1. bookVolume 73 (2022): Edition 2 (June 2022)
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1848-6312
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Fish consumption habits of pregnant women in Itaituba, Tapajós River basin, Brazil: risks of mercury contamination as assessed by measuring total mercury in highly consumed piscivore fish species and in hair of pregnant women

Publié en ligne: 07 Jul 2022
Volume & Edition: Volume 73 (2022) - Edition 2 (June 2022)
Pages: 131 - 142
Reçu: 01 Nov 2021
Accepté: 01 May 2022
Détails du magazine
License
Format
Magazine
eISSN
1848-6312
Première parution
26 Mar 2007
Périodicité
4 fois par an
Langues
Anglais
Abstract

Slijev rijeke Tapajós u amazonskom području u Brazilu jedno je od najaktivnijih područja iskopavanja zlata na svijetu. U ovoj smo studiji procijenili navike konzumiranja ribe i razinu izloženosti metil-živi u 110 stanovnica Itaitube u peripartumu mjerenjem ukupne koncentracije žive u kosi (THg). Osim toga, istražili smo sezonske razlike u koncentracijama žive u dvjema najčešćim vrstama konzumnih piscivornih riba: tucunaré (Cichla spp.) i pescada (Plagioscion squamosissimus). U tih je ribljih vrsta THg tijekom sušne sezone iznosio 0,62±0,07 mg/kg za Cichla spp. te 0,73±0,08 mg/kg za P. squamosissimus. Tijekom kišne sezone koncentracija THg bila je 0,39±0,04 mg/kg za Cichla spp. i 0,84±0,08 mg/kg za P. squamosissimus. Sudionice su izjavile da su konzumirale Cichla spp. (44 %) i P. squamosissimus (67 %). Srednja koncentracija THg izmjerena u kosi bila je 1,6±0,2 mg/kg±std. Prosječna koncentracija THg u kosi bila je viša od referentne doze Američke agencije za zaštitu okoliša (krat. US EPA) koja iznosi 1 mg/kg, a čak u 48 % sudionica izmjerena je viša koncentracija. Također, srednja vrijednost koncentracija THg u ribi bila je iznad sigurnosne granice (0,5 mg/kg) za P. squamosissimus i tijekom sušne i kišne sezone, a za Cichla spp. samo tijekom sušne sezone. Rezultati istraživanja pokazuju da bi trudnice trebale izbjegavati konzumaciju ovih piscivornih ribljih vrsta. Stoga je razvidna potreba za redovitim programom praćenja razine žive na tom području.

Key words

Ključne riječi

Since its beginning in 1970, artisanal gold mining in the Amazon region has been releasing 200 t of mercury (Hg) a year into the environment (1) and has been responsible for deforestation, forest degradation, and limited biomass recovery (2, 3). When released into rivers elemental mercury (Hg0) used in the gold extraction process can be methylated to generate a highly toxic chemical form of Hg known as methylmercury (MeHg) (4), which then undergoes biomagnification along the trophic chain. The main sources for the transfer of MeHg to humans are aquatic biota and fish (1, 5, 6, 7) with more than 85 % and 95 % of total mercury concentration (THg) found in herbivorous and piscivorous fish tissue, respectively (8). The percentage of MeHg in muscle samples, in fact can be as high or even higher than 98 %, as reported in French Guiana carnivorous species (9) and the Madeira River in Brazil (10). Large-scale gold mining activity in this region has decreased since 1990, but artisanal gold mining has not stopped and is even increasing.

As fish is the primary protein source for local people, its consumption may reach as many as nine meals a week (11). This calls for monitoring fish Hg concentrations, but the vastness of the region makes it rather difficult. Since 1995, the number of research studies of Hg in the area has increased (8, 9, 10, 11, 12, 13, 14, 15), as there are other prominent sources of aquatic environment pollution with Hg besides gold mining (16), including its natural presence in soil, which is then released through erosion and land use for agriculture (17, 18, 19). During the rainy season, river levels rise and large areas are flooded. Previous studies have shown that flooded land increases MeHg levels in the aquatic environment (20, 21, 22). Another source of pollution with MeHg from inorganic Hg are the dams (23, 24, 25, 26, 27).

