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Undernutrition in the last period of lactation may have adverse effects on skeletal development

Yıl 2024, Cilt: 18 Sayı: 3, 91 - 100, 30.12.2024

Hakan Ay , Ferruh Yücel

Öz

Objectives: Malnutrition in childhood causes permanent damage. Studies report that there are different developmental mechanisms at different stages of breastfeeding. Our study aims to observe the effects of undernutrition in the first and last weeks of lactation on body weight and skeletal development after rehabilitation until puberty, and ultimately to reveal which period of lactation is more critical.
Methods: Lactating rats were undernourished by receiving half the diet consumed by control mothers during the first (0–7th day, U1 group) or third (14–21st day, U2 group) week of lactation. Rats were weighed each week and radiographs were taken on the 21st and 49th days. All measurements were taken directly on the radiographs.
Results: On day 49, the body weight and body length of the two undernourished groups were lower than those of the controls. U2 was behind in all measurements except head, pelvic, iliac, and ischial lengths. U2 also lagged behind U1 in body, tail, spine, upper limb, and tibia lengths. While U1 did not differ from controls in many measurements, femur length, bi-iliac, bi-acetabular, and ischial width were less than controls.
Conclusion: Undernutrition in the last week of lactation affected body weight and skeletal development more than malnutrition in the first postnatal week.

