Maternal and cord blood parameters are associated with placental and newborn outcomes in indigenous mothers: A case study in the MINDI cohort
Main Article Content
Background:
Multiple infections, nutrient deficiencies and inflammation (MINDI) occur in indigenous communities, but their associations with perinatal outcomes have not been described.
Objective:
To assess maternal and cord blood micronutrient and inflammation status in peripartum mothers from the Ngäbe-Buglé comarca in Panama, and their associations with placental and infant outcomes.
Methods:
In 34 mother-newborn dyads, placental weight and diameter were measured, and maternal and cord blood were processed for complete cell counts, serum C-reactive protein, ferritin, serum transferrin receptor (sTfR), vitamins A and D. Blood volumes were calculated using Nadler’s formula.
Results:
Mothers had low plasma volume (<2.8 L, 96%), vitamin A (52.9%), vitamin D (29.4%), iron (58.8%) and hemoglobin (23.5%), but high hematocrit (>40%, 17.6%) and inflammation (C-reactive protein >8.1 mg/L, 85.3%). Birthweights were normal, but the low placental weight (35.3%), low head circumference Z-scores (17.6%), and low cord hemoglobin (5.9%), iron (79.4%), vitamin A (14.7%) and vitamin D (82.3%) were identified. Maternal and cord vitamin D were highly correlated. Higher maternal plasma volume was associated with heavier placentae (β= 0.57), and higher cord D (β= 0.43) and eosinophils (β= 0.43) with larger placentae. Hemoconcentration (higher cord hematocrit) was associated with lower newborn weight (β= -0.48) and head circumference (β= -0.56). Inflammation [higher maternal neutrophils (β= -0.50), and cord platelets (β= -0.32)] was associated with the lower newborn length and head circumference.
Conclusion:
Maternal-newborn hemoconcentration, subclinical inflammation and multiple nutrient deficiencies, particularly neonatal vitamin D deficiency, were identified as potential targets for interventions to improve pregnancy outcomes in vulnerable communities.
- indigenous population
- cord blood
- plasma volume
- vitamin D
- transferrin receptors
- blood platelets
- Midwifery
- Food Insecurity
- Vulnerable Populations
Hoover E, Cook K, Plain R, et al. Indigenous peoples of North America: environmental exposures y reproductive justice. Environmental health perspectives. 2012;120(12):1645-9. https://doi.org/10.1289/ehp.1205422 DOI: https://doi.org/10.1289/ehp.1205422
Wurtz H. Indigenous Women of Latin America: Unintended pregnancy, unsafe abortion, y reproductive health outcomes. Pimatisiwin. 2012;10(3):271-82.
Anderson I, Robson B, Connolly M, et al. Indigenous y tribal peoples' health (The Lancet-Lowitja Institute Global Collaboration): a population study. Lancet. 2016 Jul 9;388(10040):131-57. https://doi.org/10.1016/S0140-6736(16)32465-5 DOI: https://doi.org/10.1016/S0140-6736(16)32465-5
Sheppard AJ, Shapiro GD, Bushnik T, et al. Birth outcomes among First Nations, Inuit y Metis populations. Health Rep. 2017 Nov 15;28(11):11-6.
