ORIGINAL

 

Lipid profile in people with Down syndrome: a literature review

 

 

Eloise Werle de Almeida; Márcia Greguol

Departamento de Educação Física, Centro de Educação Física e Esporte, Universidade Estadual de Londrina (UEL) - Londrina (PR), Brasil

Correspondence

 

 

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ABSTRACT

BACKGROUNG: People with Down syndrome (DS) may present changes in the lipid profile. The objective of this research was to collect data from the literature on the lipid profile and the effect of exercise on this variable of people with DS. Five databases were searched (MedLine, Lilacs, EBSCO Host, Web of Science and PsycInfo) using terms related to the research objectives. At the end of the searches, 15 articles were included in the review. Five studies verified changes in the lipid profile and high incidence of dyslipidemias, with the most frequent changes being low HDL and elevated triglycerides. Two studies investigated the effect of intervention with exercise and counseling for health-friendly practices and found improvement mainly in HDL after the intervention period. Thus, the lipid profile should be investigated in people with DS and the practice of physical exercises can be used to control these variables

Keywords: Lipid profile, Down syndrome, Physical exercise, Literature review.

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Authors summary

Why was this study done?

Down syndrome involves a number of morphological and functional characteristics that require specific care. For this care to be managed, it is important to systematize information about the health of this population. The number of professionals working with people with DS is increasing and they still need subsidies to make this performance increasingly specific to the needs of disabilities. In this sense, we performed the literature review so that we could gather information from the literature on the lipid profile of people with DS, since these data are relevant to the health of this population.

What did the researchers do and find?

We gather data from the literature on the lipid profile and the effect of exercise on this variable of people with DS. Five databases were searched (MedLine, Lilacs, EBSCO Host, Web of Science and PsycInfo) using terms related to the research objectives. At the end of the searches, 15 articles were included in the review.

From the analysis of the studies included in this review, it is possible to perceive that a high portion of the population with DS presents negative results of the lipid profile. Also, important relationships between abdominal fat accumulation and lipid profile were found. Excess abdominal fat is associated with higher total cholesterol, LDL and triglycerides and lower HDL cholesterol. Finally, it was verified that both the practice of recreational physical activities and regular and systematized physical exercises seem to benefit the lipid profile, specifically the HDL cholesterol of people with DS.

What do these findings mean?

It was possible to notice that people with Down syndrome have negative results related to their lipid profile, and even though some studies seek to understand what interferes in these variables, there is still little research investigating these data.

Also, it is known that in people without disabilities, the practice of physical exercises can have benefits for the lipid profile. However, little research has verified the effects of exercise for the population with Down syndrome.

Therefore, in general, the results indicate the need to further investigate the effects of exercise on the behavior of the lipid profile of people with Down syndrome, so that an increasingly active lifestyle is stimulated among this population, and so that the benefits brought by the practice of physical exercises are manifested in the maintenance of positive health among these individuals. In addition, the results found in this study can target professionals who work together with people with Down syndrome, in order to guide new research possibilities that can be conducted with this population.

 

INTRODUCTION

Down Syndrome (DS), defined as the trisomy of chromosome 21, is the most frequent chromosomal abnormality that causes intellectual disability¹. Data indicate that, worldwide, the syndrome affects one in every 750 live births². In the majority of cases, people affected by DS present free or simple trisomy 21, in which all cells in the body have a third chromosome of pair 21^3,4.

The characteristics of this syndrome, such as muscular hypotonia, the presence of congenital heart diseases, and alterations in the hormonal and enzymatic metabolism can favor overweight and obesity in this population^3,5,6. Eberhard et al.³ suggest that chromosomal alterations that promote a neurochemical imbalance in the production of some enzymes such as phosphofructokinase and superoxide dismutase may interfere with the antioxidative process of the organism, thus favoring early aging.

With regard to the lipid metabolism of people with DS, the literature does not yet provide definite data on the values of total cholesterol, or HDL and LDL cholesterol in this population. Some studies indicate levels considered normal for these variables^3,7, however, recent research has found that the lipid profile of young and adult patients with DS are characterized by dyslipidemia, in which high levels of total cholesterol, LDL and triglycerides (TG) and low HDL levels are observed^8-10. Lifestyle and the practice of physical activities are strongly related to the control of these factors, which in turn are associated with the incidence of cardiovascular diseases^5,11,12.

