-way analysis of covariance (ancova) with body

weight as the covariate P< 0.05 was considered to

indicate statistical significance These statistical

analyses were executed by the program SPSS

v10.05 (SPSS, Chicago, IL, USA)

RESULTS Tissue-specific distribution of trace elements

Trace element concentrations in abdominal muscle, abdominal exoskeleton and

hepatopan-creas of M rosenbergii are shown in Tables 2–4,

respectively Zinc and Cu, both essential nutri-ents, had considerably higher concentrations in

all tissues analyzed in M rosenbergii, ranging

from 9.71mg/g Cu in muscle (from Site 4) and 6.01mg/g Zn in the exoskeleton (Site 2) to

17 500mg/g Cu (Site 3) and 141 mg/g Zn (Site 6) in the hepatopancreas Chromium levels ranged from 0.10mg/g in muscle (from Site 3) to 2.3 mg/g

in the hepatopancreas (Site 1) Concentrations of

Mn varied from the lowest level of 0.987mg/g in muscle (Site 3) to a high level of 734mg/g in the exoskeleton (Site 4) The range of Co levels was from 0.013mg/g in muscle (Site 3) to 1.2 mg/g in exoskeleton (Site 2) For Se and Mo, of all tissues analyzed, the hepatopancreas had the highest levels of accumulation

Concentrations of nonessential elements in

M rosenbergii varied widely across tissues Levels

of In, Sb, Pb and Bi were low and undetectable in some samples A significant level of variation in

Cd concentrations among tissues was observed

in M rosenbergii Cadmium levels in muscle, exoskeleton and hepatopancreas of M rosenbergii

were 0.048⫾ 0.065 mg/g, 0.031 ⫾ 0.044 mg/g and 13.5⫾ 14.7 mg/g, respectively Similarly, the highest concentrations of Ag (2.4⫾ 3.6 mg/g, from Site 3) were found in the hepatopancreas Particu-larly, the exoskeleton contained the highest Sr levels (1670⫾ 909 mg/g) among the tissues, which was about 300 times higher than that of muscle with the lowest concentration (5.58⫾ 3.71 mg/g)

Fig 1 Map showing sampling

locations (Sites 1–6) of

Macro-brachium rosenbergii in the

South Key Economic Zone

(SKEZ) and Mekong River Delta,

South Vietnam

† mean

‡ range

§ number

† mean

‡ range

§ number

† mean

‡ range

§ number

Statistical analysis indicated that the highest

proportion of the total internal burden of Cu, As,

Se, Mo, Ag, Cd (Wilcoxon signed ranks test,

P < 0.001) and Hg (P < 0.01) were found in

hepato-pancreatic tissue However, levels of Mn, Sr, Sn, Ba

(P < 0.001) and V (P < 0.05) in exoskeleton, and

concentrations of Rb, Cs and Bi (P< 0.001) in

muscle were the most elevated No significant

dif-ference of Sb and In (P> 0.05) was observed

between the three tissues

Analyses of correlation between trace element

pairs in tissues of M rosenbergii revealed

signifi-cant couplings, particularly in the relationship

between Ag and Cu (Spearman rank correlation

r = 0.70, P < 0.001), Se and Hg (r = 0.40, P < 0.05),

Se and Mo (r = 0.60, P < 0.01), Se and Ag (r = 0.64,

P < 0.001), and Se and Cu (r = 0.70, P < 0.001) in the

hepatopancreas

Regional variation in trace elements

The sites were divided into two regions according

to Vietnamese economic zones:3 SKEZ including

Ho Chi Minh City and Dong Nai, and the Mekong

River Delta including Can Tho, Dong Thap, Hau

Giang and Tra Vinh To compare trace element

con-centrations in M rosenbergii between SKEZ and

the Mekong River Delta, the log-transformed data

were analyzed using ancova, with body weight as

the covariate, because of the dependence of trace

element levels on body weight (data not shown)