Methylmercury is neurotoxic and easily crosses biological barriers such as the placenta and blood brain barrier (28, 29, 30). In the Amazonian basin there have been reports of impaired cognitive function in children (31), motor performance, visual function, immune system, genotoxicity, and changes in blood pressure (32). Pregnant women and their foetuses are at particular risk of adverse health effects (33, 34, 35).

Even though the vastness of the area, intensified land use, burning of forests, and artisanal gold mining make it difficult to estimate possible health risks for the local population in direct contact with Hg, fish can be very useful to biomonitor its presence in the environment (36, 37, 38, 39, 40). Establishing total Hg concentrations can provide a reasonable insight or proxy into exposure to MeHg, as it accounts for more than 95 % of THg in piscivorous fish from the region (8, 9, 10).

Among the several local fish species, some are more consumed than others because they are highly palatable and abundant, including the tucunaré (Cichla spp.) and pescada (Plagioscion squamosissimus) species chosen for this study. Both are piscivorous and available throughout the year. In addition, these species are among the most consumed by citizens. Our aim was to establish their THg concentrations over 12 months and compare them with THg concentrations in the hair of mothers who had just given birth at the municipal hospital in Itaituba, Brazil to see if mercury exposure increased the health risk for pregnant women and their future newborns.

Participants and methods
Study area

The municipality of Itaituba (04°16’34.0” S, 55°59’01.0” W) is situated in the Tapajós River basin in the southwestern region of the state of Pará, Brazil, with a population of over 98 thousand and territory of over 62 million km2 (41) (Figure 1). It is the reference centre in public health care for patients referred from other municipalities (Aveiro, Jacareacanga, Novo Progresso, Rurópolis and Trairão) and receives patients from riverbank communities, countryside, forest, and gold mining areas such as those marked in Figure 1.

Figure 1

Geographical position of Itaituba

Study participants

This study included 110 pregnant women (aged 18–40; mean age 24.6±4.8 years), admitted to the obstetric clinic at the Municipal Hospital of Itaituba (state of Pará, Brazil) to give childbirth. For the purpose of this study, we designed a specific questionnaire to collect their socio-demographic data (including residence, age, education, marital status, race, and occupation), health status, weight, height, blood pressure, smoking habit, diet, alcohol use, and fruit consumption. We also collected information about their fish consumption, including the species and weekly estimates of meals (g). To help them estimate consumption per meal, we showed them a silicon (50 and 100 g) fish filet very similar to the natural fish filet.

All participants were informed about all study details (duration, objectives, method, risks, and benefits) and signed the informed consent form before they entered the study. The study followed the principles described in the Declaration of Helsinki and was approved by the Research Ethics Committee of the University of the State of Pará (UEPA), Santarém, Brazil (approval No.: CAAE 94880318.9.0000.5168 on 11/21/2018).

Hair sampling

The participants also gave hair samples (n=110), which were taken with sterile scissors as close as possible to the scalp in the occipital region to minimise aesthetic changes. Each sample was placed in a paper envelope until analysis. Considering that hair grows 1 cm a month on average, we took only four centimetres off the tip of the hair for THg analysis to obtain an average Hg concentration in the last four months of pregnancy.

To remove impurities, hair samples were first washed with the 0.1 %, (v/v) TritonTM X-100 solution (Sigma-Aldrich, St. Louis, MO, USA) and then with ultra-pure water. Excess water was rinsed with acetone (Sigma-Aldrich) and samples dried at room temperature. Each sample was then cut into very thin pieces with sterile scissors for better homogenisation.

Fish sampling and river level information

Cichla spp. and P. squamosissimus are mostly piscivores, yet occasionally they also feed on crustaceans and other invertebrates (42, 43, 44, 45, 46). In general, they are sedentary, although they have a short lateral range of movement (47, 48). These two species are not protected by spawning regulations and are sold at markets throughout the year.

All samples used in this study were purchased from the same artisanal fishermen in Itaituba, by whose account the fish had been caught in the small lakes around the village of São Luiz do Tapajós in the municipality of Itaituba (Figure 1). This upper Tapajós river area receives water from small tributaries with artisanal gold mines. Purchases were always made between the 15th and 17th of each month from July 2018 to June 2019 to cover the dry (July–December) and the rainy (January–June) season corresponding to low and high river water levels, respectively, measured in Itaituba with a pole placed about 10 m from the bank (Figure 2). Fish were weighed and their size measured. The samples consisted of dorsolateral muscle cuts, divided by season into groups of 60 and frozen at -20 °C until analysis. The dry season group contained 30 samples of Cichla spp. and P. squamosissimus each and so did the rainy season group.