In people with disabilities, especially DS, the lack of practice of physical activities is common. Associated with the characteristics of the syndrome, sedentary behavior is one of the reasons for obesity and low levels of physical fitness in this population^13,14. Thus, a physical exercise program can act positively in physical fitness, lipid, blood pressure and glycemic profile of individuals, which can reduce blood pressure, the need for insulin, total body fat, triglyceride levels and raise HDL cholesterol levels^15,16. However, there is insufficient evidence to detail which physical exercise programs are effective in improving this profile in people with DS^17-21.

Thus Down syndrome involves a number of morphological and functional characteristics that require specific care. For this care to be managed, it is important to systematize information about the health of this population. The number of professionals working with people with DS is increasing and they still need subsidies to make this performance increasingly specific to the needs of disabilities. In this sense, the review and gathering of literature information on the lipid profile of people with DS becomes relevant to the health of this population.

Based on the above, the objective of this review is to analyze the data available in the literature on the lipid metabolism and the influence of physical exercise on these variables considered as a control for the risk of cardiovascular diseases in people with Down Syndrome

 

METHODS

The review of the literature was conducted through a search for articles indexed in databases that addressed the topic of the lipid profile in people with Down syndrome and the influence of physical exercise on this variable. The following databases were selected to conduct the search: Pubmed, Medline - Medlars Online (1950 - April 2018); Lilacs - Latin American and Caribbean Health Science Literature (1982 - April 2018); EBSCO Host (1975 - April 2018); Web of Science (1900 - April 2018); PsycInfo (2001 - April 2018).

The following Health Sciences descriptors were used to perform the search: "Down Syndrome", "Intellectual Disability", "Mental Retardation", "Blood", "Lipid Profile", "Cholesterol", "Triglycerides", "Physical Activity", "Exercise", "Fitness", "Training", "Training program", using the Boolean operators OR and AND to expand and refine the searches. No language restriction was placed on the publications. The decision to include articles was taken by two independent researchers and any disagreements were resolved by consensus.

After completing the searches, the articles were selected according to the following inclusion criteria: field studies with the participation of people with Down Syndrome; assessment of the lipid profile of participants with Down syndrome OR effects of an exercise intervention on the lipid profile of participants with Down syndrome. Review studies, as well as dissertations and theses were excluded from this study.

After this stage, the publications that met the inclusion criteria were tabulated and analyzed according to the following factors: research objective (a), characteristics of study participants (b), variables searched (c), and main findings of the research (d). Again, with this more refined analysis, if the studies were not completely in accordance with the proposed inclusion criteria, they were excluded from the review.

 

RESULTS

Selection of studies

From the searches in the selected databases, 601 studies were found using the terms described. Articles that were indexed in more than one database were excluded, giving a total of 490 articles. A thorough reading of the titles was then carried out to confirm if the publications fit the proposed research theme. After this step, 22 studies were selected.

The remaining 22 articles were then passed for complete and refined reading. After completing the readings, seven studies were excluded as they did not fully comply with the proposed inclusion criteria (did not perform field studies analyzing lipid metabolism or the effect of exercise on this variable in people with DS). Therefore, 15 studies were included in the present review.

The search results are described in Table 1 and the article selection strategy for this review is described in Figure 1.

Characteristics of the included studies

Most of the studies included in this review had a cross-sectional design. Only three studies were quasi experimental and evaluated the effect of an intervention on the participants^3,22,23. Of the 15 articles included, ten performed an analysis of the lipid profile and five evaluated the effect of exercise on this variable at a given time. Regarding the study participants, the number of individuals varied from 01 to 52, totaling 1097 people with Down Syndrome. The main findings of the studies are summarized in Tables 2 and 3.

The results of the lipid profile presented by the surveys included in this literature review were variable and different from each other. Of the ten articles in which lipid profile analysis was performed without the influence of physical exercise^7-10,24-29, in five the participants had some alteration in the lipid profile^{9,10,24,25,27}.

In the study by Rimmer et al.²⁷, 32% of the women and 54% of the participating men (17 to 72 years old) had high cholesterol values (> 200mg/dl). Similarly, de el Piedra et al.¹⁰ reported that 58% of the participants (2 to 18 years old) had some alteration in the lipid profile. Low HDL and high triglyceride levels were the most frequent changes. Asua et al.²⁴ found that 17 of the 49 participants (adults older than 18 years) with DS were diagnosed with dyslipidemia and Buonouomo et al.⁹ found that participants (2 to 19 years old) presented high values of total cholesterol (TC), LDL cholesterol and triglycerides and low HDL levels, except for girls over 15 years of age, for which normal values of these variables were observed. In the study by Draheim et al.²⁵, cholesterol levels were within normal values and only triglycerides were elevated (participants between 35 and 60 years).

