Health risk of consuming Sphoeroides spp. from the Navachiste Lagoon Complex due to its trace metals and organochlorine pesticides content

doi:10.21203/rs.3.rs-1968777/v1

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Health risk of consuming Sphoeroides spp. from the Navachiste Lagoon Complex due to its trace metals and organochlorine pesticides content

https://doi.org/10.21203/rs.3.rs-1968777/v1

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The Navachiste complex (NAV) is impacted by neighbored human activities and is located in the southwestern coastal zone of the Gulf of California. The study determines the trace metal (TM) and organochlorine pesticides (OCP) health risk content in the edible tissue of Sphoeroides spp. from NAV. The daily intakes (EDI), target hazard quotient (THQ), hazard index (HI), and carcinogenic and non-carcinogenic risks were calculated. Twenty OCP and seven TM were detected with the following trend for TM: Zn > Fe > Pb > Ni > Mn > Cu > Cd. Cd, Cu, Fe, Mn, Pb, and Zn were above MRLs. The γ‒Chlordane was the most frequent OCP. The highest average concentration was for α‒HCH, followed by γ‒chlordane. With the high ratios of γ‒HCH, p, p'‒ DDD and p, p'‒DDD, and the absence of p, p'‒ DDT, the higher ratios for dieldrin and endrin than for aldrin, α‒ chlordane, γ‒chlordane, heptachlor, and heptachlor epoxide indicates historical contamination. In contrast, the residual products of methoxychlor, endosulfan, and its isomers indicate endosulfan's recent use. The TM EDI, THQ > 1 (at 120 g day-1), and the ILCR (> 1 × 10^-6) were above minimum levels, showing a high-risk potential for cancer development in the long term.

The trace metal and organochlorine pesticides health risk by the consumption of Sphoeroides spp. from Navachiste, Mexico was calculated.

The CR_Lim of some OCPs showed that the he consumption at 32.88 g day^-1of Sphoeroides spp. fillet could be carcinogenic in the long term.

All ILCR values of trace metals analyzed were above 1 × 10^-6, indicating a high risk for cancer development in the long-term.

Seafood consumption by humans contributes significantly to the intake of EPA + DHA, vitamin D, and other micronutrients that are essential to keep a healthy life [1, 2]. Despite knowing the origin of these micronutrients, consumers usually show no preference for certain seafood products, certification, or where the seafood was captured [3], and some of these organisms could contain toxic substances above maximum residue levels (MRLs) that might risk people's health [4]. Food safety is essential to prevent these health risks regarding toxic pollutants in seafood caused by anthropogenic activities [5]. Among the most toxic anthropogenic pollutants are organochlorine pesticides (OCPs) and trace metals that are environmentally persistent, become bioaccumulated and biomagnified due to their low water solubility and slow chemical decomposition [6]. The OCPs and trace metal residues are transported to the marine ecosystems by environmental factors such as effluents, wind, and rain, becoming bioavailable from marine sediments or water columns for the marine organisms [7, 8].

The persistence of trace metals and OCPs in the environment allows them to be found as residues in areas far away from the original sites of their application [9, 10]. Trace metals, such as Pb and Cd, are elements that interfere in biochemical metabolic processes [11], where they bind to proteins and enzymes surrogating essential metals like Fe in muscle or Ca in osseous tissues [12]. Other trace metals such as Fe, Zn, and Cu, when they are above MRLs, might cause health problems inhibiting nutrient absorption [13].

The persistence of these toxic pollutants makes their study crucial to determine their health impact as a human health concern [14].

The present study was performed in the Navachiste complex coastal lagoon (NAV), which is constantly impacted by the inputs of the wastewaters of the adjacent agricultural Guasave Valley, low-density tourism, urban and aquaculture activities [15] (Fig. 1). Previous studies in the area have reported the presence of the OCPs and trace metals in edible tissues of inhabiting seafood species [16–23]. Among the polluted seafood species reported in the NAV are those of the Tetraodontidae family, like the pufferfish Sphoeroides spp. [24], its feeding habits include zoo benthivores and omnivores, including bivalves, gastropods, and macrophytes [25–27]. Due to the commercial value of this species, the constant pollution with OCPs and trace metal residues of the NAV, the risk of being subjected to carcinogenic or non-carcinogenic effects by the consumption of Sphoeroides spp. is evident. In this sense, the aim of the present study was to evaluate the carcinogenic and non-carcinogenic risk of the Sphoeroides spp. from the NAV.

Eighty-six fillet of the pufferfish Sphoeroides spp. were obtained from the local fishers with a fishery permit in the NAV, located in the southern part of the Gulf of California in Mexico between 25.4° and 25.7° N and 108.85° − 108.55° W [28, 29]. None of the specimens were taken alive to perform the following laboratory experiments that were performed in accordance to national or international agreements guidelines and regulations.

