Acute kidney injury biomarker responses to short-term heat acclimation

International Journal of Environmental Research and Public Health

Volumn 17, Issue 4, 2020, Pages

  Pryor, Riana R ^a   Pryor, J Luke ^a   Vandermark, Lesley W ^b   Adams, Elizabeth L ^c   Brodeur, Rachel M ^c   Schlader, Zachary J ^d   Armstrong, Lawrence E ^c   Lee, Elaine C ^c   Maresh, Carl M ^e   Casa, Douglas J ^c  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY OF ARKANSAS   (United States)

^c UNIVERSITY OF CONNECTICUT   (United States)

^d INDIANA UNIVERSITY   (United States)

^e OHIO STATE UNIVERSITY   (United States)

Author keywords

Acclimation; Creatinine; Heat stress; Kidney injury; Renal function

Indexed keywords

BIOLOGICAL MARKER; CREATININE;

ACCLIMATION; BIOMARKER; HEAT WAVE; INJURY; PUBLIC HEALTH; SERUM;

ACUTE KIDNEY FAILURE; ADULT; AEROBIC EXERCISE; ARTICLE; CREATININE BLOOD LEVEL; ENVIRONMENTAL FACTOR; ENVIRONMENTAL TEMPERATURE; ESTIMATED GLOMERULAR FILTRATION RATE; EXERCISE INTENSITY; HEART RATE; HEAT ACCLIMATIZATION; HUMAN; HUMAN EXPERIMENT; HUMIDITY; KIDNEY FUNCTION; MALE; NORMAL HUMAN; PLASMA VOLUME; YOUNG ADULT; ACCLIMATIZATION; DEHYDRATION; EXERCISE; FEVER; HEAT; HEAT SHOCK RESPONSE; METABOLISM;

ACCLIMATIZATION; ACUTE KIDNEY INJURY; ADULT; BIOMARKERS; CREATININE; DEHYDRATION; EXERCISE; FEVER; HEAT-SHOCK RESPONSE; HOT TEMPERATURE; HUMANS; MALE;

EID: 85079881316     PISSN: 16617827     EISSN: 16604601     Source Type: Journal    
DOI: 10.3390/ijerph17041325     Document Type: Article

References (63)