In the study by Adelekan et al.⁸ lipid profile values were within the recommended range for health, but were still higher than the results of their peers non-DS, which constituted the control group in the study. Furthermore, Ordoñez-Munoz et al.⁷, Marín and Graupera²⁸ and Wallen et al.²⁹ found that the values of the lipid profile variables of adolescents and adults were within the recommended range. The search results of Dorner et al.²⁶ indicated that adults with DS had lower cholesterol levels than participants in the "non-deficient" control group.

Of the five articles in which the effect of the exercise on the lipid profile was evaluated^{3,22,23,30,31}, three had a quasi-experimental protocol^3,22,23 and applied an intervention in the research. Carmeli et al.²² evaluated the effect of a training program with walking in a non-pain intensity range in elderly institutionalized with DS. The lipid profile was evaluated before the exercise period and the elderly had adequate cholesterol levels. However, these variables were not evaluated after the walking program and, therefore, it was not possible to verify the effect of the activities on the lipid profile of the elderly. Eberhard et al.²³ applied a diet and physical exercise counseling program for people with DS and without disabilities. No differences were found in the fractions of HDL cholesterol among the children with DS who participated in the intervention and without DS, while the children of the control group with DS had worse results in this variable after the intervention with counseling.

In the study by Eberhard et al.³, a 12-week training program was conducted with young people with SD aged 15 to 21 years. The program consisted of one hour of aerobic activity on a stationary bicycle at an intensity of 60% of VO₂max twice a week and games at school involving races and walks for one hour a day. The lipid profile was evaluated before and after an incremental test of 40 minutes in a cycle ergometer, taking the participants close to exhaustion. The test was performed before and after the training program. At the end of the 12 weeks, authors noticed an increase in HDL cholesterol in the participants after the test.

The other two studies included in this revision performed evaluations after a single session of physical exercises. In the researches of Eberhard³⁰ and Flore et al.³¹, who evaluated the acute effect of the exercise, the cholesterol results were in normal patterns among the participants. Eberhard³⁰ found that participants presented low values of HDL cholesterol and high values of VLDL cholesterol. After an effort of 40 minutes at an intensity of 57% of VO₂max, few changes in cholesterol values were found. Flore et al.³¹ evaluated cholesterol levels before exercise, but after the tests the variables of the lipid profile were not measured again. Instead, variables related to lipid oxidation after an exercise session with intensity variations of 30 to 75% of maximal VO₂ were evaluated.

 

DISCUSSION

The objective of this review study was to bring together studies in the literature that investigated the lipid profile of people with Down Syndrome, as well as the effects of exercise on these variables.

As in the population without disabilities, mortality due to cardiovascular diseases has increased among people with intellectual disabilities (ID). Adults with mild to moderate ID and belonging to lower social classes are at greater risk of developing cardiovascular diseases. In addition, age, sex, lipid and glycemic profile, and blood pressure are also risk factors for the development of this type of pathology³².

When submitted to a physical exercise program, Elmahgoub et al.³³ found that, after 10 weeks of combined aerobic resistance training, 15 adolescents aged 14-22 years with moderate to severe intellectual disability, diagnosed with Autism or fragile X syndrome, had an increase in HDL and a reduction in CT, LDL and TG when compared to a control group. The authors explain these results by decreasing body fat, also observed at the end of the training program.

Certain characteristics of Down syndrome, such as the high incidence of congenital cardiopathies and thyroid dysfunctions, as well as the frequent sedentary lifestyle in this population, may increase the risk situation of this group^3,5,6,34. In this sense, the evaluation and control of the lipid profile of people with Down syndrome may be important in the prevention of cardiovascular diseases.

Regarding the lipid profile, the studies present different results. Of the 10 articles in which these variables were analyzed without the influence of physical exercise^7-10,24-29, in five the participants had some alteration in the lipid profile^{9,10,24,25,27}, demonstrating a high incidence of these alterations in people with DS.

Increasing age may be a factor that influences higher cholesterol levels³⁵. However, when analyzing the age of participants in the studies included in this review that had inadequate levels of HDL, LDL, CT, and triglycerides, in two studies^9,10 participants had from 2 to 19 years. In the study by Rimmer et al.²⁷ in which the participants presented higher values of total cholesterol, the age of these subjects was from 17 to 72 years. Moreover, in the only study in which only elderly people were evaluated²², the results of lipid profile variables were within the normal pattern at the initial moment.

