PertanikaJ. Trop. Agric. ScL 28(1): 41 - 47 (2005) ISSN: 1511-3701© Universiti Putra Malaysia Press

Cadmium, Copper, Lead and Zinc Levels in the Green-lipped Mussel Pernaviridis (L.) from the West Coast of Peninsular Malaysia: Safe as Food?

*YAP, C. K., ISMAIL, A. & TAN, S. G.Department of Biology, Faculty of Science

Universiti Putra Malaysia43400 UPM, Serdang, Selangor, Malaysia

Keywords: Safety of mussel consumption, heavy metals, Perna viridis^ Malaysia

ABSTRAK

Kupang Perna viridis telah disampel di antara tahun 2002-2004, daripada 10 lokasi di pantai baratSemenanjung Malaysia. Sampel-sampel tersebut dianalisis untuk kadmium (Cd), kuprum (Cu), plumbum (Pb)dan zink (Zn). Kepekatan logam (fig/g berat kering) adalah di antara 0.11-5.55 bagi Cd, 3.49-31.1 bagi Cu,1.1&18.62 bagi Pb dan 60.51 A 19.5 ]Xg/g bagi Zn. Dari segi kesihatan pandangan umum, kepekatan logamadalah di bawah tahap maksimum yang dibenarkan oleh Peraturan-peraturan Makanan Malaysia (1985) danjuga di bawah standard antarabangsa median yang dianggap berbahaya mengikut FAO oleh Bangsa-bangsaBersatu. lNon-carcinogenic hazard indices' bagi logam di dalam kupang menunjukkan pemakanan kupang-kupang di dalam kajian ini adalah tidak berbahaya dan risiko pemakanan adalah bergantung pada jumlahkupang yang dimakan dan tempat di mana mereka diambil.

ABSTRACT

Green-lipped mussels, Perna viridis, were collected between 2002-2004, from 10 locations on the west coast ofPeninsular Malaysia. The samples were analysed for cadmium (Cd), copper (Cu), lead (Pb) and zinc (Zn). Themetal concentrations (\ig/g dry weight) ranged from 0.11 to 5.55 for Cd, 3.49 to 31.1 for Cu, 1.16 to 18.62for Pb and 60.51 to 119.5 for Zn. From the public health point of view, these metal concentrations were belowthe maximum permissible levels set by the Malaysian Food Regulations (1985) and were also below the levelsregarded as harmful according to the median international standards for metals in mollusks compiled by the FAOof the United Nations. Non-carcinogenic hazard indices of the metals in the mussels in this present study showedthat the consumption of the mussels was not risky and any risk is dependent on the amount of mussels consumedand the sites they were collected from.

INTRODUCTION

The west coast of Peninsular Malaysia has alwaysbeen an interesting area for investigationespecially for chemical pollution since the areais likely to receive impacts from man-inducedactivities such as urbanisation, industrialisationand other land-based activities (Hamzah 1997;Yap et al. 2002). To monitor the sustainablenatural resources from the Straits of Malacca, aneasy and practical way to fulfill such a purpose isto develop a biomonitoring agent for the westcoast of Peninsular Malaysia. Ismail et al. (2000)suggested the green-lipped mussel Perna viridis

as a potential biomonitor of heavy metals for thearea. The idea of using marine mussels as abiomonitoring agent for Malaysian coastal watersis prompted by the many studies conductedusing the blue mussel Mytilus edulis. This is dueto the practice of using mussels as biomonitoringagents of heavy metals for coastal watersdeveloped by Goldberg in 1975 and used untiltoday (Nicholson and Szefer 2003; Yap et al.2003; 2004). One of the attributes that has ledto the use of marine mussels as a biomonitoringagent for heavy metals is that they arecommercially important seafood species

Corresponding author:yapckong@hotmail com

YAP, C.K., ISMAIL, A. 8c TAN, S.G.

worldwide (Goldberg 1975; Phillips and Rainbow1993). Other attributes as to why mussels areoften chosen for biomonitoring studies are thatthey are sedentary organisms, long-living, easilyidentified and sampled, reasonably abundantand available throughout the year, and tolerantof natural environmental fluctuations andpollution. Besides, they have good netaccumulation capacities and they are importantecologically. In this region, reports on the use ofthe mussel P. viridis as a biomonitoring agentfor heavy metals had been published fromThailand (Sukasem and Tabucanon 1993),Indonesia (Hutagalung 1989), India(Senthilnathan et al 1998) and Hong Kong(Wong et al 2000). In Malaysia, studies on heavymetals in P. viridis have been conducted bySivalingam and Bhaskaran (1980), Sivalingam(1985), Devi (1986), Liong (1986), Ismail (1993),Ismail et al (2000) and Yap et al (2003; 2004).

