Nutritional status and body fat distribution in children and adolescentes with Cystic Fibrosis

Célia Regina Moutinho de Miranda Chaves Ana Lúcia Pereira da Cunha Ana Carolina da Costa Roseli de Souza Santos da Costa Speranza Vieira Lacerda About the authors

Abstracts

O objetivo deste estudo é avaliar o estado nutricional e a distribuição da gordura corporal em crianças e adolescentes com fibrose cística. Foram realizadas avaliação da distribuição de gordura corporal por meio da absorciometria de duplo feixe de energia, do estado nutricional por estatura/idade e índice de massa corporal/idade e a ingestão dietética pelo recordatório alimentar de 24horas, em 56 pacientes com idade entre 8 e 18 anos. Aproximadamente 50% da amostra apresentou estado nutricional adequado. A maioria apresentou a ingestão calórica e de lipídios inadequadas. O IMC/I foi o indicador nutricional que melhor evidenciou o aumento do percentual de gordura do tronco, razão androide/ginecoide e razão gordura tronco/gordura total. Os pacientes com Insuficiência Pancreática e os eutróficos apresentaram razão mediana androide/ginecoide maior. O aumento da adiposidade abdominal foi evidenciado pela DXA. O IMC/I não identificou a diminuição da massa magra corporal, mas quando aumentado foi significativo para adiposidade abdominal. Pacientes com fibrose cística devem associar a avaliação antropométrica à composição corporal e à distribuição de gordura corporal para um diagnóstico mais precoce de desnutrição e fatores de risco cardiometabólico.

Fibrose cística; Adiposidade abdominal; Índice de massa corporal para idade


Objective

: assessing the nutritional status and body fat distribution in children and adolescents with cystic fibrosis.

Method

: Fifty-six (56) 8-18 year old patients were assessed for fat distribution by dual energy X-ray absorptiometry, for nutritional status by height/age, and for body mass index to age and dietary intake by 24-hour dietary recall.

Results

: Approximately 50% of the sample showed adequate nutritional status. Most of it showed inadequate caloric and lipid intake. BMI/age was the nutritional indicator that best showed the increased percentage of trunk fat, android/gynecoidratio and trunk fat/total fat ratio. Patients with Pancreatic Insufficiency and eutrophic individuals showed higher median android/gynecoidratio.

Conclusion

: Increased abdominal adiposity was evidenced by DXA. The BMI did not identify decreased lean body mass. However, when body mass was high, it was significant for abdominal adiposity. The anthropometric assessment of patients with cystic fibrosis should be associated with body composition and body fat distribution to obtain an earlier malnutrition and cardiometabolic risk factor diagnosis.

Cystic fibrosis; Abdominal adiposity; Body mass index according to age


Introduction

The inadequate nutritional status (NS) is cause for concern because it is associated with increased morbidity and mortality in patients with cystic fibrosis (CF)11. Stallings VA, Stark LJ, Robinson KA, Feranchak AP, Quinton H; Clinical Practice Guidelines on Growth and Nutrition Subcommittee; Ad Hoc Working Group. Evidence-Based Practice Recommendations for Nutrition-Related Management of Children and Adults with Cystic Fibrosis and Pancreatic Insufficiency: Results of a Systematic Review. J Am Diet Assoc2008; 108(5):832-839.. The body mass index (BMI), which is commonly used to diagnose NS, does not identify body fat composition or distribution. The Dual-energy X-ray absorptiometry (DXA) is considered to be the gold standard to assess body compartments22. Thomas SR, Kalkwarf HJ, Buckley DD, Heubi JE. Effective dose of dual energy X- ray absorptiometry scans in children as a function of age.J Clin Densitom 2005; 8(4):415-422..

Abdominal fat accumulation has been already found in young and adult CF patients even if they show significant total body fat reduction as well as low weight. It is attributed to factors such as chronic inflammation, cortico therapy, physical inactivity and relative growth hormone decrease or anabolic substances found in most of these patients33. Panagopoulou P, Fotoulaki M, Manolitsas A, Pavlitou-Tsiontsi E, Tsitouridis I, Nousia-Arvanitakis S. Adiponectin and body composition in cystic fibrosis. J Cystic Fibrosis 2008; 7(3):244-251..

Increased abdominal fat is associated with cardiovascular risk factors and with peripheral insulin resistance44. Fox CS, Massaro JM, Hoffmann U, Pou KM, Maurovich-Horvat P, Liu CY, Vasan RS, Murabito JM, Meigs JB, Cupples LA, D’Agostino RB Sr, O’Donnell CJ. Abdominal Visceral and Subcutaneous Adipose Tissue Compartments: association with metabolic risk factors in the Fremingham Heart Study.Circulation 2007; 116(1):39-48.. In addition, it contributes to the development of hepatic steatosis and is negatively related to bone demineralization, which increases in the adolescence of FC patients55. Wree A, Kahraman A, Gerken G, Canbay A. Obesity Affects the liver - the link between adipocytes and hepatocytes. Digestion 2011; 83(1-2):124-133.,66. Van der Sluis IM, de Ridder MA, Boot AM, Krenning EP, Muinck Keizer-Schrama SM. Reference data for bone density and body composition measured with dual energy x ray absorptiometry in white children and young adults.Arch Dis Child 2002; 87(4):341-347..

Although abdominal adiposity is a relevant issue, there are few studies on the body fat distribution in these patients and, so far, there is no national publication on this topic. In addition, there are no studies using DXA to assess body composition in CF children and adolescents.