These data may indicate that other factors, such as lifestyle and dietary habits, which may lead to overweight and obesity, may have a greater influence on the lipid profile of people with Down's Syndrome than age³⁶. In an attempt to understand what leads to possible changes in the lipid variables of people with DS, some hypotheses are raised. Excess weight and body fat, especially in the abdominal region, common among people with DS, may possibly interfere with lipid levels. Two studies included in this review performed analyzes in this sense. Ordoñez-Munoz et al.⁷ found significant correlations between anthropometric variables (BMI, CA and Waist-to-Hip ratio) and the lipid profile of young people with a mean age of 16 years, highlighting the strong positive correlation between HDL and WHR. However, Asua et al.²⁴ found that adult participants with abdominal obesity, assessed by WHR, did not present CT, LDL, HDL and triglyceride values different from those who were not identified with excess abdominal fat.

Some studies have shown that, when compared to people without disabilities, participants with DS have higher nutritional intakes of carbohydrates and fats, and less consumption of proteins, fibers and some vitamins and minerals^37,38, and these eating habits may be related to excess weight and fat. Therefore, the analysis of food and nutritional intake may be an important strategy to understand the variations in the lipid profile of these people.

Reduced production of thyroid hormones, typical of hypothyroidism, may also be related to changes in cholesterol, especially increased LDL and reduced HDL. Lower concentrations of thyroid hormones decrease the synthesis and expression of LDL receptors, leading to a serum increase in LDL and, consequently, cholesterol. Moreover, the activity of the enzyme lectin-cholesterol-acyltransferase (LCAT), responsible for the esterification of endogenous cholesterol on the surface of HDL, is reduced in hypothyroidism, leading to the reduction of HDL cholesterol in this thyroid dysfunction^39,40.

Hypothyroidism is a common condition in people with DS. Approximately 30% to 50% of children with school-age SD present with hypothyroidism⁴¹. Thus, the importance of periodic evaluation of this variable is emphasized, also in the aid of the control of overweight and obesity and of the metabolic conditions that are associated with these dysfunctions. A study of this review carried out analyzes of thyroid hormones10 and found that 71% of adolescents with DS had been diagnosed with hypothyroidism. This group did not present significant differences in relation to the individuals without thyroid dysfunction, but a trend of higher levels of TG and lower HDL rates. This fact indicates that the care with the control of hypothyroidism is important for the maintenance of adequate levels of the lipid profile.

The practice of physical exercise can be a beneficial strategy for the control and reduction of cholesterol levels⁴². Research indicates that with physical exercise, muscle tissue increases its ability to consume fatty acids and increases lipoprotein lipase activity in muscle, reducing plasma lipid levels. In addition, the practice of physical exercises seems to increase the activity of the enzyme lectin-cholesterol-acyltransferase (LCAT), increasing HDL-cholesterol. This process removes cholesterol from circulation for its elimination^42,43.

Of the five articles in which the effect of the exercise on the lipid profile was evaluated^{3,22,23,30,31}, only two studies, of the three who applied an intervention, found improvement in the lipid profile after the exercise program³ or counseling²³ on positive health habits.

In the study by Eberhard et al.³, after a 12-week intervention with aerobic exercise in cycloergometer and school games, the authors verified the lipid profile before and after a 40-minute incremental test, and verified an increase in HDL cholesterol in the test performed after the intervention. However, even if benefits were found with the application of this training protocol, the type of play performed at school, as well as its intensity and student participation in these moments were not measured, making it difficult to generalize and extrapolate these data. But still, this is the only research found in the literature that applied an intervention with regular physical exercise practices and that evaluated its effect on the lipid profile.

In the research by Eberhard et al.²³ participants with SD and without disability received counseling related to health habits, such as the consumption of foods without sugars and fats, fruits and vegetables and the recommendation of practicing physical activities at school and at weekends. The youngsters were followed up for a year and after this period no differences were found in HDL cholesterol in children with and without disabilities who participated in the intervention, while the children in the control group with SD who did not receive counseling presented worse results in this variable. Therefore, also in this research positive effects were found in lipid profile variables investigated. However, no control was performed during the intervention period on the amount and intensity of physical exercise, as well as on the food consumed by the participants during the year. Thus, this research demonstrates that positive habits related to health can be positive even for the lipid profile, but it does not allow to draw conclusions about which exercise program brings these benefits or even if they necessarily need to be allied to food control.

Some studies included in the review present missing information that may compromise the analysis of results. In the study by Carmeli et al.²² for example an intervention was applied, and the authors investigated the effect of 15 weeks of walking performed three times a week for 40 minutes at an intensity that would not cause pain in institutionalized elderly with DS. The variables of the lipid profile were evaluated before the exercise program, but there was no evaluation of these variables after the intervention, which makes it impossible to obtain any conclusions regarding the effectiveness of the exercise program in this situation.

