bioaccumulation and health risk assessments of heavy ... - Springer Link

Environ Sci Pollut Res (2016) 23:7195–7203 DOI 10.1007/s11356-016-6484-9

BIOLOGICAL WASTE AS RESOURCE, WITH A FOCUS ON FOOD WASTE

Food wastes as fish feeds for polyculture of low-trophic-level fish: bioaccumulation and health risk assessments of heavy metals in the cultured fish Zhang Cheng 1,2 & Cheung-Lung Lam 2 & Wing-Yin Mo 2 & Xiang-Ping Nie 4 & Wai-Ming Choi 2 & Yu-Bon Man 2 & Ming-Hung Wong 2,3

Received: 17 February 2015 / Accepted: 15 March 2016 / Published online: 22 March 2016 # Springer-Verlag Berlin Heidelberg 2016

Abstract The major purpose of this study was to use different types of food wastes which serve as the major sources of protein to replace the fish meal used in fish feeds to produce quality fish. Two types of food waste-based feed pellets FW A (with cereals) and FW B (with cereals and meat products) and the commercial feed Jinfeng® were used to culture fingerlings of three low-trophic-level fish species: bighead carp, grass carp, and mud carp (in the ratio of 1:3:1) for 1 year period in the Sha Tau Kok Organic Farm in Hong Kong. Heavy metal concentrations in all of the fish species fed with food waste pellets and commercial pellets in Sha Tau Kok fish ponds were all below the local and international maximum permissible levels in food. Health risk assessments indicated that human consumption of the fish fed with food waste feed pellets was safe for the Hong Kong residents. The present results revealed that recycling of food waste for cultivating lowtrophic-level fish (mainly herbivores and detritus feeders) is feasible, and at the same time will ease the disposal pressure of

Responsible editor: Philippe Garrigues Electronic supplementary material The online version of this article (doi:10.1007/s11356-016-6484-9) contains supplementary material, which is available to authorized users. * Ming-Hung Wong [email protected]

1

College of Resources and Environment, Sichuan Agricultural University, Chengdu, China

2

Consortium on Health, Environment, Education and Research (CHEER), and Department of Science and Environmental Studies, Hong Kong Institute of Education, Tai Po, Hong Kong, China

3

College of Environment, Jinan University, Guangzhou, China

4

Institute of the Hydrobiology, Jinan University, Guangzhou, China

food waste, a common problem of densely populated cities like Hong Kong. Keywords Recycling of food wastes . Bioaccessibility of heavy metals . Carcinogenic risks . Non-carcinogenic risks

Introduction Great quantities of heavy metals are discharged into the environment as contaminants each year by anthropogenic activities. They may enter agriculture areas (e.g., crop and fish culture areas) through atmospheric deposition, sewage outfalls, and agricultural and industrial runoff. This will pose risks to human health if element accumulated in bio-tissues exceeded maximum permitted concentrations. In general, elevated concentrations of arsenic (As), cadmium (Cd), chromium (Cr), mercury (Hg), and lead (Pb) were found in freshwater fish from different fish ponds scattered around the Pearl River Delta (PRD), including Mai Po, Hong Kong (Cheng et al. 2013; Zhou and Wong 2000). Cheung et al. (2008) analyzed heavy metal concentrations in ten common marine and freshwater fish available in Hong Kong markets, and revealed that bighead carp, snakehead, and grey mullet had average concentrations of Cd and Pb greater than the China standards for maximum levels of contaminants in foods for Cd (0.1 mg/kg wet weight (ww)) and Pb (0.5 mg/kg ww) established by the China National Standard Management Department (2005). Heavy metals contained in fish that are in association with human health have also raised considerable public concerns in Hong Kong. Jarup (2003) and Ko (2004) showed that severe skin disorders and autism in children were linked with their high concentrations of Hg, Cd (coastal cities such as Hong Kong and Shanghai), As, and Pb (inland cities such as Beijing) detected in the hair which may reflect the

