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Assessment of growth and nutrition
Best Practice & Research Clinical Gastroenterology Vol. 17, No. 2, pp. 153–162, 2003 doi:10.1053/ybega.2003.363, www.elsevier.com/locate/jnlabr/ybega
2 Assessment of growth and nutrition Ranjana Gokhale*
MD
Assistant Professor of Clinical Pediatrics
Barbara S. Kirschner
MD
Professor of Pediatrics and Medicine Section of Pediatric Gastroenterology and Nutrition, The University of Chicago Children’s Hospital, 5839 S. Maryland Avenue, MC 4065, Chicago, IL 60637, USA
Growth is a dynamic process that is characterized by physiological changes in an individual from infancy into adulthood. Growth should be monitored sequentially and is an important tool in the early detection of chronic disease in children. Growth occurs in three phases: infancy, childhood and puberty (adolescence). The adequacy of nutritional status can be assessed by anthropometric measurements that include height, weight and body composition as well as laboratory evaluations. Individual patients can then be compared to normative or expected values. Impaired growth and nutritional status can be seen in a variety of gastrointestinal disorders and are described in this chapter. Key words: growth patterns; growth velocity; body mass index; DEXA; nutritional status.
Physical growth is defined as an increase in the mass of body tissues from infancy through adulthood. This process in a child who is physically and emotionally healthy, and is adequately nourished, will proceed at a normal rate. However, normal growth is not a uniform process and is dependent on the sex, pubertal stage and racial as well as ethnic background of the child. Adequate nutrition and exercise are important factors in the attainment of normal growth, maturation and bone mineral accretion. Compared with a single measurement of height or weight, which reflects previous growth, sequential growth measurements or growth velocity are much more meaningful, since they represent growth dynamics over time. Growth monitoring is an important tool in the early detection of disease in children and, on occasion, may be the initial or only manifestation of underlying chronic disease. Growth velocity is also important in evaluating the efficacy of medical or nutritional intervention. This chapter focuses on the assessment of growth and nutritional status in children and adolescents, and the impairment of this normal process as a complication of gastrointestinal disease. * Corresponding author. Tel.:þ1-773-702-6418; Fax:þ 1-773-702-0666. E-mail address: [email protected] (R. Gokhale). 1521-6918/03/$ - see front matter Q 2003 Published by Elsevier Science Ltd.
154 R. Gokhale and B. S. Kirschner
NORMAL GROWTH PATTERNS Growth can be divided into three phases on the basis of the infant –childhood– puberty (ICP) model as suggested by Karlberg et al.1 These growth periods relate to differences in various underlying genetic, hormonal and nutritional factors that occur during growth and ultimately lead to differences in skeletal maturation and development in an individual child. Infancy phase Growth during this phase, up to the age of 2 –3 years, is more rapid than at any other time including the adolescent phase. Growth during infancy is a continuation of fetal growth and in the neonatal phase it is dependent upon maternal, placental and fetal factors. Maternal factors include maternal nutrition, maternal size, infections and environmental exposure to cigarettes, alcohol and drugs. Placental factors include vascular abnormalities, placental hormones and hypoxia. Chromosomal abnormalities or syndromes, e.g. Russell –Silver syndrome, within the fetus itself also influence fetal growth. Neonates may lose weight soon after birth due to losses of extracellular fluid, but should regain their birth weight by 8 –10 days. Most healthy neonates will double their birth weight by 5 months of age and triple their weight by 1 year of age. Between the ages of 1 and 2 years an average child will gain about 3.5 kg. Increases in length also occur rapidly, with a 25 cm average increase in the first year of life followed by about a 12 cm gain over the next year. Premature infants should be plotted by corrected age on standard growth curves up to age 4 years, after which corrections are no longer necessary. Measurement of head circumference is important during the infancy phase since it is an indicator of brain growth. The brain doubles its weight by about 12 months.2 At birth, the average head circumference is 35 cm, increasing by 12 cm during the first year, and by 5 cm from 12 to 24 months of age. After 36 months of age, the average head circumference increase is about 1 cm/year. Head circumference is the last measure to be affected by malnutrition and is a less sensitive indicator of growth but is reflective of brain development and possible neurological disorders.3 Interruption of the normal growth process during the infancy phase may have long term consequences, with a decreased potential for catch-up growth even if growth is relatively normal during the childhood phase. Childhood phase The childhood phase begins around the preschool years and continues until puberty. Many hormones, primarily growth hormone, influence skeletal and somatic growth during this phase, the effects of which are mediated via somatomedin C or insulinlike growth factor 1 (IGF-1). These peptides exert an anabolic effect on cartilage, muscle and adipose tissue. Nutrition is an important component of this phase and it has been shown that chronic undernutrition, such as occurs in children with inflammatory bowel disease (IBD), lowers the levels of circulating IGF-1, with an increase in levels by up to 345% on nutritional restitution.4,5 Thyroxine, glucocorticoids, insulin, oestrogens and androgens along with polypeptide growth factors also contribute to growth. Overfeeding during this phase has important
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implications, since it may lead to childhood obesity and, subsequently, to obesity in adulthood, with associated health risks including cardiovascular disease and diabetes.6 Growth occurs at a steady pace during the childhood phase. On average, boys and girls grow about 5 –6 cm in length per year. Weight gain in boys is about 2 kg/year up to age 7, increasing steadily to about 4 kg/year around 10 years of age. Girls tend to grow and gain weight faster than boys, since they achieve puberty at an earlier age. Differences in body shape and size occur towards the end of this phase, with girls having an increase in adipose tissue of up to about 25% compared with boys.2 Also apparent are changes in body proportions, with legs and arms having a greater rate of growth compared with the trunk. Puberty phase and adolescence Adolescence is the phase that begins with the onset of pubertal changes and extends until growth and maturation are completed in adulthood. This phase is characterized not only by significant physical alterations but sexual, behavioural and psychological changes as well. Marked variations are seen between individuals at the same chronological age pertaining to the achievement of puberty, which are considered to be ‘normal’. Longitudinal follow-up of paediatric patients is much more important at this stage that at any other stage. Puberty is characterized by an acceleration of height velocity and the development of secondary sexual characteristics. Puberty in girls is easily recognized by the onset of menstruation, or menarche. In general, girls reach puberty about 2 years earlier than boys. Pubertal changes can be characterized by Tanner stages, which