Chronic Reproductive Toxicity of Fomtec Enviro USP, a Fluorine-Free Firefighting Foam, to Northern Bobwhite (Colinus virginianus)
Abstract
1. Introduction
2. Materials and Methods
2.1. Study Design and Quail Husbandry
2.2. Test Chemicals, Exposure Verification, and Average Daily Intake (ADI)
2.3. Instrumental Analyses and Quality Control
2.4. Tissue Extraction Methods
2.4.1. Liver
2.4.2. Eggs
2.4.3. Feed
2.5. Gravimetric Lipid Determination
2.6. Chronic Toxicity Values (CTVs)
2.7. Endpoints and Statistics
3. Results and Discussion
3.1. Average Daily Intake (ADI)
3.2. Adult Weight Change
3.3. Egg Collection, Incubation, and Hatching Success
3.4. Mean Arrested Embryo Development Day and Percentage of Infertile Eggs
3.5. Pipped Only Proportion
3.6. Juvenile Survival
3.7. Chick Growth
3.8. Adult Biometrics, Relative Liver Weights, and Liver Lipid Content
3.9. Chick Biometrics, Relative Liver Weights, and Liver Lipid Content
3.10. Residue Analysis
3.10.1. Adult and Chick Liver
3.10.2. Whole Egg
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Death, C.; Bell, C.; Champness, D.; Milne, C.; Reichman, S.; Hagen, T. Per- and polyfluoroalkyl substances (PFAS) in livestock and game species: A review. Sci. Total Environ. 2021, 774, 144795. [Google Scholar] [CrossRef]
- Bossi, R.; Riget, F.F.; Dietz, R.; Sonne, C.; Fauser, P.; Dam, M.; Vorkamp, K. Preliminary screening of perfluorooctane sulfonate (PFOS) and other fluorochemicals in fish, birds and marine mammals from Greenland and the Faroe Islands. Environ. Pollut. 2005, 136, 323–329. [Google Scholar] [CrossRef]
- Giesy, J.P.; Kannan, K. Global Distribution of Perfluorooctane Sulfonate in Wildlife. Environ. Sci. Technol. 2001, 35, 1339–1342. [Google Scholar] [CrossRef]
- Newsted, J.L.; Beach, S.A.; Gallagher, S.P.; Giesy, J.P. Pharmacokinetics and Acute Lethality of Perfluorooctanesulfonate (PFOS) to Juvenile Mallard and Northern Bobwhite. Arch. Environ. Contam. Toxicol. 2006, 50, 411–420. [Google Scholar] [CrossRef] [PubMed]
- Hansen, E.; Huber, N.; Bustnes, J.O.; Herzke, D.; Bårdsen, B.-J.; Eulaers, I.; Johnsen, T.V.; Bourgeon, S. A novel use of the leukocyte coping capacity assay to assess the immunomodulatory effects of organohalogenated contaminants in avian wildlife. Environ. Int. 2020, 142, 105861. [Google Scholar] [CrossRef] [PubMed]
- Newsted, J.L.; Coady, K.K.; Beach, S.A.; Butenhoff, J.L.; Gallagher, S.; Giesy, J.P. Effects of perfluorooctane sulfonate on mallard and northern bobwhite quail exposed chronically via the diet. Environ. Toxicol. Pharmacol. 2007, 23, 1–9. [Google Scholar] [CrossRef] [PubMed]
- Custer, C.M.; Custer, T.W.; Dummer, P.M.; Etterson, M.A.; Thogmartin, W.E.; Wu, Q.; Kannan, K.; Trowbridge, A.; McKann, P.C. Exposure and Effects of Perfluoroalkyl Substances in Tree Swallows Nesting in Minnesota and Wisconsin, USA. Arch. Environ. Contam. Toxicol. 2014, 66, 120–138. [Google Scholar] [CrossRef] [PubMed]
- Place, B.J.; Field, J.A. Identification of Novel Fluorochemicals in Aqueous Film-Forming Foams Used by the US Military. Environ. Sci. Technol. 2012, 46, 7120–7127. [Google Scholar] [CrossRef] [PubMed]