Pufferfishes were obtained once every quarter of a year between summer (July 2016) and autumn (October 2017). Sampling points were selected among frequent fishing areas identified by local fishers. Frozen pufferfishes were dissected to remove the fillet that was divided into two parts, one part was kept in aluminum foil for posterior OCP content analysis, and the other part was kept in Ziploc® bags for trace metal content analysis. All samples were kept frozen in an ice acid-based cooler and transported for storage in a freezer in the Pollution laboratory located in the CIIDIR-SINALOA, Mexico. During each sampling period, pH, temperature (°C), salinity (‰), and dissolved oxygen (DO) were registered with a multiparameter HANNA® HI-9828 (HANNA Instruments, Woonsocket, RI, US).

Trace metal analysis

Acid digestion with nitric acid according to Méndez et al. [30] was the procedure used for the trace metals extraction, as proposed for the extraction of heavy metals from muscle by atomic absorption spectroscopy. Each collected Sphoeroides spp. sample was dehydrated until constant weight. Five grams of dehydrated sample was digested in Erlenmeyer glasses with a concentrated HNO₃ and HCLO₄ acids (1:5) mixture. Samples in the digestion procedure were boiled on a heating plate until dryness. Cooled and dried samples were mixed in 24 mL of deionized water and 1 mL of HCl and stored at room temperature for later analysis. The trace metals were determined by atomic absorption spectrophotometry (AVANTA GBC ®, US) with an air/acetylene flame burner and hollow cathode lamps. Trace metal standards of 0.125, 0.25, 0.5, 1, 2, and 4 ppm were prepared to verify the accuracy of the instrument. The quality control of the procedure was achieved using PACS and MESS reference materials (Supplementary table 1) in blank samples that were analyzed every 10 days and digested samples of the Sphoeroides spp. fillet.

Organochlorine pesticides analysis

For the OCP extraction and purification of fillet samples, 10 g of each sample was dehydrated in an Erlenmeyer flask with 5 g of Na₂SO₄ (Sigma Aldrich, St. Louis, MO, US) and 30 mL of hexane (chromatographic grade). The extraction, analysis, and quantification of fillet samples were performed following the modified EPA-8081b [31] by gas chromatography.

The gas chromatograph (Perkin Elmer® XL, Auto System®, Perkin Elmer, Inc., Waltham, MA, US) is coupled to a 63Ni-ECD detector, TotalChrom Navigator® software, and ELITE-CLP2 column (Perkin Elmer®). A six-point calibration curve was constructed (0.001 to 0.05 µL mL^− 1). The chromatography conditions were: oven heating ramp to 120°C (for 1 min) until 240°C increasing at a rate of 4°C min^− 1; EDC at 300°C; injector at 260°C; 2 µL of sample injection; split-split less on; attenuation of 16; nitrogen as a carrier gas at 8.7 psi at 30 mL min^− 1. Pesticide mix standards (EPA 8081®) and pesticide subrogate mix (SUPELCO® Cat. CRM46845 and CRM48460, respectively), and linearity, detection limit, and recovery range (Supplementary table 2) were calculated to ensure the accuracy of the results.

A database was constructed with Microsoft Excel®, and data were statistically analyzed with Minitab17® software. A Kolmogorov Smirnoff normality test, ANOVA, and posthoc Tukey test were performed to determine significant differences.

Human health risk assessment

Estimated daily intakes (EDI) for trace metals (TM) and OCP in the Sphoeroides spp. fillet from the NAV were calculated [8, 32, 33] (Eq. 1–2):

\({EDI}_{TM}= \frac{{TM}_{C }\times {VIR}_{d}\times ED\times EF}{BW \times AT}\) (Eq. 1)

\({EDI}_{OCP}= \frac{{VIR}_{d}\times {OCP}_{C}}{BW}\) (Eq. 2)

where TM_C or OCP_C = average TM (µg g^− 1) or OCP (mg kg^− 1) concentration in fish tissue (dry weight); VIR_d = average daily fish consumed in Mexico (32.88 g day^− 1), ED = exposure duration (26 years), EF = exposure frequency (365 days year^− 1), BW = Mexican adult average human weight (74.3 kg), and AT = average time (365 days year^− 1 per 26 years).

Non-carcinogenic risk

For TM the target hazard quotient (THQ) (Eq. 3) and the hazard index (HI) (Eq. 4) [32, 34, 35] were used to calculate the non-carcinogenic risk.

\({THQ}_{noncancer}= \left(\frac{EF\times ED \times {VIR}_{d} \times {TM}_{C}}{RfD+ BW+ {AT}_{noncancer}}\right) \times {10}^{-3}\) (Eq. 3)

\(HI= \sum _{n}^{i}{THQ}_{n}\) (Eq. 4)

If THQ or HQ is below 1 represents non-carcinogenic risk; if it is above 1 non-carcinogenic risk can occur.

For OCP, the non-carcinogenic risk was assessed by the hazard quotient (HQ) (Eq. 5) and the total hazard quotient (THQ) [36, 37] (Eq. 6) :

\(\text{HQ }\text{= }\frac{EDI}{{RfD}_{OCPx}}\times 100\) (Eq. 5)

\(THQ= \sum _{i=1}^{n}{HQ}_{i}\) (Eq. 6)

where, RfD_OCPx = reference doses for “x” OCP.

HQ or THQ values lower than 100 represent a non-carcinogenic risk, but HQ or THQ above 100 means that non-carcinogenic symptoms can occur.