are based on the development of secondary sex characteristics and are assigned from a scale of 1 (prepubertal) to 5 (adult).7 In girls, the first sign of puberty is the development of breast buds and pubic hair. Peak height velocity, on average about 8.4 – 9 cm/year, begins during this phase and slows considerably after menarche, which occurs about 2 years after the onset of puberty.2 Growth still proceeds for a mean of 5 – 6 cm after the onset of menarche. The growth potential after menarche in patients with IBD varies with the age of menarche, averaging 10 cm in those with menarche at less than 13 years of age, 6 cm in those with menarche between 13 – 15 years and 2 cm above 15 years.8 Completion of puberty occurs with maturation of breasts to an adult pattern and coincides with the cessation of linear growth. In boys, the first and usually unrecognized sign of puberty is scrotal and testicular enlargement, which coincides with acceleration of linear growth by an average of 9.5 –10.3 cm/year.2 Height gains may precede further progression into puberty by up to 1 year. Tanner stages 3 and 4 are characterized by further growth of genitalia, development of facial and axillary hair, deepening of the voice and adult distribution of pubic hair. Puberty continues for a longer time in boys; it may continue until age 18 –20 years, thus resulting in a larger body size in men compared with women. In addition to changes in secondary sexual characteristics, puberty also involves changes in body composition. These changes can be measured using skinfold measurements, body mass index (BMI) and bioelectric impedence analysis as well as by newer techniques including dual energy X-ray absorptiometry (DEXA).9,10 Lean body mass (LBM), which is primarily muscle mass, increases from 25% at birth to about 50% of total body weight in adulthood. LBM increases occur at a steady rate throughout childhood until age 12– 13 years in both boys and girls. In girls, further
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increases in LBM cease at around 15 years of age but continue in boys until late adolescence, almost twice as long as girls.2,9,10 An increase in LBM is especially noticeable in the upper body and arms in boys. Deposition of adipose tissue also varies, with adolescent girls having significantly more adipose tissue around the breasts, hips, gluteal region and back of the arms.2,10 Rapid bone accretion occurs during puberty and adolescence and is an important determinant of the peak bone mass of adults. Interruption of bone accretion due to chronic disease, delay in puberty, or corticosteroid use, combined with low calcium intake and malnutrition, can lead to low bone mass which increases the potential for fractures.11 In a study of 299 healthy Caucasian children (136 boys and 163 girls) growth at the lumbar spine (trabecular bone) increased in a linear fashion until puberty, followed by a rapid increase in bone density in girls between the ages of 10 and 15 years, with a marked slowing thereafter.12 In boys, rapid increases in lumbar spine bone density began later, at 13 years, with steep increases until 17 years of age and slowing thereafter. These changes coincided with the attainment of puberty in both sexes. When compared by pubertal stages, girls showed a rise in bone mineral density (BMD) between early and mid-puberty (Tanner stages 2 and 3) compared with similar increases in BMD at mid- to late-puberty in boys.12 Cortical bone growth, as measured by radial BMD, showed less variation with an increase in males only at puberty. Weight gain, BMI and calcium intake in excess of the recommended daily allowance (RDA) for age are also, to a lesser extent, independent predictors of increases in BMD.13,14 BMD assessments are matched for age and sex using Z scores for each child. While corticosteroid dose is a risk factor for reduced BMD, our studies have demonstrated that paediatric patients with Crohn’s disease are more likely than those with ulcerative colitis to have reduced BMD.15 When assessing BMD in paediatric patients with potential skeletal delay, a bone age film should be obtained and the BMD should be interpreted on the basis of bone age rather than on chronological age.15,16
ANTHROPOMETRIC ASSESSMENT Length Length is an excellent marker of childhood growth, since it is not subject to daily variations as is weight. Serial measurements over a 3 –6 month interval are recommended and a deceleration in growth percentiles may be an early, or occasionally the only, indicator of chronic disease or suboptimal nutritional intake. Serial heights should be plotted on revised growth charts published, in 1998, by the National Center for Health Statistics (NCHS).17 Two sets of charts are available; birth to 3 years and 2 –19 years. Specialized growth charts are available for children with underlying conditions that independently affect growth, e.g. Down’s syndrome or Turner’s syndrome.18,19 Length is measured in the supine position up to 18 months of age. Ideally two persons should be available to measure an infant and care should be taken to straighten the lower extremities so as not to underestimate length. After the age of 2 years, or when the child is able to stand up, length should be measured on a stadiometer. Knemometry, measurement of lower leg length, is a non-invasive, reproducible measurement that can be used to determine daily or weekly fluctuations in growth.20
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Weight Weight is an easily measured indicator of growth but is subject to greater daily variations. Weights should be plotted on standard growth curves and each child’s percentile should be monitored over time. Weight for height measurements and percentage of ideal body weight (IBW: actual weight/IBW at 50th percentile for age £ 100) are more meaningful measures of growth. Body composition Total body fat (TBF) and fat-free mass (FFM) are useful indicators of childhood nutritional status, both undernutrition as well as obesity. These can be assessed using various techniques including skinfold measurements, water dilution assays and bioelectric impedance as well as newer techniques such as DEXA. Skinfold measurements These are simple tests that can be performed by the bedside. However, they may not be as accurate for determining percentage body fat especially in small children (since it is difficult to separate subcutaneous tissue from muscle) or in patients with oedematous tissue (as may occur with hypoalbuminaemia or corticosteroid use). Triceps and subcapsular skinfolds are used to measure the thickness of subcutaneous tissue. The triceps skinfold (TSF) is measured using a caliper on the left upper arm midway between the acromian and olecranon process, with the child standing in a relaxed position with his or her back to the examiner. The subcapsular skinfold is measured at the basal point of the scapula. Muscle stores are calculated using the mid-arm circumference (MAC), which in measured at the same point as the triceps skinfold. The mid-arm muscle circumference (MAMC) is then calculated using the following formula: MAMC (cm) ¼ MAC (cm) 2 (0.134 £ TSF (mm))21, or by using standard normograms.22 Body mass index BMI is a reliable measurement of adiposity in adults.23 BMI is derived by dividing weight in kilograms by height in meters squared (wt (kg)/ht (m2)). In the United States, standardized percentile curves have been developed that can be used to compare individuals and to screen for obesity.24 According to the International Obesity Task Force, the values of 25 and 30 kg/m2 correlate with being overweight and obese, respectively.25 BMI is a good measure of TBF, but can underestimate the percentage of LBM or FFM. After the age of 12 years (especially in males), larger BMI gains are mainly from an increase in FFM or muscle mass and, thus, are not reliable indicators of obesity.9 Serial BMI measurements (especially in children above the age of 7) may be useful for identifying children at risk for being obese as adults with increased health risks including type II diabetes and cardiovascular disease. Studies have shown a correlation between elevated parental BMI, both paternal and maternal, with elevated BMI in children.26 DEXA is a non-invasive technique for the estimation of visceral body fat and can be used in young patients since it exposes the child to less radiation compared with a computed tomography (CT) scan or magnetic resonance imaging (MRI).27
