Skip to main content

Advertisement

SpringerLink
Log in

Biological variation in kidney injury and kidney function biomarkers among farmers in Lamphun province, Thailand

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

Abstract

Frequent and long-term exposure to pesticides can induce acute kidney injury and subsequent chronic kidney diseases. In this study, we aimed to investigate the correlation between kidney injury, kidney function biomarkers, and pesticide use in farmers from the Pasang district, Lamphun province, Thailand. A cross-sectional study was performed in 59 farmers occupationally exposed to various types of pesticides. The levels of urinary neutrophil gelatinase-associated lipocalin (uNGAL), serum creatinine (sCr), urinary microalbumin-to-creatinine ratio (ACR), serum cystatin C (sCys-C), estimated glomerular filtration rate (eGFR), and exposure intensity index (EII) were evaluated. Spearman’s correlation and a linear regression analysis were carried out to investigate the association between age, pesticide use, EII, kidney injury markers, and kidney function biomarkers. The most common pesticide used in this study area was glyphosate, followed by paraquat and iprodione. Urinary NGAL levels showed a significant correlation with sCys-C levels, EII, and eGFR Cr-Cys. In addition, the sCr levels were associated with glyphosate use (B = 0.08) and EII (B = 0.01). In conclusion, occupation exposure to pesticides is likely to be linked to kidney injury and dysfunction. Pesticide mix status, pesticide application method, equipment repair status, and personal protective equipment (PPE) use are all involved in changes in kidney markers.

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

Similar content being viewed by others

References

  • Agarwal R, Tripathi N, Choudhary A, Agnihotri S (2013) Biochemical alterations among spray farmers due to chronic exposure to chlorpyrifos, an organophosphate pesticides. Int J Curr Microbiol App Sci 2:415–418

    Google Scholar 

  • Ahn JY, Lee MJ, Seo JS, Choi D, Park JB (2016) Plasma neutrophil gelatinase-associated lipocalin as a predictive biomarker for the detection of acute kidney injury in adult poisoning. Clin Toxicol (Phila) 54:127–133

    CAS  Google Scholar 

  • Andreucci M, Faga T, Pisani A, Perticone M, Michael A (2017) The ischemic/nephrotoxic acute kidney injury and the use of renal biomarkers in clinical practice. Eur J Intern Med 39:1–8

    CAS  Google Scholar 

  • Bacci MR, Chehter EZ, Azzalis LA, Costa de Aguiar Alves B, Fonseca FLA (2017): Serum NGAL and cystatin C comparison with urinary albumin-to-creatinine ratio and inflammatory biomarkers as early predictors of renal dysfunction in patients with type 2 diabetes. Kidney Int Rep 2, 152–158

  • Bachorzewska-Gajewska H, Sitniewska E, Malyszko JS, Malyszko J, Dobrzycki S (2006) Neutrophil gelatinase-associated lipocalin (NGAL) correlations with cystatin C, serum creatinine and eGFR in patients with normal serum creatinine undergoing coronary angiography. Nephrol Dial Transpl 22:295–296

    Google Scholar 

  • Black R, Jonglaekha N, Bruin G, Sukasem S, Buranaviriyakul S (1985) Purple blotch disease of garlic: development of the disease in Chiangmai-Lamphun valley, northern Thailand, considered in relation to fungicide use and other farming practices. Tropical Pest Management 31:47–54

    Google Scholar 

  • Bonventre JV, Vaidya VS, Schmouder R, Feig P, Dieterle F (2010) Next-generation biomarkers for detecting kidney toxicity. Nat Biotechnol 28:436–440

    CAS  Google Scholar 

  • Bradberry SM, Proudfoot AT, Vale JA (2004a) Poisoning due to chlorophenoxy herbicides. Toxicol Rev 23:65–73

    CAS  Google Scholar 

  • Bradberry SM, Proudfoot AT, Vale JA (2004b) Glyphosate poisoning. Toxicol Rev 23:159–167