Carcinogenic risk

For the TM the risk of cancer for each TM was calculated by the incremental lifetime cancer risk (ILCR) [38] (Eq. 7):

\(ILCR={EDI}_{TMx}\times {CSf}_{TMx}\) (Eq. 7)

CSf = Cancer slope factor of carcinogenic TM estimated [39].

For OCP the carcinogenic risk (CR_lim) was calculated [40] (Eq. 8):

\({\text{CR}}_{\text{lim}}\text{ }\text{= }\frac{\text{ARL}\text{ × }\text{BW}}{\sum _{m=1}^{x}{C}_{m} \times { CSF}_{OCPx}}\) (Eq. 8)

where CRl_im is the maximum allowable consumption rate for an aquatic product (kg day^− 1); ARL is the maximum acceptable individual lifetime risk level, which is dimensionless and a value of 10^− 5 was used in this study (Rodriguez-Hernandez et al. 2016; Yu et al. 2014); CSF_OCPx is the cancer slope factor of OCP_x for a carcinogenic risk (mg kg^− 1 day^− 1).

Morphometric data and TM and OCP concentrations in fish edible fillet

In this study, 20 OCP and seven trace metals (TM) were detected in the Sphoeroides spp. fillets from NAV. Some TM concentrations were detected above MRLs and showed a carcinogenic and non-carcinogenic risk for human consumption. A not normal distribution was found with the Kolmorov-Smirnoff (KW) test (α = 0.05), concentration of trace metals (KS = 0.117, p < 0.01), size (KS = 0.141, p = 0.010), weight (KS = 0.211, p < 0.010), and OCPs concentration (KS = 0.43, p < 0.01) (Table 1). The average length and weight of specimens (24.028 cm and 334.28 g, respectively), were similar to specimens of the same genus from shallow brackish water areas [41]. A correlation was found between weight (Pearson, α = 0.05, p = 0.001) and height (Pearson, α = 0.05 p = 0.0005) and with the concentration of trace metals (Pearson, α = 0.05 p = 0.179).

TM concentration in Sphoeroides spp.

Although comparison between size and TM concentration in fishes from contaminated environments is recommended [10, 42], in the present study no correlation between size and the TM concentration was found. Nevertheless, the presence of TM in the Sphoeroides spp. fillet suggests that the concentration of these pollutants in the environment exceeds the biological capacities to be metabolically eliminated by this species [43]. The NAV is neighbored by the largest intensive agriculture area in Mexico, the Guasave Valley [15], which has been draining for decades its irrigation surpluses containing TM (mg kg^-1) and OCP (µg kg^-1) residues. These pollutant residues inputs have become deposited in the sediments of the lagoon, particularly in areas close to agricultural drains [44], where TM or OCP residues have been reported in sediments and edible tissues of inhabitant marine species [17, 18, 20, 22, 35, 45-47].

The TM concentrations in Sphoeroides spp. presented the following trend: Zn > Fe > Pb > Ni > Mn > Cu > Cd, from which, Cd, Cu, Fe, Mn, Pb, and Zn were above MRLs established by some countries´ Environmental Protection Agencies [48-55], or were higher than in other marine fish [49, 56-60]. Cd was detected in just one specimen.

In this study, Zn was detected in 100% of samples, with an average concentration higher than the recommended MRLs. The higher concentration could be a response to lithogenic or anthropogenic sources [61]. In recent years, the number of boats has been increasing due to tourism and artisanal fisheries in the NAV [15], the paints used to avoid fouling or the nodes of batteries could be the anthropogenic sources, or the effluents from the thermal power plant [49], like the Topolobampo power plant that operates under a combined cycle using natural gas or fuel-oil. The concentration of Zn varies according to the organs analyzed [42, 62]. These studies showed how the concentration of Zn is related to the weight and size of the fish, but it has been evident that the concentration of Zn in the environment is an essential factor for its bioaccumulation [63, 64]. The high concentration of Zn found in the Sphoeroides spp. fillet can be attributed to the intensive use of chemical fertilizers in the neighbored agricultural valley of Guasave, in which wastes end up leached or discharged to the NAV. These residues settle in the sediments, and as previously reported, they increase the concentration of Zn in the tissues of aquatic organisms [63, 65].

The average concentration of Fe (80.52 mg kg^-1 dw) detected in this study was below the MRL. Iron is an important metal for life, essential as a component of proteins, such as hemoglobin, and of muscle tissue [66]. The origin of its high concentration in the analyzed fillet could be attributed to the presence and erosion of this element from the earth crust in the region, or by the untreated sewage discharges from municipal and rural populations to the lagoon [35, 67]. This Fe concentration is similar to that detected in Atherina hepsetus (78 mg kg^-1) [68], higher than in farmed snapper species (5.103-19.985 mg kg^-1) [69], and lower than in bivalves in the same region [70]. These differences can be attributed to the detritivorous feeding habits from sediments rich in Fe and the metabolic differences among species.

