Skip to main content
SpringerLink
Log in

Twenty-four-hour temporal trend of melamine and its derivatives in urine in association with meal consumption: a panel study in Shanghai, China

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Timing of sampling is important for the exposure assessment of melamine (MEL) and its derivatives. This study aimed to investigate whether MEL and its derivatives in spot urine can effectively represent individual exposure levels throughout the day in adults and to explore their temporal trend before and after meal consumption for helping understand the timing of sampling and for assessing the potential exposure risk. This is a 2-day panel study with 43 college students being enrolled to provide urine specimens in 24 h (from the morning of the first day to the second day) and to answer a questionnaire on demographic characteristics, physical measurements, and time of having meal. Spearman correlation and Wilcoxon rank-sum test were used to examine the associations of the urinary concentrations of MEL and its derivatives in different sampled times and compare the concentrations’ differences before and after meal consumption. Urinary concentrations of MEL and its derivatives (ammeline (AMN), ammelide (AMD), and cyanuric acid (CYA)) in the first-morning urine at the second day and randomly selected spot urine were positively associated with the average concentrations in the previous 24-h urine (all P ≤ 0.002). Urinary MEL concentration increased rapidly after meal consumption, reaching a maximum at approximately 3 h and then decreased gradually towards baseline (P = 0.006). Two subjects (4.65%) had a cumulative daily intake exceeding the severest tolerable daily intake. MEL and its three derivatives in spot urine can effectively represent the average concentrations in the previous 24-h urine in adults. Meal consumption is still a notable source of exposure to MEL for humans. These findings are important for choosing a better sampling strategy of performing exposure assessment. Meanwhile, the acute elevation in urinary MEL concentration following meal consumption may pose a potential health risk.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

MEL:

melamine

AMN:

ammeline

AMD:

ammelide

CYA:

cyanuric acid

WHO:

World Health Organization

HQ:

hazard quotients

FMU:

first-morning urine

RSU:

randomly selected urine specimen

UPLC-MS/MS:

ultra-performance liquid chromatography–tandem mass spectrometry

LOD:

limit of detection

LOQ:

limit of quantitation

RSDs:

relative standard deviations

CDI:

cumulative daily intake

TDI:

tolerable daily intake

References

  • Allen LM, Briggle TV, Pfaffenberger CD et al (1982) Absorption and excretion of cyanuric acid in long-distance swimmers. Drug Metab Rev 13(3):499–516

    Article  Google Scholar 

  • Baek SH, Lim HB, Chun HS (2014) Detection of melamine in foods using terahertz time-domain spectroscopy. J Agric Food Chem 62(24):5403–5407

    Article  CAS  Google Scholar 

  • Bolden AL, Rochester JR, Kwiatkowski CF (2017) Melamine, beyond the kidney: a ubiquitous endocrine disruptor and neurotoxicant? Toxicol Lett 280:181–189

    Article  CAS  Google Scholar 

  • Chien CY, Wu CF, Liu CC et al (2011) High melamine migration in daily-use melamine-made tableware. J Hazard Mater 188(1-3):350–356

    Article  CAS  Google Scholar 

  • Choi L, Kwak MY, Kwak EH, Kim DH, Han EY, Roh T, Bae JY, Ahn IY et al (2010) Comparative nephrotoxicity induced by melamine, cyanuric acid, or a mixture of both chemicals in either Sprague-Dawley rats or renal cell lines. J Toxicol Environ Health Part A 73:1407–1419

    Article  CAS  Google Scholar 

  • Dalal RP, Goldfarb DS (2011) Melamine-related kidney stones and renal toxicity. Nat Rev Nephrol 7(5):267–274

    Article  CAS  Google Scholar 

  • Dobson RL, Motlagh S, Quijano M et al (2008) Identification and characterization of toxicity of contaminants in pet food leading to an outbreak of renal toxicity in cats and dogs. Toxicol Sci 106(1):251–262

    Article  CAS  Google Scholar 

  • Dufour AP, Behymer TD, Cantú R, Magnuson M, Wymer LJ (2017) Ingestion of swimming pool water by recreational swimmers. J Water Health 15(3):429–437

    Article  CAS  Google Scholar 

  • EFSA (European Food Safety Authority) (2010) Scientific opinion on melamine in food and feed. EFSA J 8:1573–1717

    Google Scholar 

  • Hsieh DP, Chiang CF, Chiang PH, Wen CP (2009) Toxicological analysis points to a lower tolerable daily intake of melamine in food. Regul Toxicol Pharmacol 55:13–16

    Article  CAS  Google Scholar 

  • Ingelfinger JR (2008) Melamine and the global implications of food contamination. N Engl J Med 359:2745–2748