Eberhard³⁰ evaluated the acute effect of exercise on the lipid profile of 11 adolescents with DS and found that the participants had low values of HDL cholesterol and high rates of VLDL cholesterol. After a 40-minute cycle ergometer effort at 57% VO₂max, few changes in cholesterol values were found. However, the author verified an increase in free fatty acids (FFA), demonstrating that in this type of exercise the intensity in which it was performed stimulates lipid metabolism. This study presented a proposal different from the others included in this research, since it sought to investigate the effect of only one exercise session on cholesterol. The author did not find any results in this sense and pointed out that adaptations in the lipid profile would probably occur with regular physical exercise, confirming the need for research with these intervention protocols.

It is known that the practice of at least 60 minutes of physical activities at a moderate intensity by adolescents is associated with health benefits⁴⁴. However, it is common for people with disabilities, and specifically among people with DS, to be less involved in more intense physical activity practice⁴⁵. The articles presented in this review found that both the practice of physical activities performed at school or leisure time, as well as systematized exercise practices seem to bring benefits to the lipid profile of people with DS. However, the articles had different intervention protocols, making it difficult to compare results and construct more conclusive answers. Therefore, the effects of regular physical activity on this population still constitute a gap and need to be further investigated.

From this review it was possible to notice that there are not many studies that investigated the lipid profile in people with DS. And, especially, the effect of different physical exercise protocols on this variable has not yet been established. The benefits of physical exercise are widely known in people without disabilities. Considering the characteristics of DS, it is very important to study the effects of physical exercise in this population, specifically in the lipid profile, since the evidence presented in this review shows that both recreational and regular practices can bring improvements in cholesterol levels. This issue is still little discussed, perhaps due to the difficulty of adhering to physical exercise for people with disabilities. Thus, motivational proposals for this population can be placed so that the gaps found in the literature can be solved.

Research limitations

Despite the results found in the present study, some limitations need to be pointed out. Due to the still scarce amount of research produced investigating the lipid profile of people with Down syndrome, it was necessary to gather studies that investigated the cholesterol variables in different conditions: different age groups, recruitment of different participants, with or without physical exercise, or even by different methodologies. However, even with the disparities of research found, it is possible to draw an overview of the literature in the sense that further research is needed to investigate the lipid profile of this population

Still regarding the differences of the studies, the distinct methodological design of each one does not allow the accomplishment of statistical analyzes to search the evidences and to build the profile of the lipid variables of the Down syndrome population.

 

FINAL CONSIDERATIONS

From the analysis of the studies included in this review, it is possible to perceive that a high portion of the population with DS presents negative results of the lipid profile. Some hypotheses were investigated for the understanding of these results. Advanced age, which may be a factor for inadequate lipid profiles, did not seem to influence the results found in the research presented. Young individuals presented negative cholesterol and triglyceride results for health, while the elderly had adequate levels of these variables. Therefore, regardless of age, the lipid profile of people with DS should be followed up.

Also, we sought to analyze whether body composition or excess fat, mainly abdominal fat, could influence the lipid profile. Important relationships between abdominal fat accumulation and lipid profile were found. Excess abdominal fat is associated with higher total cholesterol, LDL and triglycerides and lower HDL cholesterol. Thus, control of body composition, especially abdominal fat accumulation, may be important to maintain the lipid profile at adequate levels for health.

A third aspect analyzed, which can influence the lipid profile of people with DS, is the production of thyroid hormones. Changes in the production of these hormones are frequent among people with DS, especially hypothyroidism. Individuals with this disorder tend to higher triglyceride and LDL values and lower HDL levels. Therefore, monitoring thyroid hormone levels is also important for cholesterol and triglycerides to stay at the right levels.

Finally, the practice of physical exercises was also considered, and it was verified that both the practice of recreational physical activities and regular and systematized physical exercises seem to benefit the lipid profile, specifically the HDL cholesterol of people with DS, although the shortage of studies and protocols hampers comparisons and extrapolations of data.

Therefore, it is realized that research is still needed with the purpose of investigating the chronic effect of physical exercise on the variables analyzed in this review study. There are few data in the literature on this topic. Considering the importance and benefits of regular physical activity for people without disabilities in these important variables of cardiovascular risk, we can highlight the importance of also knowing the effects of physical exercise for people with DS.