The Pb concentration was the third highest in the samples analyzed. The average concentration for Pb in this study exceeded the recommended MRL (Table 1) and was higher than in other species of carnivorous fishes [71, 72]. In the case of NAV, the Pb values in Sphoeroides spp. can be attributed to Pb in sediments and water due to agricultural residues [65]. The latter could reflect the impact of the economic development in the last decade and has been related to the increased amounts of vehicles and traffic and the use of leaded gasoline or diesel or to the mining residues that could be carried by rivers [44, 73].

The concentrations of Cu showed values above MRL, and even though Cu is an essential nutrient for the synthesis of proteins and functioning of enzymes, its consumption in excess presents adverse effects on human health [11]. In the present study, Cu showed higher concentrations compared to other carnivorous fishes [71, 72, 74]; this could be attributed to the level of TM pollution in NAV caused by human activities [15], and the position of carnivorous fishes in the food web due to biomagnification [56, 75].

The concentrations of Cd, Cu, and Ni showed the significant relationship previously reported with trophic levels. Benthic invertebrates have shown a species-specific accumulation of these TM in the food web rather than biomagnification [56], and it has been reported that bioaccumulation of TM depends on fish feeding habits and the inhabited region [58]. Sphoeroides spp. is a carnivorous species and invertebrates are an important part of its diet [76].

The pufferfish Sphoeroides spp. is a euryhaline fish that inhabits coastal lagoons and estuaries [77], and NAV is a coastal lagoon neighbored by intensive agriculture and aquaculture that extend for more than 100,000 ha of territory. These intensive activities constantly dispose of their residues, after irrigation or water exchange, directly to the lagoon through discharge channels.

Ni in the present study was detected in a third of the samples (32.56%) with an average concentration of 8.06 ± 3.56, which is below the MRLs. This element is not essential for human health, but it is toxic above 0.5 mg kg^-1. The latest reports indicate that the presence of Ni in marine organisms is due to anthropogenic or natural sources, but that in areas with high oil industrial activity the values rise [78], which may represent risks to human health. However, in NAV there is no oil industry like the one found in the Gulf of Mexico and, as in previous studies [79], its presence could be due to a lithogenic origin. The Ni values of the edible tissue of Sphoeroides spp. were higher to those reported in recent studies on other marine species of the region [35, 47, 67, 80, 81]. However, the concentration of Ni in predatory fishes has been reported to be slightly higher than those in herbivorous and omnivorous species [79].

The average concentration of Mn in this study was 6.13 ± 3.86 mg/kg in 38.37% of the samples. Mn is considered a micronutrient, enzyme activator, and main component in mitochondrial enzymes such as superoxide dismutase and pyruvate carboxylase [13], but, above certain concentrations, it generates damage at the genetic, enzymatic, or neurological level [82, 83]. Although the FAO does not establish a Mn limit for fish; some environmental protection agencies such as those in Nigeria and the World Health Organization, the Mn concentration in fishes such as Sphoeroides spp. was above these MRLs [48, 84].

The TM concentrations in Sphoeroides spp. are higher than those previously reported in marine fishes [84-86]. This higher concentration depends on various factors, the feeding habit of Sphoeroides spp. as carnivorous, the enrichment factor in the sediments and the continental crust contribution, and the grade and source of anthropogenic pollution [15, 28, 35, 87].

OCP concentrations in Sphoeroides spp.

Twenty-two OCPs were detected in the muscle of Sphoeroides spp., several of them already listed as prohibited by the member countries of the WTO [88]. γ‒Chlordane was the most frequent OCP, and the analytes with the highest average concentration were α‒HCH, followed by γ‒chlordane (Table 1). No relation was found between size and OCPs concentration (Kruskal-Wallis, α 0.05, p = 0.442), nor between weight and pesticide concentration (Kruskal-Wallis, α 0.05, p = 0.438). In fish, the concentration of OCPs in tissues follows the following order of magnitude: liver> intestine> skin> muscle [89, 90], and in the present study, the presence of these contaminants was determined only in the muscle of Sphoeroides spp. to assess their risk due to consumption.

Among the OCPs determined in the muscle of Sphoeroides spp. were HCHs, such as α‒HCH (24.7 µg kg^-1 ww), β‒HCH (3.52 µg kg^-1 ww), γ‒HCH (5.33 µg kg^-1 ww), and δ‒HCH (3.52E-03 mg kg^-1ww), none of these concentrations were above MRLs (Table 1). Technical grade HCH is a mixture of isomers of this molecule, α‒HCH (60-70%), β‒HCH (5-12%), γ‒HCH (10-15%), δ‒HCH (6- 10%), the commercial lindane product consists of 99% γ‒HCH, and the presence of all HCH isomers and the ratio of γ‒HCH to the rest indicates historical contamination from the use of lindane and technical HCH [40, 91, 92].