Among 22 trace elements, concentrations of Cs

and Pb in muscle and Sr in exoskeleton from the

SKEZ were found to be significantly higher than

those from the Mekong River Delta (ancova,

P< 0.05, Fig 2) In contrast, the Mekong River

Delta samples had higher levels of Cr, Se and Sb in

muscle, Mo, Sb and Tl in the exoskeleton, and Se,

Hg, Mo, Cd, Sb, Tl and Bi in the hepatopancreas

(P< 0.05, Fig 2) No significant difference in

con-centrations of V, Mn, Co, Cu, Zn, As, Rb, Ag, In, Sn

and Ba was found between SKEZ and the Mekong

River Delta (P> 0.05)

DISCUSSION

The present study revealed that Cu, As, Se, Mo, Ag

and Cd were highest in hepatopancreatic tissue of

M rosenbergii In decapod crustaceans, elevated

metal concentrations in hepatopancreatic tissue

suggest that this organ probably functions as a

storage and detoxification site.16–19The

hepatopan-creas has high levels of metallothionein, which can

play a role in metal detoxification.19

Most crustaceans possess hemocyanin, which contains Cu as the main oxygen-carrying blood pigment.20,21 Therefore, the high levels of this element may be related to this pigment Hepato-pancreatic Cu concentrations of these giant river prawns, however, were substantially higher than other decapod crustaceans from other areas reported in the literature.19,22–25 In Penaeus van-namei collected from the Pacific Coast of Mexico,

Cu levels in the hepatopancreas ranged 33.3– 95.3mg/g dry wt.22 Kargin et al.23 reported that

mean Cu levels in the hepatopancreas of Penaeus semiculatus and Metapenaeus monocerus, which

were collected from a polluted area in the Isk-enderun Gulf, Turkey, ranged 854–962mg/g and 619–815mg/g dry wt, respectively In studies of

Fig 2 Comparison of trace element concentrations in (a) muscle, (b) exoskeleton and (c) hepatopancreas of

giant river prawn Macrobrachium rosenbergii between

the South Key Economic Zone (䊐) (Sites 1–3) and the Mekong River Delta (䊏) (Sites 4–7) All trace elements

with a significant difference (P< 0.05) between the two regions are shown in this figure Data are mean and maximal value *, **, significant at 5% and 1%, respectively

heavy metal accumulation in American lobster

Homarus americanus and rock crab Cancer

irrora-tus from the Inner Bay of Fundy, Canada, a highly

Cu-contaminated site, Chou et al.24,25 found Cu

concentrations in the digestive glands were 110–

856mg/g and 8.8–528 mg/g wet wt, respectively

The reported values from those studies are given

in wet weight terms, which are 3–5 times lower

than those for dry weight.25 In exposure studies

using the giant river prawn M rosenbergii, Cu

accumulation in tissues tended to increase with

increased water-borne Cu concentrations and

increase in exposure time.11,26 Moreover, prawns

spend much of their time partially buried in the

soft sediment, and this may be the reason for the

high Cu accumulation in prawns Copper

concen-trations in sediments of Ho Chi Minh City and

the Mekong River Delta were relatively high,

19.4–48.4 mg/kg dry wt and 41–53 mg/kg dry wt,

respectively.4,5 Domestic wastewater is the major

anthropogenic source of Cu in waterways and

sediment is an important sink and reservoir for

Cu.27 Copper in the diet is an important route

of Cu accumulation in aquatic animals, and

food choice influences internal loadings of Cu.28

Further study of the sources of Cu accumulation

in M rosenbergii is necessary to elucidate the

present contamination status and trophic

path-ways leading to bioaccumulation

The high concentrations of Cd in the

hepatopan-creas might be due to its chemical similarity to Ca

Crustaceans with a high physiological demand for

calcium (e.g at postmolt) in a low-calcium

envi-ronment (e.g fresh water) may have an atypically

higher calcium pump activity Hence, the greater

the activity of any such calcium pump, the greater

will be the proportion of total Cd uptake by this

route.29,30 No evidence is currently available on

the regulation of internal Cd concentrations by

decapod crustaceans Using M malcolmsonii in an

exposure study, Vijayram and Geraldine10reported

that tissues accumulated Cd at all exposure levels

and reached the highest concentration at

39.7⫾ 2.57 mg Cd/g (wet wt) in the

hepatopan-creas after 22 days of exposure to 157mg Cd/L In

another exposure study on Palaemon elegans,

White and Rainbow31 showed that accumulation

and not regulation occurred even at low Cd

expo-sures (0.5mg Cd/L)

