Assessment of heavy metals in wild and farmed tilapia (Oreochromis niloticus) on Lake Kariba, Zambia: implications for human and fish health

Figures & data

Figure 1. Map of Lake Kariba showing the 5 locations (sites 1–3 and farms 1 and 2) where tilapia was collected on the Zambian side. (Courtesy of Eliezer Brown Mwakalapa 2019).

Table 1. Location and fish characteristics: Sampling time, mean and range of individual length and number of pooled muscle samples from farmed (farms 1 and 2) and wild tilapia distant (sites 1 and 2) and near farms (site 3) from Lake Kariba. Zambia

Location	Sampling time 2016	Mean of individual length (cm)	Range individual length (cm)	No. of individual samples	No. of fish per pool	No. of pooled/ individual samples
Site 1	June	35.57	28–45	29	2–3	10
Site 2	June	30.66	17–42	23	2–3	10
Site 3	June	27.6	24–33	20	2	10
Farm 1	June	23.6	13–29	16	1–3	10
Farm 2	June	27.13	22.5–36	12	1–2	10

Table 2. Descriptive statistics of heavy metal concentrations in muscles of wild and farmed tilapia (mg/kg ww) and maximum limits (ML) set by WHO/FAO, EU, FDA

		Essential metals									Non-essential metals
Location		Mg	Cr	Fe	Co	Ni	Cu	Zn	Mo	Se	As	Al	Ag	Cd	Hg	Pb	Li	V
Site 1	Mean	249	0.095	5.23	0.033	0.018	0.25	4.76	0.003	0.15	0.022	4.81	0.0011	0.0007	0.021	0.009	0.006	0.015
	Median	250	0.015	5.15	0.034	0.012	0.25	4.45	0.003	0.16	0.022	4.4	0.0011	0.0006	0.006	0.009	0.006	0.016
	Min	210	0.009	3.1	0.018	0.009	0.2	3.6	0.002	0.13	0.018	2.4	0.0005	0.0005	0.004	0.008	0.005	0.013
	Max	270	0.8	9.4	0.041	0.068	0.32	7.1	0.004	0.17	0.028	8.5	0.0024	0.0018	0.16	0.011	0.008	0.017
Site 2	Mean	263	0.016	5.34	0.036	0.019	0.33	4.75	0.011	0.18	0.042	4.28	0.0016	0.0022	0.008	0.009	0.006	0.048
	Median	260	0.012	4.9	0.034	0.018	0.32	4.7	0.006	0.17	0.042	4.25	0.0012	0.0021	0.005	0.01	0.006	0.021
	Min	240	0.008	3.4	0.027	0.011	0.26	3.7	0.004	0.16	0.024	1.5	0.001	0.0009	0.004	0.0015	0.004	0.015
	Max	290	0.051	8.2	0.054	0.031	0.45	6.1	0.044	0.22	0.057	8.7	0.0034	0.0045	0.026	0.012	0.011	0.19
Site 3	Mean	231	0.021	8.16	0.044	0.009	2.14	8.49	0.054	0.14	0.023	0.78	0.0004	0.0005	0.009	0.004	0.009	0.005
	Median	225	0.02	8.2	0.042	0.009	2.15	8.1	0.045	0.14	0.023	0.91	0.0003	0.0005	0.01	0.002	0.008	0.005
	Min	180	0.007	4.3	0.027	0.006	1.2	6.6	0.03	0.11	0.012	0.3	0.0002	0.0003	0.006	0.002	0.006	0.002
	Max	290	0.039	14	0.061	0.011	3.2	11	0.086	0.16	0.04	1.4	0.0007	0.0006	0.012	0.009	0.013	0.011
Farm 1	Mean	244	0.02	9.38	0.066	0.01	2.57	6.99	0.058	0.18	0.043	1.3	0.0011	0.0008	0.007	0.008	0.006	0.016
	Median	240	0.016	9.55	0.054	0.008	2.55	6.75	0.054	0.18	0.032	1.25	0.0007	0.0004	0.002	0.01	0.006	0.007
	Min	180	0.007	4.8	0.024	0.006	0.78	5.6	0.025	0.13	0.021	0.47	0.0003	0.0003	0.001	0.002	0.004	0.004
	Max	320	0.053	17	0.17	0.019	4.3	9.3	0.092	0.28	0.15	2.7	0.005	0.0022	0.041	0.011	0.006	0.052
Farm 2	Mean	260	0.038	5.78	0.043	0.011	3.5	7.06	0.05	0.15	0.028	1.64	0.0004	0.0004	0.002	0.007	0.007	0.005
	Median	255	0.015	5.5	0.043	0.01	2.65	7.1	0.047	0.16	0.031	0.91	0.0004	0.0003	0.002	0.009	0.008	0.004
	Min	240	0.008	2.4	0.011	0.006	0.5	4.3	0.021	0.12	0.005	0.38	0.0001	0.0003	0.001	0.002	0.008	0.002
	Max	300	0.24	8.5	0.068	0.024	9	10	0.086	0.2	0.05	8.7	0.0011	0.0005	0.003	0.011	0.008	0.012
WHO and FAO	ML			45			30	30						0.1	0.5	0.3
EU	ML													0.05	0.5	0.3
FDA	ML														1

