Abstract
This paper aims to identify the effects of maternal morbidities on the nutritional composition of human milk. This systematic review of the literature employed a PRISMA’s protocol for searching, selecting, and extracting data. The flowchart proposed for bibliographic search resulted in 1,582 papers, of which 14 were selected for this work. The papers selected for this review were published between 1987 and 2016. Nine studies found significant differences in the nutritional composition of the milk of mothers with diabetes mellitus, arterial hypertension, or overweight compared to the control group. Most studies have shown that the presence of chronic diseases leads to changes in the nutritional composition of human milk. The main results showed a lower concentration of lactose and fat in the milk of women with diabetes mellitus. Concerning hypertension, higher levels of total protein were found in colostrum and mature milk. A higher fat and energy content was observed in overweight mothers. It is imperative that these women have continuous nutritional monitoring to minimize the impact of these morbidities on the nutritional composition of breast milk.
Chronic disease; Human milk; Macronutrients
Introduction
Studies have shown an increased prevalence of diabetes mellitus, hypertension and overweight among women11. Nucci LB, Duncan BB, Mengue SS, Branchtein L, Schmidt MI, Fleck ET. Assessment of weight gain during pregnancy in general prenatal care services in Brazil. Cad Saude Publica 2001; 17(6):1367-1374.
2. Lawrence JM, Contreras R, Chen W, Sacks DA. Trends in the prevalence of preexisting diabetes and gestational diabetes mellitus among a racially/ethnically diverse population of pregnant women, 1999-2005. Diabetes Care 2008; 31(5):899-904.-33. Schmidt MI, Duncan BB, Reichelt AJ, Branchtein L, Matos MC, Costa e Forti A, Spichler ER, Pousada JM, Teixeira MM, Yamashita T. Gestational diabetes mellitus diagnosed with a 2-h 75-g oral glucose tolerance test and adverse pregnancy outcomes. Diabetes Care 2001; 24(7):1151-1155. over the years.
Concerning diabetes mellitus, a multicenter study conducted between 1999 and 2005 found that 21% of pregnancies were complicated by this disease22. Lawrence JM, Contreras R, Chen W, Sacks DA. Trends in the prevalence of preexisting diabetes and gestational diabetes mellitus among a racially/ethnically diverse population of pregnant women, 1999-2005. Diabetes Care 2008; 31(5):899-904.. In Brazil, about 7% of pregnant women have increased gestational glycemia33. Schmidt MI, Duncan BB, Reichelt AJ, Branchtein L, Matos MC, Costa e Forti A, Spichler ER, Pousada JM, Teixeira MM, Yamashita T. Gestational diabetes mellitus diagnosed with a 2-h 75-g oral glucose tolerance test and adverse pregnancy outcomes. Diabetes Care 2001; 24(7):1151-1155.. On the other hand, systemic arterial hypertension affects 5% to 10% of pregnancies44. Brasil. Ministério da Saúde (MS). Cadernos de Atenção Básica: Atenção ao Pré-natal de Baixo Risco. Brasília: MS; 2012.. Regarding overweight, a study carried out in six Brazilian capitals revealed that 28% of women started pregnancy with a weight above the recommended level11. Nucci LB, Duncan BB, Mengue SS, Branchtein L, Schmidt MI, Fleck ET. Assessment of weight gain during pregnancy in general prenatal care services in Brazil. Cad Saude Publica 2001; 17(6):1367-1374..
Diabetes mellitus and hypertension during pregnancy can cause severe maternal and fetal complications, including deteriorated hypertension, preeclampsia, eclampsia, HELLP syndrome, restricted intrauterine growth, preterm delivery, premature placental abruption, and fetal death, and is one of the primary causes of maternal and perinatal morbimortality44. Brasil. Ministério da Saúde (MS). Cadernos de Atenção Básica: Atenção ao Pré-natal de Baixo Risco. Brasília: MS; 2012..