Simonet F, Wilkins R, Luo ZC. Temporal trends in Inuit, First Nations y non-Aboriginal birth outcomes in rural y northern Quebec. Int J Circumpolar Health. 2012;71. https://doi.org/10.3402/ijch.v71i0.18791 DOI: https://doi.org/10.3402/ijch.v71i0.18791
Luo ZC, Wilkins R. Degree of rural isolation y birth outcomes. Paediatr Perinat Epidemiol. 2008 Jul;22(4):341-9. https://doi.org/10.1111/j.1365-3016.2008.00938.x DOI: https://doi.org/10.1111/j.1365-3016.2008.00938.x
O'Brien CM, Arbuckle S, Thomas S, Rode J, Turner R, Jeffery HE. Placental inflammation is associated with rural y remote residence in the Northern Territory, Australia: a cross-sectional study. BMC Pregnancy Childbirth. 2015 Feb 14;15:32. https://doi.org/10.1186/s12884-015-0458-7 DOI: https://doi.org/10.1186/s12884-015-0458-7
Morgan HG. Placental malaria y low birthweight neonates in urban Sierra Leone. Ann Trop Med Parasitol. 1994 Dec;88(6):575-80. https://doi.org/10.1080/00034983.1994.11812907 DOI: https://doi.org/10.1080/00034983.1994.11812907
Moffatt ME. Current status of nutritional deficiencies in Canadian aboriginal people. Can J Physiol Pharmacol. 1995 Jun;73(6):754-8. https://doi.org/10.1139/y95-100 DOI: https://doi.org/10.1139/y95-100
Godel JC, Basu TK, Pabst HF, Hodges RS, Hodges PE, Ng ML. Perinatal vitamina A (retinol) status of northern Canadian madres y their infants. Biol Neonate. 1996;69(3):133-9. https://doi.org/10.1159/000244288 DOI: https://doi.org/10.1159/000244288
Dallaire F, Dewailly E, Shademani R, et al. Vitamin A concentration in umbilical cord blood of infants from three separate regions of the province of Quebec (Canada). Can J Public Health. 2003 Sep-Oct;94(5):386-90. https://doi.org/10.1007/BF03403568 DOI: https://doi.org/10.1007/BF03403568
Rosique G J, Restrepo C MT, Manjarrés C LM, Gálvez A A, Santa M J. Estado nutricional y hábitos alimentarios en indígenas Embera de Colombia. Rev Chil Nutr. 2010;37:270-80. https://doi.org/10.4067/S0717-75182010000300002 DOI: https://doi.org/10.4067/S0717-75182010000300002
Mokdad AH, Colson KE, Zuniga-Brenes P, et al. Salud Mesoamerica 2015 Initiative: design, implementation, y baseline findings. Popul Health Metr. 2015;13(1):3. https://doi.org/10.1186/s12963-015-0034-4 DOI: https://doi.org/10.1186/s12963-015-0034-4
Egely GM, Johnson-Down L, Cao ZR, Sheikh N, Weiler H. Food insecurity y nutrition transition combine to affect nutrient intakes in Canadian arctic communities. J Nutr. 2011 Sep;141(9):1746-53. https://doi.org/10.3945/jn.111.139006 DOI: https://doi.org/10.3945/jn.111.139006
Grant CC, Wall CR, Yates R, Crengle S. Nutrition y indigenous health in New Zealy. J Paediatr Child Health. 2010 Sep;46(9):479-82. https://doi.org/10.1111/j.1440-1754.2010.01842.x DOI: https://doi.org/10.1111/j.1440-1754.2010.01842.x
Longvah T, Khutsoh B, Meshram, II, et al. Mother y child nutrition among the Chakhesang tribe in the state of Nagaly, North-East India. Matern Child Nutr. 2017 Nov;13 Suppl 3(Suppl 3). https://doi.org/10.1111/mcn.12558 DOI: https://doi.org/10.1111/mcn.12558
Hirschler V, Molinari C, Maccallini G, Intersimone P, Gonzalez CD. Vitamin D levels y cardiometabolic markers in indigenous Argentinean children living at different altitudes. Glob Pediatr Health. 2019;6:2333794x18821942. https://doi.org/10.1177/2333794X18821942 DOI: https://doi.org/10.1177/2333794X18821942
Mansuri S, Badawi A, Kayaniyil S, et al. Traditional foods y 25(OH)D concentrations in a subarctic First Nations community. Int J Circumpolar Health. 2016 Jan;75(1):31956. https://doi.org/10.3402/ijch.v75.31956 DOI: https://doi.org/10.3402/ijch.v75.31956
Black RE, Victora CG, Walker SP, et al. Maternal y child undernutrition y overweight in low-income y middle-income countries. Lancet. 2013 Aug 3;382(9890):427-51. https://doi.org/10.1016/S0140-6736(13)60937-X DOI: https://doi.org/10.1016/S0140-6736(13)60937-X