Figure 2. Concentration of heavy metals (Cu, Fe, Zn, Ni, Mo, Al and Cd) in muscle tissue of farmed and wild tilapia from Lake Karbia. Site with the same letter (a,b,c,d, or e) showed no significant difference in metal concentration at ** p < .01 and * p < .05.

Table 3. Estimated weekly intake (EWI) of heavy metals and Selenium health benefit values (HBV_Se) from consumption of muscle tissue from wild and farmed tilapia from Lake Kariba, Zambia

	Site 1	Site 2	Site 3	Farm 1	Farm 2	PTWI
Li	1.91 × 10^−5	1.87 × 10^−5	2.81 × 10^−5	1.76 × 10^−5	2.18 × 10^−5
Mg	7.5 × 10^−1	7.93 × 10^−1	6.96 × 10^−1	7.35 × 10^−1	7.84 × 10^−1
Al	1.45 × 10^−2	1.29 × 10^−2	2.35 × 10^−3	3.92 × 10^−3	4.95 × 10^−3	1 (EFSA 2008)
V	4.64 × 10^−5	1.43 × 10^−4	1.52 × 10^−5	4.77 × 10^−5	1.45 × 10^−5
Cr	2.86 × 10^−4	4.83 × 10^−5	6.43 × 10^−5	5.87 × 10^−5	1.16 × 10^−4	0.023 (Lin et al. 2004)
Fe	1.58 × 10^−2	1.61 × 10^−2	2.46 × 10^−2	2.83 × 10^−2	1.74 × 10^−2	5.6 (JECFA 2017)
Co	9.92 × 10^−5	1.09 × 10^−4	1.32 × 10^−4	2 × 10^−4	1.28 × 10^−4	0.21 (Finley et al. 2012)
Ni	5.43 × 10^−5	5.61 × 10^−5	2.6 × 10^−5	2.94 × 10^−5	3.19 × 10^−5	0.035 (JECFA 2017)
Cu	7.66 × 10^−4	1 × 10^−3	6.45 × 10^−3	7.74 × 10^−3	1.05 × 10^−2	3.5 (JECFA 2017)
Zn	1.43 × 10^−2	1.43 × 10^−2	2.56 × 10^−2	2.1 × 10^−2	2.13 × 10^−2	7 (JECFA 2017)
As	6.57 × 10^−5	1.26 × 10^−4	6.78 × 10^−5	1.3 × 10^−4	8.32 × 10^−5	0.01498 (JECFA 1989)
Se	4.58 × 10^−4	5.30 × 10^−4	4.07 × 10^−4	5.36 × 10^−4	4.58 × 10^−4
Mo	8.95 × 10^−6	3.43 × 10^−5	1.62 × 10^−4	1.75 × 10^−4	1.5 × 10^−4
Ag	3.34 × 10^−6	4.66 × 10^−6	1.2 × 10^−6	3.2 × 10^−6	1.33 × 10^−6
Cd	2.19 × 10^−6	6.57 × 10^−6	1.4 × 10^−6	2.48 × 10^−6	1.1 × 10^−6	0.0056 (JECFA 2011)
Hg	6.33 × 10^−5	2.36 × 10^−5	2.66 × 10^−5	2.05 × 10^−5	6.69 × 10^−6	0.004 (EFSA 2012; JECFA, 2017)
Pb	2.75 × 10^−5	2.79 × 10^−5	1.1 × 10^−5	2.41 × 10^−5	2.01938E-05	0.0105 (EFSA 2010)
HBVSe	1.92 × 10^−3	2.23 × 10^−3	1.71 × 10^−3	2.25 × 10^−3	1.92 × 10^−3