Not unlike this scenario, overweight in pregnancy can also lead to many negative consequences for fetuses (hemorrhages, macrosomia, asphyxia) and women (gestational diabetes mellitus, arterial hypertension, pre-eclampsia, eclampsia and higher weight retention postpartum)55. Barros DCD, Saunders C, Leal MDC. Avaliação nutricional antropométrica de gestantes brasileiras: uma revisão sistemática. Rev. Bras. Saúde Mater. Infant. 2008; 8(4):363-376..
Besides the adverse effects cited, some studies have shown that these chronic diseases may also lead to changes in the nutritional and immunological composition of human milk66. Ballard O, Morrow AL. Human Milk Composition Nutrients and Bioactive Factors. Pediatr Clin N Am 2013; 60(1):49-74..
Although human milk has been the subject of several studies, the influence of chronic diseases on its nutritional composition has not yet been well elucidated, and results are different, which is why it is still the target of several studies.
As a result, this study aims to identify the effects of the morbidities in question (diabetes mellitus, hypertension, overweight) on the nutritional composition of human milk.
Methods
A systematic review of the literature was performed using a pre-established protocol for searching, selecting and extracting data. The papers were identified by bibliographic search in databases Medline (through PubMed), Lilacs and SciELO (through the Virtual Health Library – BVS Brazil), Scopus and Embase. The description of this systematic review was based on the Preferred Reporting Items for Systematic Reviews (Prisma)77. Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Med 2009; 6(7):e1000097. guideline (Figure 1).
The association of diabetes mellitus, arterial hypertension and overweight with the nutritional composition of human milk was evaluated through the following descriptors: (“Human Milk”) AND (“Diabetes Mellitus” OR “Diabetes Gestational”), (“Human Milk”) AND (“Hypertension” OR “Hypertension, Pregnancy-Induced”), (“Human Milk”) AND (“Overweight” OR “Obesity”).
A search was conducted by two independent researchers and finalized in September 2016. There was no delimitation of publication period or language restriction.
The bibliographic search returned 1,582 papers. Of these, 56 were selected for full-text reading. After extensive selection, only 14 manuscripts were chosen for this work. The others were excluded because they addressed themes that were not of interest to this study. Also, we searched for other papers in the references of the selected papers for this study, but no new manuscripts were found.
The selected papers were compared against the following axes: sample size, mean age of the participants, type of design, maternal morbidity, milk evaluation period, human milk macronutrient analysis method, confounding factors controlled in the analysis and main results observed.
Results
The literature search resulted in 14 papers published between 1987 and 2016. Most studies (n = 5) were conducted in North America (United States), followed by South America (Brazil), Europe (Greece, Finland and the Netherlands), Asia (Lebanon) and Oceania (Australia). Regarding the studied population, age ranged from 17 to 43 years, and three papers did not inform the age group of the participants. The lowest sample consisted of 11 participants, and the most significant sample was 305. Regarding the language, one paper was written in Portuguese and the other in English (Table 1).
Concerning the morbidities, nine papers evaluated diabetes mellitus88. Butte NF, Garza C, Burr R, Goldman AS, Kennedy K, Kitzmiller JL. Milk composition of insulin-dependent diabetic women. J Pediatr Gastroenterol Nutr 1987; 6(6):936-941.
9. Bitman J, Hamosh M, Hamosh P. Milk composition and volume during the onset of lactation in a diabetic mother. Am J Clin Nutr 1989; 50(6):1364-1369.
10. Arthur PG, Smith M, Hartmann PE. Milk lactose, citrate, and glucose as markers of lactogenesis in normal and diabetic women. I Pediatr Gastroenterol Nutr 1989; 9(4):488-496.