    CAS  Google Scholar 

  • Charlton JR, Portilla D, Okusa MD (2014) A basic science view of acute kidney injury biomarkers. Nephrol Dial Transplant 29:1301–1311

    Google Scholar 

  • Connolly A, Basinas I, Jones K, Galea KS, Kenny L, McGowan P, Coggins MA (2018) Characterising glyphosate exposures among amenity horticulturists using multiple spot urine samples. Int J Hyg Environ Health 221:1012–1022

    CAS  Google Scholar 

  • Damalas CA, Eleftherohorinos IG (2011) Pesticide exposure, safety issues, and risk assessment indicators. Int J Environ Res Public Health 8:1402–1419

    CAS  Google Scholar 

  • Damalas CA, Abdollahzadeh G (2016) Farmers' use of personal protective equipment during handling of plant protection products: determinants of implementation. Sci Total Environ 571:730–736

    CAS  Google Scholar 

  • De Silva PMCS, Mohammed Abdul KS, Eakanayake EMDV, Jayasinghe SS, Jayasumana C, Asanthi HB, Perera HSD, Chaminda GGT, Chandana EPS, Siribaddana SH (2016) Urinary biomarkers KIM-1 and NGAL for detection of chronic kidney disease of uncertain etiology (CKDu) among agricultural communities in Sri Lanka. Plos Neglect Trop D 10:e0004979

    Google Scholar 

  • Dinis-Oliveira RJ, Duarte JA, Sanchez-Navarro A, Remiao F, Bastos ML, Carvalho F (2008) Paraquat poisonings: mechanisms of lung toxicity, clinical features, and treatment. Crit Rev Toxicol 38:13–71

    CAS  Google Scholar 

  • Dosemeci M, Alavanja MC, Rowland AS, Mage D, Zahm SH, Rothman N, Lubin JH, Hoppin JA, Sandler DP, Blair A (2002) A quantitative approach for estimating exposure to pesticides in the agricultural health study. Ann Occup Hyg 46:245–260

    CAS  Google Scholar 

  • Ferguson MA, Vaidya VS, Bonventre JV (2008) Biomarkers of nephrotoxic acute kidney injury. Toxicology 245:182–193

    CAS  Google Scholar 

  • Ferguson MA, Waikar SS (2012) Established and emerging markers of kidney function. Clin Chem 58:680–689

    CAS  Google Scholar 

  • Finney H, Dj N, Price CP (2000) Adult reference ranges for serum cystatin C, creatinine and predicted creatinine clearance. Annals of Clinical Biochemistry: International Journal of Laboratory Medicine 37:49–59

    CAS  Google Scholar 

  • Handelsman Y et al (2015) American association of clinical endocrinologists and American college of endocrinology - clinical practice guidelines for developing a diabetes mellitus comprehensive care plan - 2015. Endocrine practice: official journal of the American college of endocrinology and the American Association of Clinical Endocrinologists 21 Suppl 1:1–87

  • Hassanin NM, Awad OM, El-Fiki S, Abou-Shanab RAI, Abou-Shanab ARA, Amer RA (2018) Association between exposure to pesticides and disorder on hematological parameters and kidney function in male agricultural workers. Environ Sci Pollut Res Int 25:30802–30807

    CAS  Google Scholar 

  • Hernández-Valero MA, Bondy ML, Spitz MR, Zahm SH (2001) Evaluation of Mexican American migrant farmworker work practices and organochlorine pesticide metabolites. Am J Ind Med 40:554–560

    Google Scholar 

  • Herrera R, Orantes CM, Almaguer M, Alfonso P, Bayarre HD, Leiva IM, Smith MJ, Cubias RA, Torres CG, Almendárez WO, Cubias FR, Morales FE, Magaña S, Amaya JC, Perdomo E, Ventura MC, Villatoro JF, Vela XF, Zelaya SM, Granados DV, Vela E, Orellana P, Hevia R, Fuentes EJ, Mañalich R, Bacallao R, Ugarte M, Arias MI, Chávez J, Flores NE, Aparicio CE (2014) Clinical characteristics of chronic kidney disease of nontraditional causes in Salvadoran farming communities. MEDICC review 16:39–48