Table 4. Total hazard quotient (THQ) and hazard index (HI) for analysed heavy metals from consumption of wild and farmed tilapia

	Site 1	Site 2	Site 3	Farm 1	Farm 2	RfD (USEPA 2018)
Li	1.36 × 10^−6	1.33 × 10^−6	2.01 × 10^−6	1.26 × 10^−6	1.56 × 10^−6	0.002
Mg	2.19 × 10^−6	2.31 × 10-6	2.03 × 10^−6	2.14 × 10^−6	2.28 × 10^−6
Al	2.07 × 10^−6	1.84 × 10^−6	3.36 × 10^−7	5.6 × 10^−7	7.07 × 10^−7	1
V	1.33 × 10^−6	4.1 × 10^−6	4.35 × 10^−7	1.36 × 10^−6	4.13 × 10^−7	0.005
Cr	1.36 × 10^−5	2.3 × 10^−6	3.06 × 10^−6	2.8 × 10^−6	5.51 × 10^−6	0.003
Fe	3.22 × 10^−6	3.28 × 10^−6	5.02 × 10^−6	5.77 × 10^−6	3.56 × 10^−6	0.7
Co	4.72 × 10^−5	5.2 × 10^−5	6.27 × 10^−5	9.52 × 10^−5	6.11 × 10^−5	0.0003
Ni	3.88 × 10^−7	4.0 × 10^−7	1.86 × 10^−7	2.1 × 10^−7	2.28 × 10^−7	0.02
Cu	2.73 × 10^−6	3.57 × 10^−6	2.30 × 10^−5	2.76 × 10^−5	3.77 × 10^−5	0.04
Zn	6.83 × 10^−6	6.82 × 10^−6	1.22 × 10^−5	1.0 × 10^−5	1.0 × 10^−5	0.3
As	3.13 × 10^−5	6.0 × 10^−5	3.23 × 10^−5	6.2 × 10^−5	3.96 × 10^−5	0.0003
Se	1.31 × 10^−5	1.52 × 10^−5	1.16 × 10^−5	1.53 × 10^−5	1.31 × 10^−5	0.005
Mo	2.56 × 10^−7	9.81 × 10^−7	4.62 × 10^−6	5.0 × 10^−6	4.29 × 10^−6	0.005
Ag	9.55 × 10^−8	1.33 × 10^−7	3.43 × 10^−8	9.15 × 10^−8	3.79 × 10^−8	0.005
Cd	3.13 × 10^−7	9.39 × 10^−7	2.01 × 10^−7	3.54 × 10^−7	1.52 × 10^−7	0.001
Hg	9.04 × 10^−5	3.37 × 10^−5	3.8 × 10^−5	2.92 × 10^−5	9.56 × 10^−6	0.0001
Pb	1.12 × 10^−6	1.14 × 10^−6	4.49 × 10^−7	9.84 × 10^−7	8.24 × 10^−7
Hazard index	2.18 × 10^−4	1.9 × 10^−4	1.98 × 10^−4	2.6 × 10^−4	1.91 × 10^−4

RfD: Reference dose set by USEPA (2018).

Table 5. Estimation of cancer risk (CR) posed by a lifetime of consumption of wild and farmed tilapia from Kariba due to As, Pb, Cd, Cr and Ni

	Site 1	Site 2	Site 3	Farm 1	Farm 2	CSF (USEPA 2018)	Acceptable risk range (USEPA 1995)
As	1.41 × 10^−5	2.71 × 10^−5	1.45 × 10^−5	2.79 × 10^−5	1.78 × 10^−5	1.5	1 × 10^−4 to 1 × 10^−6
Pb	3.34 × 10^−8	3.39 × 10^−8	1.34 × 10^−8	2.93 × 10^−8	2.45 × 10^−8	0.0085
Cd	1.97 × 10^−6	5.92 × 10^−6	1.26 × 10^−6	2.23 × 10^−6	9.6 × 10^−7	6.3
Cr	2.04 × 10^−5	3.45 × 10^−6	4.59 × 10^−6	4.19 × 10^−6	8.27 × 10^−6	0.5
Ni	1.32 × 10^−5	1.36 × 10^−5	6.31 × 10^−6	7.15 × 10^−6	7.74 × 10^−6	1.7
Total CR	4.97 × 10^−5	5.01 × 10^−5	2.67 × 10^−5	4.15 × 10^−5	3.48 × 10^−5

CSF, cancer slope factor.