This paper reports the concentrations ofcadmium (Cd), copper (Cu), lead (Pb) and zinc(Zn) in the total soft tissues of P. viridis collectedfrom 10 sites on the west coast of PeninsularMalaysia in order to determine the safety of theedible mussels from the human health point ofview. The determination was based oncomparison with the permissible levels set by theMalaysian Food Regulations (1985) and medianinternational standards for metals in molluskscompiled by the Food and AgriculturalOrganization (FAO) of the United Nations(California EPA 2005) besides other food safetyguidelines. In addition, the metal concentrationsin the soft tissues of mussels were particularlyassessed based on the non-carcinogenic hazardindex established by Wong et al (2000), sincethey were consumed by human.

MATERIALS AND METHODS

The sampling locations are shown in Fig. 1. Thesampling was conducted between 2002 and 2004,from Bagan Tiang (in the northern part) toKuala Belungkor (in the southern part) ofPeninsular Malaysia. The samples were stored inclean plastic bags and brought back to thelaboratory in an ice compartment. In thelaboratory, the samples were kept at -10°C untilanalysis. Before dissection, the mussel sampleswere thawed at room temperature (27°C) and20 relatively similar sized mussels from each sitewere selected and analysed for Cd, Cu, Pb andZn. The soft tissues from the mussels were

dissected by removing the byssus and the shell.Soft tissues were dried in an oven at 105°C untilconstant dry weight (Mo and Neilson 1994).The dried soft mussel tissues were digested inconcentrated HNO3 (AnalaR grade, BDH 69%).They were placed in a hot-block digester first atlow temperature for one hour and then fullydigested at high temperature (140°C) for atleast 3 hours. The digested samples were thendiluted to a certain volume with double distilledwater (DDW). After filtration, the preparedsamples were determined for heavy metals by anair-acetylene flame atomic absorptionspectrophotometer (AAS) Perkin-Elmer Model4100. The data are presented in jUg/g dry weight.To avoid possible contamination, all glasswareand equipment used were acid-washed.Procedural blanks and quality control samplesmade from the standard solutions for Cd, Cu,Pb and Zn were analysed once for every fivesamples in order to check for accuracy.Percentages of recoveries for the analysis were110% for Cd, 96% for Cu, 92.5% for Pb and92% for Zn. The dry weight basis was convertedinto the wet weight basis by using a conversionfactor of 0.17 (Yap 1999).

Calculation of Non-Carcinogenic RiskFor the public hazard assessment of musselconsumption, the non-carcinogenic hazard indexwas determined. The non-carcinogenic hazardindex is expressed in terms of the ratio of anindividual's exposure to the defined maximumlevel of exposure. The mean concentrations ofheavy metals in all mussel populations weredetermined and were used to calculate the non-carcinogenic hazard index, according to Wonget al (2000). The formula is given as:

XT . chronic daily intakeNon-carcinogenic = 7-

reference dose

Hazard Index

The reference doses for Cd, Cu, Pb and Zn usedin this study were 20, 2000, 100 and 10,000 //g,according to Wong et al (2000).

RESULTS AND DISCUSSION

The concentrations of Cd, Cu, Pb and Zn arepresented in Table 1. The metal concentrationsranged from 0.11 to 5.55 Mg/g dry weight (0.02to 0.94 /ig/g wet weight) for Cd, 3.49 to 31.1

42 PERTANIKAJ. TROP. AGRIC. SCI. VOL. 28 NO. 1, 2005

CD, CU, PB & ZN LEVELS IN P. VIRIDIS (L.) FROM THE WEST COAST OF PENINSULAR MALAYSIA

" SOUTH CHINA SEA

V

Sampling sitesA)B)C)

B. TiangP. PanjangT. Emas

D) MerlimauE)F)G)

SebatuP. JawaPontian K.