7196

dietary difference between the two populations, for instance, the coastal population, consuming more fish. Food waste is a global problem that impacts the environment and society. The global food waste production is about 1.3 billion tonnes per year, which is about 33 % of all edible food produced for human consumption (Gustavsson et al. 2011). In developed countries and areas, food wastage is very serious, e.g. per capita food wasted by consumers in subSaharan Africa and South/Southeast is about 10–15 times lower than in North America and Europe (Gustavsson et al. 2011). In the USA, almost 14 % of the total municipal solid waste (MSW) stream was food waste (more than 34 million tonnes), and less than 3 % of which was recovered and recycled in 2010 (USEPA 2012). In 2011, food waste comprised of one third (about 330,000 tonnes) of the MSW loads at landfills (about 900,000 tonnes) (EPD 2011). In Hong Kong, the remaining capacities of the three existing landfills will be exhausted by 2018 (EPD 2011). Food processing and transportation also consume large quantities of freshwater and fossil fuels. In addition to producing wastewater, as food decompose in landfill, it releases significant quantities of methane and carbon dioxide, leading to impacts on air quality and climate change (Hall et al. 2009). The fish ponds in Mai Po Nature Reserve, northwestern Hong Kong, serve an important ecological function for the migratory birds for the north. The actively managed fish ponds provide water, food, and shelter for aquatic and terrestrial animals, and provide breeding grounds for birds and other wildlife (Young 1998). These fish ponds provide an important feeding habitat for waterbirds especially during the traditional practice of draining pond water regularly (Young 2004). Due to the decline of pond fish culture activate in Hong Kong, the conservation value of the area has gradually lost and the unmanaged fish ponds may become a sink for various pollutants and also deter pond use for wildlife (Wong et al. 2004). Fish meal is nutrient rich, with high protein supplement feed ingredients (commercial fish feeds) that are commonly used in aquaculture (Kaushik et al. 2004). However, most fish meal is derived from trash fish which are small fish or fragmented fish tissues collected from capture fisheries, with a low economic value. Our previous studies indicated the fish feeds may be an important source of heavy metals entering cultured fish (Cheung et al. 2008; Zhou and Wong 2000). Due to the declining fish stocks worldwide in recent years, alternative sources of protein for manufacturing fish feeds would be an important potential solution in aquaculture industry. It has been shown that European seabass (Dicentrarchus labrax) and sunshine bass (Morone chrysops × M. saxatilis) fed with a diet contained by 94–96 % plant protein achieved a similar growth rate to those fed with high-quality fish meal (the values of daily growth index above 1.3 %/day) (Kaushik et al. 2004; Rawles et al. 2011), and Bake et al. (2009) revealed that recycled food waste could partially replace fish meal in fish feeds.

Environ Sci Pollut Res (2016) 23:7195–7203

It is hypothesized that food waste can replace part of the fish meal used in fish feeds to produce quality fish. The major objectives of the present study were (1) to investigate the concentrations of heavy metals (arsenic (As), cadmium (Cd), chromium (Cr), lead (Pb), copper (Cu), nickel (Ni), and zinc (Zn) in the fish ponds (water and sediment samples), and food waste used as fish feeds; (2) to use in vitro digestion method for analyzing the bioaccessibility of heavy metals contained in fish muscle; and (3) to assess potential health risks based on digestible heavy metal concentrations in the fish muscle.

Materials and methods Experiment design The present experiment has been approved and supervised by the Environmental Protection Department of government of Hong Kong SAR, China. The experimental design followed the method described by our prior works (Cheng et al. 2014; Mo et al. 2014). The food wastes used in the present study included food processing waste (e.g., various types of fruit peels and leafy vegetables, rice bran, and soy bean meal) and post-consumption waste (e.g., rice grain, spaghetti, beef, pork, and chicken) collected from local hotels and restaurants. The collected food wastes were transferred to a local food waste feed pellet factory: Kowloon Biotechnology Limited located in Pak Lai, New Territories (NT), for further processing. The food wastes were classified into four major categories: vegetables and fruits, cereals, meat products, and bones (Fig. 1). They were diced into small pieces, and excessive water was squeezed out by waste compressing equipment. After drying at 80 °C for 6 h, they were ground into powder to form different food waste fish feed pellets. Different ratios of food waste products (Fig. 1) were mixed with other raw materials, such as fish meals and corn starch for pelleting fish feed. In general, food waste contributed about 75 % of the pellet to maintain feed quality. The major ingredients of food waste A (FW A) were cereal food wastes, which were ideal protein sources for herbivores and omnivores (e.g., grass carp) (Fig. 1). On the other hand, some meat products were used to replace part of the cereals in food waste B (FW B). Commercial feed Jinfeng®, 613 formulated feed (control feed), is a common fish feed used in aquaculture in Pearl River Delta and Hong Kong. The field site was located in Sha Tau Kok organic farm in Sha Tau Kok, Hong Kong, China. Three ponds (20 × 10 m) filled up with spring water (depth 4 m) were used in this experiment—each accordingly assigned experimental treatments of FW A, FW B, and control feeds. For maintaining the water quality, 30 % water of the ponds was refreshed once every 3 months.


7197

Fig. 1 Food waste fish feed formulation (% mass). Note: Each type of food waste fish feed pellets contains 75 % of food waste