Anahtar Kelimeler

lactation radiograph rat skeletal development undernutrition

Kaynakça

  • 2022 Global Nutrition Report. [Internet]. [Retrieved on April 28, 2024]. Available from: https://globalnutritionreport.org/reports/2022-global-nutrition-report/
  • 2021 Global Nutrition Report. [Internet]. [Retrieved on April 28, 2024]. Available from: https://media.globalnutritionreport.org/documents/2021_Global_Nutrition_Report_aUfTRv0.pdf.
  • Kakaei H, Nourmoradi H, Bakhtiyari S, () Effect of COVID-19 on food security, hunger, and food crisis. In: COVID-19 and the Sustainable Development Goals. Elsevier, 2022, pp. 3–29.
  • 2021 Global Report on Food Crises reveals scope of food crises as COVID-19 poses new risks to vulnerable countries. [Internet]. [Retrieved on April 20, 2024]. Available from: https://www.unicef.org/turkiye/en/press-releases/global-report-food-crises-reveals-scope-food-crises-covid-19-poses-new-risks
  • 2022 COVID-19 Brief: impact on food security. [Internet]. [Retrieved on April 20, 2024]. Available from: https://www.usglc.org/coronavirus/global-hunger/#:~:text=In%202022%2C%20COVID%2D19%20disruptions,drought%2C%20and%20the%20Ukraine%20crisis
  • 2021 Food and nutrition under the COVID-19 crisis: lessons for protecting the vulnerable and facilitating recovery. [Internet]. [Retrieved on April 11, 2024]. Available from: https://ieg.worldbankgroup.org/sites/default/files/Data/Topic/COVID19Lessons_foodandnutrition.pdf
  • 2020 Policy brief: the impact of COVID-19 on food security and nutrition. [Internet]. [Retrieved on April 12, 2024]. Available from: https://unsdg.un.org/resources/policy-brief-impact-covid-19-food-security-and-nutrition
  • Media - nutrition international. [Internet]. [Retrieved on April 12, 2024]. Available from: https://www.nutritionintl.org/media/
  • Ahmed MGE, Bedi KS, Warren MA, Kamel MM. Effects of a lengthy period of undernutrition from birth and subsequent nutritional rehabilitation on the synapse: granule cell neuron ratio in the rat dentate gyrus. J Comp Neurol 1987;263:146–58.
  • Angulo-Colmenares AG, Vaughan DW, Hinds JW. Rehabilitation following early malnutrition in the rat: body weight, brain size, and cerebral cortex development. Brain Res 1979;169:121–38.
  • Barnes D, Altman J. Effects of different schedules of early undernutrition on the preweaning growth of the rat cerebellum. Exp Neurol 1973;38:406–19.
  • Barnes D, Altman J. Effects of two levels of gastational-lactational undernutrition on the postweaning growth of the rat cerebellum. Exp Neurol 1973;38:420–8.
  • Yücel F, Akgün Z, Eğilmez H, Solak O. Effects of undernutrition and rehabilitation on the skeletal growth of rats. Turkish Journal of Medical Sciences 1996;26:231–6.
  • Bedi KS, Hall R, Davies CA, Dobbing J. A stereological analysis of the cerebellar granule and purkinje cells of 30‐day‐old and adult rats undernourished during early postnatal life. J Comp Neurol 1980;193:863–70.
  • Bedi KS, Thomas YM, Davies CA, Dobbing J. Synapse‐to‐neuron ratios of the frontal and cerebellar cortex of 30‐day‐old and adult rats undernourished during early postnatal life. J Comp Neurol 1980;193:49–56.
  • Clos J, Favre C, Selme-Matrat M, Legrand J. Effects of undernutrition on cell formation in the rat brain and specially on cellular composition of the cerebellum. Brain Res 1977;123:13–26.
  • Fish I, Winick M. Effect of malnutrition on regional growth of the developing rat brain. Exp Neurol 1969;25:534–40.
  • Spanheimer R, Zlatev T, Umpierrez G, DiGirolamo M. Collagen production in fasted and food-restricted rats: response to duration and severity of food deprivation. J Nutr 1991;121:518–24.
  • Hughes PC, Tanner JM. The assessment of skeletal maturity in the growing rat. J Anat 1970;106:371–402.
  • Hughes PC. Catch-up growth in the limbs of rats undernourished for different lengths of time during suckling. Acta Anat (Basel) 1986;125:50–8.
  • Jones DG, Dyson SE. Synaptic junctions in undernourished rat brain—an ultrastructural investigation. Exp Neurol 1976;51:529–35.
  • Warren MA, Bedi KS. The effects of a lengthy period of undernutrition on the skeletal growth of rats. J Anat 1985;141:53–64
  • Williams JP, Hughes PC. Catch-up growth in rats undernourished for different periods during the suckling period. Growth 1975;39:179–93
  • Winick M, Fish I, Rosso P. Cellular recovery in rat tissues after a brief period of neonatal malnutrition. J Nutr 1968;95:623–6.
  • Passos MCF, Ramos CF, Moura EG. Short and long term effects of malnutrition in rats during lactation on the body weight of offspring. Nutrition Research 2000;20:1603–12.
  • Pessoa DC, Lago ES, Teodósio NR, Bion FM. Dietary proteins on reproductive performance in three consecutive generations of rats. Arch Latinoam Nutr 2000;50:55–61.
  • Cambraia RPB, Vannucchi H, Almeida SS, De-Oliveira LM. Effects of malnutrition during early lactation on development and feeding behavior under the self-selection paradigm. Nutrition 2001;17:455–61.
  • Rasmussen KM. Effects of under- and overnutrition on lactation in laboratory rats. J Nutr 1998;128:390S–3S.