Gerny AD, Schulze KJ, Stewart CP, West KP, Jr., Christian P. Micronutrient deficiencies in pregnancy worldwide: health effects y prevention. Nat Rev Endocrinol. 2016 May;12(5):274-89. https://doi.org/10.1038/nrendo.2016.37 DOI: https://doi.org/10.1038/nrendo.2016.37
Rees WD. Interactions between nutrients in the maternal diet y the implications for the long-term health of the offspring. Proc Nutr Soc. 2019 Feb;78(1):88-96. https://doi.org/10.1017/S0029665118002537 DOI: https://doi.org/10.1017/S0029665118002537
Oh C, Keats EC, Bhutta ZA. Vitamin y mineral supplementation during pregnancy on maternal, birth, child health y development outcomes in low- y middle-income countries: a systematic review y meta-analysis. Nutrients. 2020 Feb 14;12(2). https://doi.org/10.3390/nu12020491 DOI: https://doi.org/10.3390/nu12020491
Gonzalez-Fernyez D, Koski KG, Sinisterra OT, Del Carmen Pons E, Murillo E, Scott ME. Interactions among urogenital, intestinal, skin, y oral infections in pregnant y lactating Panamanian Ngabe women: a neglected public health challenge. Am J Trop Med Hyg. 2015 Mar 30;92(6):1100-10. https://doi.org/10.4269/ajtmh.14-0547 DOI: https://doi.org/10.4269/ajtmh.14-0547
Gonzalez-Fernyez D, Pons EDC, Rueda D, et al. C-reactive protein is differentially modulated by co-existing infections, vitamina deficiencies y maternal factors in pregnant y lactating indigenous Panamanian women. Infect Dis Poverty. 2017 Jun 02;6(1):94. https://doi.org/10.1186/s40249-017-0307-1 DOI: https://doi.org/10.1186/s40249-017-0307-1
González-Fernández D, Pons EdC, Rueda D, et al. Identification of high-risk pregnancies in a remote setting using ambulatory blood pressure: the MINDI Cohort. Front Public Health. 2020 2020-March-24;8(86). https://doi.org/10.3389/fpubh.2020.00086 DOI: https://doi.org/10.3389/fpubh.2020.00086
Malik AY, Foster C. The revised Declaration of Helsinki: cosmetic or real change? J R Soc Med. 2016 May;109(5):184-9. https://doi.org/10.1177/0141076816643332 DOI: https://doi.org/10.1177/0141076816643332
Panamanian Ministry of Health. [Statistical Bulletin 2010]. 2011; Available from: https://www.google.com/url?sa=t&rct=j&q=&esrc=s&source=web&cd=1&ved=2ahUKEwi2ju2s3rDoAhX4g3IEHXIiBZsQFjAAegQIAhAB&url=http%3A%2F%2Fwww.minsa.gob.pa%2Fsites%2Fdefault%2Ffiles%2Fpublicacion-general%2Fanuario2010.pdf&usg=AOvVaw0Zs6zTNvI_3LG8Drrhaoma
Klabunde RE. Vascular Function. In: Taylor C, ed. Cardiovascular Physiology Concepts. Second ed. Philadelphia: Wolters Kluwer | Lippincott Williams & Wilkins, 2012:97-8.
Ayala DE, Hermida RC. Ambulatory blood pressure monitoring for the early identification of hypertension in pregnancy. Chronobiol Int. 2013 Mar;30(1-2):233-59. https://doi.org/10.3109/07420528.2012.714687 DOI: https://doi.org/10.3109/07420528.2012.714687
WHEC (Women's Health y Education Center). Obstetrics: Normal values in pregnancy. 2009; Available from: http://www.womenshealthsection.com/content/obs/obs025.php3
Almog B, Shehata F, Aljabri S, Levin I, Shalom-Paz E, Shrim A. Placenta weight percentile curves for singleton y twins deliveries. Placenta. 2011 Jan;32(1):58-62. https://doi.org/10.1016/j.placenta.2010.10.008 DOI: https://doi.org/10.1016/j.placenta.2010.10.008
Villar J, Cheikh Ismail L, Victora CG, et al. International styards for newborn weight, length, y head circumference by gestational age y sex: the Newborn Cross-Sectional Study of the INTERGROWTH-21st Project. Lancet. 2014 Sep 6;384(9946):857-68. https://doi.org/10.1016/S0140-6736(14)60932-6 DOI: https://doi.org/10.1016/S0140-6736(14)60932-6
WHO, CDC. Health Topics: Nutrition. Assessing the Iron Status of Populations. Available from: apps.who.int/iris/bitstream/10665/75368/1/9789241596107_eng.pdf?ua=1&ua=1.