Figure 2

Variations of the Tapajós River water levels (cm) in Itaituba from July 2018 to June 2019

THg analyses

Aliquots (duplicates) weighing 0.005–0.007 g of finely cut hair or 0.05–0.06 g of fresh fish were placed on quartz boats and inserted into a direct mercury analyser, DMA-80 (Milestone Srl, Sorisole, Italy), as this method does not require sample pretreatment because it involves thermal degradation of the sample, catalytic conversion, amalgamation, and spectrophotometry (a mercury lamp with a wavelength equal to 253.55 nm). Oxygen (99.99 % purity) was used as the carrier gas, and the detection limit was 0.0015 ng. To ensure analytical quality we used certified reference materials NIES 13 (human hair; National Institute for Environmental Studies, Tsukuba, Japan) and BCR-463 (tuna fish flesh; European Commission Directorate - Joint Research Centre, Geel, Belgium). Respective recoveries of 94 and 97 % were routinely observed for either.

Risk assessment calculation

The risk was calculated for each woman by dividing hair THg concentration by either the hair reference dose (RfD) proposed by the United States Environmental Protection Agency (US EPA) of 1.0 mg/kg (49) or by the lowest observable adverse effect hair concentration (LOAEHC) of 0.3 mg/kg associated with an adverse neurodevelopmental effect (50). The US EPA hair RfD corresponds to the provisional tolerable weekly Hg intake of 0.7 μg/kg body weight (PTWI) adopted in 2001 based on neurologic developmental effects in children associated with exposure to MeHg from maternal diet in utero (51). It is more protective than other relevant RfDs (52, 53), which is why we selected it to assess the risk for the newborns of our study participants.

Statistical analyses

The normality of data distribution was tested with the Kolmogorov-Smirnov and Shapiro-Wilk test significant differences (p<0.05) confirmed with one-way analysis of variance (ANOVA). The software used was Prism GraphPad 8 (GraphPad Software, San Diego, CA, USA).

Results and discussion
Fish consumption habits

Our participants declared consuming 21 fish species during pregnancy (Table 1), 13 of which are non-piscivorous. Piscivorous Cichla spp. and P. squamosissimus were at the top of consumed fish in that group, as reported by 44 and 67 % of participants, respectively.

Fish species consumed by pregnant women (n=110) from Itaituba, Brazil

Fish local name (species) Participants reporting eating listed fish (N) % Fish description by diet
Tambaqui (Colossoma macropomum) 90 82 Frugivore
Pescada branca (Plagioscion squamosissimus) 74 67 Piscivore
Pacú (Serrassalmidae spp.) 60 54 Frugivore
Tucunaré (Cichla spp.) 49 44 Piscivore
Aracú (Leporinus spp.) 41 37 Omnivore
Caratinga (Geophagus spp.) 40 36 Omnivore
Surubim (Pseudoplatystoma spp.) 37 33 Piscivore
Charutinho (Hemiodus spp.) 33 30 Omnivore
Dourada (Brachyplatystoma rousseauxii) 33 30 Carnivore
Filhote (Brachyplatystoma filamentosum) 33 30 Carnivore
Pirarucu (Arapaima gigas) 30 27 Piscivore
Curimatá (Prochilodus nigricans) 28 25 Detritivore
Acari (Pterygoplichthys spp.) 22 20 Detritivore
Matrinxã (Brycon spp.) 22 20 Omnivore
Aruanã (Osteoglossum bicirrhosum) 21 19 Carnivore
Pirarara (Phractocephalus hemioliopterus) 21 19 Omnivore
Apapá (Pellona spp.) 18 16 Carnivore
Piau (Anostomidae spp.) 16 14 Detritivore
Pirapitinga (Piaractus brachypomus) 16 14 Frugivore
Jaraqui (Semaprochilodus spp.) 2 2 Detritivore
Mapará (Hypophthalmus spp.) 2 2 Planktivore
Fish THg

The fish did not significantly differ in weight and length between the seasons (Table 2). It has been claimed that larger and heavier carnivorous fish tend to concentrate more Hg (54), but we found no significant correlation between THg concentration and fish weight or size (Figure 3), which is in line with an earlier report for Cichla spp. in Jacareacanga, which is 300 km upstream the Tapajós River from Itaituba (36), whereas contrasting correlations were reported for carnivorous species Pseudoplatystoma sp. (surubim) and Brachyplatystoma flavicans (dourada), also consumed in Itaituba (39) or herbivorous species caratinga (Geophagus spp.) and carnivorous traíra (Hoplias malabaricus) caught in Jacareacanga (36).