  • Rodríguez-Rodríguez P, Monedero-Cobeta I, Ramiro-Cortijo D, Puthong S, Quintana-Villamandos B, Gil-Ramirez A, Canas S, Ruvira S, Arribas SM. Slower growth during lactation rescues early cardiovascular and adipose tissue hypertrophy induced by fetal undernutrition in rats. Biomedicines 2022;10:2504.
  • Vargas R, Martins IP, Matiusso CCI, Casagrande RA, Zara CB, Huppes de Souza AC, Horst WP, Sieklicki TC, Becker TCA, Lucredi NC, Comar JF, Malta A, Mathias PCF. Protein restriction during lactation causes transgenerational metabolic dysfunction in adult rat offspring. Front Nutr 2023;9:1062116.
  • Hughes PC. Catch-up growth in the limbs of rats undernourished for different lengths of time during suckling. Acta Anat (Basel) 1986;125:50–8.
  • Williams JPG, Tanner JM, Hughes PCR. Catch-up growth in male rats after growth retardation during the suckling period. Pediatr Res 1974;8:149–56.
  • Léonhardt M, Lesage J, Croix D, Dutriez-Casteloot I, Beauvillain JC, Dupouy JP. Effects of perinatal maternal food restriction on pituitary-gonadal axis and plasma leptin level in rat pup at birth and weaning and on timing of puberty. Biol Reprod 2003;68:390–400.
  • Pietrobon CB, Bertasso IM, Silva BS, Peixoto-Silva N, Oliveira E, Moura EG, Lisboa PC. Body adiposity and endocrine profile of female wistar rats of distinct ages that were early weaned. Horm Metab Res 2020;52:58–66.
  • Ferraz-Pereira KN, Da Silva Aragão R, Verdier D, Toscano AE, Lacerda DC, Manhães-de-Castro R, Kolta A. Neonatal low-protein diet reduces the masticatory efficiency in rats. Br J Nutr 2015; 114:1515–30.
  • Salas M, Rubio L, Torrero C, Carreon M, Regalado M. Effects of perinatal undernutrition on the circumvallate papilla of developing Wistar rats. Acta Histochem 2016;118:581–587.
  • Vicente LL, De Moura EG, Lisboa PC, Monte Alto Costa A, Amadeu T, Mandarim-de-Lacerda CA, Passos MC. Malnutrition during lactation in rats is associated with higher expression of leptin receptor in the pituitary of adult offspring. Nutrition 2004;20:924–8.
  • Babinski MSD, Ramos CF, Fernandes RMP, Cardoso GP, Babinski MA. Maternal malnutrition diet during lactation period leads to incomplete catch-up growth in femur of the pups at adulthood. Int J Morphol 2016;34:71–7.
  • Lobe SL, Bernstein MC, German RZ. Life‐long protein malnutrition in the rat (Rattus norvegicus) results in altered patterns of craniofacial growth and smaller individuals. J Anat 2006;208:795–812.
  • Argov-Argaman N, Altman H, Janssen JN, Daeem S, Raz C, Mesilati-Stahy R, Penn S, Monsonego-Ornan E. Effect of milk fat globules on growth and metabolism in rats fed an unbalanced diet. Front Nutr 2024;10:1270171.
  • Reichling TD, German RZ. Bones, muscles and visceral organs of protein-malnourished rats (Rattus norvegicus) grow more slowly but for longer durations to reach normal final size. J Nutr 2000;130:2326–32.
  • Shrader RE, Zeman FJ. Skeletal development in rats as affected by maternal protein deprivation and postnatal food supply. J Nutr 1973;103:792–801.
  • Nemoto T, Kakinuma Y. Fetal malnutrition-induced catch up failure is caused by elevated levels of miR-322 in rats. Sci Rep 2020;10:1339.
  • Dahinten SL, Pucciarelli HM. Effects of protein‐calorie malnutrition during suckling and post‐weaning periods on discontinuous cranial traits in rats. Am J Phys Anthropol 1983;60:425–30.
  • Altman J, Bayer SA. Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 1990;301:365–81.
  • Barbeito-Andrés J, Gonzalez P, Hallgrímsson B. Prenatal development of skull and brain in a mouse model of growth restriction. Revista Argentina de Antropologia Biologica 2016;18:1–13.
  • Fernandes RM, Abreu AV, Silva RB, Silva DF, Martinez GL, Babinski MA, Ramos CF. Maternal malnutrition during lactation reduces skull growth in weaned rat pups: experimental and morphometric investigation. Anat Sci Int 2008;83:123–30.
  • Pires L, Junior A, Chagas C, Manaia JHM, Gameiro VS, Babinski MA. Maternal undernutrition during lactation leads to reduction in skull size and thickness of adult-aged Wistar rats. Arch Med Sci 2020;17:1093–9.
  • Ortiz-Valladares M, Salcedo, CA, Ortega MR, Solorio CT, Alvarado MS. Long-term alterations on the physical development of pre- and neonatally undernourished Wistar rats: a functional correlation. Neurobiología Revista Electronica 2019;10:1–14
  • Dixon AD, Gakunga PT. Morphometric changes in growth of the rat pelvis after papain administration. Anat Rec 1993;235:312–8.
  • Dickerson JWT, Hughes PCR, McAnulty PA. The growth and development of rats given a low-protein diet. Br J Nutr 1972;27:527–536.
  • Nakamoto T, Miller SA. Physical and biochemical changes of the mandible and long bone in protein-energy malnourished newborn rats. J Nutr 1979;109:1477–82.
  • Kimura T, Hino K, Kono T, Takano A, Nitta N, Ushio N, Hino S, Takase R, Kudo M, Daigo Y, Morita W, Nakao M, Nakatsukasa M, Tamagawa T, Rafiq AM, Matsumoto A, Otani H, Udagawa J. Maternal undernutrition during early pregnancy inhibits postnatal growth of the tibia in the female offspring of rats by alteration of chondrogenesis. Gen Comp Endocrinol 2018;260:58–66.
  • Prior LJ, Velkoska E, Watts R, Cameron-Smith D, Morris MJ. Undernutrition during suckling in rats elevates plasma adiponectin and its receptor in skeletal muscle regardless of diet composition: a protective effect? Int J Obes (London) 2008;32:1585–94.