The disease incidence in Brazil is 1/10,000 live births77. Santos GPC, Domingos MT, Witting EO, Riedi CA, Rosario NA. Programa de triagem neonatal para fibrose cística no estado do Paraná: avaliação após 30 meses de sua implantação. J Pediatr (Rio J) 2005; 81(3):240-244.. It indicates that 1:20 inhabitants carries the CF gene88. Ludwig Neto N. Fibrose Cística Enfoque Multidisciplinar. 2ª ed. Florianópolis: Secretaria de Estado da Saúde de Santa Catarina; 2009. Disponível em: http://acam.org.br/livro-fibrose-cistica-enfoque-multidisciplinar
http://acam.org.br/livro-fibrose-cistica...
. The 1/690299. Cabello GMK. Avanços da Genética na Fibrose Cística. Rev Hospital Universitário Pedro Ernesto 2011; 10(4):36-45. incidence was estimated in Rio de Janeiro. According to the last Brazilian Cystic Fibrosis Register data1010. Filho LVRFS, Reis FJC, Damaceni N, Hira AY. Relatório Anual de Fibrose Cística. Registro Brasileiro de Fibrose Cística (REBRAFC). São Paulo: Grupo Brasileiro de Estudos de Fibrose Cística (GBEFC); 2010 [acessado 2015 abr 5]. Disponível em: http://www.gbefc.org.br/gbefc/estudo_gbefc_2010.pdf
http://www.gbefc.org.br/gbefc/estudo_gbe...
, approximately 80% of CF patients in Brazil are under 18 years old.

In light of the foregoing and by taking under consideration that these patients survival rate ranges from 30 to 50 years, the current study aims to evaluate the NS and the body fat distribution using DXA in order to highlight the presence of cardiometabolic risks in CF children and adolescents.

Methods

This is a retrospective cross-sectional census-type study conducted at Instituto Nacional da Saúde da Mulher, da Criança e do Adolescente Fernandes Figueira. The Institute is an organ of Fundação Oswaldo Cruz, IFF/Fiocruz, and a CF Reference Center in Rio de Janeiro. The study was conducted in all patients, aged between 8 and 18 years and diagnosed with CF. Pregnant adolescents as well as obese children and adolescents were excluded from the study.

Sixty (60) out of the 120 patients enrolled in the service were initially eligible. They were aged between 8 and 18 years. Four of them were excluded because they had not been subjected to DXA examination during the data collection period (from January 2010 to December 2013). This universe represents74.5% of the CF registered patients in Rio de Janeiro, according to data provided by the last Brazilian Cystic Fibrosis Register/REBRAFC, 20121010. Filho LVRFS, Reis FJC, Damaceni N, Hira AY. Relatório Anual de Fibrose Cística. Registro Brasileiro de Fibrose Cística (REBRAFC). São Paulo: Grupo Brasileiro de Estudos de Fibrose Cística (GBEFC); 2010 [acessado 2015 abr 5]. Disponível em: http://www.gbefc.org.br/gbefc/estudo_gbefc_2010.pdf
http://www.gbefc.org.br/gbefc/estudo_gbe...
.

The nutritional status evaluation used anthropometric indices such as BMI/A and height according to age (H/A), which were analyzed according to the growth curves by the World Health Organization (WHO) and classified according to the Nutrition Consensus for CF Pediatric Patients1111. Borowitz D, Baker RD, Stallings V. Consensus report on nutrition for pediatric patients with cystic fibrosis. J Pediatr Gastroenterol Nutr 2002; 35(3):246-259..

The body fat distribution was assessed by DXA using the Lunar enCORE software -2011, version 13.6, with GE densitometer, Lunar iDEXA Promodel. Children and adolescents were instructed to wear light clothes and to remove all metal objects. The measurements were done after the patients were placed in supine position and remained motionless on the scanning bed. After the full body scan, the software provided estimates on fat mass, bone mass and lean mass in the entire body and in specific areas (torso, gynecoid, android, and upper and lower limbs). The android region was measured in the area around the waist, between the midpoint of the lumbar spine and the top of the pelvis. The gynecoid area was measured approximately between the femoral head and the mid-thigh. The software demarcated and separated the limbs from the torso and from the head by standard lines generated by the equipment itself; these lines were adjusted according to specific anatomical points determined by the manufacturer1212. US Department of Health and Human Services, Center for Disease Control and prevention (CDC), Hyattsville, MD. The National Health and Nutrition Examination Survey (NHANES) Dual Energy X-Ray Absorptiometry – Android/Gynoid Measurements (DXXAG_C). [acessado 2014 jun 1]. Disponível em: http://www.cdc.gov/nchs/nhanes/nhanes2003-2004/DXXAG_C.htm#Analytic_Notes
http://www.cdc.gov/nchs/nhanes/nhanes200...
. The body fat percentage (BF %) was calculated by dividing the total body mass by the total body fat, multiplying the result by 100. Based on the image diagnosis, the body fat percentage and torso fat percentage results were analyzed according to the age and gender of all races and ethnicities, following the National Health and Nutrition Examination Survey criteria1313. Borrud LG, Flegal KM, Looker AC, Everhart JE, Harris TB, Shepherd JA. Body composition data for individuals 8 years of age and older: U.S. population, 1999-2004. National Center for Health Statistics. Vital Health Stat 2010; 11(250):1-87.. The image diagnosis provided by DXA allowed investigating the mean fat percentage, the torso fat mass/total fat mass ratio and the android/gynecoid fat ratio.