Three low-trophic-level species fish (1000 fish fry) (bighead carp (Hypophthalmichthys nobilis) (10–12 cm), grass carp (Ctenopharyngodon idellus) (13–16 cm), and mud carp (Cirrhina molitorella) (4–6 cm), all imported from mainland China, were placed in each experimental pond, in the ratio of 1:3:1, respectively (Chen et al. 2002). Grass carp mainly consumes macrophytes and also commercial feed pellets and food waste feed pellets. Bighead carp (filter feeder) and mud carp (detritus feeder) commonly used to maintain the pond water quality in polyculture ponds (Wong et al. 2004). All fish were fed twice per day at a fixed feeding rate of 4 % body weight per day for 12 months (October 2011–December 2012). Sampling During October 2011–December 2012, water, sediment, and plankton samples were collected from the experimental ponds (sampling frequency: bi-monthly during the first half year and tri-monthly during the second half year). In April (grass carp, n = 30; bighead carp, n = 30; mud carp, n = 18) and December 2012 (grass carp, n = 30; bighead carp, n = 65; mud carp, n = 18), fish samples were collected from each pond. Fish samples were collected from the fishponds using a nylon net, with fish lengths and weights recorded. The muscles of fish (including axial and ventral muscle) were removed. The surface sediment samples (0.5–10 cm, three replicates from each site) were collected using a stainless steel shovel. Sediment and fish samples were wrapped in aluminum foil, frozen in zip-lock bags at −20 °C, and transported to the laboratory until analyses. Water and plankton were sampled at approximately 0.5– 1.0 m depth from the fish ponds of each sampling site. Water samples were collected from each site in precleaned amber glass bottles and acidified immediately with 4 M HCl to pH 1 indicates that there is potential risk to human health (USEPA 1989). HRs can be added to generate a hazard index (HI) in order to estimate the risk of mix contaminates (USEPA 1989). The guideline also stated that Bany single chemical with an exposure level greater than the toxicity value will cause the HI to exceed unity; for multiple chemical exposures, the HI can also exceed unity even if no single chemical exposure exceeds its RfD.^ HI ¼ ∑HRi

ð3Þ

where i is different elements. For the carcinogenic effects, the cancer risk (CR) was obtained by using the oral slope factor of arsenic (OSFAs)

Results and discussion Fish feeds Figure 1 shows that different ratios of food waste products contributed to about 75 % in the pellets. The major protein sources of FW A were cereals food waste (rice bran, soy bean meal, rice grain, and spaghetti), which could be easily digested by herbivores and omnivores (e.g., grass carp and grey mullet). Meat wastes were used to replace parts of cereals in FW B, and the major ingredients of FW B were similar to the control feed which contained mainly of wheat middling, flour, bean pulp, rapeseed meal, and fish meal. The protein contents of the three types of fish feed pellets (Table S1) were not significantly different (ANOVA, p > 0.05), indicating that food waste may be used as an alternative source of protein for fish culture. Metal concentrations in fish feeds used in the experiment are shown in Table 1. There was no significant difference (ANOVA, p > 0.05) between Cd and Pb concentrations in the three types of fish feed pellets. The lowest concentrations of As, Pb, Cr, Cu, Ni, and Zn were found in the control feed, and the highest concentrations of Cu and Zn were found in FW B (ANOVA, p < 0.05). The analyses of heavy metals in various food waste ingredients for making fish pellets (FW A and FW B) showed that vegetables, cereals, and bone meal were major sources of heavy metal contamination for FW A and FW B. Fish meal also contributed significant sources of As (8.23 ± 0.23 mg/kg dry weight (dw)), Cd (0.52 ± 0.02 mg/kg dw), and Zn (127 ± 5.00 mg/kg dw) in making food waste fish feed pellets.

Environ Sci Pollut Res (2016) 23:7195–7203 Table 1

7199

Heavy metals concentrations (geometric mean value, mg/kg dw ± geometric standard deviation) in fish feed which using in the experiment As

Cd

Pb

Cr

Cu

Ni

Zn

4.08 ± 0.95a 15.1 ± 4.63b 12.6 ± 7.42b

110 ± 39.1a 352 ± 21.5b 733 ± 65.6c

8.37 ± 0.02b 10.9 ± 2.15b 15.7 ± 0.47b 8.32 ± 0.80b

127 ± 35.3a 77.6 ± 6.82a 60.5 ± 2.89a 41.2 ± 1.54a

Heavy metal concentrations of the experiment feeds 0.24 ± 0.01a 1.63 ± 0.28a 11.2 ± 5.34a Control 0.87 ± 0.11a 0.12 ± 0.04a b b Food waste A 3.21 ± 0.86 0.29 ± 0.04 0.32 ± 0.05b 6.34 ± 0.93b 40.2 ± 4.62b c bc Food waste B 6.32 ± 2.06 0.63 ± 0.23 0.38 ± 0.12b 3.96 ± 0.84c 103 ± 48.2b Heavy metal concentrations in major food waste ingredients for making fish feed pellets (FW A and FW B) 0.04 ± 0.01c 1.81 ± 0.08a 3.89 ± 0.05c (1) Fish meal 8.23 ± 0.16c 0.52 ± 0.01c b a (2) Fruit and Vegetables + Cereals 2.39 ± 0.03 0.07 ± 0.01 0.77 ± 0.17d 5.60 ± 0.05b 11.9 ± 2.37a (3) Fruit and Vegetables + Bone meal 2.57 ± 0.07b 0.08 ± 0.02a 0.33 ± 0.03b 5.59 ± 0.33b 6.90 ± 0.06d b a (4) Meat products 1.83 ± 0.01 0.04 ± 0.01 0.07 ± 0.04c 2.68 ± 0.04c 4.13 ± 0.11d Different values (a, b, c) between feeding groups are significantly different (p < 0.05) FW A food waste A pellet, FW B food waste B pellet, Control commercial fish feed—Jinfeng®, 613 formulated feed