- Anderson, R.H.; Long, G.C.; Porter, R.C.; Anderson, J.K. Occurrence of select perfluoroalkyl substances at U.S. Air Force aqueous film-forming foam release sites other than fire-training areas: Field-validation of critical fate and transport properties. Chemosphere 2016, 150, 678–685. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z.; Cousins, I.T.; Scheringer, M.; Hungerbühler, K. Fluorinated alternatives to long-chain perfluoroalkyl carboxylic acids (PFCAs), perfluoroalkane sulfonic acids (PFSAs) and their potential precursors. Environ. Int. 2013, 60, 242–248. [Google Scholar] [CrossRef] [PubMed]
- Xu, B.; Liu, S.; Zhou, J.L.; Zheng, C.; Weifeng, J.; Chen, B.; Zhang, T.; Qiu, W. PFAS and their substitutes in groundwater: Occurrence, transformation and remediation. J. Hazard. Mater. 2021, 412, 125159. [Google Scholar] [CrossRef] [PubMed]
- Hossain, F.; Dennis, N.M.; Subbiah, S.; Karnjanapiboonwong, A.; Guelfo, J.L.; Suski, J.; Anderson, T.A. Acute Oral Toxicity of Nonfluorinated Fire-Fighting Foams to Northern Bobwhite Quail (Colinus virginianus). Environ. Toxicol. Chem. 2022, 41, 2003–2007. [Google Scholar] [CrossRef] [PubMed]
- Longwell, A.S. An Evaluation of the Chronic Oral Toxicity of Fomtec Enviro USP, a Flourine-Free Firefighting Foam, to Northern Bobwhite Quail (Colinus virginianus). Master’s Thesis, Texas Tech University, Lubbock, TX, USA, 2022. [Google Scholar]
- OCSPP (Office of Chemical Safety and Pollution Prevention). Ecological Effects Test Guidelines; EPA: Washington, DC, USA, 2012; p. 25. [Google Scholar]
- Guthery, F.S.; Koerth, N.E. Substandard Water Intake and Inhibition of Bobwhite Reproduction during Drought. J. Wildl. Manag. 1992, 56, 760. [Google Scholar] [CrossRef]
- Dennis, N.M.; Subbiah, S.; Karnjanapiboonwong, A.; Dennis, M.L.; McCarthy, C.; Salice, C.J.; Anderson, T.A. Species- and Tissue-Specific Avian Chronic Toxicity Values for Perfluorooctane Sulfonate (PFOS) and a Binary Mixture of PFOS and Perfluorohexane Sulfonate. Environ. Toxicol. Chem. 2021, 40, 899–909. [Google Scholar] [CrossRef]
- Karnjanapiboonwong, A.; Deb, S.K.; Subbiah, S.; Wang, D.; Anderson, T.A. Perfluoroalkylsulfonic and carboxylic acids in earthworms (Eisenia fetida): Accumulation and effects results from spiked soils at PFAS concentrations bracketing environmental relevance. Chemosphere 2018, 199, 168–173. [Google Scholar] [CrossRef] [PubMed]
- Cequier-Sánchez, E.; Rodríguez, C.; Ravelo, Á.G.; Zárate, R. Dichloromethane as a Solvent for Lipid Extraction and Assessment of Lipid Classes and Fatty Acids from Samples of Different Natures. J. Agric. Food Chem. 2008, 56, 4297–4303. [Google Scholar] [CrossRef] [PubMed]
- Hara, A.; Radin, N.S. Lipid extraction of tissues with a low-toxicity solvent. Anal. Biochem. 1978, 90, 420–426. [Google Scholar] [CrossRef] [PubMed]
- Lee, C.M.; Trevino, B.; Chaiyawat, M. A Simple and Rapid Solvent ExtractionMethod for Determining Total Lipids in Fish Tissue. J. AOAC Int. 1996, 79, 487–492. [Google Scholar] [CrossRef] [PubMed]
- OECD. Test No. 206: Avian Reproduction Test; OECD: Paris, France, 1984. [Google Scholar] [CrossRef]
- Huss, D.; Poynter, G.; Lansford, R. Japanese quail (Coturnix japonica) as a laboratory animal model. Lab Anim. 2008, 37, 513–519. [Google Scholar] [CrossRef]
- Macklin, K.S.; Blake, J.P.; Hess, J.B.; Berry, W.D.; Voitle, R.A.; Hess, T.A. Bobwhite Quail Embryo Development; Extension Alabama A & M Auburn Univerities: Auburn, AL, USA, 2019. [Google Scholar]
Mean Body Weight ± SE (kg) | Mean Water Consumption ± SE (mL/Bird/Day) | ADI (mg/kg Body Weight/Day) ± SE | |
---|---|---|---|
Control | 0.245 ± 0.008 | 34.1 ± 1.2 | NA |
342 ng/mL SDS 1 | 0.223 ± 0.017 | 30.0 ± 2.3 | 0.05 ± 0.00 |