The 24-hour recall method was used to assess the patients’ usual dietary intake. The method was applied in three non-consecutive days, with maximum interval of three months, and the data were obtained by means of visual aids and photos of utensils (Household Budget Survey)1414. Barbosa KB, de Lima Rosado LE, Franceschini SC, Priore SE. Instrumentos de inquérito dietético utilizados na avaliação do consumo alimentar em adolescentes: comparação entre métodos. Arch Latinoam Nutr2007; 57(1):43-50..

The NutWin® software, version 1.5 (2002) was used to calculate the total energy value (TEV), the saturated fat, and the polyunsaturated fat means, by double entry. Trans fat was calculated using data on fresh and processed foods obtained from the food composition tables of the United States Department of Agriculture (USDA) and from the Brazilian Table of Food Composition (TACO - Tabela Brasileira de Composição dos Alimentos)1515. United States Department of Agriculture (USDA). Food and nutrition information center, 1997. [acessado 2012 jun 12]. Disponível em: http://www.nal.usda.gov/fnic/foodcomp/data/
http://www.nal.usda.gov/fnic/foodcomp/da...
,1616. Núcleo de estudos e pesquisas em alimentação, Universidade de Campinas (NEPA/Unicamp). Tabela Brasileira de Composição de Alimentos (TACO). 4ª ed. revisada e ampliada. Campinas: NEPA, UNICAMP; 2011. 161p. [acessado 2012 maio 10]. Disponível em: http://www.unicamp.br/nepa/taco/
http://www.unicamp.br/nepa/taco/...
. The data on the composition of industrial foods and of calorie and protein supplements was collected on the product labels and/or from the manufacturers. The reference standards for energy intake, according to age and gender, were from Food and Agriculture Organization/World Health Organization1717. World Health Organization (WHO), Food and Agriculture Organization (FAO). Human Energy Requirements. Report of a Joint FAO/WHO/UNU Expert Consultation. [Technical Report Series 1]. Rome: FAO; 2004. [acessado 2010 out 15]. Disponível em: http://nla.gov.au/nla.cat-vn3537790
http://nla.gov.au/nla.cat-vn3537790...
.

The macronutrient intake taken under consideration was 15-20% for protein, 40-50% for carbohydrates, and 35-40% for lipids. The energy adequacy percentage was > 150% of the recommendations, according to the Nutrition Consensus88. Ludwig Neto N. Fibrose Cística Enfoque Multidisciplinar. 2ª ed. Florianópolis: Secretaria de Estado da Saúde de Santa Catarina; 2009. Disponível em: http://acam.org.br/livro-fibrose-cistica-enfoque-multidisciplinar
http://acam.org.br/livro-fibrose-cistica...
. The intake percentage of total polyunsaturated fatty acids (PUFA), saturated fatty acids (SFA), and trans fat in comparison to TEV was evaluated according to the WHO1818. World Health Organization (WHO), Food and Agriculture Organization (FAO). Interim summary of conclusions and dietary recommendations on total fat & fatty acids. From the Joint FAO/WHO Expert Consultation on Fats and Fatty Acids in Human Nutrition, November 10-14, 2008. Geneva: WHO; 2008. [acessado 2013 abr 20]. Disponível em: http://www.fao.org/ag/agn/nutrition/docs/Fats and Fatty Acids Summaryfin.pdf
http://www.fao.org/ag/agn/nutrition/docs...
.

Statistical Analysis

The means and standard deviations of the continuous variables were presented in the descriptive analysis with normal distribution and in median, minimum and maximum values for those without normal distribution. Normality was verified using the Kolmogorov-Smirnov test. Categorical variables were described by absolute and percentage frequencies. Pearson chi-square tests and Fisher’s exact test were used to measure the association among categorical variables, in cases in which at least one expected frequency lower than five was observed. When the normality assumption was confirmed, Student’s t test and variance analysis (ANOVA) were used to compare the continuous measurements between two and among three (or more) groups, respectively. When normality was not confirmed, the Mann-Whitney and the Kruskal-Wallis tests were used in variables with two and with three or more categories, respectively. Pearson and Spearman correlation tests were used in variables with and without normal distribution, respectively, to measure the degree of association between continuous variables. Univariate regression models containing each of the independent variables were evaluated to identify possible associations between the explanatory variables and the outcomes. All significant variables at 20% level in the univariate analysis were considered to be possible predictors in the multiple regression. Statistical tests were performed at 5% significance level. The analyses were conducted in SPSS software, version 20 (SPSS Corporation, 2011) and in R software, version 3.0.

The current study was approved by the Research Ethics Committee of at Instituto Nacional da Saúde da Mulher, da Criança e do Adolescente Fernandes Figueira/Fiocruz.

Results

Fifty-six (56) patients with mean age of 12.2 (± 2.5) years were studied. Most were women and showed exogenous pancreatic insufficiency (EPI). Approximately 50% of the cases had at least one allele for the F508 mutation The nutritional status was considered to be acceptable at 50% (BMI/A) and at 83% (H/A) (Table 1).

Table 1
Demographic, clinical and nutritional features of children and adolescents with Cystic Fibrosis, 2010-2013 (IFF/Fiocruz - RJ) (n = 56).

Energy and lipid intake was considered inadequate in more than 80.0% of the studied population. The consumption of saturated and trans fat met the recommendations for most patients.