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Underwater weighing and isotope dilution techniques are also available for the estimation of body composition, but these are cumbersome, time-consuming and available mainly at research settings. Bioelectrical impedance analysis is a simple, noninvasive method for evaluating FFM, total fat mass and percentage fat mass and is more reliable than skinfold measurements, as was seen in a recent study in 38 children aged 5 – 12 years.28
BONE AGE EVALUATION Bone age X-ray is obtained by an X-ray evaluation of the left wrist and hand.29 In children with chronic disease and growth failure, bone age can be delayed by more than 2 years compared with that of a normal child in whom the bone age should correlate with the chronological age. Using this technique, growth potential in children with IBD based on predicted adult height can be obtained using published tables, which utilize bone age and current height.29,30
GROWTH RETARDATION Impaired linear growth or growth retardation is characterized by a deceleration of growth velocity, or a fall in the percentile channels for height and weight. Growth failure is seen in a variety of gastrointestinal disorders and is usually associated with a delay in skeletal or bone age. Disease-associated growth delay should be distinguished from genetic short stature and constitutional delay in growth. Children with genetic short stature are low in height percentiles but grow at a normal velocity, with a bone age that is commensurate with chronological age. In contrast, children with constitutional delay in growth have short stature and normal growth velocity, but delayed skeletal age leading to a normal growth potential. Children with constitutional delay in growth may continue to grow into their 20s. Gastrointestinal disease frequently leads to growth retardation from impaired nutritional status in children. Nutritional insufficiency usually results from reduced nutrient intake, but impaired intestinal absorption or increased intestinal losses may also contribute. Recognition of the underlying intestinal disorder, with appropriate therapy and dietary counselling for nutritional restitution, are important approaches in reversing growth retardation so that the child can achieve his or her growth potential.
REDUCED NUTRIENT INTAKE Dietary intake is best evaluated by dietary recall or a diet diary over a 24 hour period or a 3 or a 7 day period. Energy and protein needs can be estimated utilizing the recommended dietary allowances (RDAs).31 Adolescence is considered to be a particularly vulnerable period for impaired nutritional status, both due to greater demand from rapid growth and from altered eating habits due to peer pressure and socio-cultural factors. Restriction of food intake may occur from fear of obesity,
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preoccupation with body image issues, active lifestyles, or as part of an anorexia/bulimia syndrome.32 Swallowing disorders may occur from oropharyngeal incoordination, which is usually seen in neurologically impaired children but may occasionally occur in normal healthy children. These can be evaluated radiologically by an oropharyngeal motility study and patients with abnormal studies may require feeding via a nasogastric tube or gastrostomy. Congenital disorders including oesophageal atresia and tracheooesophageal fistulae are usually manifest soon after birth and require prompt surgical intervention. Gastro-oesophageal reflux-associated oesophagitis is the commonest cause of reduced food intake in infants and children. Infants may present with recurrent emesis, irritability or, less commonly, with refusal to eat solid foods or poor weight gain. Increased incidence of oesophagitis is seen in neurologically impaired children or in children with developmental disabilities.33 Cow’s milk protein and soy protein allergy may also present with similar complaints. Definitive diagnosis can be made by endoscopic biopsies, following which targeted therapeutic intervention can be initiated. Less common causes of oesophagitis causing decreased intake include infections with cytomegalovirus, Herpes simplex virus or candida complicating mucositis induced following chemotherapy, radiation therapy or immune deficiency disorders. Inflammatory conditions of the stomach are often associated with a poor appetite due to abdominal pain or discomfort, nausea, early satiety or emesis. Examples include gastritis from acid peptic causes, Helicobacter pylori infection, antroduodenal Crohn’s disease (CD) and eosinophilic gastroenteropathy. CD and ulcerative colitis (UC) are well recognized chronic inflammatory conditions that are associated with growth failure, with a frequency of up to 40% in CD compared to 5% in UC.34 Several mechanisms contribute to malnutrition, the most important being suboptimal food intake. Children with antroduodenal CD may limit the amounts of food eaten due to abdominal pain or early satiety. Patients with diffuse small bowel or colonic CD often experience post-prandial abdominal pain followed by diarrhoea. Active CD has an anorexic effect due to the production of pro-inflammatory cytokines, including tumour necrosis factor (TNFa) and interleukins (IL 1b).35 In patients with diffuse small bowel disease or following surgical resections leading to short-gut syndrome, malabsorption may occur. Specific micronutrient deficiencies include iron, folate and cyanocobalamine deficiencies leading to anaemia, hypoalbuminaemia from protein-losing enteropathy and zinc deficiency, which may further contribute to growth failure. Chronic undernutrition also leads to low levels of IGF-1 and a delay in sexual maturation.4,5 Malabsorption of nutrients occurs in conditions where there is insufficient surface area for absorption, such as short-gut syndrome following necrotizing enterocolitis, surgical resections or enteropathies. Coeliac disease (gluten sensitive enteropathy) is a leading cause of growth failure from malabsorption. The prevalence of coeliac disease was found to be 21% among children with unexplained short stature and no associated gastrointestinal symptoms.36 Increased incidence of coeliac disease has also been noted with Down’s syndrome, insulin-dependent diabetes mellitus (IDDM) and autoimmune thyroiditis; patients with these conditions should be screened early for coeliac disease even if they have no gastrointestinal symptoms.37,38 Uncommon intestinal conditions causing malabsorption include intestinal lymphangiectasia, which leads to a deficiency of fat soluble vitamins in addition to hypoalbuminaemia. Maldigestion of nutrients occurs in conditions such as cholestatic liver disease or
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cystic fibrosis, due to abnormal digestion of nutrients, thereby leading to wastage of calories.
