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RESEARCH ARTICLE

Validation of triglyceride and glucose index as a rapid diagnostic test to diagnose insulin resistance in pregnant and lactating sows

Ruy Ortiz https://orcid.org/0000-0002-5226-5356 A , Manuel López https://orcid.org/0000-0003-2895-7384 A , Rosa E. Pérez https://orcid.org/0000-0001-6215-8653 B and Gerardo Ordaz https://orcid.org/0000-0003-4502-3727 C *
+ Author Affiliations
- Author Affiliations

A Faculty of Veterinary Medicine and Zootechnics, Universidad Michoacana de San Nicolás de Hidalgo, Morelia, Mexico.

B Faculty of Chemical Pharmacobiology, Universidad Michoacana de San Nicolás de Hidalgo, Morelia, Mexico.

C National Center of Disciplinary Research in Animal Physiology and Genetics, INIFAP, Colon, Mexico.

* Correspondence to: ordaz.gerardo@inifap.gob.mx

Handling Editor: Sathya Velmurugan

Animal Production Science 63(17) 1716-1727 https://doi.org/10.1071/AN23170
Submitted: 5 May 2023  Accepted: 21 August 2023  Published: 5 September 2023

© 2023 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Context

In sows, the development of insulin resistance (IR) during late gestation and lactation favours a productive gap associated with low feed intake during lactation, which is reflected in the herd profitability. Therefore, the development of rapid-use tests to diagnose IR on farms will be very useful.

Aims

We aimed to validate the triglyceride and glucose (T-G) index as a rapid diagnostic test to diagnose IR in sows during late gestation and lactation.

Methods

The homeostatic model to evaluate IR (HOMA-IR) was used as a reference. Sixty sows (farrowing 1–5) were selected for blood sampling during late gestation and lactation. In the total number of samples collected (n = 480), the glucose, insulin, and triglyceride concentrations were determined to estimate the HOMA-IR and T-G index. Receiver operating characteristic curves were used to determine cut-off values for diagnosing IR using the T-G index.

Key results

The highest (P < 0.05) values of HOMA-IR and T-G index were found between Day 110 of gestation and Day 3 of lactation, regardless of the farrowing number evaluated. The area under the curve for the T-G index was 0.83 (95% CI 0.78–0.88). The best overall cut-off point for diagnosing IR by using the T-G index was 4.24 (86% sensitivity and 77% specificity). The association between the T-G index and HOMA-IR was 0.68 (P < 0.0001), regardless of the farrowing number and productive stage (late gestation, early lactation, and late lactation). According to the farrowing number and productive stage, the best cut-off points were 4.21 (sensitivity 86% and specificity 73%), 4.20 (sensitivity 83% and specificity 73%), and 4.20 (sensitivity 88% and specificity 92%) for sow’s first and fourth farrowing, and late gestation respectively.

Conclusions

The T-G index is a reliable field test for IR diagnosis in sows during late gestation and lactation.

Implications

The T-G index test evaluated for the diagnosis of IR in sows is an approach that could be significantly exploited at the farm level. This test could become a support tool to maximise the productivity of the sow, since the development of IR could be modulated through zootechnical practices.

Keywords: glucose, HOMA-IR, insulin resistance, pregnant sows, sow, sow’s productivity, T-G index, triglycerides.

References

Antunes LC, Elkfury JL, Jornada MN, Foletto KC, Bertoluci MC (2016) Validation of HOMA-IR in a model of insulin-resistance induced by a high-fat diet in Wistar rats. Archives of Endocrinology and Metabolism 60, 138-142.
| Crossref | Google Scholar | PubMed |

Bell AW, Bauman DE (1997) Adaptations of glucose metabolism during pregnancy and lactation. Journal of Mammary Gland Biology and Neoplasia 2, 265-278.
| Crossref | Google Scholar | PubMed |

Bergman RN, Prager R, Volund A, Olefsky JM (1987) Equivalence of the insulin sensitivity index in man derived by the minimal model method and the euglycemic glucose clamp. The Journal of Clinical Investigation 79, 790-800.
| Crossref | Google Scholar | PubMed |

Borai A, Livingstone C, Kaddam I, Ferns G (2011) Selection of the appropriate method for the assessment of insulin resistance. BMC Medical Research Methodology 11, 158.
| Crossref | Google Scholar | PubMed |