The heavy metal concentrations in water and sediment of fish ponds collected from the studied ponds did not exceed the Chinese Water Quality Standard for fisheries (GB11607 1989) and the effect range-median guideline values (Long et al. 1995) (Table 2), respectively, indicating the pond sediment and pond water were safe for fish cultivation. Table 2 shows concentrations of As and Cd in pond water were increased during the experimental period (ANOVA, p < 0.05). On the contrary, heavy metal concentrations (except Cu) in sediment of the three ponds did not change significantly (p > 0.05) during the experimental period. There were no significant differences (ANOVA, p > 0.05) in heavy metal concentrations of water and sediment among the three ponds. Heavy metal concentrations in water and sediment samples of the three fish ponds were similar to or even lower than those in freshwater fish ponds around the PRD region (Cheng et al. 2013; Cheung et al. 2008), suggesting that the experimental site was relatively free of heavy metal contaminations and would be suitable for cultivating fish.

was obtained for Cd, Cr, Ni, and Zn concentrations in grass carp, bighead carp, and mud carp in the three experiment ponds. The results showed concentrations of heavy metals (As, Pb, and Cu) in fish muscle (grass carp and bighead carp) correspond to fish feeds which were fed to fish (Spearman correlation, p < 0.05), and no correlation to environment factors (water and sediment) (Spearman correlation, p < 0.05). Therefore, the fish feeds maybe an important source of heavy metals to cultured fish, and the phenomenon was also found in previous studies (Ciardullo et al. 2008; Lacerda et al. 2006; Liang et al. 2011). In the present study, all the elements (the mean As concentration of inorganic As was estimated by using a value of 10 % of total As (USFDA 1993)) in all fish samples were below the maximum permissible levels of the local standard (CFS 2007; GB2762 2005) and other international standards for heavy metals (HC 2007; USEPA 2000). This implied that all the fish species (grass carp, bighead carp, and mud carp), fed with food waste pellets (FW A and FW B) and commercial feed pellets (control) in Sha Tau Kok fish ponds, were safe for human consumption, in terms of heavy metals.

Biota samples

Bioaccessibility and health risk assessment

According to Table 3, the length and weight of grass carp in Sha Tau Kok fish ponds, fed with FWA and control diet, were significantly higher than these fed with FW B (ANOVA, p < 0.05). During the first half year to the second half year of experiment, concentrations of As, Cu, Ni, and Zn in grass carp, bighead carp, and mud carp in experimental ponds decreased (ANOVA, p < 0.05), while Pb in grass carp fed with food waste pellets increased (p < 0.05). In experiment ponds, concentrations of As and Cu in grass carp fed with FW A, Pb in grass carp, and As and Cu in bighead carp fed with all food waste feed pellets were higher than in the relevant fish species fed with the control diet, respectively (ANOVA, p < 0.05) (Table S2). No significant difference (ANOVA, p > 0.05)

The bioaccessibilities of As, Cd, Pb, Cr, Cu, Ni, and Zn in all fish samples varied between 10.9 and 43.7, 5.41 and 48.1, 3.80 and 27.1, 13.2 and 73.3, 10.2 and 64.6, 4.82 and 53.4, and 11.8 and 76.6 %, respectively (Table 3). The mean bioaccessibility of As (30.0 %), Cd (26.6 %), Cu (25.2 %), and Ni (23.5 %) for the digested muscles of the investigated fish (fed with food waste pellets and commercial pellets) in Sha Tau Kok were not significantly different with the fish collected from freshwater ponds in PRD of previous studies (Cheung et al. 2008). These values were comparable to those obtained in razor shell (Ensis ensis) (Cd, 21.1 %), variegated scallop (Chlamys varia) (Cd, 12.7 %), and hake (Merluccius merluccius) (Cr, 36.7 %) in Spain (Moreda-Pineiro et al.

