 |
|
Association Between Steatorrhea, Growth, and Immunologic Status in Children With Perinatally Acquired HIV Infection
Timothy A. Sentongo, MD;
Richard M. Rutstein, MD;
Nicolas Stettler, MD;
Virginia A. Stallings, MD;
Bret Rudy, MD;
Andrew E. Mulberg, MD
Arch Pediatr Adolesc Med. 2001;155:149-153.
ABSTRACT
| |
Objective To examine the prevalence of steatorrhea and exocrine pancreatic insufficiency
(EPI) and their association with growth and immune status variables in children
with perinatally acquired human immunodeficiency virus (HIV) infection.
Design Cross-sectional study.
Setting Tertiary care HIV subspecialty practice.
Participants Children with perinatally acquired HIV infection. Exclusion criteria
included being younger than 1 year and receiving mineral oil as a medication.
Methods Weight, height, and upper arm anthropometric variables were measured.
Spot stool samples were analyzed for steatorrhea using the Sudan III qualitative
test and for EPI using fecal elastase-1 enzyme assay. Hormone-stimulated pancreatic
function testing and 72-hour stool and dietary fat sample collection were
performed when fecal elastase-1 enzyme was in the range of EPI, defined as
less than 200 µg/g. HIV RNA viral load, CD4 status, type of antiretroviral
therapy, and biochemical evidence of hepatobiliary disease were measured within
3 months of stool sample collection. z Scores were
computed for height, weight, triceps skinfold, and upper arm muscle area.
Results We enrolled 44 patients (23 girls [52%]) with a mean ± SD age
of 7.4 ± 3.1 years. None had hepatobiliary disease. The prevalence
of steatorrhea was 39% (95% confidence interval, 23%-56%). The prevalence
of EPI was 0% (95% confidence interval, 0%-9%). There were no associations
between steatorrhea and EPI, growth, HIV RNA viral load, CD4 status, or type
of antiretroviral therapy. Older children had decreased z scores for height (r = -0.42; P = .006).
Conclusions The clinical significance of steatorrhea in children with HIV infection
is unclear. Furthermore, its evaluation should focus on nonpancreas-based
conditions. Continual close monitoring of growth is essential in children
with HIV infection.
INTRODUCTION
STEATORRHEA, defined as malabsorbed fat in feces, is prevalent in adults
with human immunodeficiency virus (HIV) infection even in the absence of gastrointestinal
tract symptoms.1 The prevalence and impact
of steatorrhea on growth and nutritional status in children with perinatally
acquired HIV infection is not well defined. Impaired growth in HIV infection
has multifactorial origins ranging from inadequate energy (caloric) intake
to nutrient malabsorption, inefficient utilization, and increased losses.2 Because a goal of nutritional care in children with
HIV infection is to achieve a positive energy balance and normal growth, knowledge
of the prevalence of steatorrhea and its growth-related abnormalities can
lead to optimized care. Pancreatic dysfunction has been suggested in children
and adults with HIV infection.3, 4, 5, 6, 7, 8
The aim of this study was to examine the prevalence of steatorrhea and exocrine
pancreatic insufficiency (EPI) in children with perinatally acquired HIV infection.
The hypothesis was that a significant proportion of children with HIV infection
and steatorrhea has EPI. If true, this would merit consideration of pancreatic
enzyme therapy.
PATIENTS AND METHODS
Patients were enrolled between June 1, 1998, and December 31, 1998,
from the outpatient HIV subspecialty office practice or while hospitalized
at The Children's Hospital of Philadelphia (Pa). Patients with perinatally
acquired HIV infection9 were eligible for enrollment.
Exclusion criteria included (1) being younger than 1 year because of the normal
infancy-related higher loss of dietary fat10
and (2) receiving therapy with mineral oil stool softeners because of interference
with interpretation of steatorrhea test results. Children in foster care were
also excluded because of no immediately available guardian authorized to provide
consent. Current antiretroviral therapy with nelfinavir (Agouron, La Jolla,
Calif), a protease inhibitor associated with diarrhea, or didanosine (Bristol-Myers
Squib, Princeton, NJ), a nucleoside analog associated with pancreatitis, or
both was determined by reviewing the medical record. HIV RNA viral load, CD4
status, and biochemical evidence of hepatobiliary disease (defined as liver
enzyme or bilirubin levels greater than the reference range) within 3 months
of stool sample collection were documented from medical chart review and confirmed
with the primary care team.