SCREENING FOR NUTRITIONAL DEFICIENCIES A careful history and physical examination, including anthropometric measurements, are useful in determining the presence of growth retardation and nutritional deficiencies. Further testing can establish the specific deficiencies so that proper treatment can be initiated. Blood tests A complete blood count with differential can reveal iron deficiency anaemia with microcytic, hypochromic indices in patients with CD, UC and coeliac disease. Macrocytic anaemia indicative of B12 or folate deficiency may result from diffuse malabsorption or surgical resections. Macrocytic indices are also associated with red blood cell maturation arrest due to drugs such as azathioprine and 6mercaptopurine, which are used to treat patients with IBD. Thrombocytosis and increased numbers of immature leukocytes (band forms) may also be a clue to underlying IBD. Blood chemistry screening can be used to assess albumin levels, total cholesterol and the low alkaline phosphatase levels that are seen in zinc deficiency. Specialized tests are necessary to diagnose the associated conditions. Stool analysis Carbohydrate malabsorption is diagnosed by the presence of acidic stools with a pH of less than 6.0, or the presence of reducing sugars from carbohydrate fermentation of the malabsorbed sugar. Faecal fat is detected by a Sudan stain performed on a random stool sample. Increased neutral fat in the stool suggests maldigestion from pancreatic disease, whereas split fatty acids are consistent with malabsorption from enteropathy such as coeliac disease. For total fat analysis 72 hour stool collections may be more accurate, but are cumbersome and difficult to obtain in an infant or child. Increased levels of faecal a-1 anti-trypsin are indicative of a protein-losing enteropathy and levels can be monitored to evaluate response to therapy. Specialized radiographical, endoscopic and ultrasonic evaluations are indicated for the diagnosis of specific gastrointestinal conditions, as described above.
REFERENCES 1. Karlberg J, Engstron I, Karlberg P & Fryer JG. Analyses of linear growth using a mathematical model. Acta Paediatrica Scandinavica 1987; 76(supplement): 478–488. * 2. Chumlea WC & Guo SS. Physical growth and development. In Samour PQ, Helm KK & Lang CE (eds) Handbook of Pediatric Nutrition, pp 3–15. Gaithersberg, MD: Aspen Publishers, 1999. * 3. Ekvall SW. Nutrition assessment and early intervention. In Ekwall SW (ed.) Pediatric Nutrition in Chronic Diseases and Development: Disorders, Prevention, Assessment and Treatment, pp 41. New York: Oxford University Press, 1993. 4. Kirschner BS & Sutton MM. Somatomedin-C levels in growth impaired children and adolescents with chronic inflammatory bowel disease. Gastroenterology 1986; 91: 830– 836.
Assessment of growth and nutrition 161 5. Thomas AG, Holly JM, Taylor F & Miller V. Insulin like growth factor-1, insulin like growth factor binding protein-1, and insulin in childhood Crohn’s disease. Gut 1993; 34: 944–947. 6. Wickelgren I. Obesity: how big a problem? Science 1998; 280: 1364–1367. * 7. Tanner JM. Growth in Adolescence, 2nd ed. Boston, MA: Blackwell, 1962. 8. Kirschner BS, Uebler N & Sutton MM. Growth after menarche in pediatric patients with chronic inflammatory bowel disease. Gastroenterology 1993; 104: A629. 9. Trudeau F, Shephard RJ, Arsenault F & Laurencelle L. Changes in adiposity and body mass index from late childhood to adult life in the Trois Rivieres study. American Journal of Human Biology 2001; 13: 349– 355. 10. Fuller NJ, Fewtrell MS, Dewit O et al. Segmental bioelectric impedence analysis in children aged 8–12 years. The assessment of regional body composition and muscle mass. Journal of Obesity Related Metabolic Disorders 2002; 26: 692 –700. 11. Hui SL, Slemeda CW & Johnston CC Jr. Age and bone mass as predictors of fracture in a prospective study. Journal of Clinical Investigation 1998; 81: 1804–1809. 12. Rubin K, Schirduan V, Gendreau P et al. Predictors of axial and peripheral bone mineral density in healthy children and adolescents, with special attention to the role of puberty. Journal of Pediatrics 1993; 123: 863–870. 13. Johnston CC, Miller JZ, Slemeda CW et al. Calcium supplementation and increase in bone mineral density in children. New England Journal of Medicine 1992; 327: 82–87. 14. Slemeda CW, Reister TK, Hui SL et al. Influences on skeletal mineralization in children and adolescents: evidence for varying effects of sexual maturity and physical activity. Journal of Pediatrics 1994; 125: 201–207. * 15. Gokhale R, Favus MJ, Karrison T et al. Bone mineral density assessment in children with inflammatory bowel disease. Gastroenterology 1998; 114: 902–911. 16. Herzog D, Bishop N, Glorieux F & Seidman EG. Interpretation of bone mineral density values in pediatric Crohn’s disease. Inflammatory Bowel Diseases 1998; 4: 261–267. 17. NCHS, Revised Growth Charts. National Center for Health Statistics, 2000. 18. Cronk C, Crocker AC, Pueschel SM et al. Growth charts for children with Down’s syndrome: 1 month to 18 years of age. Pediatrics 1988; 81: 102– 110. 19. Lyon AJ, Preece MA & Grant DB. Growth curve for girls with Turner syndrome. Archive of Disease in Childhood 1985; 60: 932–935. 