Buchanan TA, Watanabe RM, Xiang AH (2010) Limitations in surrogate measures of insulin resistance. The Journal of Clinical Endocrinology & Metabolism 95, 4874-4876.
| Crossref | Google Scholar | PubMed |

Cheng C, Wu X, Zhang X, Zhang X, Peng J (2020) Obesity of sows at late pregnancy aggravates metabolic disorder of perinatal sows and affects performance and intestinal health of piglets. Animals 10, 49.
| Crossref | Google Scholar | PubMed |

CIOMS (1985) International guiding principles for biomedical research involving animals. (Ed. WH Organization). (Council for International Organizations of Medical Sciences: Geneva, Switzerland) Available at https://www.ncbi.nlm.nih.gov/books/NBK25438/

Clowes EJ, Aherne FX, Schaefer AL, Foxcroft GR, Baracos VE (2003) Parturition body size and body protein loss during lactation influence performance during lactation and ovarian function at weaning in first-parity sows. Journal of Animal Science 81, 1517-1528.
| Crossref | Google Scholar | PubMed |

DeFronzo RA, Tobin JD, Andres R (1979) Glucose clamp technique: a method for quantifying insulin secretion and resistance. American Journal of Physiology-Endocrinology and Metabolism 237, E214-E223.
| Crossref | Google Scholar |

Dohoo I, Martin W, Stryhn H (2003) Screening and diagnostic tests. In ‘Veterinary epidemiologic research’. (Ed. M McPike) pp. 85–120. (AVC Incorporated: Charlottetown, Canada)

Dourmad JY, Etienne M, Noblet J, Causeur D (1997) Prediction of the chemical composition of the reproductive sows from their bodyweight and backfat depth – utilization for determining the energy recordance. Journées de la Recherche Porcine France 29, 255-262.
| Google Scholar |

Du T, Yuan G, Zhang M, Zhou X, Sun X, Yu X (2014) Clinical usefulness of lipid ratios, visceral adiposity indicators, and the triglycerides and glucose index as risk markers of insulin resistance. Cardiovascular Diabetology 13, 146.
| Crossref | Google Scholar | PubMed |

Duarte PC, Souza RF, Almeida RM, Balsamão GM, Ferraz GC, Teixeira Neto AR (2015) Evaluation of energetic metabolism of horses in long-distance exercise: Accutrend® Plus versus laboratory. Comparative Clinical Pathology 24, 311-315.
| Crossref | Google Scholar |

Giavarina D (2015) Understanding Bland Altman analysis. Biochemia Medica 25, 141-151.
| Crossref | Google Scholar | PubMed |

Guerrero-Romero F, Simental-Mendía LE, González-Ortiz M, Martínez-Abundis E, Ramos-Zavala MG, Hernández-González SO, Jacques-Camarena O, Rodríguez-Morán M (2010) The product of triglycerides and glucose, a simple measure of insulin sensitivity. Comparison with the euglycemic-hyperinsulinemic clamp. The Journal of Clinical Endocrinology & Metabolism 95, 3347-3351.
| Crossref | Google Scholar | PubMed |

Gómez González C, Pérez Castán JF (2007) Capítulo 8: Pruebas diagnósticas. Concordancia. SEMERGEN – Medicina de Familia 33, 509-519.
| Crossref | Google Scholar |

Güemes M, Rahman SA, Hussain K (2015) What is a normal blood glucose? Archives of Disease in Childhood 101, 569-574.
| Crossref | Google Scholar |

Katz A, Nambi SS, Mather K, Baron AD, Follmann DA, Sullivan G, Quon MJ (2000) Quantitative insulin sensitivity check index: a simple, accurate method for assessing insulin sensitivity in humans. The Journal of Clinical Endocrinology & Metabolism 85, 2402-2410.
| Crossref | Google Scholar | PubMed |

Koketsu Y, Dial GD, Pettigrew JE, Marsh WE, King VL (1996) Characterization of feed intake patterns during lactation on commercial swine herds. Journal of Animal Science 74, 1202-1210.
| Crossref | Google Scholar | PubMed |