1. Hostler, D.; Bednez, J.C.; Kerin, S.; Reis, S.E.; Kong, P.W.; Morley, J.; Gallagher, M., Jr.; Suyama, J. Comparison of rehydration regimens for rehabilitation of firefighters performing heavy exercise in thermal protective clothing: A report from the fireground rehab evaluation (fire) trial. Prehosp. Emerg. Care 2010, 14, 194–201.
2. DeMartini, J.K.; Martschinske, J.L.; Casa, D.J.; Lopez, R.M.; Ganio, M.S.; Walz, S.M.; Coris, E.E. Physical demands of national collegiate athletic association division I football players during preseason training in the heat. J. Strength Cond. Res. 2011, 25, 2935–2943.
3. Yeargin, S.W.; Casa, D.J.; Armstrong, L.E.; Watson, G.; Judelson, D.A.; Psathas, E.; Sparrow, S.L. Heat acclimatization and hydration status of american football players during initial summer workouts. J. Strength Cond. Res. 2006, 20, 463–470.
4. Horn, G.P.; Blevins, S.; Fernhall, B.; Smith, D.L. Core temperature and heart rate response to repeated bouts of firefighting activities. Ergonomics 2013, 56, 1465–1473.
5. Meade, R.D.; D’Souza, A.W.; Krishen, L.; Kenny, G.P. The physiological strain incurred during electrical utilities work over consecutive work shifts in hot environments: A case report. J. Occup. Environ. Hyg. 2017, 14, 986–994.
6. Radigan, L.R.; Robinson, S. Effects of environmental heat stress and exercise on renal blood flow and filtration rate. J. Appl. Physiol. 1949, 2, 185–191.
7. Smith, J.; Robinson, S.; Pearcy, M. Renal responses to exercise, heat and dehydration. J. Appl. Physiol. 1952, 4, 659–665.
8. Bellomo, R.; Ronco, C.; Kellum, J.A.; Mehta, R.L.; Palevsky, P. Acute renal failure-definition, outcome measures, animal models, fluid therapy and information technology needs: The Second International Consensus Conference of the Acute Dialysis Quality Initiative (ADQI) Group. Crit. Care 2004, 8, R204–R212.
9. Khwaja, A. KDIGO clinical practice guidelines for acute kidney injury. Nephron Clin. Pract. 2012, 120, c179–c184.
10. Schrier, R.W.; Hano, J.; Keller, H.I.; Finkel, R.M.; Gilliland, P.F.; Cirksena, W.J.; Teschan, P.E. Renal, metabolic, and circulatory responses to heat and exercise: Studies in military recruits during summer training, with implications for acute renal failure. Ann. Int. Med. 1970, 73, 213–223.
11. Schlader, Z.J.; Chapman, C.L.; Sarker, S.; Russo, L.; Rideout, T.C.; Parker, M.D.; Johnson, B.D.; Hostler, D. Firefighter work duration influences the extent of acute kidney injury. Med. Sci. Sport Exerc. 2017, 49, 1745–1753.
12. Moyce, S.; Joseph, J.; Tancredi, D.; Mitchell, D.; Schenker, M. Cumulative incidence of acute kidney injury in California’s agricultural workers. J. Occup. Environ. Med. 2016, 58, 391–397.
13. Wegman, D.H.; Apelqvist, J.; Bottai, M.; Ekström, U.; García-Trabanino, R.; Glaser, J.; Hogstedt, C.; Jakobsson, K.; Jarquín, E.; Lucas, R.A.; et al. Intervention to diminish dehydration and kidney damage among sugarcane workers. Scand. J. Work Environ. Heat 2018, 44, 16–24.
14. Divine, J.G.; Clark, J.F.; Colosimo, A.J.; Donaworth, M.; Hasselfeld, K.; Himmler, A.; Rauch, J.; Mangine, R. American football players in preseason training at risk of acute kidney injury without signs of rhabdomyolysis. Clin. J. Sport Med. 2018, doi:10.1097/jsm.0000000000000652.
15. Colombini, A.; Machado, M.; Lombardi, G.; Lanteri, P.; Banfi, G. Modifications of biochemical parameters related to protein metabolism and renal function in male soccer players after a match. J. Sports Med. Phys. Fit. 2014, 54, 658–664.
16. Hoffman, M.D.; Weiss, R.H. Does acute kidney injury from an ultramarathon increase the risk for greater subsequent injury? Clin. J. Sport Med. 2016, 26, 417–422.