11. Neubauer SH, Ferris AM, Chase CG, Fanelli J, Thompson CA, Lammi-Keefe CJ, Clark RM, Jensen RG, Bendel RB, Green KW. Delayed lactogenesis in women with insulin-dependent diabetes mellitus. Am J Clin Nutr 1993; 58(1):54-60
12. Van Beusekom CM, Zeegers TA, Martini IA, Velvis HJ, Visser GH, van Doormaal JJ, Muskiet FA. Milk of patients with tightly controlled insulin-dependent diabetes mellitus has normal macronutrient and fatty acid composition. Am J Clin Nutr 1993; 57(6):938-943.
13. Jackson MB, Lammi-Keefe CJ, Jensen RG. Total lipid and fatty acid composition of milk from women with and without insulin-dependent diabetes mellitus. Am J Clin Nutr 1994; 60(3):353-361.
14. Lammi-Keefe CJ, Jonas CR, Ferris AM, Capacchione CM. Vitamin E in plasma and milk of lactating women with insulin-dependent diabetes mellitus. J Pediatr Gastroenterol Nutr 1995; 20(3):305-309.
15. Oliveira AMDM, Cunha CC, Penha-Silva N, Abdallah VOS, Jorge PT. Interference of the blood glucose control in the transition between phases I and II of lactogenesis in patients with type 1 diabetes mellitus. Arq. Bras. Endocrinol Metabol. 2008; 52(3):473-481.
16. Morceli G, França EL, Magalhães VB, Damasceno DC, Calderon IMP, Honorio-França AC, Diabetes induced immunological and biochemical changes in human colostrum. Acta Paediatr 2011; 100(4):550-556.-1717. Dritsakou K, Liosis G, Valsami G, Polychronopoulos E, Skouroliakou M. The impact of maternal- and neonatal-associated factors on human milk’s macronutrients and energy. J Matern Fetal Neonatal Med 2017; 30(11):1302-1308., one evaluated hypertension1818. Massmann PF, França EL, Souza EG, Souza MS, Brune MFSS, Honorio-França AC. Maternal hypertension induces alterations in immunological factors of colostrum and human milk. Front Life Sci 2013; 7(3-4):155-163. and four overweight1717. Dritsakou K, Liosis G, Valsami G, Polychronopoulos E, Skouroliakou M. The impact of maternal- and neonatal-associated factors on human milk’s macronutrients and energy. J Matern Fetal Neonatal Med 2017; 30(11):1302-1308.,1919. Makela J, Linderborg K, Niinikoski H, Yang B, Lagstrom H. Breast milk fatty acid composition differs between overweight and normal weight women: the STEPS Study. Eur J Nutr 2013; 52(2):727-735
20. Fujimori M, França EL, Fiorin V, Morais TC, Honorio-França AC, Abreu LC. Changes in the biochemical and immunological components of serum and colostrum of overweight and obese mothers. BMC Pregnancy Childbirth 2015; 15:166.-2121. Bachour P, Yafawi R, Jaber F. Effects of smoking, mother’s age, body mass index, and parity number on lipid, protein, and secretory immunoglobulin A concentrations of human milk. Breastfeed Med 2012; 7(3):179-188.. Only one paper evaluated both diabetes and overweight (Table 2).
The most commonly used technique for fat content analysis was gravimetry, followed by calorimetry. For the analysis of the total protein content, the most common procedure was the Kjeldahl method. Only one study analyzed all macronutrients (fat, protein and carbohydrate) and total energy in a single procedure, and for this analysis, the author used the spectrophotometric technique from the Human Milk Analyzer – Miris (Table 2).
Regarding the time of evaluation of human milk, most studies (n = 6) analyzed all phases of milk (colostrum, transitional milk and mature milk), five analyzed only colostrum, two only mature milk and one analyzed the transition and mature milk. The number of milk analyses ranged from 1 to 7 times (Table 2).
Regarding the design used, most (n = 11) used longitudinal observational studies. Information on confounding factors controlled in the analysis was obtained in 12 studies, and the most prevalent were maternal age, gestational age at delivery, type of delivery, tobacco use, parity, and newborn birth weight. Seven papers did not mention exclusion criteria in their methods (Table 3).