Table 6. Comparison of mean concentration of heavy metals in muscle (mg/kg ww) of wild tilapia from other studies

Country	Location	Li	Mg	Al	V	Cr	Fe	Co	Ni	Cu	Zn	As	Se	Mo	Ag	Cd	Hg	Pb	Reference
Zambia^1	Lake	0.0063	249	4.81	0.0154	0.095	5.23	0.033	0.018	0.25	4.76	0.022	0.152	0.003	0.00111	0.001	0.021	0.009	This study
Zambia^2	Lake	0.0062	263	4.28	0.0476	0.016	5.34	0.036	0.019	0.33	4.75	0.042	0.176	0.011	0.00155	0.002	0.008	0.009	This study
Zambia^3	Lake	0.0093	231	0.78	0.0050	0.021	8.16	0.044	0.009	2.14	8.49	0.023	0.135	0.054	0.0004	0.001	0.009	0.004	This study
Zambia^a	Lake					1.05		nd	0.174	0.42	4.45					0.0004		0.008	(Nakayama et al. 2010)
Zimbabwe^a	Lake								2.18	1.45	10.29		1.01			0.671		1.51	(Berg et al. 1995)
Tanzania^a	Lake									0.32	28.3							0.32	(Mapenzi et al. 2020)
Kenya	Lake						63.9			5.8	17.1					1.90		6.11	(Nyingi et al. 2016)
Egypt^a	River			2.59	0.0064	0.326	2.03	0.004	0.481	0.11	0.85	0.367	0.159	0.034		<0.012		0.008	(Ibrahim et al. 2020)
Egypt	River															0.15	1.18	0.54	(Hamada et al. 2018)
Ethiopia^a	Lake					0.07						0.055	0.046			0.044	0.051	0.063	(Dsikowitzky et al. 2012)
China	Lake					0.51			3.5	1.38	29.5	0.03				0.03		8.62	(Leung et al. 2014)
Malaysia^a	Lake					1.208			0.636	0.5	9.54					0.006		0.03	(Taweel and Shuhaimi-Othman 2011)
Saudi Arabia^a	River									0.37	4.72					0.083		0.35	(Mohammed 2009)
Saudi Arabia^a	River					0.048				0.23						0.002	0.001	0.008	(Abdel-Baki et al. 2011)

Sites 1–3 from this study.

^aConverted to wet weight from dry weight using the estimated percentage 78.8% as moisture content (Miao et al. 2010)

Nd, not detected.

Table 7. Comparison of mean concentration of heavy metals in muscle (mg/kg ww) of farmed tilapia from other studies

Country	Location	Li	Mg	Al	V	Cr	Fe	Co	Ni	Cu	Zn	As	Se	Mo	Ag	Cd	Hg	Pb	Reference
Zambia^1	Cages	0.0058	244	1.3	0.0158	0.019	9.38	0.066	0.0098	2.568	6.99	0.043	0.178	0.0581	0.00106	0.00082	0.0068	0.008	This study
Zambia^2	Cages	0.0072	260	1.643	0.0048	0.038	5.78	0.043	0.0106	3.5	7.06	0.028	0.152	0.0498	0.00044	0.00035	0.0022	0.007	This study
Zimbabwe^a	Pond								2.29	1.62	11.69		0.45			0.78		1.51	(Berg et al. 1995)
Zimbabwe^a	Cage								2.52	1.79	12.53		1.06			0.73		1.51	(Berg et al. 1995)
Egypt	Pond			4.98					1.19							3.72	1.23	1.23	(Authman et al. 2012)
Egypt	Canal															0.08	0.94	0.29	(Hamada et al. 2018)
Uganda	Cage					0.56				0.57	0.58								(Birungi et al. 2007)
Malaysia^a	Pond					1.316			0.593	0.562	6.57					0.0021		0.023	(Taweel and Shuhaimi-Othman 2011)
Taiwan	Pond					2.46		1.57	2.27	3.17	61.4	1.27	2.7			0.01		0.14	(Ling et al. 2013)

Farms 1 and 2 in this study.