17. Hodgson, L.; Walter, E.; Venn, R.; Galloway, R.; Pitsiladis, Y.; Sardat, F.; Forni, L. Acute kidney injury associated with endurance events—Is it a cause for concern? A systematic review. BMJ Open Sport Exerc. Med 2017, 3, e000093.
18. McDermott, B.P.; Smith, C.R.; Butts, C.L.; Caldwell, A.R.; Lee, E.C.; Vingren, J.L.; Munoz, C.X.; Kunces, L.J.; Williamson, K.; Ganio, M.S.; et al. Renal stress and kidney injury biomarkers in response to endurance cycling in the heat with and without ibuprofen. J. Sci. Med. Sport 2018, 21, 1180–1184.
19. Chapman, C.L.; Johnson, B.D.; Sackett, J.R.; Parker, M.D.; Schlader, Z.J. Soft drink consumption during and following exercise in the heat elevates biomarkers of acute kidney injury. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2019, 316, R189–R198.
20. Heung, M.; Steffick, D.E.; Zivin, K.; Gillespie, B.W.; Banerjee, T.; Hsu, C.Y.; Powe, N.R.; Pavkov, M.E.; Williams, D.E.; Saran, R.; et al. Acute kidney injury recovery pattern and subsequent risk of CKD: An analysis of veterans health administration data. Am. J. Kidney Dis. 2016, 67, 742–752.
21. Armstrong, L.E.; Maresh, C.M. The induction and decay of heat acclimatisation in trained athletes. Sport Med. 1991, 12, 302–312.
22. Chalmers, S.; Esterman, A.; Eston, R.; Bowering, K.J.; Norton, K. Short-term heat acclimation training improves physical performance: A systematic review, and exploration of physiological adaptations and application for team sports. Sport Med. 2014, 44, 971–988.
23. Chen, T.-I.; Tsai, P.-H.; Lin, J.-H.; Lee, N.-Y.; Liang, M.T. Effect of short-term heat acclimation on endurance time and skin blood flow in trained athletes. Open Access. J. Sport Med. 2013, 4, 161–170.
24. Lorenzo, S.; Halliwill, J.R.; Sawka, M.N.; Minson, C.T. Heat acclimation improves exercise performance. J. Appl. Physiol. 2010, 109, 1140–1147.
25. Pryor, J.L.; Pryor, R.R.; Vandermark, L.W.; Adams, E.L.; VanScoy, R.M.; Casa, D.J.; Armstrong, L.E.; Lee, E.C.; DiStefano, L.J.; Anderson, J.M.; et al. Intermittent exercise-heat exposures and intense physical activity sustain heat acclimation adaptations. J. Sci. Med. Sport 2019, 22, 117–122.
26. Finberg, J.; Berlyne, G. Modification of renin and aldosterone response to heat by acclimatization in man. J. Appl. Physiol. 1977, 42, 554–558.
27. Montain, S.; Sawka, M.; Latzka, W.; Valeri, C. Thermal and cardiovascular strain from hypohydration: Influence of exercise intensity. Int. J. Sport Med. 1998, 19, 87–91.
28. Montain, S.J.; Coyle, E.F. Influence of graded dehydration on hyperthermia and cardiovascular drift during exercise. J. Appl. Physiol. 1992, 73, 1340–1350.
29. Patterson, M.J.; Stocks, J.M.; Taylor, N.A. Sustained and generalized extracellular fluid expansion following heat acclimation. J. Physiol. 2004, 559, 327–334.
30. Roberts, M.F.; Wenger, C.B.; Stolwijk, J.; Nadel, E.R. Skin blood flow and sweating changes following exercise training and heat acclimation. J. Appl. Physiol. 1977, 43, 133–137.
31. Omassoli, J.; Hill, N.E.; Woods, D.R.; Delves, S.K.; Fallowfield, J.L.; Brett, S.J.; Wilson, D.; Corbett, R.W.; Allsopp, A.J.; Stacey, M.J. Variation in renal responses to exercise in the heat with progressive acclimatisation. J. Sci. Med. Sport 2019, 22, 1004–1009..
32. Jackson, A.S.; Pollock, M.L. Prediction accuracy of body density, lean body weight, and total body volume equations. Med. Sci. Sport 1976, 9, 197–201.