H) P. LidoI)J)

K. Pasir PutehK. Belungkor

INDONESIASINGAPORE

101° 103°

Longitude-EastFig. 1: Sampling sites o /Perna viridis in the coastal waters of Peninsular Malaysia

fjg/g dry weight (0.59 to 5.28 jUg/g wet weight)for Cu, 1.16 to 18.62 ^g/g dry weight (0.20 to3 1 7 JJg/g wet weight) for Pb and 60.51 to 119.5/xg/g dry weight (10.29 to 20.32 flg/g wet weight)for Zn (Table 1).

In the present results, the metalconcentrations in the mussel samples from thewest coast were within the ranges reported byIsmail et al (2000) for mussels. The data inTable 1 were compared to the results from thesame locations in the previous collections donein 1998-2001 (Yap et al 2003). It was found thatthe concentrations of the investigated metals inthe mussels from the present study were generallyhigher than those reported in our previous study.Sukasem and Tabucanon (1993) suggested thatthe difference in metal levels from two periodsof sampling could be explained by the time ofsampling. The samples of 1998 were collectedduring the rainy season (September toDecember) while samples taken in 2000 were

obtained just at the end of the rainy season(January-April). However, little local informationon heavy metal variations due to rainy season isavailable. Therefore, this conclusion can only beconfirmed by further studies.

After conversion of the dry weight data intothe wet weight basis, the metal levels in P. viridisfound in this study were lower than those of themaximum permissible levels of heavy metals infood set by the Malaysian Food Regulations(1985) (Table 1). Our mean values (Mg/g wetweight) of these metals from all the populationswere lower than the limits for Cd (1.00 Jig/g wetweight), Cu (30.0 //g/g wet weight), Pb (2.00Mg/g w e t weight) and Zn (100 //g/g wet weight).

The metal levels were also lower than therecommended guidelines for Cd, Cu, Pb and Znset by the Ministry of Public Health of Thailand(MPHT 1986), the Australian Legal Requirementfor food safety (NHMRC 1987) and the limitsestablished by the Brazilian Ministry of Health

PERTANIKAJ. TROP. AGRIC. SCI. VOL. 28 NO. 1, 2005 43

YAP, C.R., ISMAIL, A. & TAN, S,G.

TABLE 1Ranges of Cd, Cu, Pb and Zn concentrations (mean [fig/g] ± standard error [SE]) in the total soft

tissues of Perna viridis collected from the west coast of Peninsular Malaysia

A.

B.

C.

D.

E.

F.

a

H.

L

J.

Bagan Tiang

P. Panjang

Telok Emas

Merlimau-1

Merlimau-2

Sebatu-1

Sebatu-2

Parit Jawa

Pontian Kecil

P. Lido

K.Pasir Puteh

K. Belungkor

Date of sampling

ll-Apr-02

19-Feb-04

09-Apr-04

18-Apr-02

09-Apr-04

19-FeW)2

19-Fet>02

09-Apr-04

17-Apr-02

17-Apr-O2

17-Apr-O2

18-Apr-02

Shell length (mm)