    Article  CAS  Google Scholar 

  • Lin YT, Tsai MT, Chen YL et al (2013) Can melamine levels in spot overnight urine specimens predict the total previous 24-hour melamine excretion level in school children? Clin Chim Acta 420:128–133

    Article  CAS  Google Scholar 

  • Liu CC, Wu CF, Chen BH et al (2011) Low exposure to melamine increases the risk of urolithiasis in adults. Kidney Int 80(7):746–752

    Article  CAS  Google Scholar 

  • Liu GY, Li SJ, Jia JY et al (2010) Pharmacokinetic study of melamine in rhesus monkey after a single oral administration of a tolerable daily intake dose. Regul Toxicol Pharmacol 56(2):193–196

    Article  CAS  Google Scholar 

  • Liu SJ, Huang FF, Yang QF et al (2022a) Simultaneous determination of melamine and its homologues in urine by ultra-performance liquid chromatography-tandem mass spectrometry. Hyg Res 51(1):85–98

    Google Scholar 

  • Liu SJ, Zhao Q, Huang FF, Yang QF, Wang YF, Wang HW, Sun YY, Yan YJ et al (2022b) Exposure to melamine and its derivatives in Chinese adults: the cumulative risk assessment and the effect on routine blood parameters. Ecotoxicol Environ Saf 241:113714

    Article  CAS  Google Scholar 

  • Mannoni V, Padula G, Panico O et al (2017) Migration of formaldehyde and melamine from melaware and other amino resin tableware in real life service. Food Addit Contam 34(1):113–125

    Article  CAS  Google Scholar 

  • Mast RW, Jeffcoat AR, Sadler BM et al (1983) Metabolism, disposition and excretion of [14C]melamine in male Fischer 344 rats. Food Chem Toxicol 21(6):807–810

    Article  CAS  Google Scholar 

  • Panuwet P, Nguyen JV, Wade EL, D’Souza PE, Ryan PB, Barr DB (2012) Quantification of melamine in human urine using cation-exchange based high performance liquid chromatography tandem mass spectrometry. Chromatogr B Analyt Technol Biomed Life Sci 887:48–54

    Article  Google Scholar 

  • Poovarodom N, Tangmongkollert P, Jinkarn T et al (2011) Survey of counterfeit melamine tableware available on the market in Thailand, and its migration. Food Addit Contam 28(2):251–258

    Article  CAS  Google Scholar 

  • Qin YC, Lv XW, Li J et al (2010) Assessment of melamine contamination in crop, soil and water in China and risks of melamine accumulation in animal tissues and products. Environ Int 36(5):446–452

    Article  CAS  Google Scholar 

  • Sathyanarayana S, Flynn JT, Messito MJ et al (2019) Melamine and cyanuric acid exposure and kidney injury in US children. Environ Res 171:18–23

    Article  CAS  Google Scholar 

  • Saydah SH, Pavkov ME, Zhang C, Lacher DA, Eberhardt MS, Burrows NR, Narva AS, Eggers PW, Williams DE (2013) Albuminuria prevalence in first morning void compared with previous random urine from adults in the National Health and Nutrition Examination Survey, 2009-2010. Clin Chem 59(4):675–683

    Article  CAS  Google Scholar 

  • Shi XL, Dong RH, Chen JS et al (2020) An assessment of melamine exposure in Shanghai adults and its association with food consumption. Environ Int 135:105363

    Article  CAS  Google Scholar 

  • Sinclair M, Roddick F, Nguyen T et al (2016) Measuring water ingestion from spray exposures. Water Res 99:1–6

    Article  CAS  Google Scholar 

  • Sugita T, Ishiwata H, Yoshihira K (1990) Release of formaldehyde and melamine from tableware made of melamine—formaldehyde resin. Food Addit Contam 7(1):21–27

    Article  CAS  Google Scholar 

  • Sun JR, Zhang XC, Cao YN et al (2016) Ovarian toxicity in female rats after oral administration of melamine or melamine and cyanuric acid. PLoS One 11(2):e0149063

    Article  Google Scholar 

  • Tittlemier SA, Lau BP, Menard C et al (2010) Baseline levels of melamine in food items sold in Canada. II. Egg, soy, vegetable, fish and shrimp products. Food Addit Contam Part B Surveill 3(3):140–147

    Article  CAS  Google Scholar 

  • Weidemann DK, Weaver VM, Fadrowski JJ (2016) Toxic environmental exposures and kidney health in children. Pediatr Nephrol 31(11):2043–2054

    Article  Google Scholar 

  • Wen JG, Liu XJ, Wang ZM et al (2016) Melamine-contaminated milk formula and its impact on children. Asia Pac J Clin Nutr 25(4):697–705

    CAS  Google Scholar 

  • WHO (World Health Organization), 2009. Toxicological and health aspects of melamine and cyanuric acid. Report of a WHO expert meeting in collaboration with FAO. Supported by Health Canada.