^aConverted to wet weight from dry weight using the estimated percentage 78.8% as moisture content (Miao et al. 2010).

[EFSA] European Food Safety Authority. 2008. Safety of aluminium from dietary intake1. Scientific Opinion of the Panel on Food Additives, Flavourings, Processing Aids and Food Contact Materials (AFC). Adopted on 22 May 2008. The EFSA Journal.

 Google Scholar

LIN, H. T., WONG, S. S. & LI, G.-C. 2004. Heavy metal content of rice and Shellfish in Taiwan. Journal of Food and Drug Analysis, 12, 167–174.

 Google Scholar

[JECFA] Joint FAO/WHO Expert Committee on Food Additives. 2017. Food Contaminants. http://apps.who.int/foodadditives-contaminants-jecfa-database/search.aspx

 Google Scholar

Finley, B. L, Monnot, A. D, Paustenbach, D. J, & Gaffney, S. H. (2012). Derivation of a chronic oral reference dose for cobalt. Regulatory Toxicology and Pharmacology, 64(3), 491–503. doi:https://doi.org/10.1016/j.yrtph.2012.08.022

 Google Scholar

[JECFA] Joint FAO/WHO Expert Committee on Food Additives, Food Agriculture Organization of the United, Nations World Health, Organization. 1989. Evaluation of certain food additives and contaminants: thirty-third report of the Joint FAO/WHO Expert Committee on Food Additives [meeting held in Geneva from 21 to 30 March 1988]. Geneva: World Health Organization.

 Google Scholar

[JECFA] Joint FAO/WHO Expert Committee on Food Additives. 2011. Evaluation of Certain Food Additives and Contaminants Seventy-Third Report of the Joint FAO/WHO Expert Committee on Food Additives. Evaluation of Certain Food Additives and Contaminants.

 Google Scholar

[EFSA] European Food Safety Authority. 2012. Scientific Opinion on the risk for public health related to the presence of mercury and methylmercury in food. Panel on Contaminants in the Food Chain. 10(12), 2985. doi: https://doi.org/10.2903/j.efsa.2012.2985.

 Google Scholar

[EFSA] European Food safety. 2010. EFSA Panel on Contaminants in the Food Chain Scientific Opinion on Lead in Food. 8(4), 1570. doi: https://doi.org/10.2903/j.efsa.2010.1570.

 Google Scholar

[USEPA] United States Environmental Protection Agency. 2018. US EPA Regional Screening Levels (RSLs) (November 2018)- Dataset- California open data. [accessed 2021 Jul 28] https://data.ca.gov/dataset/us-epa-regional-screening-levels-rsls-november-2018/resource/b66c9172-a61a-4131-997f-01f45a473a08

 Google Scholar

[USEPA] U.S. Environmental Protection Agency. 1995. Final water quality guidance for the Great Lakes system. Fed. Regist. 60:15365–15425.

 Google Scholar

Nakayama SMM, Ikenaka Y, Muzandu K, Choongo K, Oroszlany B, Teraoka H, Ishizuka M, Ishizuka M. 2010. Heavy metal accumulation in lake sediments, fish (Oreochromis niloticus and Serranochromis thumbergi), and Crayfish (Cherax quadricarinatus) in Lake Itezhi-tezhi and Lake Kariba, Zambia. Arch Environ Contam Toxicol. 59(2):291–300. doi:https://doi.org/10.1007/s00244-010-9483-8.

 PubMed Web of Science ®Google Scholar

Berg H, Kiibus M, Kautsky N. 1995. Heavy metals in tropical Lake Kariba, Zimbabwe. Water Air Soil Pollut. 83(3):237–252. doi:https://doi.org/10.1007/BF00477355.

 Web of Science ®Google Scholar

Mapenzi LL, Shimba MJ, Moto EA, Maghembe RS, Mmochi AJ. 2020. Heavy metals bio-accumulation in tilapia and catfish species in Lake Rukwa ecosystem Tanzania. J Geochem Explor. 208:106413. doi:https://doi.org/10.1016/j.gexplo.2019.106413

 Web of Science ®Google Scholar

Nyingi B, Gitahi KJ, Kiptoo M, Jackson K. 2016. Heavy metal concentrations in water and selected fish species (tilapia, catfish and lungfish) from Lake Baringo, Kenya. Int J Sci Environ. 5:4288–4295.