Adolescents aged 16-19 years showed the highest percentage of torso fat and those aged 12-15 years showed the highest percentage of total fat (Table 1). BMI/A was the only statistically significant variable in the bivariate analysis of the torso fat percentage evaluation.

Regarding the bivariate analysis of the total fat percentage and of the torso fat percentage, no statistically significant result (p < 0.05) was found in any studied variable.

The results from the bivariate analysis of android/gynecoid fat ratio demonstrated that the pancreatic function and the BMI/A variables were statistically significant (p < 0.05) (Table 2).

Table 2
Bivariate analysis of the android/gynecoid fat ratio using the variables of interest in children and adolescents with cystic fibrosis, 2010-2013(IFF/Fiocruz-RJ) (n = 56).

The bivariate analysis of the torso fat/ total fat ratio showed that the age, BMI/A and TEV variables were statistically significant (p < 0.05). It was observed that older patients with improved nutritional status showed higher torso fat/total fat ratio. Patients with inadequate TEV (< 150%) showed higher meant or so fat/total fat ratio (0.36 ± 0.06) (Table 3).

Table 3
Bivariate analysis of the torso fat/total fat ratio using the variables of interest in children and adolescents with cystic fibrosis, 2010-2013 (IFF/Fiocruz) (n = 56).

Age and nutritional status (BMI/A) were statistically significant variables (p < 0.05) in the multiple regression analysis of the torso fat/ total fat ratio of children and adolescents with CF, (Table 4). The multiple regression analysis of the android/gynecoid fat ratio found that the BMI/A and the carbohydrate intake were statistically significant variables (p < 0.05) (Table 5).

Table 4
Multiple linear regression analysis of the torso fat/total fat ratio in children and adolescents with cystic fibrosis, 2010-2013(IFF/Fiocruz-RJ) (n = 56).

Table 5
Multiple linear regression analysis of the android/gynecoid fat ratio logarithm in children and adolescents with cystic fibrosis, 2010-2013 (IFF/Fiocruz – RJ) (n = 56).

Discussion

The current study found that only 50% of the patients showed adequate nutritional status (BMI/A > p 25). This result is relevant because the peripuberal period is one of the most important stages in the disease’s treatment1111. Borowitz D, Baker RD, Stallings V. Consensus report on nutrition for pediatric patients with cystic fibrosis. J Pediatr Gastroenterol Nutr 2002; 35(3):246-259.. Patients followed up in reference centers in the United States are closer or above the 50th percentile for the BMI/A indicator, which is the current nutritional treatment goal due to the strong association between nutritional status and lung function11. Stallings VA, Stark LJ, Robinson KA, Feranchak AP, Quinton H; Clinical Practice Guidelines on Growth and Nutrition Subcommittee; Ad Hoc Working Group. Evidence-Based Practice Recommendations for Nutrition-Related Management of Children and Adults with Cystic Fibrosis and Pancreatic Insufficiency: Results of a Systematic Review. J Am Diet Assoc2008; 108(5):832-839..

It was observed that approximately 50% of the patients had at least one allele for the F508 mutation. This result corroborates the last Brazilian Cystic Fibrosis Register (REBRAFC, 2012)1010. Filho LVRFS, Reis FJC, Damaceni N, Hira AY. Relatório Anual de Fibrose Cística. Registro Brasileiro de Fibrose Cística (REBRAFC). São Paulo: Grupo Brasileiro de Estudos de Fibrose Cística (GBEFC); 2010 [acessado 2015 abr 5]. Disponível em: http://www.gbefc.org.br/gbefc/estudo_gbefc_2010.pdf
http://www.gbefc.org.br/gbefc/estudo_gbe...
. This mutation is the most frequent one and it has more severephenotype1919. O’Sullivan BP, Freedman SD. Cystic Fibrosis.Lancet 2009; 373(9678):1891-1904.. Thus, patients with this mutation show greater chance of malnutrition2020. Cystic Fibrosis Trust Nutrition Working Group. Nutritional Management of Cystic Fibrosis. London: Cystic Fibrosis Trust; 2002.. This fact may explain the percentage of under nourished patients found in the current study.

A relevant aspect found in the current study was the fact that most patients (83.9%) had no short height, which shows good linear growth. Another study also found similar results2121. Simon MISS, Drehmer M, Menna-Barreto SS. Associação entre o estado nutricional e a ingestão dietética em pacientes com fibrose cística. J Bras Pneumol 2009; 35(10):966-972.. It is worth highlighting that short height affects survival, since it influences lung growth and development. Thus, it is considered to be an important and independent risk factor for mortality in CF patients, because it requires nutritional rehabilitation, which is usually long, invasive and expensive2222. Vieni G, Faraci S, Collura M, Lombardo M, Traverso G, Cristadoro S, Termini L, Lucanto MC, Furnari ML, Trimarchi G, Triglia MR, Costa S, Pellegrino S, Magazzù G. Stunting is an independent predictor of mortality in patients with cystic fibrosis. Clin Nutr 2013; 32(3):382-385..

As for the body composition, there was 48% decrease and 9% increase in total body fat percentage. Although the current study did not investigate the lean body mass, one can infer that it was quite impaired. Since patients with inadequate BMI showed normal body fat percentage, it means that they had lean mass depletion. It happens because once BMI does not identify body compartments, it is unable to track subtle changes in the body composition2323. Bolton CE, Ionescu AA, Evans WD, Pettit RJ, Shale DJ. Altered tissue distribution in adults with cystic fibrosis. Thorax2003; 58(10):885-889..