20. Ahmed SF, Wallace WHB & Kelnar CJH. Knemometry in childhood: a study to compare the precision of two different techniques. Annals of Human Biology 1995; 22: 247–252. * 21. Bessler S. Nutritional assessment. In Samour PQ, Helm KK & Lang CE (eds) Handbook of Pediatric Nutrition, pp 17–42. Gaithersberg, MD: Aspen Publishers, 1999. * 22. Gurney JM & Jeliffe DB. Arm anthropometry in nutritional assessment: nomogram for rapid calculation of muscle circumference and cross-sectional muscle and fat areas. American Journal of Clinical Nutrition 1973; 26: 912 –915. 23. Garrow JS & Webster J. Quetelets index (W/H2) as a measure of fatness. International Journal of Obesity Related Metabolic Disorders 1985; 9: 147–153. * 24. Rosner B, Prineas R, Loggie J & Daniels SR. Percentiles for BMI in US children 5 to 17 years of age. Journal of Pediatrics 1998; 132: 211–222. 25. Cacciari E, Milani S, Balsamo A et al. Italian cross-sectional growth charts for height, weight and body mass index (6 to 20 years). European Journal of Clinical Nutrition 2002; 56: 171–180. 26. Safer DL, Agras WS, Bryson S & Hammer CD. Early body mass index and other anthropometric relationships between parents and children. International Journal of Obesity Related Metabolic Disorders 2001; 25: 1532–1536. * 27. Snijder MB, Visser M, Dekker JM et al. The prediction of visceral body fat by dual energy X-ray absorbtiometry in the elderly, a comparison with computed tomography and anthropometry. International Journal of Obesity Related Metabolic Disorders 2002; 26: 984–993. 28. Beertema W, Hezewijk M, Kester A et al. Measurement of total body water in children using bioelectric impedance: a comparison of several prediction equations. Journal of Pediatric Gastroenterology and Nutrition 2000; 31: 428– 432. 29. Greulich WW & Pyle SI. Radiographic Atlas of Skeletal Development of the Hand and Wrist. Palo Alto, CA: Stanford University, 1959. * 30. Kirschner BS. Growth and development in chronic inflammatory bowel disease. Acta Paediatrica Scandinavica 1990; 366(supplement): 98–104. 31. Food and Nutrition Board. Recommended Dietary Allowances, 10th ed. Washington, DC: National Academy Press, 1989. * 32. Spear B. Adolescent growth and development. In Richert VI (ed.) Adolescent Nutrition: Assessment and Management, pp 3 –23. New York: Chapman & Hall, 1995. 33. Sondheimer JM & Morris BA. Gastroesophageal reflux among severely retarded children. Journal of Pediatrics 1979; 94: 710 –714.
162 R. Gokhale and B. S. Kirschner 34. Krischner BS, Voinchet O & Rosenberg IH. Growth retardation in children with inflammatory bowel disease. Gastroenterology 1978; 75: 504–511. 35. Murch SH, Lamkin VA, Savage MO et al. Serum concentrations of tumor necrosis factor alpha in childhood chronic inflammatory bowel disease. Gut 1991; 32: 913–917. 36. Groll A, Candy DCA, Preece MA et al. Short stature as the primary manifestation of celiac disease. Lancet 1980; : 1097–1099. 37. Gale L, Wimalaratna H, Brotodiharjo A & Duggan JM. Down’s syndrome is strongly associated with celiac disease. Gut 1997; 40: 492–496. 38. Vitoria JC, Castano L, Rica I et al. Association of insulin-dependent diabetes mellitus and celiac disease: a study based on serologic markers. Journal of Pediatric Gastroenterology and Nutrition 1998; 27: 47–52.
2 Assessment of growth and nutrition Ranjana Gokhale*
MD
Assistant Professor of Clinical Pediatrics
Barbara S. Kirschner
MD
Professor of Pediatrics and Medicine Section of Pediatric Gastroenterology and Nutrition, The University of Chicago Children’s Hospital, 5839 S. Maryland Avenue, MC 4065, Chicago, IL 60637, USA
Growth is a dynamic process that is characterized by physiological changes in an individual from infancy into adulthood. Growth should be monitored sequentially and is an important tool in the early detection of chronic disease in children. Growth occurs in three phases: infancy, childhood and puberty (adolescence). The adequacy of nutritional status can be assessed by anthropometric measurements that include height, weight and body composition as well as laboratory evaluations. Individual patients can then be compared to normative or expected values. Impaired growth and nutritional status can be seen in a variety of gastrointestinal disorders and are described in this chapter. Key words: growth patterns; growth velocity; body mass index; DEXA; nutritional status.
Physical growth is defined as an increase in the mass of body tissues from infancy through adulthood. This process in a child who is physically and emotionally healthy, and is adequately nourished, will proceed at a normal rate. However, normal growth is not a uniform process and is dependent on the sex, pubertal stage and racial as well as ethnic background of the child. Adequate nutrition and exercise are important factors in the attainment of normal growth, maturation and bone mineral accretion. Compared with a single measurement of height or weight, which reflects previous growth, sequential growth measurements or growth velocity are much more meaningful, since they represent growth dynamics over time. Growth monitoring is an important tool in the early detection of disease in children and, on occasion, may be the initial or only manifestation of underlying chronic disease. Growth velocity is also important in evaluating the efficacy of medical or nutritional intervention. This chapter focuses on the assessment of growth and nutritional status in children and adolescents, and the impairment of this normal process as a complication of gastrointestinal disease. * Corresponding author. Tel.:þ1-773-702-6418; Fax:þ 1-773-702-0666. E-mail address: [email protected] (R. Gokhale). 1521-6918/03/$ - see front matter Q 2003 Published by Elsevier Science Ltd.