Regarding the results of the selected papers, it was observed that nine studies found significant differences in the nutritional composition of the milk of mothers with diabetes mellitus, hypertension, or overweight. A lower concentration of lactose (n = 3) and fat (n = 4) was observed concerning diabetes mellitus and one paper found lower protein value and higher energy value. The other papers selected (n = 2) did not find statistical differences concerning macronutrients (fat, protein, carbohydrate) and total energy. The only study that evaluated the nutritional composition of milk of women with arterial hypertension found that colostrum and mature milk from hypertensive mothers had higher levels of total protein. Regarding overweight, two studies concluded that mothers with obesity had higher fat and energy content, and the other two studies did not find statistical differences (Table 3).
Discussion
In this section, we will discuss and emphasize the main results of the papers selected for this systematic review that have investigated the possible effect of chronic diseases (diabetes mellitus, arterial hypertension or overweight) on the nutritional composition of human milk.
Insulin inadequacy in diabetes mellitus can directly affect the quantity and quality of human milk1515. Oliveira AMDM, Cunha CC, Penha-Silva N, Abdallah VOS, Jorge PT. Interference of the blood glucose control in the transition between phases I and II of lactogenesis in patients with type 1 diabetes mellitus. Arq. Bras. Endocrinol Metabol. 2008; 52(3):473-481.,1616. Morceli G, França EL, Magalhães VB, Damasceno DC, Calderon IMP, Honorio-França AC, Diabetes induced immunological and biochemical changes in human colostrum. Acta Paediatr 2011; 100(4):550-556.. The results of the studies that have investigated this issue are different.
Beusekom et al.1212. Van Beusekom CM, Zeegers TA, Martini IA, Velvis HJ, Visser GH, van Doormaal JJ, Muskiet FA. Milk of patients with tightly controlled insulin-dependent diabetes mellitus has normal macronutrient and fatty acid composition. Am J Clin Nutr 1993; 57(6):938-943. did not observe significant differences between glucose, lipid and sodium levels in mature milk of diabetic women. Similarly, Butte et al.88. Butte NF, Garza C, Burr R, Goldman AS, Kennedy K, Kitzmiller JL. Milk composition of insulin-dependent diabetic women. J Pediatr Gastroenterol Nutr 1987; 6(6):936-941. found no change in lactose and protein (colostrum, transition and mature milk) among people with diabetes. Authors believe this result may be partly explained because the selected diabetic women have controlled glycemia.
However, Neubauer et al.1111. Neubauer SH, Ferris AM, Chase CG, Fanelli J, Thompson CA, Lammi-Keefe CJ, Clark RM, Jensen RG, Bendel RB, Green KW. Delayed lactogenesis in women with insulin-dependent diabetes mellitus. Am J Clin Nutr 1993; 58(1):54-60 found lower lactose and higher protein on the second and third day postpartum among people with diabetes. Oliveira et al.1515. Oliveira AMDM, Cunha CC, Penha-Silva N, Abdallah VOS, Jorge PT. Interference of the blood glucose control in the transition between phases I and II of lactogenesis in patients with type 1 diabetes mellitus. Arq. Bras. Endocrinol Metabol. 2008; 52(3):473-481. also observed lower lactic concentration in the group of diabetic women during the first five days postpartum.
Dritsakou et al.1717. Dritsakou K, Liosis G, Valsami G, Polychronopoulos E, Skouroliakou M. The impact of maternal- and neonatal-associated factors on human milk’s macronutrients and energy. J Matern Fetal Neonatal Med 2017; 30(11):1302-1308. identified higher levels of fat in the milk of diabetic women. This may be partly explained by the abnormal lipid metabolism in diabetics, which is marked by an elevation of lipoprotein lipase and lipolysis. It is worth noting that 50% of diabetics were diagnosed with overweight. However, the authors did not control any possible confounding factors.