Environmental samples

0.05 ± 0.01a 0.08 ± 0.05a 0.04 ± 0.01a 0.12 ± 0.04a 0.03 ± 0.01a 0.06 ± 0.02a – – 0.005 × 103

1.71 ± 0.98a 4.46 ± 0.31b 2.01 ± 1.07a 6.68 ± 0.58c 1.85 ± 0.92a 10.7 ± 4.46c – – 0.05 × 103

0.49 ± 0.16a 1.16 ± 0.71b 0.29 ± 0.39a 1.52 ± 0.21b 0.50 ± 0.36a 1.18 ± 0.11b – – 0.05 × 103

0.70 ± 0.11a 1.57 ± 0.71a 0.49 ± 0.17a 29.8 ± 9.05b 0.57 ± 0.07a 35.1 ± 4.15b – – 0.1 × 103

1.13 ± 0.29a 3.62 ± 1.89b 1.86 ± 0.65ab 1.23 ± 0.53a 1.67 ± 0.83ab 0.68 ± 0.23a – – 0.01 × 103

Ni 0.78 ± 0.23a 2.21 ± 0.08b 1.14 ± 0.47a 1.72 ± 0.03c 0.93 ± 0.75ac 1.34 ± 0.37ac – – 0.05 × 103

Zn 8.77 ± 5.57a 25.2 ± 0.32b 8.60 ± 1.17a 23.5 ± 4.29b 22.0 ± 6.65b 10.4 ± 2.06a – – 0.1 × 103

6.26 ± 2.46a 5.35 ± 3.04a 5.87 ± 0.98a 8.62 ± 3.52a 5.38 ± 0.52a 5.42 ± 2.05a 8.2 70 –

Cd 0.05 ± 0.03a 0.04 ± 0.02a 0.02 ± 0.01a 0.03 ± 0.01a 0.03 ± 0.01a 0.05 ± 0.02a 1.2 9.6 –

Pb 9.39 ± 1.46a 6.22 ± 2.37a 5.10 ± 0.84a 5.27 ± 0.28a 6.69 ± 1.23a 8.17 ± 0.91a 81 370 –

Cu

Chinese water quality standard for fisheries (GB11607 1989)

ERM (effects range—median) guideline values indicate concentrations above which adverse effects on biota are frequently observed (Long et al. 1995)

ERL (effects range—low) guideline values indicate concentrations below which adverse effects on biota are rarely observed (Long et al. 1995)

21.4 ± 3.61a 14.7 ± 9.80b 20.7 ± 3.86a 11.8 ± 5.18b 23.9 ± 2.92a 17.2 ± 8.36ab 47 218 –

Cr 6.67 ± 1.50a 11.3 ± 4.72ab 4.72 ± 1.15a 18.0 ± 4.48b 4.74 ± 1.12a 23.6 ± 6.92b 34 270 –

Ni

2.29 ± 1.47a 2.23 ± 0.16a 1.61 ± 0.93a 4.33 ± 1.94b 2.12 ± 0.84a 3.34 ± 0.71a 21 52 –

Zn 26.3 ± 14.3a 33.7 ± 14.7a 22.1 ± 9.06a 18.5 ± 1.22a 26.9 ± 10.1a 37.9 ± 2.77a 150 410 –

Control feed FW A FW B Control feed FW A FW B Control feed FW A FW B

11 9 10 19 25 21 6 6 6

Weight kga 0.43 ± 0.04a 0.46 ± 0.05a 0.31 ± 0.03b 0.13 ± 0.05c 0.11 ± 0.01c 0.10 ± 0.02c 0.02 ± 0.01d 0.02 ± 0.01d 0.02 ± 0.01d

Total length cma

32.6 ± 1.74a 35.7 ± 0.58a 29.4 ± 0.58b 23.5 ± 2.41c 23.2 ± 071c 21.2 ± 1.48c 15.1 ± 2.76d 18.0 ± 0.63d 15.0 ± 3.64d

0.34 ± 0.04a 0.47 ± 0.09a 0.46 ± 0.10a 0.62 ± 0.15b 0.88 ± 0.13b 0.77 ± 0.07b 0.40 ± 0.04a 0.34 ± 0.08a 0.36 ± 0.10a

As C 17.9 18.2 29 20.6 43.7 38.6 33.3 42.1 43.7

BA (%) 0.004 ± 0.001a 0.015 ± 0.003a 0.011 ± 0.004a 0.004 ± 0.001a 0.016 ± 0.004a 0.011 ± 0.002a 0.016 ± 0.007a 0.022 ± 0.007a 0.013 ± 0.009a

Cd C 14.8 48.1 22.1 33.6 23.7 15.1 14.1 17.4 27.8

BA (%)

0.05 ± 0.03a 0.04 ± 0.01a 0.09 ± 0.02a 0.10 ± 0.02a 0.05 ± 0.01a 0.08 ± 0.03a 0.07 ± 0.03a 0.10 ± 0.02a 0.06 ± 0.02a

Pb C

13.5 11.5 3.8 12.4 8.49 3.51 12.2 20.4 27

BA (%)

0.10 ± 0.04a 0.13 ± 0.02a 0.19 ± 0.02a 0.23 ± 0.04ab 0.16 ± 0.02a 0.19 ± 0.01a 0.48 ± 0.07c 0.15 ± 0.02a 0.19 ± 0.04a

Cr C

14.8 73.3 49.9 34.1 44.2 70.5 13.2 30.2 30.1

BA (%)

0.56 ± 0.24a 0.48 ± 0.06a 0.66 ± 0.18a 0.79 ± 0.21a 0.64 ± 0.11a 0.64 ± 0.03a 0.82 ± 0.10a 0.77 ± 0.11a 0.68 ± 0.20a