33. Kaminsky, L.A.; Arena, R.; Myers, J. Reference standards for cardiorespiratory fitness measured with cardiopulmonary exercise testing: Data from the fitness registry and the importance of exercise national database. In Mayo Clinic Proceedings; Elsevier: Amsterdam, The Netherlands, 2015; pp. 1515–1523.
34. Pryor, R.R.; Pryor, J.L.; Vandermark, L.W.; Adams, E.L.; Brodeur, R.M.; Armstrong, L.E.; Lee, E.C.; Maresh, C.M.; Andersen, J.M.; Casa, D.J. Exacerbated heat strain during consecutive days of repeated exercise sessions in heat. J. Sci. Med. Sport 2019, 22, 1084–1089.
35. Utter, A.C.; Robertson, R.J.; Green, J.M.; Suminski, R.R.; McAnulty, S.R.; Nieman, D.C. Validation of the Adult OMNI Scale of perceived exertion for walking/running exercise. Med. Sci. Sport Exerc. 2004, 36, 1776–1780.
36. Stearns, R.L.; Belval, L.N.; Casa, D.J.; Klau, J.F.; Emmanuel, H.; Armstrong, L.E.; Maresh, C.M. Two environmental symptoms questionnaires during 10 days of exercise-heat acclimation. Aviat. Space Environ. Med. 2013, 84, 797–802.
37. Dill, D.B.; Costill, D.L. Calculation of percentage changes in volumes of blood, plasma, and red cells in dehydration. J. Appl. Physiol. 1974, 37, 247–248.
38. Levey, A.S.; Stevens, L.A.; Schmid, C.H.; Zhang, Y.L.; Castro, A.F.; Feldman, H.I.; Kusek, J.W.; Eggers, P.; Van Lente, F.; Greene, T. A new equation to estimate glomerular filtration rate. Ann. Int. Med. 2009, 150, 604–612.
39. Pruessner, J.C.; Kirschbaum, C.; Meinlschmid, G.; Hellhammer, D.H. Two formulas for computation of the area under the curve represent measures of total hormone concentration versus time-dependent change. Psychoneuroendocrino 2003, 28, 916–931.
40. Junglee, N.A.; Di Felice, U.; Dolci, A.; Fortes, M.B.; Jibani, M.M.; Lemmey, A.B.; Walsh, N.P.; Macdonald, J.H. Exercising in a hot environment with muscle damage: Effects on acute kidney injury biomarkers and kidney function. Am. J. Physiol. Ren. 2013, 305, F813–F820.
41. Schlader, Z.J.; Colburn, D.; Hostler, D. Heat strain is exacerbated on the second of consecutive days of fire suppression. Med. Sci. Sport Exerc. 2017, 49, 999–1005.
42. Armstrong, L.; Costill, D.; Fink, W. Changes in body water and electrolytes during heat acclimation: Effects of dietary sodium. Aviat. Space Environ. Med. 1987, 58, 143–148.
43. Shvartz, E.; Bhattacharya, A.; Sperinde, S.; Brock, P.; Sciaraffa, D.; Van Beaumont, W. Sweating responses during heat acclimation and moderate conditioning. J. Appl. Physiol. 1979, 46, 675–680.
44. Hodge, D.; Jones, D.; Martinez, R.; Buono, M.J. Time course of the attenuation of sympathetic nervous activity during active heat acclimation. Auton. Neurosci. 2013, 177, 101–103.
45. Jones, S.; Musacchia, X.; Tempel, G. Mechanisms of temperature regulation in heat-acclimated hamsters. Am. J. Physiol 1976, 231, 707–712.
46. Chayoth, R.; Kleinman, D.; Kaplanski, J.; Sod Moriah, U. Renal clearance of urea, inulin, and p-aminohippurate in heat-acclimated rats. J. Appl. Physiol. 1984, 57, 731–732.
47. Rowell, L.B.; Marx, H.J.; Bruce, R.A.; Conn, R.D.; Kusumi, F. Reductions in cardiac output, central blood volume, and stroke volume with thermal stress in normal men during exercise. J. Clin. Investig. 1966, 45, 1801–1816.
48. Sawka, M.N.; Burke, L.M.; Eichner, E.R.; Maughan, R.J.; Montain, S.J.; Stachenfeld, N.S. American College of Sports Medicine position stand. Exercise and fluid replacement. Med. Sci. Sport Exerc. 2007, 39, 377–390.
49. Borg, G. Perceived exertion as an indicator of somatic stress. Scand. J. Rehab. Med. 1970, 2, 92–98.