Abbassi-Ghanavati M, Greer LG, Cunningham FG. Pregnancy y laboratory studies: a reference table for clinicians. Obstet Gynecol. 2009 Dec;114(6):1326-31. https://doi.org/10.1097/AOG.0b013e3181c2bde8 DOI: https://doi.org/10.1097/AOG.0b013e3181c2bde8
Budak YU, Polat M, Huysal K. The use of platelet indices, plateletcrit, mean platelet volume y platelet distribution width in emergency non-traumatic abdominal surgery: a systematic review. Biochem Med (Zagreb). 2016;26(2):178-93. https://doi.org/10.11613/BM.2016.020 DOI: https://doi.org/10.11613/BM.2016.020
Glasser L, Sutton N, Schmeling M, Machan JT. A comprehensive study of umbilical cord blood cell developmental changes y reference ranges by gestation, gender y mode of delivery. J Perinatol. 2015 Jul;35(7):469-75. https://doi.org/10.1038/jp.2014.241 DOI: https://doi.org/10.1038/jp.2014.241
Basu S, Kumar N, Srivastava R, Kumar A. Effect of severe maternal iron deficiency anemia on neonatal platelet indices. Indian J Pediatr. 2015 Dec;82(12):1091-6. https://doi.org/10.1007/s12098-015-1775-6 DOI: https://doi.org/10.1007/s12098-015-1775-6
Hay G, Refsum H, Whitelaw A, Melbye EL, Haug E, Borch-Iohnsen B. Predictors of serum ferritin y serum soluble transferrin receptor in newborns y their associations with iron status during the first 2 y of life. Am J Clin Nutr. 2007 Jul;86(1):64-73. https://doi.org/10.1093/ajcn/86.1.64 DOI: https://doi.org/10.1093/ajcn/86.1.64
Kitano T, Takagi K, Arai I, et al. Elevated C-reactive protein in umbilical cord blood: Neonatal case review. Pediatr Int. 2019 Jun;61(6):583-6. https://doi.org/10.1111/ped.13866 DOI: https://doi.org/10.1111/ped.13866
Wiseman EM, Bar-El Dadon S, Reifen R. The vicious cycle of vitamina A deficiency: A review. Crit Rev Food Sci Nutr. 2016 Apr 29:0.
McCauley ME, van den Broek N, Dou L, Othman M. Vitamin A supplementation during pregnancy for maternal y newborn outcomes. Cochrane Database Syst Rev. 2015(10):CD008666. https://doi.org/10.1002/14651858.CD008666.pub3 DOI: https://doi.org/10.1002/14651858.CD008666.pub3
Balvers MG, Brouwer-Brolsma EM, Endenburg S, de Groot LC, Kok FJ, Gunnewiek JK. Recommended intakes of vitamina D to optimize health, associated circulating 25-hydroxyvitamina D concentrations, y dosing regimens to treat deficiency: workshop report y overview of current literature. J Nutr Sci. 2015;4:e23. https://doi.org/10.1017/jns.2015.10 DOI: https://doi.org/10.1017/jns.2015.10
Ariyawatkul K, Lersbuasin P. Prevalence of vitamina D deficiency in cord blood of newborns y the association with maternal vitamina D status. Eur J Pediatr. 2018 Oct;177(10):1541-5. https://doi.org/10.1007/s00431-018-3210-2 DOI: https://doi.org/10.1007/s00431-018-3210-2
Hauser RG, Kwon RJ, Ryder A, Cheng C, Charifa A, Tormey C. Transfusion medicine equations made internet accessible. Transfus Med Rev. 2020 Jan;34(1):5-9. https://doi.org/10.1016/j.tmrv.2019.10.003 DOI: https://doi.org/10.1016/j.tmrv.2019.10.003
Colavita D, Kim HC, Friedman DF. The sex parameter in estimation of total blood volume for pediatric erythrocytapheresis. J Clin Apher. 2019 Dec;34(6):692-9. https://doi.org/10.1002/jca.21748 DOI: https://doi.org/10.1002/jca.21748
Nagano K, Kusaka T, Okubo K, et al. Estimation of circulating blood volume in infants using the pulse dye densitometry method. Paediatr Anaesth. 2005 Feb;15(2):125-30. https://doi.org/10.1111/j.1460-9592.2005.01406.x DOI: https://doi.org/10.1111/j.1460-9592.2005.01406.x
Stleglitz E, Huang J. Plasmapheresis Technique. 2018; Available from: https://emedicine.medscape.com/article/1895577-technique
de Haas S, Ghossein-Doha C, van Kuijk SM, van Drongelen J, Spayerman ME. Physiological adaptation of maternal plasma volume during pregnancy: a systematic review y meta-analysis. Ultrasound Obstet Gynecol. 2017 Feb;49(2):177-87. https://doi.org/10.1002/uog.17360 DOI: https://doi.org/10.1002/uog.17360
Mannan H. A Practical application of a simple bootstrapping method for assessing predictors selected for epidemiologic risk models using automated variable selection. Int J Stat Appl 2017;7(5):239-49.