Cu C

26.1 28.6 64.6 21.5 24.4 61 18.6 22.9 35.1

BA (%)

0.73 ± 0.11a 1.20 ± 0.16b 0.60 ± 0.10a 1.83 ± 0.41c 1.46 ± 0.24bc 0.85 ± 0.05a 0.79 ± 0.17a 0.72 ± 0.16a 0.61 ± 0.17a

Ni C

4.82 29.1 10.7 16.6 11.8 8.97 24.5 53.4 40.3

BA (%)

27.4 ± 4.24a 26.9 ± 3.85a 28.6 ± 4.56a 35.7 ± 3.61a 20.9 ± 2.83b 33.3 ± 0.77a 29.4 ± 2.69a 18.0 ± 2.30b 26.7 ± 8.62a

Zn C

11.8 20.4 20.3 28.4 13.5 21.6 21.6 10.9 28.8

BA (%)

a

Mean value ± standard deviation

GC grass carp, BH bighead carp, MD mud carp, C concentration, BA bioaccessibility (%), FW A food waste A, FW B food waste B, control feed commercial fish feed—Jinfeng®, 613 formulated feed

Different values (a, b, c) between feeding groups are significantly different (p < 0.05)

MD

BH

GC

n

Table 3 Concentrations of heavy metals (geometric mean value, mg/kg ww ± geometric standard deviation) in fish (fed with food waste fish feed pellets and commercial fish feed pellets) from experiment ponds (second half-year experiment period)

c

b

a

FW A food waste A pellet, FW B food waste B pellet, Control commercial fish feed—Jinfeng®, 613 formulated feed, – not available

Different values (a, b, c) between feeding groups are significantly different (p < 0.05)

1st half year 2nd half year FW A 1st half year 2nd half year FW B 1st half year 2nd half year ERL guidelinea ERM guidelineb Water quality standardc

Control

Cu

As

Cr

As

Pb

Sediment (mg/kg dw)

Water (μg/l)

Fish feeds

Cd

Concentrations (geometric mean value ± geometric standard deviation) of heavy metals in water and sediment of experiment ponds

Table 2

7200 Environ Sci Pollut Res (2016) 23:7195–7203


7201

2012), but were considerably lower than the mean bioaccessibilities determined for freshwater crayfish (Procambarus clarkia) (As, 69 %) (Williams et al. 2009) and cod (Gadus gadidae) (Cr, 13.1 %) (Moreda-Pineiro et al. 2012). Previous studies revealed that the Hg, Cd, Cr, Ni, Cu, and Zn bioaccessbility ratios exhibit a positive correlation with the carbohydrate and dietary fiber content, and a negative correlation with the protein content (Cabanero et al. 2007; Moreda-Pineiro et al. 2012). In the present study, the major parameters used for the risk assessment were BW of 58.6 kg used for adults (Wang et al. 2005) and 21.8 kg for preschool children (Leung et al. 2000), and daily consumption rate of fish in Hong Kong was estimated as 93 g/day for adults and 50 g/day for children (Leung et al. 2000). Figure 2 shows the hazard index (HI) of heavy metals through freshwater fish consumption for Hong Kong residents based on digestible concentrations of all the fish. A HI higher than 1 implies that the EDI exceeds the RfD for the contaminant of interest and that may occur. There were unlikely non-cancer

risk for heavy metals to be exerted on adults and children via consumption of the three fish species fed with food waste pellets and commercial pellets. Only the arsenic was used to evaluate the carcinogenic effect. A risk above 10−6 value considered by the USEPA (USEPA 1989) as an acceptable risk for cancer when estimating the lifetime excess CR of As. The CR values of fish were all above 10−6 based on the 10 % of inorganic As out of the total As condition (USFDA 1993). In reality, due to different dietary habits of residents, the species and frequency of fish consumption varied tremendously, and many other factors such as cooking method, doneness, and food processing could all affect the final lifetime cancer risk for Hong Kong residents by ingesting these freshwater fish. However, the present results provided some useful information showing that grass carp, bighead, and mud carp fed with food waste fish feed pellets were safe to consume (for Hong Kong residents), and more importantly, commercial fish pellets could be partially replaced by food waste for culturing these fish species.