 Google Scholar

Ibrahim M, Sayed E-S, Shaban A, Abdel-Ghafour S, Abouzied S, Abdel-Rahman R, Hassan M, El-Lahamy A, Adel, Abo–Zeid S, et al. 2020. Effect of location and grilling process on heavy metals concentration in muscles of different fish species, Egypt %J. Egypt J Aquat Biol Fish. 24(6):15–24. doi:https://doi.org/10.21608/ejabf.2020.109083.

 Google Scholar

Hamada M, Elbayoumi Z, Khader R, Elbagory A. 2018. Assessment of heavy metal concentration in fish meat of wild and farmed nile tilapia (Oreochromis Niloticus), Egypt. Alexandria J Vet Sci. 57:30. doi:https://doi.org/10.5455/ajvs.295019

 Google Scholar

Dsikowitzky L, Tsegaye M, Dadebo E, Carvalho C, Sindern S. 2012. Assessment of heavy metals in water samples and tissues of edible fish species from Awassa and Koka Rift Valley Lakes, Ethiopia. Environ Monit Assessment, 185. doi:https://doi.org/10.1007/s10661-012-2777-8

 Google Scholar

Leung HM, Leung AOW, Wang HS, Ma KK, Liang Y, Ho KC, Yung KKL, Tohidi F, Yung KKL. 2014. Assessment of heavy metals/metalloid (As, Pb, Cd, Ni, Zn, Cr, Cu, Mn) concentrations in edible fish species tissue in the Pearl River Delta (PRD), China. Mar Pollut Bull. 78(1):235–245. doi:https://doi.org/10.1016/j.marpolbul.2013.10.028.

 PubMed Web of Science ®Google Scholar

Taweel A, Shuhaimi-Othman M. 2011. Heavy metals concentration in different organs of tilapia fish (Oreochromis niloticus) from selected areas of Bangi, Selangor, Malaysia. Afr J Biotechnol. 10(55).

 Google Scholar

Mohammed AA-K. 2009. Accumulation of heavy metals in Tilapia Fish (Oreochromis niloticus) from Al-Khadoud Spring, Al-Hassa, Saudi Arabia. Am J Appl Sci. 6(12). doi:https://doi.org/10.3844/ajassp.2009.2024.2029.

 Google Scholar

Abdel-Baki AS, Dkhil MA, Al-Quraishy S. 2011. Bioaccumulation of some heavy metals in tilapia fish relevant to their concentration in water and sediment of Wadi Hanifah, Saudi Arabia. AFR J BIOTECHNOL. 10:2541–2547. doi:https://doi.org/10.5897/AJB10.1772

 Web of Science ®Google Scholar

Miao, L, Liu, B, He, J, Xie, J, Ge, X, Xu, P, . . . Liang, Z. (2010). Evaluation of nutritive quality and nutritional components in the muscle of GIFT strain of Nile tilapia (Oreochromis niloticus). Journal of Shanghai Ocean University, 19(5), 635–641

 Google Scholar

Authman MM, Abbas WT, Gaafar AY. 2012. Metals concentrations in Nile tilapia Oreochromis niloticus () from illegal fish farm in Al-Minufiya Province, Egypt, and their effects on some tissues structures. Ecotoxicol Environ Saf. 84:163–172. doi:https://doi.org/10.1016/j.ecoenv.2012.07.005

 PubMed Web of Science ®Google Scholar

Birungi Z, Masola B, Zaranyika MF, Naigaga I, Marshall B. 2007. Active biomonitoring of trace heavy metals using fish (Oreochromis niloticus) as bioindicator species. The case of Nakivubo wetland along Lake Victoria. Phys Chem Earth Parts A/B/C. 32(15):1350–1358. doi:https://doi.org/10.1016/j.pce.2007.07.034.

 Web of Science ®Google Scholar

Ling M-P, Wu -C-C, Yang K-R, Hsu H-T. 2013. Differential accumulation of trace elements in ventral and dorsal muscle tissues in tilapia and milkfish with different feeding habits from the same cultured fishery pond. Ecotoxicol Environ Saf. 89:222–230. doi:https://doi.org/10.1016/j.ecoenv.2012.12.002

 PubMed Web of Science ®Google Scholar