Figure 3

Relationship between mercury concentration and weight and total length of fish caught and consumed in Itaituba. Left columns: Cichla spp. (tucunaré; n=48); right columns: P. squamosissimus (pescada; n=48)

Biometric parameters in two predator fish species from the Tapajós River basin, Amazon, Brazil

Biometric parameters Dry season Rainy season
Mean ± SD Min–Max Mean ± SD Min–Max
Plagioscion squamosissimus Weight (g) 224±40 150–315 207±32 149–261
Total length (cm) 27.2±0.5 25.0–30.5 27.1±1.2 25.4–29.7
Standard length (cm) 22.4±1.4 20.1–24.8 22.4±1.2 20.7–25.4
Cichla spp. Weight (g) 344±129 195–792 271±69 194–406
Total length (cm) 29.4±3.1 25.0–38.5 27.8±2.0 25.5–32.1
Standard length (cm) 24.5±2.8 20.7–32 23.2±1.7 21.0–27.3

SD – standard deviation

Table 3 shows fish THg concentrations for both species by season. Dry season concentrations did not significantly differ between the two species, but Cichla spp. showed a 37 % lower THg (p<0.05) in the dry season, whereas THg concentrations in P. squamosissimus did not significantly differ between seasons.

Total mercury concentrations (mg/kg) in Cichla spp. (tucunaré) and P. squamosissimus (pescada) fish caught in the Tapajós River basin, Brazil

Dry season (July – December 2018) Rainy season (January – June 2019)
Cichla spp. (n=26) P. squamosissimus (n=24) Cichla spp. (n=24) P. squamosissimus (n=24)
Mean ± SD 0.62±0.35 0.73±0.37 0.39±0.21* 0.54±0.37
Min–max 0.17–1.68 0.05–1.37 0.12–0.94 0.25–1.65
Median 0.59 0.83 0.29 0.89
25th quartile 0.39 0.55 0.24 0.55
75th quartile 0.75 0.92 0.54 1.12

* Significantly different from dry season (p<0.05). SD – standard deviation

The maximum Hg concentration in fresh fish flesh recommended by the joint Food and Drug Administration (FDA) and the US EPA for consumption by pregnant or breastfeeding women and children below 12 years of age is 0.5 mg/kg (55). The following fish species should be avoided by this vulnerable population group: king mackerel, marlin, orange roughy, shark, swordfish, tilefish, and tuna bigeye (55), as they contain mean THg (recorded between 1990 and 2012) of 0.73, 0.49, 0.57, 0.98, 1.00, 1.12, 0.69 mg/kg fresh weight, respectively (56). In the dry season, 71 % of Cichla spp. and 80 % of P. squamosissimus specimens had THg above this recommended limit of 0.5 mg/kg. In the rainy season, this percentage dropped to 37 % for Cichla spp. and to 71 % for P. squamosissimus specimens.

Total mercury concentrations found in the present study are in the range of those previously reported for carnivorous fish from the Tapajós River basin (40), ranging from 0.4 to 1.51 mg/kg, and Itaituba in particular (8), ranging from 0.9 to 3.2 mg/kg. Previous studies showed that near Itaituba, THg concentrations in Cichla spp. ranged from 0.19 to 1.00 mg/kg (10, 57, 58) and in P. squamosissimus from 0.09 to 1.35 mg/kg (11, 58). Nowadays, after more than twenty years of studies at the Tapajós River basin, the THg levels in carnivorous fish are still above the safe limit of 0.5 mg/kg, and the same is true for THg concentrations in P. squamosissimus of the upper Amazon (59).

Hair THg and associated risks

Most of our study participants lived in the urban (n=75) area of Itaituba, followed by rural residents (n=17) and other (n=10) cities close to Itaituba (Figure 4). We found no difference in hair THg levels between these three groups of residents.