    Google Scholar 

  • Hoffmann D, Fuchs TC, Henzler T, Matheis KA, Herget T, Dekant W, Hewitt P, Mally A (2010) Evaluation of a urinary kidney biomarker panel in rat models of acute and subchronic nephrotoxicity. Toxicology 277:49–58

    CAS  Google Scholar 

  • Inker LA, Schmid CH, Tighiouart H, Eckfeldt JH, Feldman HI, Greene T, Kusek JW, Manzi J, Van Lente F, Zhang YL, Coresh J, Levey AS, Investigators C-E (2012) Estimating glomerular filtration rate from serum creatinine and cystatin C. N Engl J Med 367:20–29

    CAS  Google Scholar 

  • International Society of Nephrology (2013) Chapter 1: definition and classification of CKD. Kidney international supplements 3:19–62

    Google Scholar 

  • Jayasumana C, Paranagama P, Agampodi S, Wijewardane C, Gunatilake S, Siribaddana S (2015) Drinking well water and occupational exposure to herbicides is associated with chronic kidney disease, in Padavi-Sripura, Sri Lanka. Environ Health 14:6

    Google Scholar 

  • Jayasumana C, Orantes C, Herrera R, Almaguer M, Lopez L, Silva LC, Ordunez P, Siribaddana S, Gunatilake S, De Broe ME (2017) Chronic interstitial nephritis in agricultural communities: a worldwide epidemic with social, occupational and environmental determinants. Nephrol Dial Transpl 32:234–241

    CAS  Google Scholar 

  • Johnson RJ, Sanchez-Lozada LG, Newman LS, Lanaspa MA, Diaz HF, Lemery J, Rodriguez-Iturbe B, Tolan DR, Butler-Dawson J, Sato Y, Garcia G, Hernando AA, Roncal-Jimenez CA (2019a) Climate change and the kidney. Ann Nutr Metab 74:38–44

    CAS  Google Scholar 

  • Johnson RJ, Sanchez-Lozada LG, Newman LS, Lanaspa MA, Diaz HF, Lemery J, Rodriguez-Iturbe B, Tolan DR, Butler-Dawson J, Sato Y, Garcia G, Hernando AA, Roncal-Jimenez CA (2019b) Climate change and the kidney. Ann Nutr Metab 74 Suppl 3:38–44

  • Khan DA, Bhatti MM, Khan FA, Naqvi ST, Karam A (2008) Adverse effects of pesticides residues on biochemical markers in Pakistani tobacco farmers. Int J Clin Exp Med 1:274–282

    CAS  Google Scholar 

  • Kim S, Gil H, Yang J, Lee E, Hong S (2008) The clinical features of acute kidney injury in patients with acute paraquat intoxication. Nephrol Dial Transpl 24:1226–1232

    Google Scholar 

  • Laws RL, Brooks DR, Amador JJ, Weiner DE, Kaufman JS, Ramírez-Rubio O, Riefkohl A, Scammell MK, López-Pilarte D, Sánchez JM, Parikh CR, McClean MD (2015) Changes in kidney function among Nicaraguan sugarcane workers. Int J Occup Environ Health 21:241–250

    Google Scholar 

  • Laws RL, Brooks DR, Amador JJ, Weiner DE, Kaufman JS, Ramírez-Rubio O, Riefkohl A, Scammell MK, López-Pilarte D, Sánchez JM, Parikh CR, McClean MD (2016) Biomarkers of kidney injury among Nicaraguan sugarcane workers. American journal of kidney diseases : the official journal of the National Kidney Foundation 67:209–217