Contrary to the findings made explicit above, Jackson et al.1313. Jackson MB, Lammi-Keefe CJ, Jensen RG. Total lipid and fatty acid composition of milk from women with and without insulin-dependent diabetes mellitus. Am J Clin Nutr 1994; 60(3):353-361. and Morceli et al.1616. Morceli G, França EL, Magalhães VB, Damasceno DC, Calderon IMP, Honorio-França AC, Diabetes induced immunological and biochemical changes in human colostrum. Acta Paediatr 2011; 100(4):550-556. observed that the amount of fat in the human milk of diabetic women was lower compared to the control group. Despite the results’ unanimity, different methods were used to evaluate the nutritional composition of human milk.
Another point worth mentioning is the influence exerted by diabetes mellitus on milk volume. Lactation is marked by two phases – lactogenesis I and II. Phase I begins at the 20th gestation week and may be marked by increased lactose and alpha-lactalbumin. Phase II occurs between 24 and 48 hours postpartum and is marked by increased lactose. Oliveira et al.1515. Oliveira AMDM, Cunha CC, Penha-Silva N, Abdallah VOS, Jorge PT. Interference of the blood glucose control in the transition between phases I and II of lactogenesis in patients with type 1 diabetes mellitus. Arq. Bras. Endocrinol Metabol. 2008; 52(3):473-481. found an 18-hour delay in the diabetic group to complete the transition from phase I to phase II of lactogenesis, which hindered the establishment of breastfeeding. Similar to the specified, Bitman et al.99. Bitman J, Hamosh M, Hamosh P. Milk composition and volume during the onset of lactation in a diabetic mother. Am J Clin Nutr 1989; 50(6):1364-1369., Arthur et al.1010. Arthur PG, Smith M, Hartmann PE. Milk lactose, citrate, and glucose as markers of lactogenesis in normal and diabetic women. I Pediatr Gastroenterol Nutr 1989; 9(4):488-496. and Neubauer et al.1111. Neubauer SH, Ferris AM, Chase CG, Fanelli J, Thompson CA, Lammi-Keefe CJ, Clark RM, Jensen RG, Bendel RB, Green KW. Delayed lactogenesis in women with insulin-dependent diabetes mellitus. Am J Clin Nutr 1993; 58(1):54-60 observed that the transition from phase I to II of lactogenesis was delayed among diabetic patients with inadequate glycemic control, which led to reduced milk volume from the third to the seventh day postpartum.
The delayed lactogenesis transition in diabetic patients can be partially explained by the action of insulin in the uptake of glucose by the mammary gland. Therefore, the control of glucose in diabetic women is of paramount importance for the achievement of an adequate nutritional composition of human milk as well as for the establishment of breastfeeding1616. Morceli G, França EL, Magalhães VB, Damasceno DC, Calderon IMP, Honorio-França AC, Diabetes induced immunological and biochemical changes in human colostrum. Acta Paediatr 2011; 100(4):550-556..
Hypertension is often associated with metabolic, functional, or structural changes in target organs. Also, it is considered one of the diseases that causes more harmful effects to the maternal, fetal and neonatal body2222. Sociedade Brasileira de Cardiologia, Sociedade Brasileira de Hipertensão, Sociedade Brasileira de Nefrologia. VI Diretrizes Brasileiras de Hipertensão. Arq. Bras. Cardiol. 2010; 95(1):1-51.,2323. Freire CMV, Tedoldi CL. Hipertensão arterial na gestação. Arq. Bras. Cardiol. 2009; 93(6):159-165..