Thus, the data collected here may offer subsidies for professionals who prescribe physical exercise for people with DS, in order to guide practices that may also benefit the lipid profile and also suggest that this variable be monitored in the follow-up of physical exercise practice.

 

REFERENCES

1.Ordonez FJ, Rosety M, Rosety-Rodriguez M. Influence of 12-week exercise training on fat mass percentage in adolescents with Down syndrome. Med Sci Monit. 2006;12(10):CR416-19.         [ Links ]

2.Lana-Elola E, Watson-Scales SD, Fisher EM, Tybulewicz VL. Down syndrome: searching for the genetic culprits. Dis Models Mech. 2011;4(5):586-95. DOI: http://dx.doi.org/10.1242/dmm.008078        [ Links ]

3.Eberhard Y, Enterradossi J, Debû B. Biological changes induced by physical activity in individuals with Down's Syndrome. Adapt Phys Activ Q. 1997;14(2):166-75. DOI: https://doi.org/10.1123/apaq.14.2.166        [ Links ]

4. Pietti K, Baynard T, Agiovlastis S. Children and adolescents with Down syndrome, physical fitness and physical activity. J Sport Health Sci. 2013;2(1):47-57. DOI: https://doi.org/10.1016/j.jshs.2012.10.004        [ Links ]

5.González-Agüero A, Vicente-Rodríguez G, Moreno LA, Guerra-Balic M, Ara I, Casajús JA. Health-related physical fitness in children and adolescents with Down syndrome and response to training. Scand J Med Sci Sports. 2010;20(5):716-42. DOI: https://doi.org/10.1111/j.1600-0838.2010.01120.x        [ Links ]

6.Rimmer JH, Yamaki K, Davis BM, Wang E, Vogel LC. Obesity and Overweight Prevalence Among Adolescents with Disabilities. Prev Chronic Dis. 2011;8(2):A41.         [ Links ]

7.Ordoñez-Munoz FJ, Rosety-Rodríguez M, Rosety-Rodríguez JM, Rosety-Plaza M. Medidas antropométricas como predictoresdel comportamento lipídico sérico em adolescentes com síndrome de Down. Rev Invest Clin. 2005;57(5):691-4.         [ Links ]

8.Adelekan T, Magge S, Shults J, Stallings V, Settler N. Lipid profiles of children with Down Syndrome compared with their siblings. Pediatrics. 2012;129(6):1382-7. DOI: https://doi.org/10.1542/peds.2011-1262        [ Links ]

9.Buonuomo PS, Bartuli A, Mastrogiorgio G, Vittucci A, Di Camilo C, Bianchi S, et al. Lipid profiles in a large cohort os italian children with Down Syndrome. Eur J Med Genet. 2016;59(8):392-5. DOI: https://doi.org/10.1016/j.ejmg.2016.06.005        [ Links ]

10.de la Piedra MJ, Alberti G, Cerda J, Cárdenas A, Paul MA. Lizama M. High frequency of dyslipidemia in children and adolescents with Down Syndrome. Rev Chil Pediatr. 2017;88(5):595-601. DOI: http://dx.doi.org/10.4067/S0370-41062017000500004        [ Links ]

11.Haskell WL, Lee IM, Pate RR, Powell KE, Blair SN, Franklin BA, et al. Physical activity and public health: updated recommendation for adults from the American College of Sports Medicine and the American Heart Association. Med Sci Sports Exerc. 2007;116(9):1081-93. DOI: http://dx.doi.org/10.1249/mss.0b013e3180616b27        [ Links ]

12.Hootman J, Macera CA, Ainsworth BE, Martin M, Addy CL, Blair SN. Association among physical activity level, cardiorespiratory fitness, and risk of musculoskeletal injury. Am J Epidemiol. 2001;154(3):251-8. DOI: https://doi.org/10.1093/aje/154.3.251        [ Links ]

13.Balic MG, Mateos EC, Blasco CG, Fernhall B. Physical fitness levels of physically active and sedentary adults with Down syndrome. Adapt Phys Activ Q. 2000;17(3):310-21. DOI: https://doi.org/10.1123/apaq.17.3.310        [ Links ]

14.Dodd KJ, Shields NA. Systematic Review of the Outcomes of Cardiovascular Exercise Programs for People with Down Syndrome. Arch Phys Med Rehabil. 2005;86(10):2051-8. DOI: https://doi.org/10.1016/j.apmr.2005.06.003        [ Links ]