Royston P, Sauerbrei W. Multivariable model-building : a pragmatic approach to regression analysis based on fractional polynomials for modelling continuous variables. Chichester, Engly; John Wiley, 2008. DOI: https://doi.org/10.1002/9780470770771
Liu X. Classification accuracy y cut point selection. Stat Med. 2012 Oct 15;31(23):2676-86. https://doi.org/10.1002/sim.4509 DOI: https://doi.org/10.1002/sim.4509
Salavati N, Smies M, Ganzevoort W, et al. The possible role of placental morphometry in the detection of fetal growth restriction. Front Physiol. 2019;9:1884-. https://doi.org/10.3389/fphys.2018.01884 DOI: https://doi.org/10.3389/fphys.2018.01884
Salas SP, Rosso P, Espinoza R, Robert JA, Valdes G, Donoso E. Maternal plasma volume expansion y hormonal changes in women with idiopathic fetal growth retardation. Obstet Gynecol. 1993 Jun;81(6):1029-33.
Salas SP, Rosso P. [Reduced plasma volume y changes in vasoactive hormones in underweight pregnant women]. Rev Med Chil. 1998 May;126(5):504-10.
Roy-Clavel E, Picard S, St-Louis J, Brochu M. Induction of intrauterine growth restriction with a low-sodium diet fed to pregnant rats. Am J Obstet Gynecol. 1999 Mar;180(3 Pt 1):608-13. https://doi.org/10.1016/S0002-9378(99)70262-0 DOI: https://doi.org/10.1016/S0002-9378(99)70262-0
Bibeau K, Sicotte B, Bély M, et al. Placental underperfusion in a rat model of intrauterine growth restriction induced by a reduced plasma volume expansion. PLoS One. 2016;11(1):e0145982-e. https://doi.org/10.1371/journal.pone.0145982 DOI: https://doi.org/10.1371/journal.pone.0145982
Lykkedegn S, Beck-Nielsen SS, Sorensen GL, et al. Vitamin D supplementation, cord 25-hydroxyvitamina D y birth weight: Findings from the Odense Child Cohort. Clin Nutr. 2017 Dec;36(6):1621-7. https://doi.org/10.1016/j.clnu.2016.10.008 DOI: https://doi.org/10.1016/j.clnu.2016.10.008
Gerny AD, Simhan HN, Klebanoff MA, Bodnar LM. Maternal serum 25-hydroxyvitamina D y measures of newborn y placental weight in a U.S. multicenter cohort study. J Clin Endocrinol Metab. 2013 Jan;98(1):398-404. https://doi.org/10.1210/jc.2012-3275 DOI: https://doi.org/10.1210/jc.2012-3275
Budhwar S, Verma P, Verma R, et al. Altered cord serum 25-hydroxyvitamina D signaling y placental inflammation is associated with pre-term birth. Am J Reprod Immunol. 2020 Feb;83(2):e13201. https://doi.org/10.1111/aji.13201 DOI: https://doi.org/10.1111/aji.13201
Menon R, Taylor BD. Exploring inflammatory mediators in fetal y maternal compartments during human parturition. Obstet Gynecol. 2019 Oct;134(4):765-73. https://doi.org/10.1097/AOG.0000000000003470 DOI: https://doi.org/10.1097/AOG.0000000000003470
Friis H, Gomo E, Mashange W, et al. The acute phase response to parturition: a cross-sectional study in Zimbabwe. Afr J Reprod Health. 2009 Jun;13(2):61-8.