When we observed the impact of hypertension on the nutritional composition of human milk, only the study conducted by Massmann et al.1818. Massmann PF, França EL, Souza EG, Souza MS, Brune MFSS, Honorio-França AC. Maternal hypertension induces alterations in immunological factors of colostrum and human milk. Front Life Sci 2013; 7(3-4):155-163. was selected. In this study, the authors concluded that colostrum and mature milk from hypertensive mothers had higher levels of total protein. However, the effects of changes in blood pressure on the nutritional composition of human milk are still not fully understood, especially for mothers who have had hypertension-aggravated pregnancies2424. Sírio MAO, Silva ME, Paula H, Passos MC, Sobrinho AOS. Estudo dos determinantes clínicos e epidemiológicos das concentrações de sódio e potássio no colostro de nutrizes hipertensas e normotensas. Cad Saude Publica 2007; 23(9):2205-2214..
Regarding the influence of overweight on the nutritional composition of human milk, Bachour et al.2121. Bachour P, Yafawi R, Jaber F. Effects of smoking, mother’s age, body mass index, and parity number on lipid, protein, and secretory immunoglobulin A concentrations of human milk. Breastfeed Med 2012; 7(3):179-188. found that the nutritional composition of the milk of overweight women had a lower amount of protein. According to the authors, this change may be partially explained by a higher level of oxidative stress among overweight patients.
Fujimori et al.2020. Fujimori M, França EL, Fiorin V, Morais TC, Honorio-França AC, Abreu LC. Changes in the biochemical and immunological components of serum and colostrum of overweight and obese mothers. BMC Pregnancy Childbirth 2015; 15:166. and Dritsakou et al.1717. Dritsakou K, Liosis G, Valsami G, Polychronopoulos E, Skouroliakou M. The impact of maternal- and neonatal-associated factors on human milk’s macronutrients and energy. J Matern Fetal Neonatal Med 2017; 30(11):1302-1308. found higher levels of fat and energy in the milk of overweight women. However, Makela et al.1919. Makela J, Linderborg K, Niinikoski H, Yang B, Lagstrom H. Breast milk fatty acid composition differs between overweight and normal weight women: the STEPS Study. Eur J Nutr 2013; 52(2):727-735 concluded that the milk fat content did not change. It is noteworthy that the milk of these overweight women had a higher amount of saturated fatty acids, reduced amount of omega 3 and a high proportion of omega 6 compared to omega 3.
In short, most studies have shown that the presence of chronic diseases leads to changes in the nutritional composition of human milk. The main results were: 1) three papers that evaluated the nutritional composition of human milk of women with diabetes mellitus found a lower concentration of lactose1010. Arthur PG, Smith M, Hartmann PE. Milk lactose, citrate, and glucose as markers of lactogenesis in normal and diabetic women. I Pediatr Gastroenterol Nutr 1989; 9(4):488-496.,1111. Neubauer SH, Ferris AM, Chase CG, Fanelli J, Thompson CA, Lammi-Keefe CJ, Clark RM, Jensen RG, Bendel RB, Green KW. Delayed lactogenesis in women with insulin-dependent diabetes mellitus. Am J Clin Nutr 1993; 58(1):54-60,1515. Oliveira AMDM, Cunha CC, Penha-Silva N, Abdallah VOS, Jorge PT. Interference of the blood glucose control in the transition between phases I and II of lactogenesis in patients with type 1 diabetes mellitus. Arq. Bras. Endocrinol Metabol. 2008; 52(3):473-481., and four of fat99. Bitman J, Hamosh M, Hamosh P. Milk composition and volume during the onset of lactation in a diabetic mother. Am J Clin Nutr 1989; 50(6):1364-1369.,1212. Van Beusekom CM, Zeegers TA, Martini IA, Velvis HJ, Visser GH, van Doormaal JJ, Muskiet FA. Milk of patients with tightly controlled insulin-dependent diabetes mellitus has normal macronutrient and fatty acid composition. Am J Clin Nutr 1993; 57(6):938-943.,1313. Jackson MB, Lammi-Keefe CJ, Jensen RG. Total lipid and fatty acid composition of milk from women with and without insulin-dependent diabetes mellitus. Am J Clin Nutr 1994; 60(3):353-361.,1616. Morceli G, França EL, Magalhães VB, Damasceno DC, Calderon IMP, Honorio-França AC, Diabetes induced immunological and biochemical changes in human colostrum. Acta Paediatr 2011; 100(4):550-556.. Concerning hypertension, a higher total protein concentration was found in both colostrum and mature milk1818. Massmann PF, França EL, Souza EG, Souza MS, Brune MFSS, Honorio-França AC. Maternal hypertension induces alterations in immunological factors of colostrum and human milk. Front Life Sci 2013; 7(3-4):155-163.. In the case of overweight, half of the studies observed a higher fat and energy content in the milk of these mothers1717. Dritsakou K, Liosis G, Valsami G, Polychronopoulos E, Skouroliakou M. The impact of maternal- and neonatal-associated factors on human milk’s macronutrients and energy. J Matern Fetal Neonatal Med 2017; 30(11):1302-1308.,2020. Fujimori M, França EL, Fiorin V, Morais TC, Honorio-França AC, Abreu LC. Changes in the biochemical and immunological components of serum and colostrum of overweight and obese mothers. BMC Pregnancy Childbirth 2015; 15:166..