Figure 4

Distribution of participants by residence in and around Itaituba along the Tapajós River (Amazon, Brazil). The left panel shows residences as green dots. The lower part of the right panel shows the legend, translated as follows: Itaituba (Cidade de Itaituba); Urban area (Área urbana); Rural zone (Zona rural); Other cities (Outras cidades); Access roads (Vias deacesso) ; Water (Hidrographia); the Tapajós River (Rio Tapajós) ; Pará Municipalities (Municipios do Pará); State of Amazonas (Estado do Amazonas)

Table 4 shows hair THg levels by age, education level, marital status, race, and occupation groups. It does not include smoking as none reported to have smoked. None of these parameters significantly influenced hair THg concentration, nor did alcohol and fruit consumption (data not shown). The same is true for body mass index (mean ± SD: 27.4±4.4, median: 26.7, interquartile range: 24.4–30.2, n=110) (Table 5), and systolic/diastolic blood pressure (Table 6).

Relationship between socio-demographic characteristics of participating pregnant women from Itaituba and hair THg concentrations (mg/kg)

n % Hair THg (mean ± SD)
Age 18–20 40 36.4 2.3±3.5
21–30 57 51.8 1.6±1.4
31–40 13 11.8 1.5±2.3
Schooling Elementary school 54 49.2 2.1±2.3
High school 38 34.5 1.7±2.1
Academic education 18 16.3 1.5±2.3
Marital status Married or living as married 85 77.2 1.5±1.7
Single 25 22.8 2.5±4.3
Race White 2 1.8 0.6±0.01
Black 7 6.3 3.9±6.3
Mixed race 101 91.9 1.7±1.9
Occupation Housewife 90 81.9 1.8±2.0
Student 7 6.3 3.6±6.4
Other occupation 13 11.8 1.3±1.5

Relationship between body mass index (BMI) of participating pregnant women from Itaituba and hair THg concentration (mg/kg)

BMI Weight status n Hair THg (mean ± SD)
18.5–24.9 normal 33 1.9±2.8
25.0–29.9 overweight 49 1.8±2.7
30.0–39.9 obese 24 1.8±1.4
≥40.0 severe obesity 4 1.4±0.6

BMI was calculated as weight (kg) divided by height squared (m2)

Relationship between blood pressure in participating pregnant women from Itaituba and hair THg concentration (μg/g)

Blood pressure (mmHg, mean ± SD)a n Fish intake (g/week) Hair THg (mg/kg, mean ± SD)
Systolic Diastolic
101±7 65±6 40 0–100 1.1±0.9
103±8 68±8 26 101–200 1.7±1.3
101±10 67±5 23 201–400 1.6±1.3
103±12 69±10 21 401–800 2.43±2.2

a Blood pressure data are the mean of the last five months of pregnancy

Mean (±SD) hair THg concentration of all participants (n=110) was 1.6±1.5 mg/kg, ranging from 0.09 to 17.97 mg/kg (median: 0.95 mg/kg, interquartile range: 0.6–2.2 mg/kg, n=108), which is below previously reported means in small villages along the Tapajós River (10, 12, 14, 39, 54, 58, 60, 61, 62, 63, 64, 65, 66, 67, 68, 69, 70, 71, 72, 73). However, it exceeds the US EPA RfD (49) of 1 mg/kg for hair. In 30 participants (27 %) it was 2–6 mg/kg, in four (3.6 %) >6 μg/g, and in one as high as 17.9 mg/ kg.

Table 7 shows hair THg concentrations by fish consumption. Only the group consuming >400 g/week had significantly higher THg than the group consuming the lowest amounts (0–100 g/week) (p<0.05). Considering the US EPA RfD, health risk was increased in 33 % of the women consuming up to 100 g of study fish a week and in 56 % of those consuming more than that (Table 7). Considering the LOAEHC, neurodevelopmental risks of MeHg to the unborn child from maternal fish consumption (49) were increased in 85 % of women consuming up to 200 g/week and in all women consuming more than that (Table 7).