    CAS  Google Scholar 

  • Lebov JF, Engel LS, Richardson D, Hogan SL, Hoppin JA, Sandler DP (2016) Pesticide use and risk of end-stage renal disease among licensed pesticide applicators in the agricultural health study. Occup Environ Med 73:3–12

    Google Scholar 

  • Lee K, Park E-K, Stoecklin-Marois M, Koivunen ME, Gee SJ, Hammock BD, Beckett LA, Schenker MB (2009) Occupational paraquat exposure of agricultural workers in large Costa Rican farms. Int Arch Occ Env Hea 82:455–462

    CAS  Google Scholar 

  • Lermen J, Bernieri T, Rodrigues IS, Suyenaga ES, Ardenghi PG (2018) Pesticide exposure and health conditions among orange growers in southern Brazil. J Environ Sci Health B 53:215–221

    CAS  Google Scholar 

  • Levey AS, Stevens LA, Schmid CH, Zhang Y, Castro AF, Feldman HI, Kusek JW, Eggers P, Van Lente F, Greene T, Coresh J (2009) A new equation to estimate glomerular filtration rate. Ann Intern Med 150:604–612

    Google Scholar 

  • Lopez-Giacoman S, Madero M (2015) Biomarkers in chronic kidney disease, from kidney function to kidney damage. World Journal of Nephrology 4:57–73

    Google Scholar 

  • Marrer E, Dieterle F (2010) Impact of biomarker development on drug safety assessment. Toxicol Appl Pharm 243:167–179

    CAS  Google Scholar 

  • Mohamed F, Buckley NA, Pickering JW, Wunnapuk K, Dissanayake S, Chathuranga U, Gawarammana I, Jayamanne S, Endre ZH (2017) Nephrotoxicity-induced proteinuria increases biomarker diagnostic thresholds in acute kidney injury. BMC Nephrol 18:122–122

    CAS  Google Scholar 

  • Myers JP, Antoniou MN, Blumberg B, Carroll L, Colborn T, Everett LG, Hansen M, Landrigan PJ, Lanphear BP, Mesnage R, Vandenberg LN, Vom Saal FS, Welshons WV, Benbrook CM (2016) Concerns over use of glyphosate-based herbicides and risks associated with exposures: a consensus statement. Environ Health 15:19

    Google Scholar 

  • Okoffo ED, Mensah M, Fosu-Mensah BY (2016) Pesticides exposure and the use of personal protective equipment by cocoa farmers in Ghana. Environmental Systems Research 5:17

    Google Scholar 

  • Peralta CA, Katz R, Bonventre JV, Sabbisetti V, Siscovick D, Sarnak M, Shlipak MG (2012) Associations of urinary levels of kidney injury molecule 1 (KIM-1) and neutrophil gelatinase-associated lipocalin (NGAL) with kidney function decline in the multi-ethnic study of atherosclerosis (MESA). Am J Kidney Dis 60:904–911

    CAS  Google Scholar 

  • Rankin GO, Teets VJ, Nicoll DW, Brown PI (1989) Comparative acute renal effects of three N-(3,5-dichlorophenyl)carboximide fungicides: N-(3,5-dichlorophenyl)succinimide, vinclozolin and iprodione. Toxicology 56:263–272

    CAS  Google Scholar 

  • Rifkin DE, Katz R, Chonchol M, Fried LF, Cao J, de Boer IH, Siscovick DS, Shlipak MG, Sarnak MJ (2010) Albuminuria, impaired kidney function and cardiovascular outcomes or mortality in the elderly. Nephrology, dialysis, transplantation : official publication of the European Dialysis and Transplant Association - European Renal Association 25:1560–1567

    CAS  Google Scholar 

  • Roberts DM, Wilks MF, Roberts MS, Swaminathan R, Mohamed F, Dawson AH, Buckley NA (2011) Changes in the concentrations of creatinine, cystatin C and NGAL in patients with acute paraquat self-poisoning. Toxicol Lett 202:69–74