15.Colombo CM, Macedo RM, Fernandes-Silva MM, Caporal AM, Stinghen AE, Constantini CR, et al. Short-term effects of moderate intensity physical activity in patients with metabolic syndrome. Einstein. 2013;11(3):324-30. DOI: https://doi.org/10.1590/S1679-45082013000300011        [ Links ]

16.Mendes GF, Rodrigues GBA, Nogueira JAD, Meiners MMMA, Lins TCL, Dullius J. Evidências sobre efeitos da atividade física no controle glicêmico: importância da adesão a programas de atenção em diabetes. Rev Bras Ativ Fís Saúde. 2013;18(4):412-14. DOI: http://dx.doi.org/10.12820/rbafs.v.18n4p412        [ Links ]

17.Andriolo RB, El Dib RP, Ramos L, Atallah AN, Silva EM. Aerobic exercise training programmes for improving physical and psychosocial health in adults with Down syndrome. Cochrane Database Syst Rev. 2010;(5):CD005176. DOI: https://doi.org/10.1002/14651858.CD005176.pub4        [ Links ]

18.Millar AL, Fernhall B, Burkett LN. Effects of aerobic training in adolescents with Down Syndrome. Med Sci Sports Exerc. 1993;25(2):270-4.         [ Links ]

19.Rimmer JH, Heller T, Wang E, Valerio I. Improvements in Physical Fitness in Adults with Down Syndrome. Am J Ment Retard. 2004;109(2):165-74. DOI: https://doi.org/10.1016/j.amepre.2004.02.002        [ Links ]

20.Tsimaras VK, Fotiadou EG. Effect of training on the muscle strength and dynamic balance ability of adults with Down Syndrome. J Strength Cond Res. 2003;18(2):343-7. DOI: https://doi.org/10.1519/R-12832.1        [ Links ]

21.Varella AM, Sardinha LB, Pitetti KH. Effects of an Aerobic Rowing Training Regimen in Young Adults with Down Syndrome. Am J Ment Retard. 2001;106(2):135-44. DOI: https://doi.org/10.1352/0895-8017(2001)106<0135:EOAART>2.0.CO;2        [ Links ]

22.Carmeli E, Barchad S, Masharwi Y, Coleman R. Impact of a walking program in people with Down Syndrome. J Strength Cond Res. 2004;18(1):180-4. DOI: https://doi.org/10.1519/1533-4287(2004)018<0180:IOAWPI>2.0.CO;2        [ Links ]

23.Eberhard Y, Flore P, Enterradossi J, Foulon T, Groslambert P. Influence conjugue de conseils alimentaires et de l'activité physique d'endurance sur les lipoproteines plasmatiques de jeunes sujets trisomiques 21. Sci Sports. 1996;11(3):145-51. DOI: https://doi.org/10.1016/0765-1597(96)84026-3        [ Links ]

24.Asua DR, Parra P, Costa R, Moldenhauer F, Suarez C. Evaluation of the impact of abdominal obesity on glucose and lipid metabolism disorders in adults with Down Syndrome. Res Dev Disabil. 2014;35(11):2942-9. DOI: https://doi.org/10.1016/j.ridd.2014.07.038        [ Links ]

25.Draheim CC, Geijer JR, Dengel DR. Comparison of intima-media thickness of the carotid artery and cardiovascular disease risk factors in adults with versus without the Down Syndrome. Am J Cardiol. 2010;106(10):1512-16. DOI: https://doi.org/10.1016/j.amjcard.2010.06.079        [ Links ]

26.Dorner K, Gaethke AS, Tolksdorf M, Schumann KP, Gustmann H. Cholesterol fraction and triglycerides in children and adults with Down's Syndrome. Clin Chim Acta. 1984;142(3):307-11. DOI: https://doi.org/10.1016/0009-8981(84)90267-5        [ Links ]

27.Rimmer JH, Braddock D, Fujiura G. Blood lipid and percent body fat levels in Down Syndrome versus non-DS persons with mental retardation. Adapt Phys Activ Q. 1992;9:123-9. DOI: https://doi.org/10.1123/apaq.9.2.123        [ Links ]

28.Marín AS, Graupera JMX. Nutricional status of intelectual disabled person with Down Syndrome. Nutr J. 2011;26(5):1059-66.         [ Links ]

29.Wallen EF, Mullersdorf M, Christensson K, Malm G, Ekblom O, Marcus C. Hihg prevalence of cardio-metabolic risk factors among adolescentes with intelectual disability. Acta Pediatr. 2009;98(5):853-9. DOI: https://doi.org/10.1111/j.1651-2227.2008.01197.x        [ Links ]