Hair THg levels in participating pregnant women from Itaituba and distribution of increased health risks from Hg exposure by fish consumption

Fish consumption (g/week) Hair THg (mg/kg, mean ± SD) Risk rate based on US EPA RfD a Risk rate based on LOAEHC b
0–100 (n=37) 1.1±0.9 0.7 (33 %) 2.3 (83 %)
101–200 (n=25) 1.7±1.3 1.7 (58 %) 5.7 (87 %)
201–400 (n=24) 1.6±1.3 1.1 (54 %) 3.8 (100 %)
> 400 (n=22) 2.4±2.2* 1.2 (57 %) 3.9 (100 %)

* Significant difference (p<0.05) from the group of women consuming 0–100 g of fish a week. a reference dose of 1.0 mg/kg (49). b lowest observable adverse effect hair concentration of 0.3 mg/kg, (50). Both risk rates are given as medians of distribution. Percentage in parentheses refers to women above these safety limits (raw data and calculations are available from the authors upon request)

Our hair THg findings are comparable with those reported for women of childbearing age from the island of Vieques offshore from Puerto Rico (median: 0.66 mg/kg, in 26.8 % of these women above the US EPA RfD) (74), Sweden (median: 0.7 mg/kg, in 20 % above the US EPA RfD) (75), and Moroccan coastal communities (median: 1.18 mg/kg, in 50 % above the US EPA RfD) (76).

Exposure in newborns has already been evidenced by a Spanish study (77) which established hair THg concentrations of 1.4 and 2.0 mg/kg in Madrid and Sabadell, exceeding the US EPA RfD in 39 and 60 % of newborns, respectively. Adverse effects have been highlighted worldwide for maternal hair THg concentrations in the range and even below those measured in our study: lower cognitive scores in six month-old US children associated with maternal hair THg concentration of 0.55 mg/kg (78, 79), impairment in behavioural ability in Chinese newborns associated with maternal hair THg concentration of 1.25 mg/kg (80), and lower psychomotor development index in 30-month-old Seychelles children associated with maternal hair THg concentration of 5.7 mg/kg (81). In indigenous Suriname communities, preterm birth (<37 weeks) was associated with maternal hair THg concentration of 3.5 mg/kg (82), and Michigan women who delivered too early (<35 weeks) had hair THg concentrations between 0.55 and 2.5 mg/kg (83).

Although mean hair THg concentration found in this study (1.6±0.2 mg/kg) is below that of the Barreiras community close to Itaituba (10.38 mg/kg) (13), it is nevertheless quite higher than those recorded in women of childbearing age from Barreiras and São Luis do Tapajós (villages close to Itaituba) between 1999 and 2012 (1.07±0.03 and 0.74±0.05 mg/kg, respectively) (84) and between hair THg concentrations found in women of childbearing age living in Santarém (300,000 inhabitants, a city located at the confluence of the Tapajós and Amazon Rivers) and Oriximiná (63,000 inhabitants, a city located on the Trombetas River, 40 km upstream from its confluence with the Amazon River) of 1.1±0.2 mg/kg and 2.5±1.0 mg/kg, respectively (85).

Previous studies conducted in women from villages located in the Tapajós River basin showed higher consumption of fish than our study participants: the mean amounts of fish ingested by women during one meal varied from 80±25 g in Açaituba to 147±72 g in São Luis do Tapajós (58). Mean fish portions (fish per meal per capita) of 243±135 g (median: 200 g) have been reported for the riverside general population (including adult men and women) of the Madeira River basin (86), and an average fish consumption of 110 g/day for fishermen of the Alta Floresta region (87) and for villagers of the Balbina reservoir (88). One should also take into account socioeconomic implications. The two piscivorous fish species evaluated in this study are more expensive than other species and most of our participants are of modest means, judging by self-reported elementary school level in nearly 50 % and unemployment in nearly 82 %, (Table 4), who therefore eat other, cheaper fish. This suggests that women with higher income may be at higher risk of Hg exposure than those with low income.

Previous studies have shown that non-piscivorous fish from the Tapajós River basin have considerably lower THg concentrations than piscivorous fish: 0.18 vs 1.66 mg/kg (8), 0.03–0.30 mg/kg vs 0.40–1.51 mg/kg (40), 0.095 vs 0.297 mg/kg (36), 0.05–0.08 vs 0.37–0.84 mg/kg (39), and 0.01–0.04 vs 0.12–0.66 mg/kg (89), respectively.