The DDT was detected in only two samples below the detection limit, but isomers, p, p'‒DDE (0.12 µg kg^-1 ww) and p, p'‒DDD (10.11 µg kg^-1 ww) were detected with a frequency of 26.74 and 10.47%, respectively. The high ratios of p, p'‒ DDD (0.52) and p, p'‒DDD (0.48), and the absence of p, p'‒ DDT suggest that there have been no recent applications of p, p'‒DDT in the area. DDE is the most persistent metabolite of p, p'‒DDT in the environment that can last up to 10 years available in the environment [93]. The presence of non-detected p, p'‒DDT concentration in the edible tissue of Sphoeroides spp. suggests the persistence of residues from the 60's to the '90s in the sediments of NAV. During that time, p, p'‒DDT was an insecticide used intensively to control insects in crops [94]. This persistence can be corroborated by the present detected low concentrations of p, p'‒ DDT in Sphoeroides spp. previously detected in fishes from the same study area [17, 18] Currently, in Mexico, technical p, p'‒ DDT is an OCP commercially banned but of restricted use exclusively by the Mexican Ministry of Health for the control of vectors of infectious diseases such as the mosquito that mainly transmits dengue.

From the aldrin family, aldrin (0.8 µg kg^-1 ww), dieldrin (0.13 µg kg^-1 ww), and endrin (2.22 µg kg^-1 ww) were detected, with a frequency of 3.49, 15.12 and 16.28%, respectively. None of these OCPs were detected above MRLs. Previous studies determined that high aldrin and lower endrin and dieldrin concentrations could be due to the recent use of the three pesticides on agricultural crops [50, 95]. In the present study, the higher ratios for dieldrin (0.43) and endrin (0.47) than for aldrin (0.1) indicate historical contamination. In this case, most of the dieldrin available in the environment could be originated from the oxidation of aldrin, as previously reported [96]; in Mexico, as stated above it is actually prohibited, but it was very popular in the past as an insecticide in agriculture [94, 97].

Chlordane for technical use consists of a mixture of the stereoisomers α‒chlordane, γ‒chlordane, heptachlor, and heptachlor epoxide, which present concentrations of 0.02, 22.94, 0.17, and 0.07 µg kg^-1, and a frequency of 60.47, 3.49, 1.16 and 3.49%, respectively. In the present study, the detected concentrations of these OCPs were lower than the MRLs (Table 1). Nevertheless, technical chlordane has a restricted use as a termiticide, and it is not prohibited in Mexico. The ratios of the isomers, α‒ chlordane (0.0007), γ‒chlordane (0.98), heptachlor (0.007), and heptachlor epoxide (0.003), and the low frequency of the last two in the samples imply a historical use and might be attributed to atmospheric transport or their runoff in the last decades from the neighboring agricultural area.

The endosulfan technical product consists of 70% endosulfan I and 30% endosulfan II, whose concentrations (0.25 and 0.21 µg kg^-1, respectively) were below the MLRs (Table 1). A degradation product of technical endosulfan is endosulfan sulfate, a product of the metabolism of some fungi such as Trametes. versicolor and Pleurotus ostreatus [98]; and which was detected with an average concentration of 4.93 µg kg^-1 and a frequency of 11.63% of the samples. In this way, it is plausible that the residual products of endosulfan and its isomers from the neighboring agricultural valley indicate endosulfan's recent use due to its low persistence between 30 and 150 days [99], resulting in the bioaccumulation by Sphoeroides spp.

Methoxychlor at a mean concentration of 6.14 µg kg^-1 ww, was detected in 18.6 % of the samples. This OCP is used as a larvicide in crops and can persist in the environment for up to 6 months [100]. Indeed, the detection in the fillet of Sphoeroides spp. would imply a recent use in the agricultural area of the Valle de Guasave. Although the concentration detected is within the permissible limits (Table 1), in Mexico, its use is restricted to the exclusive use in seed treatment for sowing in crops of rice, oats, barley, peas, beans, corn, sorghum [101].

Table 1. Frequency percentage, mean concentration, standard deviation (±SD) of trace metals and OCPs in the fillet of Sphoeroides spp. from NAV, Mexico.

Trace metal (mg kg^-1 dry weight)	Frequency (n 86)	Concentration	±SD	MRLs
Cd	1.16	1.45	0	3x10^-5ai- 0.002^a
Cu	41.86	5.06	21.06	0.03-0.12^b
Fe	100	80.52	73.54	0.7- 0.8^c
Mn	38.37	6.13	3.86	1^ab
Ni	32.56	8.06	3.53	0.0005^a-0.14^b
Pb	83.72	18.42	16.53	0.0003^ai - 0.004^a
Zn	100	189.55	1062.73	0.03-0.12^ab
OCPs (µg kg^-1 wet weight)	Frequency (n 86)	Concentration	±SD	MRLs
Aldrin	3.49	0.80	0.93	10^d
p, p'‒DDD	10.47	0.11	0.07	1250^e
p, p'‒DDE	26.74	0.12	0.19	1250^e
p, p'‒DDT	2.33	ND	ND	1250^e
Dieldrin	15.12	0.13	0.23	10^d-100^h
Endosulfan I	32.56	0.25	0.38	50
Endosulfan II	22.09	0.21	0.16	50
Endosulfan sulfate	11.63	4.93	9.85	50
Endrin	16.28	2.22	4.94	10^d-50^h
Endrin aldehyde	33.72	0.05	0.09	10^d
Endrin ketone	13.95	4.93	6.96	50^h
Heptachlor	1.16	0.17	0	10^d-20^e
Heptachlor epoxide	3.49	0.07	2.02x10^-6	10^d
Methoxychlor	18.6	6.14	22.8	10^f
α‒HHC	12.79	24.7	32.3	10-250^e
β‒HHC	6.98	3.52	7.14	10-250^e
γ‒HHC	1.16	1.71		5-250^e
δ‒HHC	10.47	5.33	13.2	250^e
α‒Chlordane	3.49	0.02	0	2−50^g
γ‒Chlordane	60.47	22.94	72.5	NE
^a NSSP [102]; ^bAnandkumar et al. [48]; ^cSelvam et al. [49]; ^dAdeleye et al. [50]; ^eBaqar et al. [51]; ^fBuah-Kwofie et al. [52]; ^gOyekunle et al. [53]; ^hChandra et al. [54]; ^IRajkowska-Myśliwiec et al. [55]; NE = Not established; Grey boxes are pollutants concentration above MRLs; ND Below limit of detection