Fig. 2 Hazard indexes of heavy metals and cancer risk of inorganic As through freshwater fish by adults and children in Hong Kong. The consumption rates are 93 g/day for adults and 50 g/day for children, respectively. Each box represents interquartile range (25th and 75th

percentile) of hazard ratios and cancer risk of each fish. MD mud carp, BC bighead carp, GC grass carp, FW A food waste A, FW B food waste B, Control commercial fish feed—Jinfeng®, 613 formulated feed

7202

Conclusion The present results showed that heavy metal concentrations in pond water and sediment samples of the three experimental fish ponds were similar to or even lower than those in freshwater fish ponds around the PRD region obtained, suggesting that the experimental site was relatively free of heavy metal contaminations and would be suitable for cultivating fish. Heavy metal concentrations in all of the fish species fed with food waste pellets and commercial pellets in Sha Tau Kok fish ponds were all below the local and international maximum permissible levels. The results of health risk assessments showed that consumption of grass carp, bighead, and mud carp fed with food waste pellets was no health risk from the heavy metals via ingestion of the freshwater fish for Hong Kong residents. It can lower the cost of fish farming and at the same time, partially ease the disposal pressure of food waste and conserve the ecological value of fish ponds. Acknowledgments Financial support from Environmental and Conservation Fund (37/2009), Seed Collaborative Research Fund from the State Key Laboratory in Marine Pollution (SCRF0003), and Special Equipment Grant (SEG, HKBU 09) of the Research Grants Council of Hong Kong are gratefully acknowledged. Compliance with ethical standards The research works in the above study was funded by the research grant Seed Collaborative Research Fund provided by the State Key Laboratory in Marine Pollution (SCRF0003), Environment and Conservation Fund (37/2009) and Special Equipment Grant (SEG, HKBU 09) of the Research Grants Council of Hong Kong. The authors would like to declare that there was no potential conflicts of interest (financial or non-financial). This research involved experiments on animals, bighead carp, grass carp, and mud carp, due to the fact that heavy metal present in fish is an important indicator of their health statuses and is associated with human health. Post-experimental care of animals was provided including minimizing discomfort and the consequences of any disability resulting from the experiment.

References Bake GG, Endo M, Akimoto A, Takeuchi T (2009) Evaluation of recycled food waste as a partial replacement of fishmeal in diets for the initial feeding of Nile tilapia Oreochromis niloticus. Fish Sci 75:1275–1283 Cabanero AI, Madrid Y, Camara C (2007) Mercury-selenium species ratio in representative fish samples and their bioaccessibility by an in vitro digestion method. Biol Trace Elem Res 119:195–211 CFS (2007) Food Adulteration (Metallic Contamination) Regulations. Centre for Food Safety (CFS), the Government of the Hong Kong Special Administrative Region of the People’s Republic of China Chen CY, Stemberger RS, Klaue B, Blum JD, Pickhardt PC, Folt CL (2000) Bioaccumulation and diminution of arsenic and lead in a freshwater food web. Environ Sci Technol 34:3878–3884 Chen YL, Zhun XP, Huang ZX, Wu RQ (2002) The freshwater aquaculture utility technology in southern China. Nanfang Daily Press, Guangzhou, pp 5–6

Environ Sci Pollut Res (2016) 23:7195–7203 Cheng Z, Man YB, Nie XP, Wong MH (2013) Trophic relationships and health risk assessments of trace metals in the aquaculture pond ecosystem of Pearl River Delta, China. Chemosphere 90:2142–2148 Cheng Z, Mo WY, Man YB, Nie XP, Li KB, Wong MH (2014) Replacing fish meal by food waste in feed pellets to culture lower trophic level fish containing acceptable levels of organochlorine pesticides: health risk assessments. Environ Int 73:22–27 Cheung KC, Leung HM, Wong MH (2008) Metal concentrations of common freshwater and marine fish from the Pearl River Delta, South China. Arch Environ Contam Toxicol 54:705–715 Ciardullo S, Aureli F, Coni E, Guandalini E, Lost F, Raggi A, Rufo G, Cubadda F (2008) Bioaccumulation potential of dietary arsenic, cadmium, lead, mercury, and selenium in organs and tissues of rainbow trout (Oncorhyncus mykiss) as a function of fish growth. J Agric Food Chem 56:2442–2451 EPD (2011) Update on the progress of the key initiatives in the BPolicy Framework for the Management of Municipal Solid Waste (2005– 2014)^. Environmental Protection Department (EPD), Hong Kong SAR Government Available at: http://www.epd.gov.hk/epd/english/ boards/advisory_council/files/ACE_Paper_1_2011.pdf. Accessed 18 Dec 2012 GB11607 (1989) Water quality standard for fisheries. China National Standards Management Department, Beijing GB2762 (2005) Maximum levels of contaminants in foods. China National Standards Management Department, Beijing Gustavsson J, Cederberg C, Sonesson U, van Otterdijk R, Meybeck A (2011) Global food losses and food waste. Food and Agriculture Organization of the United Nations, Rom Hall KD, Guo J, Dore M, Chow CC (2009) The progressive increase of food waste in America and its environmental impact. Plos One 4:e7940 HC (2007) Health Canada (HC)’s revised assessment of mercury in fish enhances protection while reflecting advice in Canada’s Food Guide. Pulic works and Goverment Services Canda, Canada Jarup L (2003) Hazards of heavy metal contamination. Br Med Bull 68: 167–182 Kang Y, Man YB, Cheung KC, Wong MH (2012) Risk assessment of human exposure to bioaccessible phthalate esters via indoor dust around the Pearl River Delta. Environ Sci Technol 46:8422–8430 Kaushik SJ, Coves D, Dutto G, Blanc D (2004) Almost total replacement of fish meal by plant protein sources in the diet of a marine teleost, the Eur opean seabass, Dicentrarchus labrax. Aquaculture 230:391–404 Ko LYY (2004) A pilot study on the effect of heavy metals detoxification in children with chronic allergy. The 6th Asia Pacific Congress of Allergology and Clinical Immunology. Tokyo, Japan Lacerda LD, Santos JA, Madrid RM (2006) Copper emission factors from intensive shrimp aquaculture. Mar Pollut Bull 52:1823–1826 Leung SSF, Chan SM, Lui S, Lee WTK, Davies DP (2000) Growth and nutrition of Hong Kong children aged 0–7 years. J Paediatr Child Health 36:56–65 Liang P, Shao DD, Wu SC, Shi JB, Sun XL, Wu FY, Lo SCL, Wang WX, Wong MH (2011) The influence of mariculture on mercury distribution in sediments and fish round Hong Kong and adjacent mainland China waters. Chemosphere 82:1038–1043 Long ER, Macdonald DD, Smith SL, Calder FD (1995) Incidence of adverse biological effects within ranges of chemical concentrations in marine and estuarine sediments. Environ Manag 19:81–97 Mo WY, Cheng Z, Choi WM, Man YB, Liu Y, Wong MH (2014) Application of food waste based diets in polyculture of low trophic level fish: effects on fish growth, water quality and plankton density. Mar Pollut Bull 85:803–809 Moreda-Pineiro J, Moreda-Pineiro A, Romaris-Hortas V, MoscosoPerez C, Lopez-Mahia P, Muniategui-Lorenzo S, BermejoBarrera P, Prada-Rodriguez D (2011) In-vivo and in-vitro testing to assess the bioaccessibility and the bioavailability of arsenic,