    CAS  Google Scholar 

  • Sapbamrer R, Nata S (2014) Health symptoms related to pesticide exposure and agricultural tasks among rice farmers from northern Thailand. Environ Health Prev Med 19:12–20

    CAS  Google Scholar 

  • Sapbamrer R, Hongsibsong S, Kerdnoi T (2017) Urinary dialkylphosphate metabolites and health symptoms among farmers in Thailand. Archives of Environmental & Occupational Health 72:145–152

    CAS  Google Scholar 

  • Schley G, Köberle C, Manuilova E, Rutz S, Forster C, Weyand M, Formentini I, Kientsch-Engel R, Eckardt K-U, Willam C (2015) Comparison of plasma and urine biomarker performance in acute kidney injury. PLoS One 10:e0145042

    Google Scholar 

  • Sirisena U, Watson G, Hemachandra K, Wijayagunasekara HNP (2013): Mealybugs (Hemiptera: Pseudococcidae) species on economically important fruit crops in Sri Lanka. 25, 69-83

  • Siriwong W, Robson M (2014) Pesticides use and human health effects in agricultural farmworkers in the kingdom of Thailand: current situation and concerns. Journal of Agromedicine 19:240–241

    Google Scholar 

  • Vaidya VS, Ferguson MA, Bonventre JV (2008) Biomarkers of acute kidney injury. Annu Rev Pharmacol Toxicol 48:463–493

    CAS  Google Scholar 

  • Verhave JC, Fesler P, Ribstein J, du Cailar G, Mimran A (2005) Estimation of renal function in subjects with normal serum Creatinine levels: influence of age and body mass index. Am J Kidney Dis 46:233–241

    CAS  Google Scholar 

  • Wasung ME, Chawla LS, Madero M (2015) Biomarkers of renal function, which and when? Clin Chim Acta 438:350–357

    CAS  Google Scholar 

  • World Health Organization (2009) The World Health Organization recommended classification of pesticides by hazard and guideline to classification. WHO, Geneva, Switzerland

    Google Scholar 

  • Yan Q, Sun D, Li X, Chen G, Zheng Q, Li L, Gu C, Feng B (2016) Association of blood glucose level and hypertension in elderly Chinese subjects: a community based study. BMC Endocr Disord 16:40

    Google Scholar 

Download references

Acknowledgments

This research was supported by the Faculty of Medicine, Chiang Mai University Research Fund, Grant No. 140-2561 and Grant No. 30-2562. The funding body had no role in the design and execution of this study or interpretation of the data.

Authors’ contributions

KW and PM conceived the presented idea. KW, PS, RS, and AL were involved in planning and supervised the work. PM, KW, SK, MS, and PJ performed the experiments. KW and SK verified the analytical methods. PM, KW, and RS processed the experimental data and performed the statistical analysis. All authors discussed the results and contributed to the final manuscript.

Author information

Authors and Affiliations

  1. Department of Forensic Medicine, Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand

    Patthawee Mueangkhiao, Supakit Khacha-ananda, Pittaya Jaikwang & Klintean Wunnapuk

  2. Department of Community Medicine, Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand

    Penprapa Siviroj, Ratana Sapbamrer & Mathuramat Seesen

  3. Department of Physiology, Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand

    Anusorn Lungkaphin

Authors
  1. Patthawee Mueangkhiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Penprapa Siviroj
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ratana Sapbamrer
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Supakit Khacha-ananda
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Anusorn Lungkaphin
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mathuramat Seesen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pittaya Jaikwang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Klintean Wunnapuk
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Klintean Wunnapuk.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Philippe Garrigues

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mueangkhiao, P., Siviroj, P., Sapbamrer, R. et al. Biological variation in kidney injury and kidney function biomarkers among farmers in Lamphun province, Thailand. Environ Sci Pollut Res 27, 12386–12394 (2020). https://doi.org/10.1007/s11356-020-07661-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-020-07661-3

Keywords

Search

Navigation