Qualitative steatorrhea was measured using the Sudan III qualitative
fecal fat test, as described by Drumey et al,11
on a sample of at least 5 g of stool. Screening for EPI was conducted using
stool sample analysis with the fecal elastase-1 enzyme (FE-1) assay.12, 13, 14 Patients with FE-1
levels in the range for EPI, defined as less than 200 µg/g, had confirmatory
testing for EPI using the 72-hour stool and dietary fat sample collection15 for quantitative steatorrhea and the hormone-stimulated
pancreatic function test.16 Informed consent
was obtained before the study from the parent(s) or guardian(s), and assent
was obtained from patients older than 6 years. The institutional review board
at The Children's Hospital of Philadelphia approved the study.
CD4 STATUS AND HIV RNA VIRAL LOAD
CD4 counts obtained as part of routine outpatient clinical care visits
were used for the analysis and were categorized as normal ( 25% of normal),
moderately suppressed (15%-24% of normal), or severely suppressed (<15%
of normal) based on reference ranges of age-specific CD4 counts.17
HIV RNA viral load from blood samples obtained within 3 months of the date
of stool sample collection was used for the analysis. Plasma HIV RNA levels
were measured using the method of branched DNA signal amplification (r-nasba;
Organon, Durham, NC).18
GROWTH ASSESSMENT
Height was measured using a stadiometer accurate to 0.1 cm (Holtain,
Crymych, England). Weight was measured using a digital scale accurate to 0.1
kg (Scaltronix, White Plains, NJ). All measurements were taken with children
in light clothing and shoeless. Middle upper arm circumference was measured
using a nonstretchable plastic measuring tape. Triceps skinfold was measured
using a skinfold caliper (Holtain). Both measurements were performed in triplicate
on the right upper arm by one of us (T.A.S.) using a standard technique,19 and the mean was used for analysis. Total upper arm
muscle area was calculated from upper arm muscle circumference and triceps
skinfold measurements.20
STOOL STUDIES AND HORMONE-STIMULATED PANCREATIC FUNCTION TEST
Spot fecal specimens were collected, aliqouted, and stored at –70°C
before measurement of qualitative steatorrhea and FE-1 analysis. Qualitative
steatorrhea was assessed using the Sudan III qualitative stain11
(Mayo Clinic Laboratories, Rochester, Minn), which is specific for detecting
triglycerides and fatty acids in the stool matrix21
and reliable for excluding steatorrhea.22 The
FE-1 content of the spot stool specimen was measured using enzyme-linked immunosorbent
assay (ScheBo-Tech, Wettenberg, Germany). After age 1 month, normal FE-1 levels
are greater than 200 µg/g. Thereafter, levels of 100 to 200 µg/g
indicate moderate EPI. Levels less than 100 µg/g indicate severe EPI.23, 24 Fecal elastase-1 enzyme has high
stability at room and cold storage temperatures23
and has demonstrated high specificity (96%) and sensitivity (100%) for the
detection of EPI in children with cystic fibrosis.24
Patients were admitted to the inpatient General Clinical Research Center
at The Children's Hospital of Philadelphia for the 72-hour stool and dietary
fat sample collections, which were performed while the patient consumed a
diet containing 3 g of fat per kilogram of body weight (maximum, 100 g). Percent
coefficient of fat absorption (%CoA) was calculated according to the following
formula:
The normal range of %CoA is 93% or greater.10
The stool analysis was conducted using the method of Jeejeebhoy et al15 (Mayo Clinic Laboratories).
The hormone-stimulated pancreatic test was performed using a modified
technique. After a 6-hour fast, a double-lumen nasoduodenal tube was inserted
through the nose and positioned in the duodenum with fluoroscopic guidance.