Laktasyonun son dönemindeki yetersiz beslenme iskelet gelişimi üzerinde olumsuz etkilere neden olabilir

Yıl 2024, Cilt: 18 Sayı: 3, 91 - 100, 30.12.2024

Hakan Ay , Ferruh Yücel

Öz

Amaç: Çocukluk çağında yetersiz beslenme kalıcı hasara neden olur. Çalışmalar emzirmenin farklı aşamalarında farklı gelişim mekanizmaları olduğunu bildirmektedir. Çalışmamızın amacı laktasyonun ilk ve son haftalarındaki yetersiz beslenmenin rehabilitasyon sonrası puberte dönemine kadar vücut ağırlığı ve iskelet gelişimi üzerindeki etkilerini gözlemlemek ve sonuçta laktasyonun hangi döneminin daha kritik olduğunu ortaya koymaktır.
Metot: Emziren sıçanlar, laktasyonun ilk (0-7. gün, U1 grubu) veya üçüncü (14-21. gün, U2 grubu) haftasında kontrol anneleri tarafından tüketilen diyetin yarısını alarak yetersiz beslendi. Sıçanlar her hafta tartılmış ve 21. ve 49. günlerde radyografileri çekilmiştir. Tüm ölçümler doğrudan radyografiler üzerinden alınmıştır.
Bulgular: 49. günde, yetersiz beslenen iki grubun vücut ağırlığı ve vücut uzunluğu kontrol grubundan daha düşüktü. U2 baş, pelvik, iliak ve iskial uzunlukları hariç tüm ölçümlerde gerideydi. U2 ayrıca gövde, kuyruk, omurga, üst ekstremite ve tibia uzunluklarında da U1'in gerisinde kalmıştır. U1 birçok ölçümde kontrollerden farklı değilken, femur uzunluğu, bi-iliak, bi-asetabular ve iskial genişlik kontrollerden daha azdı.
Sonuç: Laktasyonun son haftasındaki yetersiz beslenme, vücut ağırlığını ve iskelet gelişimini postnatal ilk haftadaki yetersiz beslenmeden daha fazla etkilemiştir.