Considering that fish is beneficial for humans, non-piscivorous fish should be the best choice for consumption, especially during pregnancy. The supply of non-piscivorous fish bred in aquacultures has increased around Itaituba in recent times, such as that of the species Colossoma macropomum (the local name is tambaqui), which most of our participants (n=90) have reported eating. With its THg content of 0.08±0.03 mg/kg (39), 0.03±0.01 mg/kg (89), and 0.04±0.01 mg/kg (40), it may provide a healthier alternative at lower price. In addition, Itaituba is nowadays connected with the rest of the country by roads, which makes diet choices more diversified. This, however, is still not true for small villages along the Tapajós River banks. Furthermore, the expansion of local cattle and farms has increased the supply of beef and chicken at prices lower than those of fish.

This study has some limitations. The number of participants (n=110) is low, although it allows statistical analysis. Only two fish species have been sampled (although they are the two most favoured piscivorous species by our participants), and the ideal experimental protocol would have been to sample all of the species consumed and then collect consumption data for each participant (weight consumed on a weekly or monthly basis for each species) in order to calculate dietary exposure. However, its implementation was not feasible, as people are reluctant to measure the weight of each fish in their meal, and we could only get a rough estimation of weekly servings.

Conclusion

The consumption of Cichla spp. and P. squamosissimus should be completely avoided by pregnant women, since these species contain THg levels higher than 0.5 mg/kg and put their and newborns’ health at risk. However, fish is important for healthy diet, especially during pregnancy, and eating non-piscivorous fish seems to be a better alternative, since it contains much lower levels of Hg.

Our findings call for a continuous environmental biomonitoring programme for Hg in the Tapajós River basin.

Figure 1

Geographical position of Itaituba
Geographical position of Itaituba

Figure 2

Variations of the Tapajós River water levels (cm) in Itaituba from July 2018 to June 2019
Variations of the Tapajós River water levels (cm) in Itaituba from July 2018 to June 2019

Figure 3

Relationship between mercury concentration and weight and total length of fish caught and consumed in Itaituba. Left columns: Cichla spp. (tucunaré; n=48); right columns: P. squamosissimus (pescada; n=48)
Relationship between mercury concentration and weight and total length of fish caught and consumed in Itaituba. Left columns: Cichla spp. (tucunaré; n=48); right columns: P. squamosissimus (pescada; n=48)

Figure 4

Distribution of participants by residence in and around Itaituba along the Tapajós River (Amazon, Brazil). The left panel shows residences as green dots. The lower part of the right panel shows the legend, translated as follows: Itaituba (Cidade de Itaituba); Urban area (Área urbana); Rural zone (Zona rural); Other cities (Outras cidades); Access roads (Vias deacesso) ; Water (Hidrographia); the Tapajós River (Rio Tapajós) ; Pará Municipalities (Municipios do Pará); State of Amazonas (Estado do Amazonas)
Distribution of participants by residence in and around Itaituba along the Tapajós River (Amazon, Brazil). The left panel shows residences as green dots. The lower part of the right panel shows the legend, translated as follows: Itaituba (Cidade de Itaituba); Urban area (Área urbana); Rural zone (Zona rural); Other cities (Outras cidades); Access roads (Vias deacesso) ; Water (Hidrographia); the Tapajós River (Rio Tapajós) ; Pará Municipalities (Municipios do Pará); State of Amazonas (Estado do Amazonas)

Hair THg levels in participating pregnant women from Itaituba and distribution of increased health risks from Hg exposure by fish consumption

Fish consumption (g/week) Hair THg (mg/kg, mean ± SD) Risk rate based on US EPA RfD a Risk rate based on LOAEHC b
0–100 (n=37) 1.1±0.9 0.7 (33 %) 2.3 (83 %)
101–200 (n=25) 1.7±1.3 1.7 (58 %) 5.7 (87 %)
201–400 (n=24) 1.6±1.3 1.1 (54 %) 3.8 (100 %)
> 400 (n=22) 2.4±2.2* 1.2 (57 %) 3.9 (100 %)

Total mercury concentrations (mg/kg) in Cichla spp. (tucunaré) and P. squamosissimus (pescada) fish caught in the Tapajós River basin, Brazil

Dry season (July – December 2018) Rainy season (January – June 2019)
Cichla spp. (n=26) P. squamosissimus (n=24) Cichla spp. (n=24) P. squamosissimus (n=24)
Mean ± SD 0.62±0.35 0.73±0.37 0.39±0.21* 0.54±0.37
Min–max 0.17–1.68 0.05–1.37 0.12–0.94 0.25–1.65
Median 0.59 0.83 0.29 0.89
25th quartile 0.39 0.55 0.24 0.55
75th quartile 0.75 0.92 0.54 1.12