Pancreatic and duodenal secretions mixed with infused marker was aspirated
by low-pressure suction before, during, and after infusing intravenous secretin
and cholecystokinin at doses known to cause maximal pancreatic secretion (secretin,
0.033 µg/kg per dose, and cholecystokinin, 0.2 µg/kg per dose).
No sedation was required.
STATISTICAL ANALYSIS
To compare growth of children of different sexes and ages, the weight,
height, and upper arm anthropometry data are expressed in mean ± SD z scores. z Scores for height
for age (HAZ), weight for age (WAZ), and weight for height (WHZ) were computed
using an anthropometric software program (version 3.1; Division of Nutrition,
Centers for Disease Control and Prevention, Atlanta, Ga). z Scores for triceps skinfold (TSFZ) and upper arm muscle area (UAMAZ)
were computed using US reference data.20 Patients
were grouped according to HIV RNA viral load tertile ranges of less than 40
to 3000, 3001 to 30 000, and greater than 30 000 copies/mL. A descriptive
analysis was performed to assess the prevalence and 95% confidence intervals
(CIs) of steatorrhea and EPI. Differences in growth variables (WAZ, HAZ, WHZ,
TSFZ, and UAMAZ) between patients with and without steatorrhea were examined
using the t test. The  2 test was
used to test associations between steatorrhea and HIV RNA viral load tertile
and CD4 status (normal, moderately suppressed, and severely suppressed). Pearson
correlation was used to examine associations between age and growth variables.
Statistical significance was defined as P .05.
All analyses were performed using statistical software (Stata 5.0; Stata Corp,
College Station, Tex).
RESULTS
Of 65 children within the age range of interest, 44 (23 girls [52%])
enrolled in the study. Participants were aged 7.4 ± 3.1 years, and
their growth characteristics were as follows: HAZ, –0.70 ± 1.36;
WAZ, –0.40 ± 1.20; WHZ, –0.17 ± 1.34; TSFZ, –0.19
± 0.65; and UAMAZ, –0.05 ± 1.23. None of the study patients
had hepatobiliary disease. Reasons for nonparticipation included disinterest
in the study (n = 14) and foster care (n = 7). Nonparticipants were aged 6.7
± 4.0 years, and their growth characteristics were as follows: HAZ,
–0.36 ± 1.28; WAZ, 0.08 ± 1.54; and WHZ, 0.23 ±
1.23 (not statistically significantly different from study patients). Two
patients had chronic (>2 weeks) pathogen-negative diarrhea at the time of
stool sample collection. One patient had Mycobacterium avium-intracellulare infection complicated by acute pancreatitis at the time of stool sample
collection. Levels of HIV RNA ranged from less than 40 to 900 000 copies/mL.
There were 11 patients with HIV RNA viral loads in the tertile range of less
than 40 to 3000 copies/mL and 10 each with HIV RNA viral loads in the tertile
ranges of 3001 to 30 000 and greater than 30 000 copies/mL. The
CD4 status was normal in 17 patients (55%), moderately suppressed in 11 (35%),
and severely suppressed in 3 (10%).
Thirty-three patients provided fecal specimens for analysis, and their
clinical characteristics are shown in Table
1. The prevalence of steatorrhea by Sudan III qualitative stain
was 39% (95% CI, 23%-56%). There were no significant associations between
presence of steatorrhea and any of the growth variables (HAZ, WAZ, WHZ, TSFZ,
and UAMAZ), HIV RNA viral load, and CD4 status (Table 1). No patient had both steatorrhea and decreased FE-1 levels
in the range for EPI. Only 2 patients had FE-1 levels in the range for EPI.
One was a 9-year-old girl with chronic pathogen-negative diarrhea (negative
for Giardia, Clostridium difficile, Cryptosporidium, Salmonella,
Shigella, Yersinia, Campylobacter, Plesiomonas, and Aeromonas), impaired growth (HAZ, –4.06; WAZ, –2.50; and
WHZ, 0.38), and an FE-1 level of 174 µg/g. Her %CoA was 96% (normal, 93%).