The current study found that most of the studied sample ingested less than 150% of the recommended energy intake, showing little adhesion to the nutritional treatment or anorexia, which is commonly found in these patients. This result meets the research conducted by Schall et al. who observed that only 28% of the sample ingested the recommended minimum energy intake2424. Schall JI, Bentley T, Stallings VA. Meal patterns, dietary fat intake and pancreatic enzyme use in preadolescent children with cystic fibrosis.J Pediatr Gastroenterol Nutr 2006; 43(5):651-659..

Regarding lipids, 89% of the studied population ingested less than the recommended amount. These results were also found in other studies2121. Simon MISS, Drehmer M, Menna-Barreto SS. Associação entre o estado nutricional e a ingestão dietética em pacientes com fibrose cística. J Bras Pneumol 2009; 35(10):966-972.,2424. Schall JI, Bentley T, Stallings VA. Meal patterns, dietary fat intake and pancreatic enzyme use in preadolescent children with cystic fibrosis.J Pediatr Gastroenterol Nutr 2006; 43(5):651-659.. These data demonstrate that despite the nutritional counseling received in the Reference Center, CF patients showed difficulty in achieving the recommendations. This is concerning because according to a classic study on the differences in mean survival and growth parameters of patients from two major CF Reference Centers (Boston and Toronto), those with more adequate NS showed greater nutritional intake of lipids2525. Corey M, McLaughlin F J, Williams M, H Levison. A comparison of survival, growth, and pulmonary function in patients with cystic fibrosis in Boston and Toronto. J Clin Epidemiol 1988; 41(6):583-591..

It is worth emphasizing that lipids are the main source of energy in food and that they have important metabolic functions. In addition, CF shows deficiency and imbalance of essential fatty acids (EFA)2626. Calder PC. Fatty acids and inflammation: The cutting edge between food and pharma. Eur J Pharmacol 2011; 668(Supl. 1):S50-S58.,2727. Strandvik B. Fatty acid metabolism in cystic fibrosis.Prostaglandins Leukot Essent Fatty Acids 2010; 83(3): 121-129..

The analysis of the trans fatty acid intake (trans FA) percentage was adequate (< 1% TEV), according to the WHO/FAO (2008) recommendations for the prevention of chronic diseases in most patients1818. World Health Organization (WHO), Food and Agriculture Organization (FAO). Interim summary of conclusions and dietary recommendations on total fat & fatty acids. From the Joint FAO/WHO Expert Consultation on Fats and Fatty Acids in Human Nutrition, November 10-14, 2008. Geneva: WHO; 2008. [acessado 2013 abr 20]. Disponível em: http://www.fao.org/ag/agn/nutrition/docs/Fats and Fatty Acids Summaryfin.pdf
http://www.fao.org/ag/agn/nutrition/docs...
. It is relevant because the high trans fatty acids consumption associated with low EFA intake is harmful due to enzymes competition in the enzymatic cascade for long-chain metabolites biosynthesis2828. Innis SM. Fatty acids and early human development. Early Hum Dev 2007; 83(12):761-766.. The low trans-fat consumption in the studied sample may result from instructions received in consultations with the dietician or from the reduction of this fat in processed foods, as established by the Ministry of Health in 2006.

The saturated fatty acids (SFA) intake percentage was also adequate in most of the studied patients. This result differs from that found by Smith et al.2929. Smith C, Winn A, Seddon P, Ranganathan S. A fat lot of good: balance and trends in fat intake in children with cystic fibrosis. J Cyst Fibros 2012; 11(2):154-157. who reported high SFA intake among CF children. It is important because the systemic inflammatory reaction is a risk factor for a thermogenesis and once associated with high SFA intake it increases the risk of cardiovascular diseases2828. Innis SM. Fatty acids and early human development. Early Hum Dev 2007; 83(12):761-766.,3030. World Health Organization (WHO). World Health Organization. Diet, nutrition and the prevention of chronic diseases. In: WHO. Report of a Joint WHO/FAO Expert Consultation. Geneva: WHO; 2003. p. 23-25; 56 (WHO Technical Report Series, 916)..

The carbohydrate intake was statistically significant in the torso fat percentage, possibly because although most patients have consumed normal carbohydrate percentages, this consumption might have been based on simple carbohydrates. The software used to assess food intake (Nutwin) does not separate simple from complex carbohydrates.

Approximately 9% of the studied sample showed increased torso fat, and it was higher in older and male patients. It possibly occurred because central obesity tends to increase due to aging – it begins in childhood and in adolescence and continues in adulthood – and due to the male gender tendency to accumulate fat in this region3131. Taylor RW, Jones IA, Williams SM, Goulding A. Evaluation of waist circumference, waist to-hip ratio, and the conicity index as screening tools for high trunk fat mass, as measured by dual-energy X-ray absorptiometry, in children aged 3-19y. Am J Clin Nutr 2000; 72(2):490-495.. Therefore, the patients in the current study were stratified by different age groups between genders, based on the differentiation of the sexual maturation process in which important changes in fat and lean mass compartments differently occur.

Since these patients already show survival rate ranging from 30 to 50 years and since there is ample evidence that risk factors that begin in childhood and adolescence are perpetuated into adulthood, the current result is concerning because increased torso fat leads to increased abdominal and visceral fat and this is a predictor of increased risk of cardiometabolic diseases. The endocrinal and inflammatory function of the fat tissue located in the abdominal cavity causes increased secretion of pro-inflammatory and atherogenic adipokines, free fatty acids and inflammatory markers. It also causes circulating adiponectin decrease, which in turn seems to lead to dyslipidemia, insulin resistance and vascular inflammation3232. Trayhurn P, Wood IS. Adipokines: inflammation and the pleiotropic role of white adipose tissue. Br J Nutr 2007; 92(3):347..