50. García-Trabanino, R.; Jarquín, E.; Wesseling, C.; Johnson, R.J.; González-Quiroz, M.; Weiss, I.; Glaser, J.; Vindell, J.J.; Stockfelt, L.; Roncal, C.; et al. Heat stress, dehydration, and kidney function in sugarcane cutters in El Salvador—A cross-shift study of workers at risk of Mesoamerican nephropathy. Environ. Res. 2015, 142, 746–755.
51. Jayasekara, K.; Kulasooriya, P.; Wijayasiri, K.; Rajapakse, E.; Dulshika, D.; Bandara, P.; Fried, L.; De Silva, A.; Albert, S. Relevance of heat stress and dehydration to chronic kidney disease (CKDu) in Sri Lanka. Prev. Med. Rep. 2019, 15, 100928.
52. Nickolas, T.L.; O’Rourke, M.M.J.; Yang, J.; Sise, M.M.E.; Canetta, P.A.; Barasch, M.N.; Buchen, M.C.; Khan, F.; Mori, K.; Giglio, J.; et al. Sensitivity and specificity of a single emergency department measurement of urinary neutrophil gelatinase-associated lipocalin for diagnosing acute kidney injury. Ann. Int. Med. 2008, 148, 810–819.
53. Haase, M.; Devarajan, P.; Haase-Fielitz, A.; Bellomo, R.; Cruz, D.N.; Wagener, G.; Krawczeski, C.D.; Koyner, J.L.; Murray, P.; Zappitelli, M.; et al. The outcome of neutrophil gelatinase-associated lipocalin-positive subclinical acute kidney injury: A multicenter pooled analysis of prospective studies. J. Am. Coll. Cardio 2011, 57, 1752–1761.
54. Singer, E.; Schrezenmeier, E.V.; Elger, A.; Seelow, E.R.; Krannich, A.; Luft, F.C.; Schmidt-Ott, K.M. Urinary NGAL-positive acute kidney injury and poor long-term outcomes in hospitalized patients. Kidney Int. Rep. 2016, 1, 114–124.
55. Bulluck, H.; Maiti, R.; Chakraborty, B.; Candilio, L.; Clayton, T.; Evans, R.; Jenkins, D.P.; Kolvekar, S.; Kunst, G.; Laing, C.; et al. Neutrophil gelatinase-associated lipocalin prior to cardiac surgery predicts acute kidney injury and mortality. Heart 2018, 104, 313–317.
56. Bennett, M.; Dent, C.L.; Ma, Q.; Dastrala, S.; Grenier, F.; Workman, R.; Syed, H.; Ali, S.; Barasch, J.; Devarajan, P. Urine NGAL predicts severity of acute kidney injury after cardiac surgery: A prospective study. Clin. J. Am. Soc. Nephrol. 2008, 3, 665–673.
57. Au, V.; Feit, J.; Barasch, J.; Sladen, R.N.; Wagener, G. Urinary neutrophil gelatinase-associated lipocalin (NGAL) distinguishes sustained from transient acute kidney injury after general surgery. Kidney Int. Rep. 2016, 1, 3–9.
58. Tidbury, N.; Browning, N.; Shaw, M.; Morgan, M.; Kemp, I.; Matata, B. Neutrophil gelatinase-associated lipocalin as a marker of postoperative acute kidney injury following cardiac surgery in patients with preoperative kidney impairment. Card Hematol. Disord. Dr. 2019, 19, 239–248.
59. Gocze, I.; Koch, M.; Renner, P.; Zeman, F.; Graf, B.M.; Dahlke, M.H.; Nerlich, M.; Schlitt, H.J.; Kellum, J.A.; Bein, T. Urinary biomarkers TIMP-2 and IGFBP7 early predict acute kidney injury after major surgery. PLoS ONE 2015, 10, e0120863.
60. Wetz, A.J.; Richardt, E.M.; Wand, S.; Kunze, N.; Schotola, H.; Quintel, M.; Bräuer, A.; Moerer, O. Quantification of urinary TIMP-2 and IGFBP-7: An adequate diagnostic test to predict acute kidney injury after cardiac surgery? Crit. Care 2015, 19, 1–7.
61. Pilarczyk, K.; Edayadiyil-Dudasova, M.; Wendt, D.; Demircioglu, E.; Benedik, J.; Dohle, D.S.; Jakob, H.; Dusse, F. Urinary [TIMP-2]*[IGFBP7] for early prediction of acute kidney injury after coronary artery bypass surgery. Ann. Intensive Care 2015, 5, 50.
62. Schlader, Z.J.; Hostler, D.; Parker, M.D.; Pryor, R.R.; Lohr, J.W.; Johnson, B.D.; Chapman, C.L. The potential for renal injury elicited by physical work in the heat. Nutrients 2019, 11, 2087.
63. Périard, J.; Racinais, S.; Sawka, M.N. Adaptations and mechanisms of human heat acclimation: Applications for competitive athletes and sports. Scand. J. Med. Sci. Sport 2015, 25, 20–38.