The hormone-stimulated pancreatic test results showed normal pancreatic enzyme
and electrolyte output, and, therefore, EPI was excluded. The second patient
was an 8-year-old boy with Mycobacterium avium-intracellulare infection complicated by acute pancreatitis with an FE-1 level of
170 µg/g. His FE-1 level after recovery from the Mycobacterium avium-intracellulare infection was normal (593 µg/g),
and further testing for EPI was not performed. Therefore, in this sample of
children with perinatally acquired HIV infection, the prevalence of EPI was
0% (95% CI, 0%-9%).
|
|
|
|
Table 1. Clinical Characteristics of 33 Patients Who Provided Fecal
Specimens for Analysis*
|
|
|
Older patients had significantly lower HAZ than younger patients (Figure 1). There was a significant trend
for HAZ to decline with advancing chronological age (r
= -0.42; P = .006). No similar trend was observed
with the other growth variables: WAZ, P = .2; WHZ, P = .3; TSFZ, P = .8; and UAMAZ, P = .5.
|
|
|
|
Correlation between height-for-age z score and age in
children with perinatally acquired human immunodeficiency virus infection
(r= -0.42, P= .006).
|
|
|
COMMENT
In this sample of children with perinatally acquired HIV infection,
steatorrhea was prevalent but had no consistent association with EPI, growth
variables, HIV RNA viral load, CD4 status, or type of antiretroviral therapy.
These findings suggest that steatorrhea, although prevalent in our sample,
was of unclear clinical significance.
Steatorrhea from EPI occurs when pancreatic lipase output is less than
10% of normal.25, 26 Kapembwa et
al3 and Carroccio et al5
independently reported an association among HIV infection, fat malabsorption,
and pancreatic function. Using the 14C-triolein breath test, Kapembwa
et al3 detected fat malabsorption in 48% of
25 adults with HIV infection. Further evaluation with the tyrosyl–p-aminobenzoic acid test (PABA) revealed that 3 patients
(12%) had mild pancreatic insufficiency.3 One
of the 3 patients also had cryptosporidial enteritis, which may be associated
with PABA malabsorption and therefore a false-positive test result for EPI.
In the study by Carroccio et al,5 47 children
with HIV infection were evaluated for steatorrhea and pancreatic function
using the acid steatocrit test and the FE-1 and fecal chymotrypsin tests,
respectively. Steatorrhea was detected in 25% of their sample, and the severity
was inversely correlated with FE-1 levels (levels >200 µg/g inclusive).
They found no correlation among FE-1 levels, clinical symptoms, immunologic
variables, or nutritional status. In our study, confirmatory testing was pursued
when FE-1 levels were in the range for EPI (Table 2). These findings suggested that in children with perinatally
acquired HIV infection, FE-1 less than 200 µg/g without further confirmatory
testing is inadequate for making the diagnosis of EPI.