Seasonal concentrations of OCPs

The presence of OCPs in Sphoeroides spp. tissue was detected in the five collection periods. The seasons with the highest concentration of OCP were the spring and summer of 2016, standing out the spring in which methoxychlor, α‒HCH endosulfan sulfate, and γ‒chlordane were the OCPs with the highest concentration (94.29, 56.95, 23.94, and 10.80 µg kg^-1 dw, respectively). In the summer, they were β‒HCH and γ‒chlordane (99.18 and 19.48 µg kg^-1 dw, respectively) (Fig. 2). The bioavailability of OCPs has been correlated with the yearly seasons, their concentrations have been reported to be higher in the seasons after the rainy season or in the dry season [103, 104]. In this study, the same characteristics are presented when the highest concentrations occur in the spring after the intensive agriculture irrigation season in the zone [35], or after the rainy season due to atmospheric deposition and effluent increase on NAV [105], when OCP become bioaccumulated by marine organisms [106].

Seasonal concentrations of TM

The highest concentration of TM was detected in the spring of 2017 (516 mg kg^-1). Some TMs were detected at low concentrations, but all TM were detected in the summer of 2016. Fe, Pb, and Zn were the TM detected in all seasons (Fig. 3). The bioavailability of TM depends mainly on the sediment's physicochemical characteristics, chemical fractions, and pH, most of them affect their bioavailability [107]. However, the chemical form in which they are found and the anthropogenic contributions increase their basal concentration in a specific site. In the case of NAV, it is adjacent to more than 150,000 ha of intensive agricultural activities (> 160,000 ha). The presence of Cd, Zn, and Cu coincides with the use of fertilizers and pesticides from this agricultural area [108], shrimp culture and domestic sludge, which influence the concentration of Ni and Pb in seawater and sediments in the region of NAV [67].

Mexico.

TM risk of Sphoeroides spp.

The EDI values for the consumption of Sphoeroides spp. and their TM content indicate that most of the TM analyzed, except for Pb, do not exceed the EDI values. Pb exceeded the maximum recommended daily limit by 28.8-times at a rate of 32 g day^-1 of Sphoeroides spp. fillet, representing a potential risk of long-term non-carcinogenic effects due to its consumption (Table 2). Compared with recent reports on the concentration of TM in the muscle of other marine fish species, the concentrations of Cd, Ni, Zn, and Pb in the Sphoeroides spp. fillet were higher. Lower concentrations of Cu and Fe have been reported in Apocryptes bato, Harpadon nehereus, Polynemus paradiseus, and Otolothoides pama from coastal areas around the mouth of the Meghna River in Bangladesh, as well as of Mn in Cepola macrophthalma in Karatas, Turkey [60, 109-112] (Table 3). The concentration of TM depends on the degree and sources of anthropogenic contamination present in the areas and the feeding habits of the species. As explained above, Navachiste is constantly impacted by effluents from intensive irrigation residues from the neighboring agricultural valley, and Sphoerpoides spp. is a pelagic and benthic carnivorous species. Therefore, its location in the food web allows it to bioaccumulate biomagnified TM. The same occurs with the species reported for Bangladesh. Although the area where species were caught are defined as marine species [109], they possibly were captured from coastal areas impacted by human activities.

Table 2. Concentration, estimated daily intake (EDI), target hazard quotient (THQ), and hazard index (HI) for trace metals analyzed in the edible fillet of Sphoeroides spp. from Navachiste, Mexico.

Metal	Concentration (mg kg^-1 dw)	EDI (mg kg^-1 dw)		THQ	ILCR
Cu	1.45	2.38		0.06	9.5 × 10^-2
Fe	5.06	37.82		0.05	2.6 × 10^-1
Mn	80.52	2.88		0.02	4.0 × 10^-1
Ni	6.13	3.79		0.19	7.6 × 10^-2
Zn	8.06	89.03		0.30	6.8 × 10^-4
Cd	18.42	0.68		0.68	2.7 × 10^-1
Pb	189.55	8.65		2.16	3.5 × 10^-2
			HI = 2.84

Table 3. Trace metal concentrations (mg kg^-1wet weight) in marine fishes, Sphoeroides spp. (this study in gray cells) and other regions of the world.