Koketsu Y, Tani S, Iida R (2017) Factors for improving reproductive performance of sows and herd productivity in commercial breeding herds. Porcine Health Management 3, 1.
| Crossref | Google Scholar | PubMed |

Lavery A, Lawlor PG, Magowan E, Miller HM, O’Driscoll K, Berry DP (2019) An association analysis of sow parity, live-weight and back-fat depth as indicators of sow productivity. Animal 13, 622-630.
| Crossref | Google Scholar | PubMed |

Lebovitz H (2001) Insulin resistance: definition and consequences. Experimental and Clinical Endocrinology & Diabetes 109, S135-S148.
| Crossref | Google Scholar | PubMed |

Lucy MC, Safranski TJ (2017) Heat stress in pregnant sows: thermal responses and subsequent performance of sows and their offspring. Molecular Reproduction and Development 84, 946-956.
| Crossref | Google Scholar | PubMed |

Mandrekar JN (2010) Receiver operating characteristic curve in diagnostic test assessment. Journal of Thoracic Oncology 5, 1315-1316.
| Crossref | Google Scholar | PubMed |

Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and β-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28, 412-419.
| Crossref | Google Scholar | PubMed |

Mazidi M, Kengne A-P, Katsiki N, Mikhailidis DP, Banach M (2018) Lipid accumulation product and triglycerides/glucose index are useful predictors of insulin resistance. Journal of Diabetes and its Complications 32, 266-270.
| Crossref | Google Scholar | PubMed |

Miller M, Stone NJ, Ballantyne C, Bittner V, Criqui MH, Ginsberg HN, Goldberg AC, Howard WJ, Jacobson MS, Kris-Etherton PM, Lennie TA, Levi M, Mazzone T, Pennathur S (2011) Triglycerides and cardiovascular disease: a scientific statement from the American Heart Association. Circulation 123, 2292-2333.
| Crossref | Google Scholar | PubMed |

Mosnier E, Etienne M, Ramaekers P, Pére MC (2010) The metabolic status during the peri partum period affects the voluntary feed intake and the metabolism of the lactating multiparous sow. Livestock Science 127, 127-136.
| Crossref | Google Scholar |

Mosnier E, Le Floc’h N, Etienne M, Ramaekers P, Sève B, Père M-C (2013) Reduced feed intake of lactating primiparous sows is associated with increased insulin resistance during the peripartum period and is not modified through supplementation with dietary tryptophan. Journal of Animal Science 88, 612-625.
| Crossref | Google Scholar |

Muniyappa R, Lee S, Chen H, Quon MJ (2008) Current approaches for assessing insulin sensitivity and resistance in vivo: advantages, limitations, and appropriate usage. American Journal of Physiology-Endocrinology and Metabolism 294, E15-E26.
| Crossref | Google Scholar | PubMed |

National Research Council (2012) ‘Nutrient requirements of swine.’ 11th revised edn. (National Academies Press: Washington, DC, USA)

Norma Oficial Mexicana NOM-062- ZOO-1999 (2001) Especificaciones técnicas para la producción, cuidado y uso de los animales de laboratorio. Diario Oficial de la Federación. Available at https://www.dof.gob.mx/nota_detalle.php?codigo=762506&fecha=22/08/2001

Nunnelley WZ, Maxwell HS, Bayne JE, Brandebourg TD (2018) Validation of glucometer technology for measurement of glycaemia during glucose tolerance tests and endotoxin challenge in pigs. Journal of Animal Science 96, 82.
| Crossref | Google Scholar |

Otero YF, Stafford JM, McGuinness OP (2014) Pathway-selective insulin resistance and metabolic disease: the importance of nutrient flux. Journal of Biological Chemistry 289, 20462-20469.
| Crossref | Google Scholar | PubMed |

Park HM, Lee HS, Lee Y-J, Lee J-H (2021) The triglyceride–glucose index is a more powerful surrogate marker for predicting the prevalence and incidence of type 2 diabetes mellitus than the homeostatic model assessment of insulin resistance. Diabetes Research and Clinical Practice 180, 109042.
| Crossref | Google Scholar | PubMed |

Pierozan CR, Callegari MA, Días CP, de Souza KL, Gasa J, da Silva CA (2021) Herd-level factors associated with non-productive days and farrowing rate in commercial pig farms in two consecutive years. Livestock Science 244, 104312.
| Crossref | Google Scholar |