Environ Sci Pollut Res (2016) 23:7195–7203 selenium and mercury species in food samples. TrAC-Trends Anal Chem 30:324–345 Moreda-Pineiro J, Moreda-Pineiro A, Romaris-Hortas V, DominguezGonzalez R, Alonso-Rodriguez E, Lopez-Mahia P, MuniateguiLorenzo S, Prada-Rodriguez D, Bermejo-Barrera P (2012) Trace metals in marine foodstuff: bioavailability estimation and effect of major food constituents. Food Chem 134:339–345 Rawles SD, Thompson KR, Brady YJ, Metts LS, Aksoy MY, Gannam AL, Twibell RG, Ostrand S, Webster CD (2011) Effects of replacing fish meal with poultry by-product meal and soybean meal and reduced protein level on the performance and immune status of pondgrown sunshine bass (Morone chrysops x M. saxatilis). Aquac Nutr 17:E708–E721 USEPA (1989) Risk assessment guidance for superfund, vol 1. EPA/540/ 1-89/002. Office of Emergency and Remedial Response USEPA, Washington, DC USEPA (2000) Guidance for Assessing Chemical Contaminant Data for Use in Fish Advisories. http://www.epa.gov/region6/qa/ qadevtools/mod4references/supplemental/volume1.pdf. Accessed 22 January 2015 USEPA (2012) Resource Conservation - Food Waste. Available at: http:// www.epa.gov/foodrecovery/. Accessed 18 Dec 2012 USEPA (2014) Integrated Risk Information System (IRIS) summary table. United State Environmental Protection Agency (USEPA), Wachington, DC

7203 USFDA (1993) Guidance documents for trace elements in seafood. Center for Food Safety and Applied Nutrition, Washington, DC Wang XL, Sato T, Xing BS, Tao S (2005) Health risks of heavy metals to the general public in Tianjin, China via consumption of vegetables and fish. Sci Total Environ 350:28–37 WHO (1992) Assessment of dietary intake of chemical contaminants. WHO/HPP/FOS/92.6, UNEP/GEMS/92.F2, United. Nations Environmental program, Nairobi Williams G, West JM, Koch I, Reimer KJ, Snow ET (2009) Arsenic speciation in the freshwater crayfish, Cherax destructor Clark. Sci Total Environ 407:2650–2658 Wong MH, Cheung KC, Yediler A (2004) The dike-pond systems in South China: past, present and future. In: Wong MH (ed) Wetlands ecosystems in Asia: function and management. Elsevier, Amsterdam, pp 69–86 Young L (1998) The importance to ardeids of the deep bay fish ponds, Hong Kong. Biol Conserv 84:293–300 Young L (2004) Conflicts in the management of a wetland nature reserve—case study of the Mai Po Nature Reserve, Hong Kong. In: Wong MH (ed) Wetlands ecosystems in Asia: function and management. Elsevier, Amsterdam, pp 145–160 Zhou HY, Wong MH (2000) Mercury accumulation in freshwater fish with emphasis on the dietary influence. Water Res 34: 4234–4242