|
|
|
|
Table 2. Test Results in 33 Patients Who Provided Fecal Specimens for
Analysis*
|
|
|
The Sudan qualitative fecal fat test is reliable for detecting quantitative
steatorrhea in the range of 35 mmol or more (approximately 10 g) per 24 hours
of stool,22 and when the %CoA is less than
94%11 (normal, 93%).10
The absence of EPI and hepatobiliary disease in our sample of children with
HIV infection implied that the qualitative steatorrhea had other causes, eg,
small-bowel enteropathy and bacterial overgrowth. There is also the possibility
that the qualitative test may have falsely classified some fecal samples as
positive for steatorrhea.11 Nonetheless, numerous
investigators have similarly detected evidence of fat malabsorption in patients
with HIV infection using the qualitative fecal fat test,1, 8
quantitative fecal fat test,1, 4
acid steatocrit test,4, 5, 27
serum carotene level,28 tyrosyl-PABA test,3 and triolein breath test.3, 5
Partial jejunal villous atrophy can occur at any clinical stage of HIV infection
and has been associated with fat malabsorption.29
Altered lipid transport across the duodenal mucosa leading to fat malabsorption
also has been reported with HIV infection.30
The HIV itself is a primary enteric pathogen and may cause histological inflammation
in the absence of other enteric pathogens.31, 32
Fat malabsorption in HIV infection might not always be accompanied by
clinical symptoms.1, 27 There was
no consistent association between steatorrhea and impaired growth in our sample
of children with HIV infection. Mean z scores for
height and weight were less than zero, thereby documenting that growth was
generally impaired compared with the National Center for Health Statistics
reference population.33 There was a significant
trend of declining HAZ with advancing chronological age, but a similar trend
was not observed with WAZ, WHZ, TSFZ, and UAMAZ. The decline in HAZ with advancing
chronological age in study patients was not explained by delayed pubertal
growth because most patients (>90%) were younger than the average age for
progression into puberty. Two possible explanations for this significant trend
are (1) a direct impact of chronic HIV infection on growth, leading to a cumulative
decline in HAZ as infected children get older, or (2) unavailability of highly
active antiretroviral therapy (HAART) during infancy and early childhood in
patients born before 1996.34 In general, patients
with decreased HAZ were older children born before HAART become widely available.34 Therefore, less effective control of HIV viral load
during the critical growth periods of infancy and early childhood may have
contributed to stunted growth patterns. Conversely, better control of HIV
viral load using HAART initiated early in infancy may have led to a decreased
impact of the disease on the linear growth patterns of patients born after
1996. Therefore, availability and use of HAART may be heralding a positive
change from the impaired growth patterns and devastating clinical manifestations
previously commonly observed in children with perinatally acquired HIV infection.
The main limitations of this study are related to its cross-sectional
design. The duration and impact of steatorrhea on individual growth patterns
was not specifically examined. The degree of steatorrhea was also not quantified;
however, a positive Sudan III qualitative fecal fat test result generally
corresponds to a %CoA of less than 94%11 and
quantitative steatorrhea in the range of 4 or more to 10 g of stool fat per
24 hours.22 These data suggest that although
the Sudan III qualitative test provides convenient, rapid, and noninvasive
screening, a positive result represents broad ranges of quantitative steatorrhea.
Therefore, the wide sensitivity range of the Sudan III qualitative test may
have limited our ability to detect any associations between steatorrhea and
growth patterns in this sample of children with perinatally acquired HIV infection.
Finally, inferring a trend of impaired linear growth with advancing chronological
age using cross-sectional data, and in the absence of information about genetic
input to linear growth (biological parental heights) has limitations. Nonetheless,
comparisons with the National Center for Health Statistics reference data
indicated that the linear growth in this sample of children with perinatally
acquired HIV infection was decreased.
In conclusion, in this sample of children with perinatally acquired
HIV infection, there was a high prevalence of steatorrhea (39%) that was neither
secondary to EPI nor consistently associated with impaired growth, HIV RNA
viral load, CD4 status, or type of antiretroviral therapy. Therefore, the
clinical significance of steatorrhea in children with HIV infection is unclear.
Furthermore, its evaluation should focus on nonpancreatic-based causes. Even
with improved HAART, continual close monitoring of growth is essential for
optimal care of children with HIV infection.
AUTHOR INFORMATION
Accepted for publication September 26, 2000.
This study was supported in part by grant RR00240 from the General Clinical
Research Center and by the Nutrition Center at The Children's Hospital of
Philadelphia.
We thank Hans Scheefers, PhD, at ScheBo-Tech for conducting all the
fecal elastase-1 enzyme assays; the children and families participating in
this study; and the staff of the General Clinical Research Center at The Children's
Hospital of Philadelphia for processing and triaging the fecal specimens.
From the Divisions of Gastroenterology and Nutrition (Drs Sentongo,
Stettler, Stallings, and Mulberg) and General Pediatrics (Drs Rutstein and
Rudy), The Children's Hospital of Philadelphia, University of Pennsylvania
School of Medicine, Philadelphia. Dr Sentongo is now with the Division of
Gastroenterology, Hepatology, and Nutrition, Children's Memorial Medical Center,
Northwestern University School of Medicine, Chicago, Ill.