Relatively higher levels of Ag have been reported

in digestive glands of American lobsters (2.5–

11.5mg/g wet wt),24 rock crabs (0.57–8.24mg/g

wet wt)25and entrails of freshwater fish Carasius

auratus langsdorfii (12mg/g dry wt).32Silver

inter-acts metabolically with Cu in American lobster and

rock crab, in which Ag increases as Cu increases.24,25

This relationship in the hepatopancreas of

M rosenbergii was observed from some sites in

the present study At Site 3, Cu levels were

3950⫾ 7590 mg/g and Ag was 2.4 ⫾ 3.6 mg/g; at Site 2, Cu was 423⫾ 565 mg/g and Ag was 0.79⫾ 1.3 mg/g; at Site 7, Cu was 246 ⫾ 16 mg/g and Ag was 0.62⫾ 0.25 mg/g and at Site 4, Cu was

234⫾ 198 mg/g and Ag was 0.27 ⫾ 0.16 mg/g Nev-ertheless, at Site 1, the relatively elevated Cu value (523⫾ 777 mg/g) was not accompanied by propor-tionally higher Ag values (only 0.081⫾ 0.017 mg/g) compared with the other sites According to Chou

et al.,24the low Ag concentration in this case may

be related to disruption of the Ag–Cu relationship

by other metals, such as Cd, which compete for

protein metal-binding sites In C auratus langs-dorfii, the high Ag content is considered to be

strongly related to its feeding habit This is because

C auratus langsdorfii feeds on benthic plants and

animals in muddy bottom sediments, in which Ag would be highly concentrated.32

In M rosenbergii, Zn was present in large

quan-tities in the hepatic materials (35.7–141mg/g) and muscle (49.9–85.8mg/g) Zinc is an essential element required for many biological processes and is usually stored in phosphorus-rich granules

in the R cells of the hepatopancreas.33There is evi-dence that the ability to regulate internal concen-trations of Zn is a feature of decapod crustaceans

For example, the caridean decapod Palaemon elegans is able to regulate total internal

concentra-tions to approximately 80mg Zn/g dry wt up to a threshold aqueous exposure concentration (between 177 and 316.2mg Zn/L), after which regu-lation breakdown and net accumuregu-lation begins.34

The prawn M malcolmsonii regulates its tissue

concentration of the essential metal Zn to an approximately constant level when exposed to a wide range of dissolved Zn concentrations (26–

653mg/L) until a threshold dissolved concentra-tion (373mg/L) is reached, above which regulation collapses and net accumulation of Zn begins.9 The high concentrations of Mn, Sr and Ba in the exoskeleton might be caused by their chemical similarity to Ca As shown above, giant river prawns with a high physiological demand for calcium in a low-calcium freshwater environment may have a higher calcium pump activity Hence, the greater the activity of any such calcium pump, the greater will be the proportion of total Mn, Sr and Ba uptake

by this route.14,29,30,35–39Vanadate (VO43–and HVO42–) might enter cells by an anionic channel as phos-phate (HPO42–) and becomes bound to intracellular components so that it is not available for return to the medium.30The high concentrations of Rb and