Species	Cu	Fe	Mn	Ni	Cd	Zn	Pb
Apocryptes bato^c	46.98	151.17	-	-	-	101.38	0.65
Blennius ocellaris^b	0.26	10.75	1.15	0.14	-	7.98	0.11
Sphoeroides spp	5.06	80.52	6.13	8.06	1.45	189.55	18.42
Centropristis striata^d	0.154	-	-	-	-	3	0.009
Cepola macrophthalma^b	0.26	3.72	6.45	0.29	-	10.47	0.22
Chelidonichthys lucerna^b	0.21	3.42	0.035	0.11	-	4.02	0.04
Citharus linguatula^b	0.27	3.13	0.94	0.14	-	5.87	0.07
Coilia nasus^a	0.48	-	-	-	0.02	6.94	0.06
Collichthys lucidus^a	0.36	-	-	-	0.02	4.93	0.06
Conger conger^b	0.25	2.88	0.69	0.13	-	8.06	0.1
Cynoglossus joyneri^a	0.44	-	-	-	0.01	6.18	0.06
Cynoscion regalis^d	0.216				0.022	3.48	0.001
Engraulis encrasicolus^b	2.78	27.58	2.57	0.22	0.04	40.36	0.57
Gaidropsarus mediterraneus^b	0.33	5.36	1.1	0.17	-	6.57	0.29
Gaidropsarus spp.^b	0.23	2.71	0.36	0.12	-	3.99	0.07
Gobius niger^b	0.24	4.83	1.42	0.13	-	7.05	0.32
Harpadon nehereus^a	0.35	-	-	-	0.06	4.8	0.07
Harpadon nehereus^c	35.4	148.82	-	-	-	106.72	0.2
Lophiogobius ocellicauda^a	0.65	-	-	-	0.04	6.16	0.05
Lophius budegassa^b	0.3	3.44	0.47	0.16	-	7.14	0.02
Merlangius merlangus^b	0.23	7.41	1.12	0.12	-	5.86	0.21
Merluccius merluccius^b	0.21	2.42	0.25	0.11	-	4.76	0.16
Miichthys miiuy^a	0.48	-	-	-	0.04	4.77	0.03
Mullus barbatus^b	0.42	6.62	0.49	0.17	-	7.18	0.3
Mullus surmuletus^b	0.46	14.03	0.59	0.16	-	5.83	0.16
Ophidion spp^b	0.23	3.92	0.22	0.12	-	6.31	0.13
Otolothoides pama^c	30.29	177.46	-	-	-	107.22	0.38
Pagellus acarne^b	0.27	4.85	2.95	0.25	-	7.56	0.78
Paralichthys dentatus^d	0.231	-	-	-	0.005	3.36	0.055
Pegusa lascaris^e	0.16	-	-	-	0.005	0.2	0.11
Phycis blennoides^b	3.18	120.5	0.53	0.02	0.01	13.42	0.07
Polynemus paradiseus^c	33.95	188.15	-	-	-	101.38	0.48
Pomatomus saltatrix^b	0.19	10.14	0.51	0.1	-	4.72	0.05
Pomatomus saltatrix^d	0.364	-	-	-	0.011	6.31	0.02
Scomber scombrus^b	1.18	11.11	0.49	0.14	0.01	6.61	0.14
Scyliorhinous canicula^b	0.27	7.05	0.7	0.15	-	11.67	0.09
Serranus cabrilla^b	0.44	3.77	1.65	0.17	-	8.79	0.43
Serranus hepatus^b	0.36	5.69	0.39	0.15	-	8.33	0.12
Solea spp.^b	0.23	4.98	0.54	0.12	-	0.12	0.12
Sparus aurata^e	0.13	-	-	-	0.002	0.2	0.05
Spicara flexuosa^b	0.61	3.9	0.52	0.13	0.01	6.33	0.25
Tautoga onitis^d	0.296				0.002	3	0.007
Torpedo torpedo^b	0.1	1.2	0.21	0.06	-	2.52	0.03
Trachinus draco^b	0.25	2.9	0.32	0.13	-	7.62	0.17
Trachurus mediterraneus^e	0.23	-	-	-	0.03	0.3	0.05
Trachurus trachurus^b	0.79	10.2	0.81	0.17	-	8.04	1.72
Uranoscopus scaber^b	0.2	3.07	0.29	0.11	-	4.91	0.05
^aNoman et al., 2022; ^bVetsis, et al., 2021; ^cHossain et al., 2022; ^dYe et al., 2022; ^eKarayakar et al., 2022

The THQ for each metal, except for Pb (THQ = 2.16), was less than 1. The Pb value indicates a high possibility of suffering non-carcinogenic effects in the mid-term due to the consumption of Spheroides spp. from NAV at 32.88 g day^-1. However, if the consumption ratio were increased to a rate of 120 g day^-1 on average (equivalent to three "tacos" of Sphoeroides spp. fillet), the chances of presenting symptoms due to non-carcinogenic effects increase substantially for Pb (THQ = 7.89) and other TMs such as Cd (2.49) and Zn (1.08).

Regarding the carcinogenicity risk, the ILCR values were greater than 1 × 10^-6 (lifetime cancer risk probability), and the risk is not significant if the ILCR value is lower than 1 × 10^-6. In the present study, all ILCR values of TM analyzed were above 1 × 10^-6, indicating a high risk for cancer development in the long-term (Table 2) [113].