Corresponding author and reprints: Timothy A. Sentongo, MD, Division
of Gastroenterology, Hepatology, and Nutrition, Children's Memorial Medical
Center, 2300 Children's Plaza No. 65, Chicago, IL 60614 (e-mail: TSentongo{at}childrensmemorial.org).
REFERENCES
| |
1. Koch J, Yvette L, Garcia-Shelton YL, et al. Steatorrhea: a common manifestation in patients with HIV/AIDS. Nutrition. 1996;12:507-510.
FULL TEXT
|
ISI
| PUBMED
2. Seidman EG, Russo P. Gastrointestinal manifestation of AIDS and other secondary immunodeficiencies. In: Walker WA, Durie PR, Hamilton JR, Walker-Smith JA, Watkins JB,
eds. Pediatric Gastrointestinal Disease. 2nd ed.
St Louis, Mo: Mosby–Year Book Inc; 1996:609-623.
3. Kapembwa MS, Fleming SC, Griffin GE, et al. Fat absorption and exocrine pancreatic function in human immunodeficiency
virus infection. Q J Med. 1990;74:49-56.
4. Spagnuolo MI, Carroccio A, Fontana M, et al. Pancreatic dysfunction in children with symptomatic HIV infection. Abstract presented at: the 30th Annual ESPGAN Meeting, May 21-24,
1997; Thessaloniki, Greece. Poster 98.
5. Carroccio A, Fontana M, Spagnuolo MI, et al. Pancreatic dysfunction and its association with fat malabsorption in
HIV infected children. Gut. 1998;43:558-563.
FREE FULL TEXT
6. Machado FR, Coelho LGV, Chausson Y, et al. Fat malabsorption assessed by 14C-triolein-breath test in
HIV-positive patients in different stages of infection: is it an early event? Int Conf AIDS. 1996;11:26. Abstract Mo.B.24.
7. Heller TD, Tierney AR, Kotler DP. Variable localization of intestinal cryptosporidosis in AIDS. Int Conf AIDS. 1989;5:358. Abstract W.B.P.38.
8. Craig GB, Darnell BE, Weinsier RL, et al. Decreased fat and nitrogen losses in patients with AIDS receiving medium-chain-triglyceride-enriched
formula vs those receiving long-chain-triglyceride containing formula. J Am Diet Assoc. 1997;97:605-611.
FULL TEXT
|
ISI
| PUBMED
9. American Academy of Pediatrics, Committee on Pediatric AIDS. Perinatal human immunodeficiency virus testing. Pediatrics. 1995;95:303-307.
FREE FULL TEXT
10. Van De Kamer JH, Weijers HA. Malabsorption syndrome. Fed Proc. 1961;S7:335-344.
11. Drumey GD, Benson JA, Jones CM. Microscopical examination of the stool for steatorrhea. N Engl J Med. 1961;264:85-87.
12. Sziegoleit A, Linder D. Studies on the sterol-binding capacity of human pancreatic elastase. Gastroenterology. 1991;100:768-774.
ISI
| PUBMED
13. Stein J, Jung M, Sziegoleit A, et al. Immunoreactive elastase 1: clinical evaluation of a new noninvasive
test of pancreatic function. Clin Chem. 1996;42:222-226.
FREE FULL TEXT
14. Löser C, Möllgaard A, Fölsch UR. Fecal elastase 1: a novel, highly sensitive, and specific tubeless
pancreatic function test. Gut. 1996;39:580-586.
FREE FULL TEXT
15. Jeejeebhoy KN, Ahmad S, Kozak G. Determination of fecal fats containing both medium and long chain triglycerides
and fatty acids. Clin Biochem. 1970;3:157-163.
ISI
| PUBMED
16. Durie PR. Pancreatic function tests. Med Clin North Am. 1988;20:3842-3845.
17. Centers for Disease Control and Prevention. 1994 Revised classification system for human immunodeficiency virus
in children less than 13 years of age. MMWR Morb Mortal Wkly Rep. 1994;43(R-12):1-10.