Cs in muscle may be caused by the effects of Rb and Cs ions on muscle tissues, similar to potassium ions.40Yamazaki et al.32and Agusa et al.41have also

reported high Rb and Cs concentrations in muscle

among tissues of several fish species

These inter-element relationships may be

attrib-utable to similar physical or chemical properties of

the elements involved; also, it has been regarded as

indicative of similar biochemical pathways.36Chou

et al.24,25reported that Ag interacts highly with Cu

in American lobster and rock crab, as indicated

above Transition metals such as Hg, Ag and Cd are

known to interact with Se in the body; the toxicity

of both transition metals and Se is reduced by the

interaction.42

The regional-specific results revealed that, of 22

elements, the Mekong River Delta samples had

higher levels of Cr, Se, Sb, Mo, Tl, Hg, Cd and Bi,

while SKEZ samples only had higher levels of Cs,

Pb and Sr The higher concentration of various

elements in the Mekong River Delta suggests that

contamination from several sources, especially Hg

and Cd, exists somewhere in the Mekong River

Delta, even though industrial activities in the

Mekong River Delta are lower than those in the

SKEZ Of the elements higher in the Mekong River

Delta, Hg and Cd are believed to have originated

from agricultural use of mineral fertilizers and

pesticides: phosphate fertilizers are a main source

of cadmium input to agricultural soils The

con-centration of cadmium in phosphate fertilizers

ranges 0.05–170 mg/kg.43 For Hg, approximately

15% of the total Hg is released to the soil from

fer-tilizers, fungicides and municipal solid waste.44

Internal concentrations of the nonessential

metals such as Cd or Hg do not appear to be

regu-lated by any crustacean, decapod or other

inver-tebrates, and follow closely Cd/Hg availabilities in

the medium Therefore, concentrations of Cd/Hg

are more likely to be related to ambient levels of

Cd/Hg.18

The observed discrepancies between the two

regions could also be caused by different metallic

bioavailability in the environment Seasonal

fluc-tuation of salinity is important in these areas,

which influences partitioning and bioavailability

of metals In the Mekong River, salinity intrusion

was observed more than 30 km upstream in March,

but fresh water was found throughout the whole

river in October Trace elements such as As, Co, Cr,

Ni, Pb and Al showed higher concentrations in

March than in October, with an average

two-fold increase.5 In addition, PO43– is an important

constituent of fresh water that reduces

bioac-cumulation of metals Concentrations of PO43– in

the SKEZ ranging 0.1–0.4 mg/L were lower than the

Mekong River Delta (0.8–2 mg/L).45 According to

Guhathakurta and Kaviraj,46high concentrations of

PO43– in water of Malancha (Sunderban, India)

might be responsible for relatively lower

accumu-lations of Zn in shrimp muscle in spite of its high concentration in the sediment

Selenium showed high coaccumulation with Hg and Mo in the giant river prawn, and a similar geo-graphic pattern was observed This result is in agreement with observations of marine fauna from Greenland.47

Of the elements with higher concentrations in the SKEZ, pollution sources for the element Pb may have occurred from higher motorized traffic activ-ity Automobile exhausts are one of the main Pb pollution sources Exhaust gases from motorized vehicles usually diffuse and are diluted over a wide area With a large increase in automobile traffic in

Ho Chi Minh City and its surrounding area, the amount of Pb in the water environment from pol-luted air has increased substantially.2,4

The human health risk estimations, using US Environmental Protection Agency Region III risk-based concentration table,48 indicated that con-sumption of giant river prawns from these areas were not harmful to consumers

To our knowledge, this is the first report on accu-mulation profiles of trace elements in tissues of the giant river prawn from Vietnam Our results indi-cate potential sources of contamination by Hg and

Cd in the Mekong River Delta, and Pb and Cs in the

Ho Chi Minh City metropolitan area The geo-graphic differences in contamination patterns of the trace elements likely reflect differences in agri-cultural and urban- and industrial-related activity Further studies are necessary to elucidate the sources of contamination and possible implica-tions of toxic trace elements on aquatic ecosystems and human health in the Mekong River Delta

ACKNOWLEDGMENTS

We express sincere thanks to Dr T.B Minh and Dr

T Miller for critical review of the manuscript The study was partially supported by a grant from Research Revolution 2002 (RR2002) of the Project for Sustainable Coexistence of Human, Nature and the Earth (FY2002) from the Ministry of Education, Culture, Sports, Science and Technology, Japan and

a Research Grant-in-Aid for Scientific Research from the Japan Society for Promotion of Science (No 16310042)

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