The different results among the selected studies can be partly explained by the numerous methodological differences, such as sample size, the method used in the evaluation of human milk, control of confounding factors, nutritional components evaluated, lactation stage (colostrum, and transition and mature milk).
It is noteworthy that while chronic diseases cause nutritional changes in human milk, it is universally agreed that breastfeeding should be strongly encouraged exclusively until the 6th month of life of the newborn and that, from then on, breastfeeding is maintained for two years or more, together with appropriate complementary foods.
It is of the utmost importance that women have continuous nutritional monitoring in prenatal and postpartum care to have effective control of blood glucose, blood pressure and gestational weight gain in order to minimize the impact of diabetes mellitus, arterial hypertension and overweight on the nutritional composition of milk, as well as on the early establishment of breastfeeding.
References
- 1Nucci LB, Duncan BB, Mengue SS, Branchtein L, Schmidt MI, Fleck ET. Assessment of weight gain during pregnancy in general prenatal care services in Brazil. Cad Saude Publica 2001; 17(6):1367-1374.
- 2Lawrence JM, Contreras R, Chen W, Sacks DA. Trends in the prevalence of preexisting diabetes and gestational diabetes mellitus among a racially/ethnically diverse population of pregnant women, 1999-2005. Diabetes Care 2008; 31(5):899-904.
- 3Schmidt MI, Duncan BB, Reichelt AJ, Branchtein L, Matos MC, Costa e Forti A, Spichler ER, Pousada JM, Teixeira MM, Yamashita T. Gestational diabetes mellitus diagnosed with a 2-h 75-g oral glucose tolerance test and adverse pregnancy outcomes. Diabetes Care 2001; 24(7):1151-1155.
- 4Brasil. Ministério da Saúde (MS). Cadernos de Atenção Básica: Atenção ao Pré-natal de Baixo Risco Brasília: MS; 2012.
- 5Barros DCD, Saunders C, Leal MDC. Avaliação nutricional antropométrica de gestantes brasileiras: uma revisão sistemática. Rev. Bras. Saúde Mater. Infant 2008; 8(4):363-376.
- 6Ballard O, Morrow AL. Human Milk Composition Nutrients and Bioactive Factors. Pediatr Clin N Am 2013; 60(1):49-74.
- 7Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group. Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Med 2009; 6(7):e1000097.
- 8Butte NF, Garza C, Burr R, Goldman AS, Kennedy K, Kitzmiller JL. Milk composition of insulin-dependent diabetic women. J Pediatr Gastroenterol Nutr 1987; 6(6):936-941.
- 9Bitman J, Hamosh M, Hamosh P. Milk composition and volume during the onset of lactation in a diabetic mother. Am J Clin Nutr 1989; 50(6):1364-1369.
- 10Arthur PG, Smith M, Hartmann PE. Milk lactose, citrate, and glucose as markers of lactogenesis in normal and diabetic women. I Pediatr Gastroenterol Nutr 1989; 9(4):488-496.