18. Hodinka RL. The clinical utility of viral quantitation using molecular methods. Clin Diagn Virol. 1998;10:25-47.
FULL TEXT
|
ISI
| PUBMED
19. Lohman TG, Roche AR, Martorell R. Anthropometric Standardization Reference Manual. Champaign, Ill: Human Kinetics; 1988.
20. Frisancho A. New norms of upper limb fat and muscle areas for assessment of nutritional
status. Am J Clin Nutr. 1981;34:2540-2545.
FREE FULL TEXT
21. Khouri MR, Huang G, Shiau YF. Sudan stain of fecal fat: new insight into an old test. Gastroenterology. 1989;96:421-427.
ISI
| PUBMED
22. Ghosh SK, Littlewood JM, Goddard D, et al. Stool microscopy in screening for steatorrhea. J Clin Pathol. 1977;30:749-753.
FREE FULL TEXT
23. Wallis C, Leung T, Cubbit D, Reynolds A. Stool elastase as a diagnostic test for pancreatic function in children
with cystic fibrosis [letter]. Lancet. 1997;350:1001.
FULL TEXT
|
ISI
| PUBMED
24. Soldan W, Henker J, Sprossig C. Sensitivity and specificity of quantitative determination of pancreatic
elastase-1 in feces of children. J Pediatr Gastroenterol Nutr. 1997;24:53-55.
FULL TEXT
|
ISI
| PUBMED
25. DiMagno EP, Go VLW, Summerskill WHJ. Relations between pancreatic enzyme output and malabsorption in severe
pancreatic insufficiency. N Engl J Med. 1973;288:813-815.
26. Gaskin KJ, Durie PR, Lee L, et al. Colipase and lipase secretion in childhood-onset pancreatic insufficiency:
delineation of patients with steatorrhea secondary to relative colipase deficiency. Gastroenterology. 1984;86:1-7.
ISI
27. Italian Paediatric Intestinal/HIV Study Group. Intestinal malabsorption of HIV-infected children: relationship to
diarrhea, failure to thrive, enteric micro-organisms and immune impairment. AIDS. 1993;7:1435-1440.
ISI
| PUBMED
28. Ulrich R, Schneider T, Heise W, et al. Serum carotene deficiency in HIV-infected patients. AIDS. 1994;8:661-665.
ISI
| PUBMED
29. Miller AR, Griffin GE, Batman P, et al. Jejunal mucosal architecture and fat absorption in male homosexuals
infected with human immunodeficiency virus. Q J Med. 1988;69:1009-1019.
30. Benhamou Y, Hilmarsdottir I, Desportes-Livage I, et al. Association of lipid accumulation in small intestinal mucosa with decreased
serum triglyceride and cholesterol levels in AIDS. Dig Dis Sci. 1994;39:2163-2169.
FULL TEXT
|
ISI
| PUBMED
31. Ehrenpreis ED, Patterson BK, Brainer JA, et al. Histopathological findings of duodenal biopsy specimens in HIV-infected
patients with and without diarrhea and malabsorption. Am J Clin Pathol. 1992;97:21-28.
ISI
| PUBMED
32. Reka S, Kotler DP. An inflammatory bowel disease associated with HIV infection [abstract]. Gastroenterology. 1990;98:471A.
33. Centers for Disease Control and Prevention. CDC standard deviation–derived growth reference curves derived
from NCHS/CDC reference population: NCHS growth curves for children, birth
to 18 years. Atlanta, Ga: Centers for Disease Control and Prevention; 1996. US
Ser. 11-No. 165. DHEW publication (PHS)78-1650.
34. Palella FJ, Delaney KM, Moorman AC, et al. Declining morbidity and mortality among patients with advanced human
immunodeficiency virus infection. N Engl J Med. 1998;338:853-860.
FREE FULL TEXT
THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES
HIV infection and the pancreas: risk factors and potential management guidelines
Manfredi and Calza
Int J STD AIDS 2008;19:99-105.
ABSTRACT
| FULL TEXT
|