OCP risk in Sphoeroides spp.

The non-carcinogenic and carcinogenic risk values were obtained for each OCP, considering a probability of 5/100,000 individuals having symptoms during a lifetime (Table 4). The average concentration of each OCP did not exceed the RfD values. The calculated HQ values < 100 and THQ = 55.2 do not imply a risk of having symptoms of non-carcinogenic diseases in the mid- or long-term after consuming this species. Regarding the carcinogenic risk (CR_Lim), only aldrin, p, p'‒ DDD, p, p'‒ DDE, dieldrin, endosulfan, heptachlor, heptachlor epoxide, α‒HCH, β‒HCH, and γ‒HCH CR_Lim showed values that represent a high probability for developing cancer in the long-term (Table 4). These values were higher than those reported on edible muscle in fishes, their whose CR_Lim could allow eating higher portions of meals before reaching a potential health risk [40, 114]. In the present study, the CR_Lim of some OCPs was remarkably lower than the meal size analyzed here (32.88 g), implying that the consumption of the edible fillet of Sphoeroides spp. over a long time could be a potential cause of cancer at this meal portion. Nevertheless, the amount of OCP in raw fish tissue was considered here, and factors such as the bioavailability of pesticides in the tissue, the possibility that the ingested OCPs are totally or partially excreted, or the amount lost during the cooking process of the fillet may alter the concentration of OCP [40, 115].

Table 4. OCP concentration (mg kg^-1), oral slope factor (OSF), reference dose (RfD), estimated daily intake (EDI), target hazard quotient (THQ), hazard quotient (HQ), and cancer risk limit (CR_Lim) in Sphoeroides spp. of the Navachiste Lagoon System.

*OCP*	*Concentration*	*OSF*	*RFD*	*EDI*	HQ	*CR_Lim*	*THQ* *55.2*
Aldrin	0.00062	17	0.0003	0.00028	1.257487	0.0053
p, p'‒DDD	0.0003	0.24	ND	0.00014		2.7812
p, p'‒DDE	0.00012	ND	ND	0.00005		1.7769
Dieldrin	0.00014	0.34	ND	0.00006	0.123454	0.0342
Endosulfan	0.00022	ND	0.006	0.0001	0.001957
Endosulfan II	0.0002	ND	ND	0.00009
Endosulfan sulfate	0.0027	ND	ND	0.0012
Endrin	0.002	ND	ND	0.0009	0.347707
Endrin aldehyde	0.00005	ND	ND	0.00002
Endrin ketone	0.0025	ND	0.0003	0.0011
Heptachlor	0.00011	4.50	0.00005	0.00005	0.015652	0.0960
Heptachlor epoxide	0.0011	9.10	0.00001	0.0005	0.269983	0.1059
Methoxychlor	0.0052	ND	0.005	0.0024	0.057705
α‒Chlordane	0.00009	ND	ND	0.00004
γ‒Chlordane	0.022	ND	ND	0.0099
α‒HCH	0.025	6.3	0.008	0.0113	0.144997	0.0005
β‒HCH	0.0035	1.8	ND	0.0017		0.0113
δ‒HCH	40.005	0.24	ND	0.0022
γ‒HCH	0.0017	ND	0.0003	0.0008	0.268175	0.0053
NOTE: ND = below detection limits

The health risk posed by the TM and OCPs concentration in the edible tissue of Sphoeroides spp from the NAV in the southwestern part of the Gulf of California was evaluated. The results of non-carcinogenic and carcinogenic risks showed that the Pb value indicates a high possibility of suffering non-carcinogenic effects in the mid-term. However, if the consumption ratio increases up to 120 g day^-1 of edible tissue (equivalent to three tacos per day), the non-carcinogenic effects symptoms increase substantially for Pb and become potential for Cd and Zn. The carcinogenic risks evaluated, highlighted that the ILCR values were more significant for a lifetime cancer risk probability, and the TM analyzed here were above minimum ILCR (> 1 × 10^-6), showing a high-risk potential for cancer development in the long-term. These results showed how the NAV continues to be polluted by the pesticides and chemical residues from agriculture, aquaculture, and urban drainages that end in the NAV.

Data availability

The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.

Acknowledgement

Thanks to Mrs. Ingrid Mascher for the English grammar and edition improvement of the manuscript.

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Health risk of consuming Sphoeroides spp. from the Navachiste Lagoon Complex due to its trace metals and organochlorine pesticides content

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Abstract

Figures

Highlights

Introduction

Methods

Trace metal analysis

Organochlorine pesticides analysis

Human health risk assessment

Non-carcinogenic risk

Carcinogenic risk

Results And Discussion

Morphometric data and TM and OCP concentrations in fish edible fillet

TM concentration in Sphoeroides spp.

OCP concentrations in Sphoeroides spp.

Seasonal concentrations of OCPs

Seasonal concentrations of TM

TM risk of Sphoeroides spp.

OCP risk in Sphoeroides spp.

Conclusions

Declarations

References

Additional Declarations

Supplementary Files

Status:

Version 1