- 11Neubauer SH, Ferris AM, Chase CG, Fanelli J, Thompson CA, Lammi-Keefe CJ, Clark RM, Jensen RG, Bendel RB, Green KW. Delayed lactogenesis in women with insulin-dependent diabetes mellitus. Am J Clin Nutr 1993; 58(1):54-60
- 12Van Beusekom CM, Zeegers TA, Martini IA, Velvis HJ, Visser GH, van Doormaal JJ, Muskiet FA. Milk of patients with tightly controlled insulin-dependent diabetes mellitus has normal macronutrient and fatty acid composition. Am J Clin Nutr 1993; 57(6):938-943.
- 13Jackson MB, Lammi-Keefe CJ, Jensen RG. Total lipid and fatty acid composition of milk from women with and without insulin-dependent diabetes mellitus. Am J Clin Nutr 1994; 60(3):353-361.
- 14Lammi-Keefe CJ, Jonas CR, Ferris AM, Capacchione CM. Vitamin E in plasma and milk of lactating women with insulin-dependent diabetes mellitus. J Pediatr Gastroenterol Nutr 1995; 20(3):305-309.
- 15Oliveira AMDM, Cunha CC, Penha-Silva N, Abdallah VOS, Jorge PT. Interference of the blood glucose control in the transition between phases I and II of lactogenesis in patients with type 1 diabetes mellitus. Arq. Bras. Endocrinol Metabol. 2008; 52(3):473-481.
- 16Morceli G, França EL, Magalhães VB, Damasceno DC, Calderon IMP, Honorio-França AC, Diabetes induced immunological and biochemical changes in human colostrum. Acta Paediatr 2011; 100(4):550-556.
- 17Dritsakou K, Liosis G, Valsami G, Polychronopoulos E, Skouroliakou M. The impact of maternal- and neonatal-associated factors on human milk’s macronutrients and energy. J Matern Fetal Neonatal Med 2017; 30(11):1302-1308.
- 18Massmann PF, França EL, Souza EG, Souza MS, Brune MFSS, Honorio-França AC. Maternal hypertension induces alterations in immunological factors of colostrum and human milk. Front Life Sci 2013; 7(3-4):155-163.
- 19Makela J, Linderborg K, Niinikoski H, Yang B, Lagstrom H. Breast milk fatty acid composition differs between overweight and normal weight women: the STEPS Study. Eur J Nutr 2013; 52(2):727-735
- 20Fujimori M, França EL, Fiorin V, Morais TC, Honorio-França AC, Abreu LC. Changes in the biochemical and immunological components of serum and colostrum of overweight and obese mothers. BMC Pregnancy Childbirth 2015; 15:166.
- 21Bachour P, Yafawi R, Jaber F. Effects of smoking, mother’s age, body mass index, and parity number on lipid, protein, and secretory immunoglobulin A concentrations of human milk. Breastfeed Med 2012; 7(3):179-188.
- 22Sociedade Brasileira de Cardiologia, Sociedade Brasileira de Hipertensão, Sociedade Brasileira de Nefrologia. VI Diretrizes Brasileiras de Hipertensão. Arq. Bras. Cardiol. 2010; 95(1):1-51.
- 23Freire CMV, Tedoldi CL. Hipertensão arterial na gestação. Arq. Bras. Cardiol. 2009; 93(6):159-165.
- 24Sírio MAO, Silva ME, Paula H, Passos MC, Sobrinho AOS. Estudo dos determinantes clínicos e epidemiológicos das concentrações de sódio e potássio no colostro de nutrizes hipertensas e normotensas. Cad Saude Publica 2007; 23(9):2205-2214.
Publication Dates
- Publication in this collection
22 July 2019 - Date of issue
July 2019
History
- Received
30 Dec 2016 - Reviewed
19 Oct 2017 - Accepted
21 Oct 2017