Relationship between socio-demographic characteristics of participating pregnant women from Itaituba and hair THg concentrations (mg/kg)

n % Hair THg (mean ± SD)
Age 18–20 40 36.4 2.3±3.5
21–30 57 51.8 1.6±1.4
31–40 13 11.8 1.5±2.3
Schooling Elementary school 54 49.2 2.1±2.3
High school 38 34.5 1.7±2.1
Academic education 18 16.3 1.5±2.3
Marital status Married or living as married 85 77.2 1.5±1.7
Single 25 22.8 2.5±4.3
Race White 2 1.8 0.6±0.01
Black 7 6.3 3.9±6.3
Mixed race 101 91.9 1.7±1.9
Occupation Housewife 90 81.9 1.8±2.0
Student 7 6.3 3.6±6.4
Other occupation 13 11.8 1.3±1.5

Biometric parameters in two predator fish species from the Tapajós River basin, Amazon, Brazil

Biometric parameters Dry season Rainy season
Mean ± SD Min–Max Mean ± SD Min–Max
Plagioscion squamosissimus Weight (g) 224±40 150–315 207±32 149–261
Total length (cm) 27.2±0.5 25.0–30.5 27.1±1.2 25.4–29.7
Standard length (cm) 22.4±1.4 20.1–24.8 22.4±1.2 20.7–25.4
Cichla spp. Weight (g) 344±129 195–792 271±69 194–406
Total length (cm) 29.4±3.1 25.0–38.5 27.8±2.0 25.5–32.1
Standard length (cm) 24.5±2.8 20.7–32 23.2±1.7 21.0–27.3

Relationship between body mass index (BMI) of participating pregnant women from Itaituba and hair THg concentration (mg/kg)

BMI Weight status n Hair THg (mean ± SD)
18.5–24.9 normal 33 1.9±2.8
25.0–29.9 overweight 49 1.8±2.7
30.0–39.9 obese 24 1.8±1.4
≥40.0 severe obesity 4 1.4±0.6

Fish species consumed by pregnant women (n=110) from Itaituba, Brazil

Fish local name (species) Participants reporting eating listed fish (N) % Fish description by diet
Tambaqui (Colossoma macropomum) 90 82 Frugivore
Pescada branca (Plagioscion squamosissimus) 74 67 Piscivore
Pacú (Serrassalmidae spp.) 60 54 Frugivore
Tucunaré (Cichla spp.) 49 44 Piscivore
Aracú (Leporinus spp.) 41 37 Omnivore
Caratinga (Geophagus spp.) 40 36 Omnivore
Surubim (Pseudoplatystoma spp.) 37 33 Piscivore
Charutinho (Hemiodus spp.) 33 30 Omnivore
Dourada (Brachyplatystoma rousseauxii) 33 30 Carnivore
Filhote (Brachyplatystoma filamentosum) 33 30 Carnivore
Pirarucu (Arapaima gigas) 30 27 Piscivore
Curimatá (Prochilodus nigricans) 28 25 Detritivore
Acari (Pterygoplichthys spp.) 22 20 Detritivore
Matrinxã (Brycon spp.) 22 20 Omnivore
Aruanã (Osteoglossum bicirrhosum) 21 19 Carnivore
Pirarara (Phractocephalus hemioliopterus) 21 19 Omnivore
Apapá (Pellona spp.) 18 16 Carnivore
Piau (Anostomidae spp.) 16 14 Detritivore
Pirapitinga (Piaractus brachypomus) 16 14 Frugivore
Jaraqui (Semaprochilodus spp.) 2 2 Detritivore
Mapará (Hypophthalmus spp.) 2 2 Planktivore

Relationship between blood pressure in participating pregnant women from Itaituba and hair THg concentration (μg/g)

Blood pressure (mmHg, mean ± SD)a n Fish intake (g/week) Hair THg (mg/kg, mean ± SD)
Systolic Diastolic
101±7 65±6 40 0–100 1.1±0.9
103±8 68±8 26 101–200 1.7±1.3
101±10 67±5 23 201–400 1.6±1.3
103±12 69±10 21 401–800 2.43±2.2

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