Pongratz MC, Junge HK, Riond B, Schwarzwald CC (2016) Validation of the Accutrend Plus point-of-care triglyceride analyzer in horses, ponies, and donkeys. Journal of Veterinary Emergency and Critical Care 26, 682-690.
| Crossref | Google Scholar | PubMed |

Père M-C, Etienne M (2007) Insulin sensitivity during pregnancy, lactation, and postweaning in primiparous gilts. Journal of Animal Science 85, 101-110.
| Crossref | Google Scholar | PubMed |

Père MC, Etienne M, Dourmad JY (2000) Adaptations of glucose metabolism in multiparous sows: effects of pregnancy and feeding level. Journal of Animal Science 78, 2933-2941.
| Crossref | Google Scholar | PubMed |

Pérez RE, González CM, López M, Vargas K, Ordaz G, Ortiz R (2022) Hemoglobin A1c, hemoglobin glycation index, and triglyceride and glucose index: useful tools to predict low feed intake associated with glucose intolerance in lactating sows. PLoS ONE 17, e0267644.
| Crossref | Google Scholar |

Roa Barrios M, Arata-Bellabarba G, Valeri L, Velázquez M (2009) Relationship between the triglyceride/high-density lipoprotein-cholesterol ratio, insulin resistance index and cardiometabolic risk factors in women with polycystic ovary syndrome. Endocrinología y Nutrición 56, 59-65.
| Crossref | Google Scholar | PubMed |

Rodríguez-López JM, Lachica M, González-Valero L, Fernández-Fígares I (2021) Determining insulin sensitivity from glucose tolerance tests in Iberian and landrace pigs. PeerJ 9, e11014.
| Crossref | Google Scholar | PubMed |

Ruopp MD, Perkins NJ, Whitcomb BW, Schisterman EF (2008) Youden Index and optimal cut-point estimated from observations affected by a lower limit of detection. Biometrical Journal 50, 419-430.
| Crossref | Google Scholar | PubMed |

Rya EA, Enns L (1988) Role of gestational hormones in the induction of insulin resistance. The Journal of Clinical Endocrinology & Metabolism 67, 341-347.
| Crossref | Google Scholar |

Simental-Mendía LE, Guerrero-Romero F (2020) The correct formula for the triglycerides and glucose index. European Journal of Pediatrics 179, 1171.
| Crossref | Google Scholar | PubMed |

Tan CQ, Sun HQ, Wei HK, Tan JJ, Long G, Jiang SW, Peng J (2018) Effects of soluble fiber inclusion in gestation diets with varying fermentation characteristics on lactational feed intake of sows over two successive parities. Animal 12, 1388-1395.
| Crossref | Google Scholar | PubMed |

Temming LA, Tuuli MG, Stout MJ, Macones GA, Cahill AG (2016) Maternal and perinatal outcomes in women with insulin resistance. American Journal of Perinatology 33, 776-780.
| Crossref | Google Scholar | PubMed |

Unger G, Benozzi SF, Perruzza F, Pennacchiotti GL (2014) Triglycerides and glucose index: a useful indicator of insulin resistance. Endocrinología y Nutrición 61, 533-540.
| Crossref | Google Scholar | PubMed |

Wallace TM, Levy JC, Matthews DR (2004) Use and abuse of HOMA modeling. Diabetes Care 27, 1487-1495.
| Crossref | Google Scholar | PubMed |

Weldon WC, Lewis AJ, Louis GF, Kovar JL, Miller PS (1994) Postpartum hypophagia in primiparous sows: II. Effects of feeding level during gestation and exogenous insulin on lactation feed intake, glucose tolerance, and epinephrine-stimulated release of nonesterified fatty acids and glucose. Journal of Animal Science 72, 395-403.
| Crossref | Google Scholar | PubMed |

Yang Y, Deng M, Chen J, Zhao X, Xiao K, He W, Qiu X, Xu Y, Yin Y, Tan C (2021) Starch supplementation improves the reproductive performance of sows in different glucose tolerance status. Animal Nutrition 7, 1231-1241.
| Crossref | Google Scholar | PubMed |