30.Eberhard Y, Eterradossi J, Chug AM. Effort et trisomique s21: descriptif de quellques reponses metaboliques lors de l'activite physique. STAPS. 1990;23:57-65.         [ Links ]

31.Flore P, Bricout VA, van Biesen DB, Guinot M, Laporte F, Pépin JL, et al. Oxidative stress and metabolism at rest and during exercise in persons with Down Syndrome. Eur J Cardiovasc Prev Rehabil. 2008;15(1):35-42. DOI: https://doi.org/10.1097/HJR.0b013e3282f2bff3        [ Links ]

32.van Louw J, Vorstenbosch R, Vinck L, Penning C, Evenhuis H. Prevalence of hypertension in adults with intellectual disability in Netherlands. J Intellect Disabil Res. 2009;53(1):78-84. DOI: https://doi.org/10.1111/j.1365-2788.2008.01130.x        [ Links ]

33.Elmahgoub SM, Lambers S, Stegen S, van Laethem C, Cambier D, Calders P. The influence of combined exercise training on indices of obesity, physical fitness and lipid profile in overweight and obese adolescents with mental retardation. Eur J Paediatr. 2009;168(1):1327-33. DOI: https://doi.org/10.1007/s00431-009-0930-3        [ Links ]

34.Wuang Y, Su, CY. Patterns of participation and enjoyment in adolescents with Down syndrome. Res Dev Disabil. 2012;33(3):841-8. DOI: https://doi.org/10.1016/j.ridd.2011.12.008        [ Links ]

35.Valentino G, Acevedo M, Orellana L, Bustamante MJ, Kramer V, Adasme M, et al. Does good aerobic capacity attenuate the effects os aging on cardiovascular risk factors? Results from a cross-sectional study in a latino population. Int J Endocrinol. 2017;2017. DOI: https://doi.org/10.1155/2017/8351635        [ Links ]

36.Mazurek D, Wyka J. Down Syndrome-genetic and nutritional aspects of accompanying disordes. Rocz Panstw Zakl Hig. 2015;66(3):189-94.         [ Links ]

37.Abdallah AM, Raffa S, Alaidroos T, Obaid R, Abuznada J. Nutritional status of some children and adolescents with Down Syndrome in Jeddah. Life Sci J. 2013;10(3):1310-18.         [ Links ]

38.Smarkandy MM, Mohamed BA, AI-Hamdan AA. Nutricional assessment and obesity in Down Syndrome children and their siblings in Saudi Arabia. Saudi Med J. 2012;33(11):1216-21.         [ Links ]

39.Haghi AR, Solhjoo M, Tavakoli MH. Correlation between subclinical hypothyroidism and dyslipidemia. Iran J Pathol. 2017;12(2):106-11.         [ Links ]

40.Teixeira PFS, Reis FAA, Reuters VS, Almeida CP, Vaisman M. Hipotireoidismo subclínico e risco cardiovascular. Rev SOCERJ. 2004;17(1):50-7.         [ Links ]

41.Murray J, Ryan-Krause P. Obesity in children with Down syndrome: background and recommendations for management. Pediatr Nurs. 2010;36(6):314-19.         [ Links ]

42.Mann S, Beedie C, Jimenez A. Differential Effects of Aerobic Exercise, Resistance Training and Combined Exercise Modalities on Cholesterol and the Lipid Profile: Review, Synthesis and Recommendations. Sports Med. 2014;44(2):211-21. DOI: https://doi.org/10.1007/s40279-013-0110-5        [ Links ]

43.Faludi AA, Izar MCO, Saraiva JFK, Chacra APM, Bianco HT, Afiune Neto A, et al. Atualização da diretriz Brasileira de dislipidemias e prevenção da aterosclerose: 2017. Arq Bras Cardiol 2017;109(2 Supl 1):1-76.         [ Links ]

44.Matute-Llorente A, González-Agüero A, Gómez-Cabello A, Vicente-Rodríguez G, Casajús JA. Physical activity and cardiorespiratory fitness in adolescents with Down Syndrome. Nutr Hosp. 2013;28(4):1151-5. DOI: https://doi.org/10.3305/nh.2013.28.4.6509        [ Links ]

45. Whitt-Glover MC, O'Neil KL, Stettler N. Physical activity patterns in children with and without Down Syndrome. Pediatr Rehabil. 2006;9(2):158-64. DOI: https://doi.org/10.1080/13638490500353202        [ Links ]

 

 

Correspondence:
eloisewalmeida@gmail.com

Manuscript received: September 2019
Manuscript accepted: January 2020
Version of record online: May 2020