154 R. Gokhale and B. S. Kirschner
NORMAL GROWTH PATTERNS Growth can be divided into three phases on the basis of the infant –childhood– puberty (ICP) model as suggested by Karlberg et al.1 These growth periods relate to differences in various underlying genetic, hormonal and nutritional factors that occur during growth and ultimately lead to differences in skeletal maturation and development in an individual child. Infancy phase Growth during this phase, up to the age of 2 –3 years, is more rapid than at any other time including the adolescent phase. Growth during infancy is a continuation of fetal growth and in the neonatal phase it is dependent upon maternal, placental and fetal factors. Maternal factors include maternal nutrition, maternal size, infections and environmental exposure to cigarettes, alcohol and drugs. Placental factors include vascular abnormalities, placental hormones and hypoxia. Chromosomal abnormalities or syndromes, e.g. Russell –Silver syndrome, within the fetus itself also influence fetal growth. Neonates may lose weight soon after birth due to losses of extracellular fluid, but should regain their birth weight by 8 –10 days. Most healthy neonates will double their birth weight by 5 months of age and triple their weight by 1 year of age. Between the ages of 1 and 2 years an average child will gain about 3.5 kg. Increases in length also occur rapidly, with a 25 cm average increase in the first year of life followed by about a 12 cm gain over the next year. Premature infants should be plotted by corrected age on standard growth curves up to age 4 years, after which corrections are no longer necessary. Measurement of head circumference is important during the infancy phase since it is an indicator of brain growth. The brain doubles its weight by about 12 months.2 At birth, the average head circumference is 35 cm, increasing by 12 cm during the first year, and by 5 cm from 12 to 24 months of age. After 36 months of age, the average head circumference increase is about 1 cm/year. Head circumference is the last measure to be affected by malnutrition and is a less sensitive indicator of growth but is reflective of brain development and possible neurological disorders.3 Interruption of the normal growth process during the infancy phase may have long term consequences, with a decreased potential for catch-up growth even if growth is relatively normal during the childhood phase. Childhood phase The childhood phase begins around the preschool years and continues until puberty. Many hormones, primarily growth hormone, influence skeletal and somatic growth during this phase, the effects of which are mediated via somatomedin C or insulinlike growth factor 1 (IGF-1). These peptides exert an anabolic effect on cartilage, muscle and adipose tissue. Nutrition is an important component of this phase and it has been shown that chronic undernutrition, such as occurs in children with inflammatory bowel disease (IBD), lowers the levels of circulating IGF-1, with an increase in levels by up to 345% on nutritional restitution.4,5 Thyroxine, glucocorticoids, insulin, oestrogens and androgens along with polypeptide growth factors also contribute to growth. Overfeeding during this phase has important
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implications, since it may lead to childhood obesity and, subsequently, to obesity in adulthood, with associated health risks including cardiovascular disease and diabetes.6 Growth occurs at a steady pace during the childhood phase. On average, boys and girls grow about 5 –6 cm in length per year. Weight gain in boys is about 2 kg/year up to age 7, increasing steadily to about 4 kg/year around 10 years of age. Girls tend to grow and gain weight faster than boys, since they achieve puberty at an earlier age. Differences in body shape and size occur towards the end of this phase, with girls having an increase in adipose tissue of up to about 25% compared with boys.2 Also apparent are changes in body proportions, with legs and arms having a greater rate of growth compared with the trunk. Puberty phase and adolescence Adolescence is the phase that begins with the onset of pubertal changes and extends until growth and maturation are completed in adulthood. This phase is characterized not only by significant physical alterations but sexual, behavioural and psychological changes as well. Marked variations are seen between individuals at the same chronological age pertaining to the achievement of puberty, which are considered to be ‘normal’. Longitudinal follow-up of paediatric patients is much more important at this stage that at any other stage. Puberty is characterized by an acceleration of height velocity and the development of secondary sexual characteristics. Puberty in girls is easily recognized by the onset of menstruation, or menarche. In general, girls reach puberty about 2 years earlier than boys. Pubertal changes can be characterized by Tanner stages, which are based on the development of secondary sex characteristics and are assigned from a scale of 1 (prepubertal) to 5 (adult).7 In girls, the first sign of puberty is the development of breast buds and pubic hair. Peak height velocity, on average about 8.4 – 9 cm/year, begins during this phase and slows considerably after menarche, which occurs about 2 years after the onset of puberty.2 Growth still proceeds for a mean of 5 – 6 cm after the onset of menarche. The growth potential after menarche in patients with IBD varies with the age of menarche, averaging 10 cm in those with menarche at less than 13 years of age, 6 cm in those with menarche between 13 – 15 years and 2 cm above 15 years.8 Completion of puberty occurs with maturation of breasts to an adult pattern and coincides with the cessation of linear growth. In boys, the first and usually unrecognized sign of puberty is scrotal and testicular enlargement, which coincides with acceleration of linear growth by an average of 9.5 –10.3 cm/year.2 Height gains may precede further progression into puberty by up to 1 year. Tanner stages 3 and 4 are characterized by further growth of genitalia, development of facial and axillary hair, deepening of the voice and adult distribution of pubic hair. Puberty continues for a longer time in boys; it may continue until age 18 –20 years, thus resulting in a larger body size in men compared with women. In addition to changes in secondary sexual characteristics, puberty also involves changes in body composition. These changes can be measured using skinfold measurements, body mass index (BMI) and bioelectric impedence analysis as well as by newer techniques including dual energy X-ray absorptiometry (DEXA).9,10 Lean body mass (LBM), which is primarily muscle mass, increases from 25% at birth to about 50% of total body weight in adulthood. LBM increases occur at a steady rate throughout childhood until age 12– 13 years in both boys and girls. In girls, further