Anahtar Kelimeler

laktasyon yetersiz beslenme iskelet gelişimi sıçan radyografi

Kaynakça

  • 2022 Global Nutrition Report. [Internet]. [Retrieved on April 28, 2024]. Available from: https://globalnutritionreport.org/reports/2022-global-nutrition-report/
  • 2021 Global Nutrition Report. [Internet]. [Retrieved on April 28, 2024]. Available from: https://media.globalnutritionreport.org/documents/2021_Global_Nutrition_Report_aUfTRv0.pdf.
  • Kakaei H, Nourmoradi H, Bakhtiyari S, () Effect of COVID-19 on food security, hunger, and food crisis. In: COVID-19 and the Sustainable Development Goals. Elsevier, 2022, pp. 3–29.
  • 2021 Global Report on Food Crises reveals scope of food crises as COVID-19 poses new risks to vulnerable countries. [Internet]. [Retrieved on April 20, 2024]. Available from: https://www.unicef.org/turkiye/en/press-releases/global-report-food-crises-reveals-scope-food-crises-covid-19-poses-new-risks
  • 2022 COVID-19 Brief: impact on food security. [Internet]. [Retrieved on April 20, 2024]. Available from: https://www.usglc.org/coronavirus/global-hunger/#:~:text=In%202022%2C%20COVID%2D19%20disruptions,drought%2C%20and%20the%20Ukraine%20crisis
  • 2021 Food and nutrition under the COVID-19 crisis: lessons for protecting the vulnerable and facilitating recovery. [Internet]. [Retrieved on April 11, 2024]. Available from: https://ieg.worldbankgroup.org/sites/default/files/Data/Topic/COVID19Lessons_foodandnutrition.pdf
  • 2020 Policy brief: the impact of COVID-19 on food security and nutrition. [Internet]. [Retrieved on April 12, 2024]. Available from: https://unsdg.un.org/resources/policy-brief-impact-covid-19-food-security-and-nutrition
  • Media - nutrition international. [Internet]. [Retrieved on April 12, 2024]. Available from: https://www.nutritionintl.org/media/
  • Ahmed MGE, Bedi KS, Warren MA, Kamel MM. Effects of a lengthy period of undernutrition from birth and subsequent nutritional rehabilitation on the synapse: granule cell neuron ratio in the rat dentate gyrus. J Comp Neurol 1987;263:146–58.
  • Angulo-Colmenares AG, Vaughan DW, Hinds JW. Rehabilitation following early malnutrition in the rat: body weight, brain size, and cerebral cortex development. Brain Res 1979;169:121–38.
  • Barnes D, Altman J. Effects of different schedules of early undernutrition on the preweaning growth of the rat cerebellum. Exp Neurol 1973;38:406–19.
  • Barnes D, Altman J. Effects of two levels of gastational-lactational undernutrition on the postweaning growth of the rat cerebellum. Exp Neurol 1973;38:420–8.
  • Yücel F, Akgün Z, Eğilmez H, Solak O. Effects of undernutrition and rehabilitation on the skeletal growth of rats. Turkish Journal of Medical Sciences 1996;26:231–6.
  • Bedi KS, Hall R, Davies CA, Dobbing J. A stereological analysis of the cerebellar granule and purkinje cells of 30‐day‐old and adult rats undernourished during early postnatal life. J Comp Neurol 1980;193:863–70.
  • Bedi KS, Thomas YM, Davies CA, Dobbing J. Synapse‐to‐neuron ratios of the frontal and cerebellar cortex of 30‐day‐old and adult rats undernourished during early postnatal life. J Comp Neurol 1980;193:49–56.
  • Clos J, Favre C, Selme-Matrat M, Legrand J. Effects of undernutrition on cell formation in the rat brain and specially on cellular composition of the cerebellum. Brain Res 1977;123:13–26.
  • Fish I, Winick M. Effect of malnutrition on regional growth of the developing rat brain. Exp Neurol 1969;25:534–40.
  • Spanheimer R, Zlatev T, Umpierrez G, DiGirolamo M. Collagen production in fasted and food-restricted rats: response to duration and severity of food deprivation. J Nutr 1991;121:518–24.
  • Hughes PC, Tanner JM. The assessment of skeletal maturity in the growing rat. J Anat 1970;106:371–402.
  • Hughes PC. Catch-up growth in the limbs of rats undernourished for different lengths of time during suckling. Acta Anat (Basel) 1986;125:50–8.
  • Jones DG, Dyson SE. Synaptic junctions in undernourished rat brain—an ultrastructural investigation. Exp Neurol 1976;51:529–35.
  • Warren MA, Bedi KS. The effects of a lengthy period of undernutrition on the skeletal growth of rats. J Anat 1985;141:53–64
  • Williams JP, Hughes PC. Catch-up growth in rats undernourished for different periods during the suckling period. Growth 1975;39:179–93
  • Winick M, Fish I, Rosso P. Cellular recovery in rat tissues after a brief period of neonatal malnutrition. J Nutr 1968;95:623–6.
  • Passos MCF, Ramos CF, Moura EG. Short and long term effects of malnutrition in rats during lactation on the body weight of offspring. Nutrition Research 2000;20:1603–12.
  • Pessoa DC, Lago ES, Teodósio NR, Bion FM. Dietary proteins on reproductive performance in three consecutive generations of rats. Arch Latinoam Nutr 2000;50:55–61.
  • Cambraia RPB, Vannucchi H, Almeida SS, De-Oliveira LM. Effects of malnutrition during early lactation on development and feeding behavior under the self-selection paradigm. Nutrition 2001;17:455–61.
  • Rasmussen KM. Effects of under- and overnutrition on lactation in laboratory rats. J Nutr 1998;128:390S–3S.
  • Rodríguez-Rodríguez P, Monedero-Cobeta I, Ramiro-Cortijo D, Puthong S, Quintana-Villamandos B, Gil-Ramirez A, Canas S, Ruvira S, Arribas SM. Slower growth during lactation rescues early cardiovascular and adipose tissue hypertrophy induced by fetal undernutrition in rats. Biomedicines 2022;10:2504.