135.0 ± 10.2Wet

82.15 ± 0.99Wet

84.7 ± 0.69Wet

6.79 ± 0.09Wet

82.5 ± 1.15Wet

62.9 ± 0.78Wet

63.0410.81Wet

77.18±4.59Wet

7.89 ±0.13Wet

89.08 ± 2.60Wet

92.84 ± 3.21Wet

63.4 ± 1.10Wet

Dry2.40

Dry1.51

Dry0.59

Dry1.88

Dry1.52

Dry2.67

Dry1.63

Dry2.00

Dry1.79

Dry2.43

Dry5.28

Dry1.35

Cu

14.14

8.89

3.49

11.07

8.94

15.72

9.57

11.75

10.554

14.27

31.09

7.96

SE

1.7711.18

0.9720.32

0.0017.36

0.9515.07

0.6719.02

1.9917.92

0.5110.29

0.1816.65

1.0511.61

1.5817.94

2.4811.88

0.9814.66

Zn

65.75

119.50

102.13

88.64

111.86

105.38

60.51

97.97

68.03

105.52

69.89

86.26

SE

4.880.05

18.450.07

14.680.25

8.640.38

2.140.25

6.190.33

4.270.06

1.400.39

3.530.02

23.210.07

5.070.94

16.770.02

Cd

0.32

0.44

1.47

2.24

1.46

1.95

0.35

2.31

0.14

0.43

5.55

0.11

SE

0.091.75

0.080.20

0.430.67

0.672.38

0.140.43

0.563.17

0.041.87

0.111.23

0.0011.12

0.141.03

1.052.01

0.020.47

Pb

10.32

1.16

3.92

13.99

2.53

18.62

11.01

7.26

6.56

6.09

11.85

2.78

SE

3.73

0.02

1.20

2.80

0.99

2.17

0.00

4.59

0.85

1.71

1.24

1.32

Note: Alphabets follows those indicated in Fig. 1.

(ABIA 1991) (Table 2). When compared tomedian international standards for metals inmollusks compiled by FAO of the United Nations,again our ranges of Cd, Cu, Pb and Zn are lowerthan the FAO limits and therefore our musselsare safe for human consumption.

However, the potential hazards of metalstransferred to humans are probably dependenton the amount (g wet weight) of musselsconsumed by an individual For example, anadult who consumed 2.50 g/day of P. viridisdaily from Sebatu-1 would take in approximately7.93 ;xg (3.17 /ig/g x 2.50 g) of Pb per day. If theconsumer were to take the mussel for 7 days,then he would have consumed 55.5 fig Pb (7.93fig x 7 days). This is slightly higher than the

recommended limit for the provisional tolerableweekly intake of Pb (50.0 /ig/adult) (FAO/WHO1984). Tukimat et al (2002) reported that thedaily intake of Pb in seafood by a populationfrom Kuala Kemaman, Terengganu (east coastof Peninsular Malaysia), was 2.82 flg/d^y. Theestimate of Pb intake from the present study(55.5 fig Pb) is higher than a week's consumptionof seafood by a person from Kemaman (2.82/xg/day x 7 days= 20.0 fig Pb).

Similarly, if an adult roughly consumed 2.50g of mussel per day, then the person whoconsumed mussels collected from Kg. Pasir Putehwould consume approximately 2.35 fig (0.94fig/g x 2.50 g) of Cd each day. If the consumertakes mussels for 7 consecutive days, then he

44 PERTANIKAJ. TROP. AGRIC. SCI. VOL. 28 NO. 1, 2005

CD, CU, PB 8c ZN LEVELS IN P. VIRIDIS (L.) FROM THE WEST COAST OF PENINSULAR MALAYSIA

TABLE 2Guidelines on heavy metals for food safety set by different countries

Location WB Cd (//g/g) Cu Gug/g) Pb Gug/g) Zn (jig/g)

Permissible limits set by Malaysian FoodRegulations (1985)Maximum permissible levels established byBrazilian Ministry of Health (ABIA 1991)Permissible limit set by Ministry of Public Health,Thailand (MPHT 1986)Australian Legal Requirements (NHMRC 1987)Median international standards for metals inmollusks compiled by the Food and AgriculturalOrganization of the United Nations (CaliforniaEPA 2005)

Metal levels of P. viridis from Peninsular Malaysia(This study)

Wet

Dry

Dry

DryWet

1.00

5.00

-

10.02.00

30.0

150

133

35010-30

2.00

10.0

6.67

1-6

100

250

667

75040-100

Wet 0.02-0.94 0.29-5.28 0.20-3.17 10.3-20.3(0.24 ± 0.08) (2.09 ± 0.33) (1.36 ± 0.26) (15.33 ± 0.98)

Dry 0.11-5.55 3.49-31.1 1.16-18.6 60.5-119.5(1.39 ± 0.45) (12.3 ± 1.95) (8.01 ± 1.52) (90.1 ± 5.77)

Note: WB= weight basis.

would have consumed 16.5 mg Cd (2.35 x 7days). Again, this is higher than therecommended limit for the provisional tolerableweekly intake of Cd (6.70-8.30 jig/adult) (FAO/WHO 1984). Tukimat et al (2002) reported thatthe daily intake of Cd in seafood by a populationfrom Kuala Kemaman, Terengganu, was 0.74/ig/day. The present estimate (16.5 /J,g Cd) isalso higher than a week's consumption of seafoodfrom Kemaman (0.74 fig/day x 7 days= 5.18 /lgCd). Therefore the above calculations show thatthe risk of metal toxicity could be dependent onthe amount of mussels consumed.