The produced pro inflammatory adipokines are also negatively related to bone demineralization and hepatic steatosis, which occur in CF patients55. Wree A, Kahraman A, Gerken G, Canbay A. Obesity Affects the liver - the link between adipocytes and hepatocytes. Digestion 2011; 83(1-2):124-133.,66. Van der Sluis IM, de Ridder MA, Boot AM, Krenning EP, Muinck Keizer-Schrama SM. Reference data for bone density and body composition measured with dual energy x ray absorptiometry in white children and young adults.Arch Dis Child 2002; 87(4):341-347.. Since applying biomarkers to establish the overall risk and performing early diagnosis to prevent cardiovascular events are still a challenge, metabolic changes may be early identified in central obesity patients using DXA3333. Oliveira JL, Lopes LL, Pelúzio MCG, Hermsdorff HHM. Fenótipo Cintur Hipertrigliceridêmica e Risco Cardiometabólico em Indivíduos Dislipidêmicos.Rev Bras Cardiol 2014; 27(6):395-402.

Moriconi et al.3434. Moriconi N, Kraenzlin M, Muller B, Keller U, Nusbaumer CPG, Stöhr S, Tamm M, Puder JJ. Body composition and adiponectin serum concentrations in adult patients with cystic fibrosis. J Clinic Endocrinol Metab2006; 91(4):1586-1590 studied the evaluation of body fat composition and distribution in adult CF patients using DXA and also found increased abdominal fat even in patients with low weight.

The current study demonstrated that approximately 9% of the patients showed total body fat increase. This result may due to changes in living habits – which were seen in the general population – or to the use of high-calorie supplements, diet by gastrostomy and to enteral nutrition, because obesity is unusual in CF patients, since the disease is characterized by negative energy balance. The significant increase in the prevalence of overweight and obesity in many countries, including Brazil, turns obesity into a major public health issue affecting all age groups. Epidemiological evidence has demonstrated that the relation between obesity and the risk of cardiometabolic diseases is perceived both earlier in life and during the individuals’ growth and development3535. Barbosa Filho VC, Campos W, Lopes AS. Epidemiology of physical inactivity, sedentary behaviors, and unhealthy eating habits among Brazilians adolescents: a systematic review. Cien Saude Colet 2014; 19(1):173-193.

36. Magalhães VC, Mendonça GAS. Prevalência e fatores associados a sobrepeso e obesidade em adolescentes de 15 a 19 anos das regiões Nordeste e Sudeste do Brasil, 1996 a 1997. Cad Saude Publica 2003; 19(Supl. 1):129-139.
-3737. Malta DC, Sardinha LMV, Mendes I, Barreto SM, Giatti L, Castro IRR, Moura L, Dias AJR, Crespo C. Prevalência de fatores de risco e proteção de doenças crônicas não transmissíveis em adolescentes: resultados da Pesquisa Nacional de Saúde do Escolar (PeNSE), Brasil, 2009. Cien Saude Colet 2009; 15(Supl. 2):3009-3019..

The results in the current study showed that the BMI/A was statistically significant in torso fat percentage. Patients presenting poorer nutritional status showed the lowest torso fat accumulation, as it usually occurs in children and adolescents without CF. However, Panagopoulou et al.33. Panagopoulou P, Fotoulaki M, Manolitsas A, Pavlitou-Tsiontsi E, Tsitouridis I, Nousia-Arvanitakis S. Adiponectin and body composition in cystic fibrosis. J Cystic Fibrosis 2008; 7(3):244-251. found abdominal fat accumulation in young and adult CF patients, even in the presence of significant total body fat reduction. These authors suggested that the responsible factors are chronic inflammation, cortico therapy, physical inactivity, relative growth hormone decrease or anabolic substances. Other chronic inflammatory diseases also show increased abdominal fat distribution associated with chronic inflammatory condition, insulin resistance and cardiovascular risk.

There was higher android/gynecoid fat ratio in the presence of EPI. It may have happened because EPI is usually associated with worse phenotype, which is probably associated with chronic inflammation that may cause abdominal fat accumulation. This increased ratio in adolescents and adults accounts for the higher risk of metabolic and cardiovascular complications.

A limitation of the current study lies on the fact that, since it is across-sectional analysis, it points only to associations, without establishing a cause-effect relationship. In addition, the disease severity varies in these patients, thus making the population more heterogeneous. The lack of cut-off point for the android-gynecoid ratio and for the total torso ratio in the DXA also hinders the data analysis.

Conclusion

Although 50% of the cases showed nutritional status adequacy by BMI/A, this percentage would be lower if the lean body mass had been assessed. Most patients presented an inappropriate energy and lipids consumption, thus showing little adherence to the nutritional treatment. However, it was observed adherence to the contemporary society diet with exaggerated carbohydrate intake.

Increased abdominal adiposity was evidenced by the DXA. It is a fast and easy examination, which exposes individuals to small radiation doses. Thus, the body composition and the body fat distribution of CF patients should be evaluated during their nutritional follow-up in order to early diagnose malnutrition and cardiometabolic risk factors.