  • Vargas R, Martins IP, Matiusso CCI, Casagrande RA, Zara CB, Huppes de Souza AC, Horst WP, Sieklicki TC, Becker TCA, Lucredi NC, Comar JF, Malta A, Mathias PCF. Protein restriction during lactation causes transgenerational metabolic dysfunction in adult rat offspring. Front Nutr 2023;9:1062116.
  • Hughes PC. Catch-up growth in the limbs of rats undernourished for different lengths of time during suckling. Acta Anat (Basel) 1986;125:50–8.
  • Williams JPG, Tanner JM, Hughes PCR. Catch-up growth in male rats after growth retardation during the suckling period. Pediatr Res 1974;8:149–56.
  • Léonhardt M, Lesage J, Croix D, Dutriez-Casteloot I, Beauvillain JC, Dupouy JP. Effects of perinatal maternal food restriction on pituitary-gonadal axis and plasma leptin level in rat pup at birth and weaning and on timing of puberty. Biol Reprod 2003;68:390–400.
  • Pietrobon CB, Bertasso IM, Silva BS, Peixoto-Silva N, Oliveira E, Moura EG, Lisboa PC. Body adiposity and endocrine profile of female wistar rats of distinct ages that were early weaned. Horm Metab Res 2020;52:58–66.
  • Ferraz-Pereira KN, Da Silva Aragão R, Verdier D, Toscano AE, Lacerda DC, Manhães-de-Castro R, Kolta A. Neonatal low-protein diet reduces the masticatory efficiency in rats. Br J Nutr 2015; 114:1515–30.
  • Salas M, Rubio L, Torrero C, Carreon M, Regalado M. Effects of perinatal undernutrition on the circumvallate papilla of developing Wistar rats. Acta Histochem 2016;118:581–587.
  • Vicente LL, De Moura EG, Lisboa PC, Monte Alto Costa A, Amadeu T, Mandarim-de-Lacerda CA, Passos MC. Malnutrition during lactation in rats is associated with higher expression of leptin receptor in the pituitary of adult offspring. Nutrition 2004;20:924–8.
  • Babinski MSD, Ramos CF, Fernandes RMP, Cardoso GP, Babinski MA. Maternal malnutrition diet during lactation period leads to incomplete catch-up growth in femur of the pups at adulthood. Int J Morphol 2016;34:71–7.
  • Lobe SL, Bernstein MC, German RZ. Life‐long protein malnutrition in the rat (Rattus norvegicus) results in altered patterns of craniofacial growth and smaller individuals. J Anat 2006;208:795–812.
  • Argov-Argaman N, Altman H, Janssen JN, Daeem S, Raz C, Mesilati-Stahy R, Penn S, Monsonego-Ornan E. Effect of milk fat globules on growth and metabolism in rats fed an unbalanced diet. Front Nutr 2024;10:1270171.
  • Reichling TD, German RZ. Bones, muscles and visceral organs of protein-malnourished rats (Rattus norvegicus) grow more slowly but for longer durations to reach normal final size. J Nutr 2000;130:2326–32.
  • Shrader RE, Zeman FJ. Skeletal development in rats as affected by maternal protein deprivation and postnatal food supply. J Nutr 1973;103:792–801.
  • Nemoto T, Kakinuma Y. Fetal malnutrition-induced catch up failure is caused by elevated levels of miR-322 in rats. Sci Rep 2020;10:1339.
  • Dahinten SL, Pucciarelli HM. Effects of protein‐calorie malnutrition during suckling and post‐weaning periods on discontinuous cranial traits in rats. Am J Phys Anthropol 1983;60:425–30.
  • Altman J, Bayer SA. Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 1990;301:365–81.
  • Barbeito-Andrés J, Gonzalez P, Hallgrímsson B. Prenatal development of skull and brain in a mouse model of growth restriction. Revista Argentina de Antropologia Biologica 2016;18:1–13.
  • Fernandes RM, Abreu AV, Silva RB, Silva DF, Martinez GL, Babinski MA, Ramos CF. Maternal malnutrition during lactation reduces skull growth in weaned rat pups: experimental and morphometric investigation. Anat Sci Int 2008;83:123–30.
  • Pires L, Junior A, Chagas C, Manaia JHM, Gameiro VS, Babinski MA. Maternal undernutrition during lactation leads to reduction in skull size and thickness of adult-aged Wistar rats. Arch Med Sci 2020;17:1093–9.
  • Ortiz-Valladares M, Salcedo, CA, Ortega MR, Solorio CT, Alvarado MS. Long-term alterations on the physical development of pre- and neonatally undernourished Wistar rats: a functional correlation. Neurobiología Revista Electronica 2019;10:1–14
  • Dixon AD, Gakunga PT. Morphometric changes in growth of the rat pelvis after papain administration. Anat Rec 1993;235:312–8.
  • Dickerson JWT, Hughes PCR, McAnulty PA. The growth and development of rats given a low-protein diet. Br J Nutr 1972;27:527–536.
  • Nakamoto T, Miller SA. Physical and biochemical changes of the mandible and long bone in protein-energy malnourished newborn rats. J Nutr 1979;109:1477–82.
  • Kimura T, Hino K, Kono T, Takano A, Nitta N, Ushio N, Hino S, Takase R, Kudo M, Daigo Y, Morita W, Nakao M, Nakatsukasa M, Tamagawa T, Rafiq AM, Matsumoto A, Otani H, Udagawa J. Maternal undernutrition during early pregnancy inhibits postnatal growth of the tibia in the female offspring of rats by alteration of chondrogenesis. Gen Comp Endocrinol 2018;260:58–66.
  • Prior LJ, Velkoska E, Watts R, Cameron-Smith D, Morris MJ. Undernutrition during suckling in rats elevates plasma adiponectin and its receptor in skeletal muscle regardless of diet composition: a protective effect? Int J Obes (London) 2008;32:1585–94.
Toplam 54 adet kaynakça vardır.