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increases in LBM cease at around 15 years of age but continue in boys until late adolescence, almost twice as long as girls.2,9,10 An increase in LBM is especially noticeable in the upper body and arms in boys. Deposition of adipose tissue also varies, with adolescent girls having significantly more adipose tissue around the breasts, hips, gluteal region and back of the arms.2,10 Rapid bone accretion occurs during puberty and adolescence and is an important determinant of the peak bone mass of adults. Interruption of bone accretion due to chronic disease, delay in puberty, or corticosteroid use, combined with low calcium intake and malnutrition, can lead to low bone mass which increases the potential for fractures.11 In a study of 299 healthy Caucasian children (136 boys and 163 girls) growth at the lumbar spine (trabecular bone) increased in a linear fashion until puberty, followed by a rapid increase in bone density in girls between the ages of 10 and 15 years, with a marked slowing thereafter.12 In boys, rapid increases in lumbar spine bone density began later, at 13 years, with steep increases until 17 years of age and slowing thereafter. These changes coincided with the attainment of puberty in both sexes. When compared by pubertal stages, girls showed a rise in bone mineral density (BMD) between early and mid-puberty (Tanner stages 2 and 3) compared with similar increases in BMD at mid- to late-puberty in boys.12 Cortical bone growth, as measured by radial BMD, showed less variation with an increase in males only at puberty. Weight gain, BMI and calcium intake in excess of the recommended daily allowance (RDA) for age are also, to a lesser extent, independent predictors of increases in BMD.13,14 BMD assessments are matched for age and sex using Z scores for each child. While corticosteroid dose is a risk factor for reduced BMD, our studies have demonstrated that paediatric patients with Crohn’s disease are more likely than those with ulcerative colitis to have reduced BMD.15 When assessing BMD in paediatric patients with potential skeletal delay, a bone age film should be obtained and the BMD should be interpreted on the basis of bone age rather than on chronological age.15,16
ANTHROPOMETRIC ASSESSMENT Length Length is an excellent marker of childhood growth, since it is not subject to daily variations as is weight. Serial measurements over a 3 –6 month interval are recommended and a deceleration in growth percentiles may be an early, or occasionally the only, indicator of chronic disease or suboptimal nutritional intake. Serial heights should be plotted on revised growth charts published, in 1998, by the National Center for Health Statistics (NCHS).17 Two sets of charts are available; birth to 3 years and 2 –19 years. Specialized growth charts are available for children with underlying conditions that independently affect growth, e.g. Down’s syndrome or Turner’s syndrome.18,19 Length is measured in the supine position up to 18 months of age. Ideally two persons should be available to measure an infant and care should be taken to straighten the lower extremities so as not to underestimate length. After the age of 2 years, or when the child is able to stand up, length should be measured on a stadiometer. Knemometry, measurement of lower leg length, is a non-invasive, reproducible measurement that can be used to determine daily or weekly fluctuations in growth.20
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Weight Weight is an easily measured indicator of growth but is subject to greater daily variations. Weights should be plotted on standard growth curves and each child’s percentile should be monitored over time. Weight for height measurements and percentage of ideal body weight (IBW: actual weight/IBW at 50th percentile for age £ 100) are more meaningful measures of growth. Body composition Total body fat (TBF) and fat-free mass (FFM) are useful indicators of childhood nutritional status, both undernutrition as well as obesity. These can be assessed using various techniques including skinfold measurements, water dilution assays and bioelectric impedance as well as newer techniques such as DEXA. Skinfold measurements These are simple tests that can be performed by the bedside. However, they may not be as accurate for determining percentage body fat especially in small children (since it is difficult to separate subcutaneous tissue from muscle) or in patients with oedematous tissue (as may occur with hypoalbuminaemia or corticosteroid use). Triceps and subcapsular skinfolds are used to measure the thickness of subcutaneous tissue. The triceps skinfold (TSF) is measured using a caliper on the left upper arm midway between the acromian and olecranon process, with the child standing in a relaxed position with his or her back to the examiner. The subcapsular skinfold is measured at the basal point of the scapula. Muscle stores are calculated using the mid-arm circumference (MAC), which in measured at the same point as the triceps skinfold. The mid-arm muscle circumference (MAMC) is then calculated using the following formula: MAMC (cm) ¼ MAC (cm) 2 (0.134 £ TSF (mm))21, or by using standard normograms.22 Body mass index BMI is a reliable measurement of adiposity in adults.23 BMI is derived by dividing weight in kilograms by height in meters squared (wt (kg)/ht (m2)). In the United States, standardized percentile curves have been developed that can be used to compare individuals and to screen for obesity.24 According to the International Obesity Task Force, the values of 25 and 30 kg/m2 correlate with being overweight and obese, respectively.25 BMI is a good measure of TBF, but can underestimate the percentage of LBM or FFM. After the age of 12 years (especially in males), larger BMI gains are mainly from an increase in FFM or muscle mass and, thus, are not reliable indicators of obesity.9 Serial BMI measurements (especially in children above the age of 7) may be useful for identifying children at risk for being obese as adults with increased health risks including type II diabetes and cardiovascular disease. Studies have shown a correlation between elevated parental BMI, both paternal and maternal, with elevated BMI in children.26 DEXA is a non-invasive technique for the estimation of visceral body fat and can be used in young patients since it exposes the child to less radiation compared with a computed tomography (CT) scan or magnetic resonance imaging (MRI).27
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Underwater weighing and isotope dilution techniques are also available for the estimation of body composition, but these are cumbersome, time-consuming and available mainly at research settings. Bioelectrical impedance analysis is a simple, noninvasive method for evaluating FFM, total fat mass and percentage fat mass and is more reliable than skinfold measurements, as was seen in a recent study in 38 children aged 5 – 12 years.28
BONE AGE EVALUATION Bone age X-ray is obtained by an X-ray evaluation of the left wrist and hand.29 In children with chronic disease and growth failure, bone age can be delayed by more than 2 years compared with that of a normal child in whom the bone age should correlate with the chronological age. Using this technique, growth potential in children with IBD based on predicted adult height can be obtained using published tables, which utilize bone age and current height.29,30
GROWTH RETARDATION Impaired linear growth or growth retardation is characterized by a deceleration of growth velocity, or a fall in the percentile channels for height and weight. Growth failure is seen in a variety of gastrointestinal disorders and is usually associated with a delay in skeletal or bone age. Disease-associated growth delay should be distinguished from genetic short stature and constitutional delay in growth. Children with genetic short stature are low in height percentiles but grow at a normal velocity, with a bone age that is commensurate with chronological age. In contrast, children with constitutional delay in growth have short stature and normal growth velocity, but delayed skeletal age leading to a normal growth potential. Children with constitutional delay in growth may continue to grow into their 20s. Gastrointestinal disease frequently leads to growth retardation from impaired nutritional status in children. Nutritional insufficiency usually results from reduced nutrient intake, but impaired intestinal absorption or increased intestinal losses may also contribute. Recognition of the underlying intestinal disorder, with appropriate therapy and dietary counselling for nutritional restitution, are important approaches in reversing growth retardation so that the child can achieve his or her growth potential.