References

  • 1
    Stallings VA, Stark LJ, Robinson KA, Feranchak AP, Quinton H; Clinical Practice Guidelines on Growth and Nutrition Subcommittee; Ad Hoc Working Group. Evidence-Based Practice Recommendations for Nutrition-Related Management of Children and Adults with Cystic Fibrosis and Pancreatic Insufficiency: Results of a Systematic Review. J Am Diet Assoc2008; 108(5):832-839.
  • 2
    Thomas SR, Kalkwarf HJ, Buckley DD, Heubi JE. Effective dose of dual energy X- ray absorptiometry scans in children as a function of age.J Clin Densitom 2005; 8(4):415-422.
  • 3
    Panagopoulou P, Fotoulaki M, Manolitsas A, Pavlitou-Tsiontsi E, Tsitouridis I, Nousia-Arvanitakis S. Adiponectin and body composition in cystic fibrosis. J Cystic Fibrosis 2008; 7(3):244-251.
  • 4
    Fox CS, Massaro JM, Hoffmann U, Pou KM, Maurovich-Horvat P, Liu CY, Vasan RS, Murabito JM, Meigs JB, Cupples LA, D’Agostino RB Sr, O’Donnell CJ. Abdominal Visceral and Subcutaneous Adipose Tissue Compartments: association with metabolic risk factors in the Fremingham Heart Study.Circulation 2007; 116(1):39-48.
  • 5
    Wree A, Kahraman A, Gerken G, Canbay A. Obesity Affects the liver - the link between adipocytes and hepatocytes. Digestion 2011; 83(1-2):124-133.
  • 6
    Van der Sluis IM, de Ridder MA, Boot AM, Krenning EP, Muinck Keizer-Schrama SM. Reference data for bone density and body composition measured with dual energy x ray absorptiometry in white children and young adults.Arch Dis Child 2002; 87(4):341-347.
  • 7
    Santos GPC, Domingos MT, Witting EO, Riedi CA, Rosario NA. Programa de triagem neonatal para fibrose cística no estado do Paraná: avaliação após 30 meses de sua implantação. J Pediatr (Rio J) 2005; 81(3):240-244.
  • 8
    Ludwig Neto N. Fibrose Cística Enfoque Multidisciplinar. 2ª ed. Florianópolis: Secretaria de Estado da Saúde de Santa Catarina; 2009. Disponível em: http://acam.org.br/livro-fibrose-cistica-enfoque-multidisciplinar
    » http://acam.org.br/livro-fibrose-cistica-enfoque-multidisciplinar
  • 9
    Cabello GMK. Avanços da Genética na Fibrose Cística. Rev Hospital Universitário Pedro Ernesto 2011; 10(4):36-45.
  • 10
    Filho LVRFS, Reis FJC, Damaceni N, Hira AY. Relatório Anual de Fibrose Cística. Registro Brasileiro de Fibrose Cística (REBRAFC) São Paulo: Grupo Brasileiro de Estudos de Fibrose Cística (GBEFC); 2010 [acessado 2015 abr 5]. Disponível em: http://www.gbefc.org.br/gbefc/estudo_gbefc_2010.pdf
    » http://www.gbefc.org.br/gbefc/estudo_gbefc_2010.pdf
  • 11
    Borowitz D, Baker RD, Stallings V. Consensus report on nutrition for pediatric patients with cystic fibrosis. J Pediatr Gastroenterol Nutr 2002; 35(3):246-259.
  • 12
    US Department of Health and Human Services, Center for Disease Control and prevention (CDC), Hyattsville, MD. The National Health and Nutrition Examination Survey (NHANES) Dual Energy X-Ray Absorptiometry – Android/Gynoid Measurements (DXXAG_C). [acessado 2014 jun 1]. Disponível em: http://www.cdc.gov/nchs/nhanes/nhanes2003-2004/DXXAG_C.htm#Analytic_Notes
    » http://www.cdc.gov/nchs/nhanes/nhanes2003-2004/DXXAG_C.htm#Analytic_Notes
  • 13
    Borrud LG, Flegal KM, Looker AC, Everhart JE, Harris TB, Shepherd JA. Body composition data for individuals 8 years of age and older: U.S. population, 1999-2004. National Center for Health Statistics. Vital Health Stat 2010; 11(250):1-87.
  • 14
    Barbosa KB, de Lima Rosado LE, Franceschini SC, Priore SE. Instrumentos de inquérito dietético utilizados na avaliação do consumo alimentar em adolescentes: comparação entre métodos. Arch Latinoam Nutr2007; 57(1):43-50.
  • 15
    United States Department of Agriculture (USDA). Food and nutrition information center, 1997. [acessado 2012 jun 12]. Disponível em: http://www.nal.usda.gov/fnic/foodcomp/data/
    » http://www.nal.usda.gov/fnic/foodcomp/data/
  • 16
    Núcleo de estudos e pesquisas em alimentação, Universidade de Campinas (NEPA/Unicamp). Tabela Brasileira de Composição de Alimentos (TACO). 4ª ed. revisada e ampliada. Campinas: NEPA, UNICAMP; 2011. 161p. [acessado 2012 maio 10]. Disponível em: http://www.unicamp.br/nepa/taco/
    » http://www.unicamp.br/nepa/taco/
  • 17
    World Health Organization (WHO), Food and Agriculture Organization (FAO). Human Energy Requirements. Report of a Joint FAO/WHO/UNU Expert Consultation [Technical Report Series 1]. Rome: FAO; 2004. [acessado 2010 out 15]. Disponível em: http://nla.gov.au/nla.cat-vn3537790