For the calculation of the non-carcinogenicrisk of all mussels collected, the meanconcentrations of Cd, Cu, Pb and Zn in themussels are summarized in Table 3. For a personwho takes one mussel per day (13.5 g wet weight/day), all the indices are below 1 (Table 3a),indicating that there is no non-carcinogenic risk.However, for a person who takes five musselsper day (67.3 g wet weight /day) (Table 3), theindices for the concentrations of Cd in musselscollected from Merlimau-1, Parit Jawa and Kg.Pasir Puteh are above 1, whereas the indices forPb concentrations in mussels collected fromBagan Tiang, Merlimau-1, Sebatu-1, Sebatu-2 andKg. Pasir Puteh are above 1. The samephenomenon of metal risk can be seen if anindividual consumed 10 mussels per day in whicha greater proportion of the populations is

estimated to be at risk of Cd and Pb toxicitysince 50% and 58.3% of the population havetheir non-carcinogenic risk indices higher than1. According to Wong et al (2000), the non-carcinogenic value of 1 or greater indicates arisk of potential concern (Wong et al 2000).Therefore, the mean concentrations of Cd andPb indicated a risk if one consumes five or moremussels per day.

CONCLUSION

Although the present data indicate that thepossibility of the occurrence of acute toxicitiesof Cd, Cu, Pb and Zn is unlikely, low-level andchronic toxicities to consumers may still causehealth problems in human beings. The latter ispoorly understood although this would beexpected based on the information found in theliterature. By using P. viridis as a biomonitoringagent, the contamination of Cd, Cu, Pb and Znin the west coast of Peninsular Malaysia wasfound to be not serious. The heavy metalconcentrations in the mussels from the westcoast of Peninsular Malaysia could be attributedto natural or anthropogenic metal sourcesaffecting their habitats. From the human publichealth point of view, these results seem to showno possibility of acute toxicities of Cd, Cu, Pband Zn if edible mussels are consumed. However,the risk is dependent on the amount of musselsconsumed and the sites from where the musselsare collected.

PERTANIKAJ. TROP. AGRIC. SCI. VOL. 28 NO. 1, 2005 45

YAP, C.K., ISMAIL, A. 8c TAN, S.G.

TABLE 3Non<arcinogenic hazard index (CDI/RfD) for oral intake of 1 day, 5 and 10 consecutive days

1.2.3.4.

5.

6.7.8.9.10.

Sites

Bagan TiangP. PanjangTelok EmasMerlimau-1Merlimau-2Sebatu-1Sebatu-2Parit JawaPontian KecilP. LidoK. Pasir PutehK. Belungkor

1

0.020.010.000.010.010.020.010.010 010.020.040 01

Cu

Day(s)5

0.080.050.020.060.050.090.060.070 060.080.180.05

10

0.160.100.040.120.100.180.120.140 120.160.360 10

1

0.020.030.020.020.030.020.010.020.020.020.020 0?

Zn

Day(s)5

0.080.140.120.100.130.120.070.110.080.120.080.10

10

0.160.240.240.200.260.240.140.220.160.240.160?0

1

0.030.050.170.260.170.220.040.260.010.050.630 01

Cd

Day(s)5

0.170.240.841.280.841.110.201.320.070.243.170.07

10

0.340.481.682.481.682.220.402.640.140.486.340.14

1

0.240.030.090.320.060.430.250.170.150.140.270.06

Pb

Day(s)5

1.180.140.451.610.292.141.260.830 750.701.360.32

10

2.360.280.903.220.584.282.521.661.500.142.72064

Note: Values in bold indicate a risk of potential concern (Wong et al 2000) since they are > 1.0.

ACKNOWLEDGEMENT

This work is partly supported by Young LecturersResearch Scheme (Vote: 53153) funded byUniversiti Putra Malaysia and funds from theMinistry of Science, Technology and theEnvironment, Malaysia through IRPA No. 09-02-04-0353-EA00L

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(Received: 25 February 2005)(Accepted: 19 July 2005)

PERTANIKAJ. TROP. AGRIC. SCI. VOL. 28 NO. 1, 2005 47