REDUCED NUTRIENT INTAKE Dietary intake is best evaluated by dietary recall or a diet diary over a 24 hour period or a 3 or a 7 day period. Energy and protein needs can be estimated utilizing the recommended dietary allowances (RDAs).31 Adolescence is considered to be a particularly vulnerable period for impaired nutritional status, both due to greater demand from rapid growth and from altered eating habits due to peer pressure and socio-cultural factors. Restriction of food intake may occur from fear of obesity,
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preoccupation with body image issues, active lifestyles, or as part of an anorexia/bulimia syndrome.32 Swallowing disorders may occur from oropharyngeal incoordination, which is usually seen in neurologically impaired children but may occasionally occur in normal healthy children. These can be evaluated radiologically by an oropharyngeal motility study and patients with abnormal studies may require feeding via a nasogastric tube or gastrostomy. Congenital disorders including oesophageal atresia and tracheooesophageal fistulae are usually manifest soon after birth and require prompt surgical intervention. Gastro-oesophageal reflux-associated oesophagitis is the commonest cause of reduced food intake in infants and children. Infants may present with recurrent emesis, irritability or, less commonly, with refusal to eat solid foods or poor weight gain. Increased incidence of oesophagitis is seen in neurologically impaired children or in children with developmental disabilities.33 Cow’s milk protein and soy protein allergy may also present with similar complaints. Definitive diagnosis can be made by endoscopic biopsies, following which targeted therapeutic intervention can be initiated. Less common causes of oesophagitis causing decreased intake include infections with cytomegalovirus, Herpes simplex virus or candida complicating mucositis induced following chemotherapy, radiation therapy or immune deficiency disorders. Inflammatory conditions of the stomach are often associated with a poor appetite due to abdominal pain or discomfort, nausea, early satiety or emesis. Examples include gastritis from acid peptic causes, Helicobacter pylori infection, antroduodenal Crohn’s disease (CD) and eosinophilic gastroenteropathy. CD and ulcerative colitis (UC) are well recognized chronic inflammatory conditions that are associated with growth failure, with a frequency of up to 40% in CD compared to 5% in UC.34 Several mechanisms contribute to malnutrition, the most important being suboptimal food intake. Children with antroduodenal CD may limit the amounts of food eaten due to abdominal pain or early satiety. Patients with diffuse small bowel or colonic CD often experience post-prandial abdominal pain followed by diarrhoea. Active CD has an anorexic effect due to the production of pro-inflammatory cytokines, including tumour necrosis factor (TNFa) and interleukins (IL 1b).35 In patients with diffuse small bowel disease or following surgical resections leading to short-gut syndrome, malabsorption may occur. Specific micronutrient deficiencies include iron, folate and cyanocobalamine deficiencies leading to anaemia, hypoalbuminaemia from protein-losing enteropathy and zinc deficiency, which may further contribute to growth failure. Chronic undernutrition also leads to low levels of IGF-1 and a delay in sexual maturation.4,5 Malabsorption of nutrients occurs in conditions where there is insufficient surface area for absorption, such as short-gut syndrome following necrotizing enterocolitis, surgical resections or enteropathies. Coeliac disease (gluten sensitive enteropathy) is a leading cause of growth failure from malabsorption. The prevalence of coeliac disease was found to be 21% among children with unexplained short stature and no associated gastrointestinal symptoms.36 Increased incidence of coeliac disease has also been noted with Down’s syndrome, insulin-dependent diabetes mellitus (IDDM) and autoimmune thyroiditis; patients with these conditions should be screened early for coeliac disease even if they have no gastrointestinal symptoms.37,38 Uncommon intestinal conditions causing malabsorption include intestinal lymphangiectasia, which leads to a deficiency of fat soluble vitamins in addition to hypoalbuminaemia. Maldigestion of nutrients occurs in conditions such as cholestatic liver disease or
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cystic fibrosis, due to abnormal digestion of nutrients, thereby leading to wastage of calories.
SCREENING FOR NUTRITIONAL DEFICIENCIES A careful history and physical examination, including anthropometric measurements, are useful in determining the presence of growth retardation and nutritional deficiencies. Further testing can establish the specific deficiencies so that proper treatment can be initiated. Blood tests A complete blood count with differential can reveal iron deficiency anaemia with microcytic, hypochromic indices in patients with CD, UC and coeliac disease. Macrocytic anaemia indicative of B12 or folate deficiency may result from diffuse malabsorption or surgical resections. Macrocytic indices are also associated with red blood cell maturation arrest due to drugs such as azathioprine and 6mercaptopurine, which are used to treat patients with IBD. Thrombocytosis and increased numbers of immature leukocytes (band forms) may also be a clue to underlying IBD. Blood chemistry screening can be used to assess albumin levels, total cholesterol and the low alkaline phosphatase levels that are seen in zinc deficiency. Specialized tests are necessary to diagnose the associated conditions. Stool analysis Carbohydrate malabsorption is diagnosed by the presence of acidic stools with a pH of less than 6.0, or the presence of reducing sugars from carbohydrate fermentation of the malabsorbed sugar. Faecal fat is detected by a Sudan stain performed on a random stool sample. Increased neutral fat in the stool suggests maldigestion from pancreatic disease, whereas split fatty acids are consistent with malabsorption from enteropathy such as coeliac disease. For total fat analysis 72 hour stool collections may be more accurate, but are cumbersome and difficult to obtain in an infant or child. Increased levels of faecal a-1 anti-trypsin are indicative of a protein-losing enteropathy and levels can be monitored to evaluate response to therapy. Specialized radiographical, endoscopic and ultrasonic evaluations are indicated for the diagnosis of specific gastrointestinal conditions, as described above.
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162 R. Gokhale and B. S. Kirschner 34. Krischner BS, Voinchet O & Rosenberg IH. Growth retardation in children with inflammatory bowel disease. Gastroenterology 1978; 75: 504–511. 35. Murch SH, Lamkin VA, Savage MO et al. Serum concentrations of tumor necrosis factor alpha in childhood chronic inflammatory bowel disease. Gut 1991; 32: 913–917. 36. Groll A, Candy DCA, Preece MA et al. Short stature as the primary manifestation of celiac disease. Lancet 1980; : 1097–1099. 37. Gale L, Wimalaratna H, Brotodiharjo A & Duggan JM. Down’s syndrome is strongly associated with celiac disease. Gut 1997; 40: 492–496. 38. Vitoria JC, Castano L, Rica I et al. Association of insulin-dependent diabetes mellitus and celiac disease: a study based on serologic markers. Journal of Pediatric Gastroenterology and Nutrition 1998; 27: 47–52.