945 ng/mL SDS 2 | 0.224 ± 0.013 | 33.4 ± 1.6 | 0.15 ± 0.01 |
2015 ng/mL SDS 3 | 0.257 ± 0.009 | 37.4 ± 0.2 | 0.32 ± 0.01 |
3518 ng/mL DGMBE 1 | 0.223 ± 0.017 | 30.0 ± 2.3 | 0.49 ± 0.01 |
42,345 ng/mL DGMBE 2 | 0.224 ± 0.013 | 33.4 ± 1.6 | 6.5 ± 0.28 |
117,634 ng/mL DGMBE 3 | 0.257 ± 0.009 | 37.4 ± 0.2 | 18.4 ± 0.37 |
Reproductive Parameter | Control (n = 6) | FL (n = 3) | FM (n = 3) | FH (n = 3) |
---|---|---|---|---|
Eggs laid | 351 | 85 | 154 | 169 |
Eggs set | 102 | 52 | 68 | 71 |
Live 21 d embryos | 82 | 43 | 56 | 54 |
Hatchlings/eggs set (%) | 80 | 83 | 82 | 76 |
21-day-old survivors/hatchlings (%) | 88 | 84 | 91 | 87 |
Mean hatch success (%) | 80 ± 4.5 | 79 ± 8.6 | 83 ± 4.6 | 78 ± 16 |
Mean arrested development day | 15.7 ± 1.9 | 15.1 ± 1.8 | 16.0 ± 3.4 | 18.0 ± 2.3 |
Average percentage infertile (%) | 5.56 | 3.90 | 4.42 | 8.97 |
Juvenile survival rate (%) | 89 ± 4.2 | 83 ± 12 | 91 ± 3.8 | 87 ± 9.5 |
CTV Parameter | Fomtec ADI (mg/kg/day) | SDS ADI (mg/kg/day) | DGMBE ADI (mg/kg/day) | |||
---|---|---|---|---|---|---|
NOEL | LOAEL | NOEL | LOAEL | NOEL | LOAEL | |
Eggs laid/hen/day | NA | 14.3 | NA | 0.05 | NA | 0.5 |
Wt change—female initial to final | 14.2 | 394.2 | 0.05 | 0.3 | 0.5 | 18.4 |
Eggs laid/hen | NA | 14.3 | NA | 0.05 | NA | 0.5 |
Adult left tarsal | 14.2 | 394.2 | 0.05 | 0.3 | 0.5 | 18.4 |
Chick left wing | 14.2 | 155.6 | 0.05 | 0.1 | 0.5 | 6.5 |
Chick right wing | NA | 14.2 | NA | 0.05 | NA | 0.5 |
Chick left tarsal | NA | 14.2 | NA | 0.05 | NA | 0.5 |
Chick right tarsal | NA | 14.2 | NA | 0.05 | NA | 0.5 |
Chick liver | NA | 14.2 | NA | 0.05 | NA | 0.5 |
Control | FL (0.01%) | FM (0.1%) | FH (0.25%) | |||||
---|---|---|---|---|---|---|---|---|
SDS | DGMBE | SDS | DGMBE | SDS | DGMBE | SDS | DGMBE | |
Adult liver tissue | 104 ± 53 | 1372 ± 94 | 55 ± 15 | 836 ± 104 | 170 ± 62 | 855 ± 117 | 450 ± 98 | 1302 ± 53 |
Offspring liver tissue | 138 ± 27 | 1587 ± 97 | 98 ± 10 | 1045 ± 108 | 81 ± 7.4 | 103 ± 343 | 117 ± 60 | 794 ± 85 |
Whole egg | 16 ± 1.1 | 570 ± 16 | 16 ± 1.5 | 587 ± 11 | 83 ± 21 | 851 ± 75 | 316 ± 41 | 1163 ± 84 |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2025 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Longwell, A.S.; Hossain, F.; Subbiah, S.; Karnjanapiboonwong, A.; Suski, J.G.; Anderson, T.A. Chronic Reproductive Toxicity of Fomtec Enviro USP, a Fluorine-Free Firefighting Foam, to Northern Bobwhite (Colinus virginianus). Toxics 2025, 13, 474. https://doi.org/10.3390/toxics13060474
Longwell AS, Hossain F, Subbiah S, Karnjanapiboonwong A, Suski JG, Anderson TA. Chronic Reproductive Toxicity of Fomtec Enviro USP, a Fluorine-Free Firefighting Foam, to Northern Bobwhite (Colinus virginianus). Toxics. 2025; 13(6):474. https://doi.org/10.3390/toxics13060474
Chicago/Turabian StyleLongwell, Anna S., Farzana Hossain, Seenivasan Subbiah, Adcharee Karnjanapiboonwong, Jamie G. Suski, and Todd A. Anderson. 2025. "Chronic Reproductive Toxicity of Fomtec Enviro USP, a Fluorine-Free Firefighting Foam, to Northern Bobwhite (Colinus virginianus)" Toxics 13, no. 6: 474. https://doi.org/10.3390/toxics13060474
APA StyleLongwell, A. S., Hossain, F., Subbiah, S., Karnjanapiboonwong, A., Suski, J. G., & Anderson, T. A. (2025). Chronic Reproductive Toxicity of Fomtec Enviro USP, a Fluorine-Free Firefighting Foam, to Northern Bobwhite (Colinus virginianus). Toxics, 13(6), 474. https://doi.org/10.3390/toxics13060474