Ayrıntılar

Birincil Dil İngilizce
Konular Radyoloji ve Organ Görüntüleme, Klinik Tıp Bilimleri (Diğer)
Bölüm Original Articles
Yazarlar

Hakan Ay 0000-0003-4638-0750

Ferruh Yücel 0000-0002-1238-1483

Yayımlanma Tarihi 30 Aralık 2024
Gönderilme Tarihi 5 Haziran 2024
Kabul Tarihi 28 Kasım 2024
Yayımlandığı Sayı Yıl 2024 Cilt: 18 Sayı: 3

Kaynak Göster

APA Ay, H., & Yücel, F. (2024). Undernutrition in the last period of lactation may have adverse effects on skeletal development. Anatomy, 18(3), 91-100.
AMA Ay H, Yücel F. Undernutrition in the last period of lactation may have adverse effects on skeletal development. Anatomy. Aralık 2024;18(3):91-100.
Chicago Ay, Hakan, ve Ferruh Yücel. “Undernutrition in the Last Period of Lactation May Have Adverse Effects on Skeletal Development”. Anatomy 18, sy. 3 (Aralık 2024): 91-100.
EndNote Ay H, Yücel F (01 Aralık 2024) Undernutrition in the last period of lactation may have adverse effects on skeletal development. Anatomy 18 3 91–100.
IEEE H. Ay ve F. Yücel, “Undernutrition in the last period of lactation may have adverse effects on skeletal development”, Anatomy, c. 18, sy. 3, ss. 91–100, 2024.
ISNAD Ay, Hakan - Yücel, Ferruh. “Undernutrition in the Last Period of Lactation May Have Adverse Effects on Skeletal Development”. Anatomy 18/3 (Aralık 2024), 91-100.
JAMA Ay H, Yücel F. Undernutrition in the last period of lactation may have adverse effects on skeletal development. Anatomy. 2024;18:91–100.
MLA Ay, Hakan ve Ferruh Yücel. “Undernutrition in the Last Period of Lactation May Have Adverse Effects on Skeletal Development”. Anatomy, c. 18, sy. 3, 2024, ss. 91-100.
Vancouver Ay H, Yücel F. Undernutrition in the last period of lactation may have adverse effects on skeletal development. Anatomy. 2024;18(3):91-100.
 Kapak Resmi İndir

Anatomy is the official journal of Turkish Society of Anatomy and Clinical Anatomy (TSACA).