    » http://nla.gov.au/nla.cat-vn3537790
  • 18
    World Health Organization (WHO), Food and Agriculture Organization (FAO). Interim summary of conclusions and dietary recommendations on total fat & fatty acids From the Joint FAO/WHO Expert Consultation on Fats and Fatty Acids in Human Nutrition, November 10-14, 2008. Geneva: WHO; 2008. [acessado 2013 abr 20]. Disponível em: http://www.fao.org/ag/agn/nutrition/docs/Fats and Fatty Acids Summaryfin.pdf
    » http://www.fao.org/ag/agn/nutrition/docs/Fats and Fatty Acids Summaryfin.pdf
  • 19
    O’Sullivan BP, Freedman SD. Cystic Fibrosis.Lancet 2009; 373(9678):1891-1904.
  • 20
    Cystic Fibrosis Trust Nutrition Working Group. Nutritional Management of Cystic Fibrosis London: Cystic Fibrosis Trust; 2002.
  • 21
    Simon MISS, Drehmer M, Menna-Barreto SS. Associação entre o estado nutricional e a ingestão dietética em pacientes com fibrose cística. J Bras Pneumol 2009; 35(10):966-972.
  • 22
    Vieni G, Faraci S, Collura M, Lombardo M, Traverso G, Cristadoro S, Termini L, Lucanto MC, Furnari ML, Trimarchi G, Triglia MR, Costa S, Pellegrino S, Magazzù G. Stunting is an independent predictor of mortality in patients with cystic fibrosis. Clin Nutr 2013; 32(3):382-385.
  • 23
    Bolton CE, Ionescu AA, Evans WD, Pettit RJ, Shale DJ. Altered tissue distribution in adults with cystic fibrosis. Thorax2003; 58(10):885-889.
  • 24
    Schall JI, Bentley T, Stallings VA. Meal patterns, dietary fat intake and pancreatic enzyme use in preadolescent children with cystic fibrosis.J Pediatr Gastroenterol Nutr 2006; 43(5):651-659.
  • 25
    Corey M, McLaughlin F J, Williams M, H Levison. A comparison of survival, growth, and pulmonary function in patients with cystic fibrosis in Boston and Toronto. J Clin Epidemiol 1988; 41(6):583-591.
  • 26
    Calder PC. Fatty acids and inflammation: The cutting edge between food and pharma. Eur J Pharmacol 2011; 668(Supl. 1):S50-S58.
  • 27
    Strandvik B. Fatty acid metabolism in cystic fibrosis.Prostaglandins Leukot Essent Fatty Acids 2010; 83(3): 121-129.
  • 28
    Innis SM. Fatty acids and early human development. Early Hum Dev 2007; 83(12):761-766.
  • 29
    Smith C, Winn A, Seddon P, Ranganathan S. A fat lot of good: balance and trends in fat intake in children with cystic fibrosis. J Cyst Fibros 2012; 11(2):154-157.
  • 30
    World Health Organization (WHO). World Health Organization. Diet, nutrition and the prevention of chronic diseases. In: WHO. Report of a Joint WHO/FAO Expert Consultation Geneva: WHO; 2003. p. 23-25; 56 (WHO Technical Report Series, 916).
  • 31
    Taylor RW, Jones IA, Williams SM, Goulding A. Evaluation of waist circumference, waist to-hip ratio, and the conicity index as screening tools for high trunk fat mass, as measured by dual-energy X-ray absorptiometry, in children aged 3-19y. Am J Clin Nutr 2000; 72(2):490-495.
  • 32
    Trayhurn P, Wood IS. Adipokines: inflammation and the pleiotropic role of white adipose tissue. Br J Nutr 2007; 92(3):347.
  • 33
    Oliveira JL, Lopes LL, Pelúzio MCG, Hermsdorff HHM. Fenótipo Cintur Hipertrigliceridêmica e Risco Cardiometabólico em Indivíduos Dislipidêmicos.Rev Bras Cardiol 2014; 27(6):395-402
  • 34
    Moriconi N, Kraenzlin M, Muller B, Keller U, Nusbaumer CPG, Stöhr S, Tamm M, Puder JJ. Body composition and adiponectin serum concentrations in adult patients with cystic fibrosis. J Clinic Endocrinol Metab2006; 91(4):1586-1590
  • 35
    Barbosa Filho VC, Campos W, Lopes AS. Epidemiology of physical inactivity, sedentary behaviors, and unhealthy eating habits among Brazilians adolescents: a systematic review. Cien Saude Colet 2014; 19(1):173-193.
  • 36
    Magalhães VC, Mendonça GAS. Prevalência e fatores associados a sobrepeso e obesidade em adolescentes de 15 a 19 anos das regiões Nordeste e Sudeste do Brasil, 1996 a 1997. Cad Saude Publica 2003; 19(Supl. 1):129-139.
  • 37
    Malta DC, Sardinha LMV, Mendes I, Barreto SM, Giatti L, Castro IRR, Moura L, Dias AJR, Crespo C. Prevalência de fatores de risco e proteção de doenças crônicas não transmissíveis em adolescentes: resultados da Pesquisa Nacional de Saúde do Escolar (PeNSE), Brasil, 2009. Cien Saude Colet 2009; 15(Supl. 2):3009-3019.

Publication Dates

  • Publication in this collection
    Nov 2015

History

  • Received
    03 Dec 2014
  • Reviewed
    28 May 2015
  • Accepted
    30 May 2015
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