# Compound-specific recording of gadolinium pollution in coastal waters by great scallops

## Abstract

Gadolinium-based contrast agents (GBCAs), routinely used in magnetic resonance imaging (MRI), end up directly in coastal seawaters where gadolinium concentrations are now increasing. Because many aquatic species could be sensitive to this new pollution, we have evaluated the possibility of using shellfish to assess its importance. Gadolinium excesses recorded by scallop shells collected in Bay of Brest (Brittany, France) for more than 30 years do not reflect the overall consumption in GBCAs, but are largely controlled by one of them, the gadopentetate dimeglumine. Although its use has been greatly reduced in Europe over the last ten years, gadolinium excesses are still measured in shells. Thus, some gadolinium derived from other GBCAs is bioavailable and could have an impact on marine wildlife.

## Introduction

For thirty years now, linear or macrocyclic gadolinium-based contrast agents (GBCAs) are routinely used in magnetic resonance imaging (MRI)1. They were initially assumed to have virtually no side effects, but gadolinium can accumulate in tissue, bone and brain2,3,4. Moreover, linear GBCAs cause nephrogenic systemic fibrosis, a debilitating and potentially life-threatening disease, for patients with kidney failure5,6. Thus, the use of some linear GBCAs has been reduced over the last decade, and recently banned in Europe7. As GBCAs are not recovered during wastewater treatment, more than 200 tons of anthropogenic gadolinium are conveyed each year by rivers of developed and densely populated areas, and end up directly in coastal seawaters where gadolinium concentrations, still low, are now increasing8,9,10,11,12. Aquatic species are sensitive to this new pollution: for example, gadolinium accumulates in the livers of fish and induces antioxidant enzyme productions13; in presence of gadolinium, larvae of sea urchins display abnormal shapes and growth14; gadolinium exposure produces mitochondrial and anti-inflammatory pathways in freshwater mussels15.

The incorporation of anthropogenic gadolinium by shellfish is evidenced by their Rare Earth Elements (REE) patterns. Unlike cerium which has two valence states in aqueous systems, and is easily decoupled from lanthanum and praseodymium, its neighbouring REEs, gadolinium has only one trivalent valence state, and cannot be easily decoupled from other rare earth elements by natural processes. Thus rocks and unpolluted waters do not show any large anomalies in gadolinium. Some mollusc shells from densely populated coastal areas such as Tokyo Bay16 or the southern North Sea17 now display positive gadolinium anomalies explained by pollution. Similar anomalies are also measured in shells from the Canary Islands and the French coasts, showing that this pollution affects vast regions (Fig. 1). Consequently, coastal shellfish could represent valuable archives of this pollution. Among non-motile shellfish, the great scallop (Pecten maximus) could be considered as a fixed sensor recording environmental variations because of its longevity (up to 12 years), high growth rate of its shells (up to 350–400 µm/day during growing phase) and production of both seasonal and daily growth bands18. We have studied a collection of wild great scallops collected alive during the last thirty years at the same sampling site of Bay of Brest at a mean depth of 20 m (Supplementary Fig. 1). All these scallops were fished in late fall and were between 3 and 4 years old (estimated with winter marks, see Fig. S2). Their sizes ranged from 8 to 10 cm. We analysed fragments of their left valves, corresponding to the carbonate formed since the winter preceding their catch.

## Results and Discussion

The abundances of REEs in shells Fig. 2 and Supplementary Table 2) are low and highly variable: they range between 6 × 10−5 and 3 × 10−3 times the shale reference19. The shapes of the REE patterns are similar to those of other coastal shellfish (e.g., Fig. 1), with variable negative cerium anomalies (Ce/Ce* = 0.65–1.33, see Methods for the calculations of REE anomalies). In bivalves, shells result from the activity of the mantle epithelium inside specific internal liquid20. Their components are derived from organic matter, inorganic particles and water that have been assimilated by the mollusks16. Thus, their REE patterns are different from those of local seawater21, with less marked LREE depletions relative to shales. Furthermore, they display small but significant positive gadolinium anomalies (Gd/Gd* = 1.00–1.50, Fig. 3), which indicate that shells incorporated small amounts of anthropogenic gadolinium.

The gadolinium anomalies (Gd/Gd*) in scallop shells do not show a clear temporal evolution (Fig. 3). Since shells have very different levels of REE concentrations, a given amount of anthropogenic gadolinium can result in very different Gd/Gd* ratios in carbonates. To reduce this effect, we estimated the gadolinium excess in each sample using the difference between the measured gadolinium concentration and the interpolated one (ΔGd = Gd − Gd*). These excesses in scallop shells (ΔGd = 0–2.3 ng/g) display a complex temporal evolution (Fig. 3b). The oldest sample collected in 1960, before the use of GBCAs, does not show any significant excess in gadolinium. A marked increase in gadolinium excesses is seen from 1989 to 2005, followed by a sharp decline until 2010 when normal levels are observed again. Afterwards, the excesses seem to increase again without reaching the 2005 maximum, but the data show some spread. Such an evolution is unexpected because the use of GBCAs has always been increasing since their introduction on the market. It could depend on the bioavailability of anthropogenic gadolinium as determined by its speciation in seawater.

## Methods

For each sample, about 100 mg of carbonates were spiked with a solution of pure Tm and dissolved in HNO3 in a Teflon beaker. REE have been separated from the major elements and concentrated before analysis27. Abundances were determined using a high-resolution inductively coupled plasma-mass spectrometer Thermo Element HR at Institut Universitaire Européen de la Mer (IUEM), Plouzané, France. Each sample was analysed in duplicate or in triplicate, and the results were averaged28. Results on a carbonate standard obtained during the sessions are given in Supplementary Information.

The Gd anomalies are calculated using the Gd/Gd* ratio, where Gd* is the interpolated Gd concentration for a smooth Post Archean Australian Shale-normalized REE pattern and Xn is the concentration of element X normalised to PAAS:

$${{{\rm{Gd}}}^{\ast }}_{{\rm{n}}}={{{\rm{Sm}}}_{{\rm{n}}}}^{1/3}\times {{{\rm{Tb}}}_{{\rm{n}}}}^{2/3}$$

The gadolinium excesses are simply given by the following equation:

$${\rm{\Delta }}\mathrm{Gd}={\rm{Gd}}-{{\rm{Gd}}}^{\ast }$$

Based on standards and sample replicates, the precisions for abundances and element ratios (including Gd/Gd* ratios) are in most cases much better than 5% (2 RSD) (see Supplementary Information). Typical errors for Gadolinium excesses in shells are assumed to be about 0.25 ng/g (2 σ).

## Data Availability

All data is available in the main text or the Supplementary Materials.

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## Acknowledgements

We are grateful to Sebastien Seuron for his help with gadolinium consumption data, to Richard Greenwood (Open University) and Michel Rafini (UBO) for discussions and grammatical corrections, and to Jean-Charles Larsonneur for stimulating discussions. This work was supported by the “Laboratoire d’Excellence” LabexMER (ANR-10-LABX-19) and co-funded by grants from the French Government under the program “Investissements d’Avenir”.

## Author information

L.C. and Y.-M.P. provided the supply of the biological material thanks to the archives of biogenic carbonates (“Saint-Jacothèque”) preserved at the European Institute for Marine Sciences (IUEM), Plouzané. S.L.G. and J.-A.B. performed chemical separations and wrote the first draft of the manuscript. B.G. analyzed the prepared samples by ICP-MS. S.L.G., J.-A.B., D.B.S., L.C. and Y.-M.P. contributed to interpretation of the results and preparation of the manuscript.

Correspondence to Jean-Alix Barrat.

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