  • Wittassek M, Koch HM, Angerer J, Bruning T (2011) Assessing exposure to phthalates-the human biomonitoring approach. Mol Nutr Food Res 55:7–31

    Article  CAS  Google Scholar 

  • Wu YT, Huang CM, Lin CC, Ho WA, Lin LC, Chiu TF, Tarng DC, Lin CH, Tsai TH (2010) Oral bioavailability, urinary excretion and organ distribution of melamine in Sprague-Dawley rats by high-performance liquid chromatography with tandem mass spectrometry. J Agric Food Chem 58(1):108–111

    Article  CAS  Google Scholar 

  • Xin H, Stone R (2008) Tainted milk scandal. Chinese probe unmasks high-tech adulteration with melamine. Science 322(5906):1310–1311

    Article  CAS  Google Scholar 

  • Yin RH, Dong Q, Li HS et al (2017) The effects of melamine with or without cyanuric acid on immune function in ovalbumin-sensitized mice. Res Vet Sci 114:254–261

    Article  CAS  Google Scholar 

  • Zhu HK, Kannan K (2018a) Continuing occurrence of melamine and its derivatives in infant formula and dairy products from the United States: implications for environmental sources. Environ Sci Technol Lett 5(11):641–648

    Article  CAS  Google Scholar 

  • Zhu HK, Kannan K (2018b) Distribution profiles of melamine and its derivatives in indoor dust from 12 countries and the implications for human exposure. Environ Sci Technol 52(21):12801–12808

    Article  CAS  Google Scholar 

  • Zhu HK, Kannan K (2019a) Inter-day and inter-individual variability in urinary concentrations of melamine and cyanuric acid. Environ Int 123:375–381

    Article  CAS  Google Scholar 

  • Zhu HK, Kannan K (2019b) Melamine and cyanuric acid in foodstuffs from the United States and their implications for human exposure. Environ Int 130:104950

    Article  CAS  Google Scholar 

  • Zhu HK, Kannan K (2020) Occurrence and distribution of melamine and its derivatives in surface water, drinking water, precipitation, wastewater, and swimming pool water. Environ Pollut 258:113743

    Article  CAS  Google Scholar 

Download references

Funding

This study was funded by the National Natural Science Foundation of China (Grant number: 82173520) and the Zhejiang Provincial Basic Public Welfare Research Project (the Analysis and Measurement Foundation) (Grant Number: LGC20B050005).

Author information

Author notes

  1. Shaojie Liu and Ruihua Dong contributed equally to this work.

Authors and Affiliations

  1. Department of Clinical Nutrition, The First Affiliated Hospital of Xiamen University, School of Medicine, Xiamen University, Xiamen, 361003, China

    Shaojie Liu & Zhiping Yang

  2. School of Public Health, Key Lab of Public Health Safety of the Ministry of Education, Fudan University, Shanghai, 200032, China

    Shaojie Liu, Ruihua Dong, Yifei Wang, Gengsheng He & Bo Chen

Authors
  1. Shaojie Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ruihua Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yifei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Zhiping Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gengsheng He
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bo Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

We would like to thank all the participants for their participation and kind assistance. S.L. and B.C. contributed to the conception and study design; S.L., Y.W., Z.Y., and B.C. contributed to the acquisition of data; S.L. and B.C. performed data analysis; S.L. and B.C. contributed to the interpretation of the data; S.L., R.D., and B.C. contributed to manuscript writing; G.H. and B.C. critically revised the manuscript. All authors read and approved the final manuscript.

Corresponding author

Correspondence to Bo Chen.

Ethics declarations

Ethical approval

The study was approved by the Medical Research Ethics Committee of the School of Public Health at Fudan University (approval number: 2021-TYSQ-03-72). We hereby certify that this manuscript represents original work and has not been submitted or published elsewhere. We confirm that all data and information presented in this manuscript are accurate and authentic to the best of our knowledge.

Consent to participate

Informed consent was obtained from all individual participants included in the study.

Consent for publication

The authors of this manuscript, titled Twenty-four-hour temporal trend of melamine and its derivatives in urine in association with meal consumption: a panel study in Shanghai, China, hereby provide their full consent for its publication in the Journal of Environmental Science and Pollution Research.

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible Editor: Lotfi Aleya

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

ESM 1

(DOCX 1561 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, S., Dong, R., Wang, Y. et al. Twenty-four-hour temporal trend of melamine and its derivatives in urine in association with meal consumption: a panel study in Shanghai, China. Environ Sci Pollut Res 30, 120225–120235 (2023). https://doi.org/10.1007/s11356-023-30740-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-023-30740-0

Keywords

Search

Navigation