Kovar IZ, Riches PG. C3 y C4 complement components y acute phase proteins in late pregnancy y parturition. J Clin Pathol. 1988 Jun;41(6):650-2. https://doi.org/10.1136/jcp.41.6.650 DOI: https://doi.org/10.1136/jcp.41.6.650
Yasuda K, Nakanishi K. Host responses to intestinal nematodes. Int Immunol. 2018 Mar 10;30(3):93-102. https://doi.org/10.1093/intimm/dxy002 DOI: https://doi.org/10.1093/intimm/dxy002
Starr LM, Scott ME, Koski KG. Protein deficiency y intestinal nematode infection in pregnant mice differentially impact fetal growth through specific stress hormones, growth factors, y cytokines. J Nutr. 2015 Jan;145(1):41-50. https://doi.org/10.3945/jn.114.202630 DOI: https://doi.org/10.3945/jn.114.202630
Chen YH, Liu ZB, Ma L, et al. Gestational vitamina D deficiency causes placental insufficiency y fetal intrauterine growth restriction partially through inducing placental inflammation. J Steroid Biochem Mol Biol. 2020 Aug 9:105733. https://doi.org/10.1016/j.jsbmb.2020.105733 DOI: https://doi.org/10.1016/j.jsbmb.2020.105733
Morikawa M, Yamada T, Yamada T, et al. Antithrombin activity, platelet count, hemoglobin concentration y hematocrit value determined immediately before vaginal delivery among healthy women. Hokkaido Igaku Zasshi. 2012 Aug;87(4-5):141-6.
Fairlie FM, Lang GD, Lowe GG, Walker JJ. Umbilical artery flow velocity waveforms y cord blood viscosity. Am J Perinatol. 1991 Jul;8(4):239-43. https://doi.org/10.1055/s-2007-999387 DOI: https://doi.org/10.1055/s-2007-999387
Meberg A, Jakobsen E, Halvorsen K. Humoral regulation of erythropoiesis y thrombopoiesis in appropriate y small for gestational age infants. Acta Paediatr Scy. 1982 Sep;71(5):769-73. https://doi.org/10.1111/j.1651-2227.1982.tb09517.x DOI: https://doi.org/10.1111/j.1651-2227.1982.tb09517.x
Vlug RD, Lopriore E, Janssen M, Middeldorp JM, Rath ME, Smits-Wintjens VE. Thrombocytopenia in neonates with polycythemia: incidence, risk factors y clinical outcome. Expert Rev Hematol. 2015 Feb;8(1):123-9. https://doi.org/10.1586/17474086.2015.997705 DOI: https://doi.org/10.1586/17474086.2015.997705
Dundar B, Dincgez Cakmak B, Ozgen G, Tasgoz FN, Guclu T, Ocakoglu G. Platelet indices in preterm premature rupture of membranes y their relation with adverse neonatal outcomes. J Obstet Gynaecol Res. 2018 Jan;44(1):67-73. https://doi.org/10.1111/jog.13484 DOI: https://doi.org/10.1111/jog.13484
Cecinati V, Brescia L, Esposito S. Thrombocytosis y infections in childhood. Pediatr Infect Dis J. 2012;31(1):80-1. https://doi.org/10.1097/INF.0b013e318241f47a DOI: https://doi.org/10.1097/INF.0b013e318241f47a
Syed NN, Usman M, Khurshid M. Thrombocytosis: age dependent aetiology y analysis of platelet indices for differential diagnosis. Indian J Pathol Microbiol. 2007 Jul;50(3):628-33.
Solomons NW. Vision of research on human linear growth. Food Nutr Bull. 2019 Dec;40(4):416-31. https://doi.org/10.1177/0379572119885475 DOI: https://doi.org/10.1177/0379572119885475
Prendergast AJ, Rukobo S, Chasekwa B, et al. Stunting is characterized by chronic inflammation in Zimbabwean infants. PLoS One. 2014;9(2):e86928. https://doi.org/10.1371/journal.pone.0086928 DOI: https://doi.org/10.1371/journal.pone.0086928
Wren-Atilola HM, Solomons NW, Scott ME, Koski KG. Infant growth faltering linked to subclinical mastitis, maternal faecal-oral contamination, y breastfeeding. Matern Child Nutr. 2019 Jul;15(3):e12756. https://doi.org/10.1111/mcn.12756 DOI: https://doi.org/10.1111/mcn.12756
Downloads
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
The copy rights of the articles published in Colombia Médica belong to the Universidad del Valle. The contents of the articles that appear in the Journal are exclusively the responsibility of the authors and do not necessarily reflect the opinions of the Editorial Committee of the Journal. It is allowed to reproduce the material published in Colombia Médica without prior authorization for non-commercial use