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1999, a Cluster of Microvillous Inclusion Disease in the Navajo

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1999, a Cluster of Microvillous Inclusion Disease in the Navajo A cluster of microvillous inclusion disease in the Navajo population John F. Pohl, MD, Mitchell D. Shub, MD, Eric E. Trevelline, MD, Kristy Ingebo, MD, Gary Silber, MD, ANancy Rayhorn, RN, BSN, Steve Holve, MD, and Diana Hu, MD riod.1 The prognosis is generally poor, We report 4 unrelated patients with characteristic microscopic findings of with most patients dying by the second microvillous inclusion disease (MID) with early-onset phenotype. All 4 pa- decade of life as a result of complica- tients came from the Navajo reservation in northern Arizona. A literature tions of parenteral alimentation includ- 4 search revealed a fifth unrelated Navajo child with MID. The unusually ing liver failure or sepsis. Various high incidence in this population indicates that a founder effect might be re- treatments including glucocorticoids, sponsible for an increased frequency of this rare genetic disorder in the pentagastrin, human epidermal growth factor, disodium cromoglycate, adreno- Navajo. It is recommended that all Navajo infants presenting with severe corticotropic hormone, prednisolone, diarrhea during early infancy undergo investigation for MID. (J Pediatr and elemental formula feedings have 1999;134:103-6) failed.5-7 However, somatostatin, which is not universally successful,8 reduced stool output in 2 patients,9,10 with an increased weight velocity Microvillous inclusion disease, a rare children with a specific subset of in- noted in 1.10 Loperamide has only disorder with an unknown cause, re- tractable diarrhea and described com- transiently decreased stool output.1 sults in an intractable secretory diar- plete villous atrophy, crypt hypoplasia, Three patients have received intestinal rhea that begins in early infancy. MID absence of a brush border, and an in- or multivisceral transplantation.11-13 is characterized by histologic abnor- crease in the number of inclusions malities such as total villous atrophy, within the enterocytes that appeared MID Microvillous inclusion disease shortened microvilli, membrane- similar to lysosomal structures. Elec- bound inclusions, and increased num- tron microscopy has revealed a de- bers of secretory granules within en- crease in surface epithelial cell height Several reported cases of MID have terocytes.1 and characteristic membrane-bound occurred in members of the same family Avery et al2 first described infants inclusions containing microvilli found and also in children who were the result with intractable diarrhea in 1968 and in the apical aspect of the villous en- of a consanguineous marriage.3,14-16 In attempted to differentiate potential terocytes with normal appearance of this report a cluster of MID is described causes. In 1978 Davidson et al3 looked the crypt cells and basal enterocytes.4,5 involving 4 unrelated children from the at duodenal biopsy specimens of 5 The term “microvillous inclusion dis- Navajo nation in whom MID was diag- ease” was first used in 1989 to describe nosed within the past 8 years. A previ- From the Department of Pediatric Gastroenterology 9 children with such inclusions who ous report by others describes a fifth and Nutrition, Phoenix Children’s Hospital, Phoenix, had an autosomal recessive inheritance child with MID from the Navajo nation Arizona, and the Indian Health Service, Tuba City In- pattern.6 Polyhydramnios has typically who was unrelated to the children de- dian Medical Center, Tuba City, Arizona. not been noted before birth in patients scribed herein.13 Submitted for publication Apr 17, 1998; revi- sion Sept 21, 1998; accepted Sept 30, 1998. with MID, and until now there seems to be no racial predilection. There Reprint requests: Mitchell Shub, MD, Di- ASE EPORTS vision of Pediatric Gastroenterology and tends to be a female predominance. C R Nutrition, Phoenix Children’s Hospital, Symptoms usually develop in the first 909 East Brill St, Phoenix, AZ 85006. few days of life; however, late-onset Four unrelated Navajo children Copyright © 1999 by Mosby, Inc. MID has been described with symp- were given the diagnosis of MID at 0022-3476/99/$8.00 + 0 9/22/94846 toms developing after the neonatal pe- Phoenix Children’s Hospital. The pre- 103 POHL ET AL THE JOURNAL OF PEDIATRICS JANUARY 1999 DISCUSSION ing of 5 unrelated Navajo children with MID suggests an unexpectedly MID is a well-defined entity charac- high incidence in this population. The terized by intestinal villous atrophy, current Navajo population in the Unit- cellular disarray, absence of crypt hy- ed States is 225,000,20 and the average perplasia, and ultrastructural abnor- number of enrolled Navajo births has malities of enterocytes including in- been approximately 6000 per year over creased secretory granules, vacuolation the past decade.21 These 5 cases would in the apical cytoplasm, and microvilli suggest an incidence of MID in the that are isolated in intracytoplasmic in- Navajo as high as 1 per 12,000 live clusions.4,13,14 The cause of the intracy- births. toplasmic inclusions is unknown. Acid The high incidence of this disorder phosphatase, a lysosomal marker asso- in the Navajo may be the result of a ciated with degradation products, has “founder effect” in which a gene that not been associated with these inclu- is rare in the general population oc- sions.6 Decreased levels of myosin in curs in a small, isolated, and rapidly Figure. Representative transmission electron the brush border cytoskeleton have expanding population and leads to in- micrograph of small bowel from patient no. 1 showing characteristic microvillous inclusion in been found in MID, which suggests creased gene frequency and increased apical aspect of enterocyte (arrow). that myosin is unable to bind to the frequency of disease.22 Such founder base of microvilli; this might result in effects have been described in a num- defective assembly of microvilli and ber of populations that have remained natal course had been uneventful in all formation of inclusions.6,13,14,17 Al- isolated by geography, ethnicity, or cases. There was no family history of though MID usually affects the small religious preference.23-29 Navajo his- intractable diarrhea or consanguinity. intestine, previous reports have noted tory supports this hypothesis. In the All patients presented within the first similar findings in the gastric antrum, 1860s, during a period of warfare few days of life with high-output diar- gallbladder, renal tubular cells, colon, with the United States Army and sub- rhea (Table I), severe metabolic acido- and rectum.13,18 Abnormally low disac- sequent imprisonment, the Navajo sis, and dehydration. Infectious, en- charidase levels have been described in population underwent a reduction of docrine, and metabolic diseases were previous patients,5 as has an abnormal nearly 30%.30-31 After the Navajo Na- excluded, and intestinal biopsy speci- accumulation of periodic acid-Schiff tion was created in 1868 on their tra- mens were obtained. In all cases light staining in the apical cytoplasm be- ditional lands in the Southwestern microscopy of the duodenum revealed cause of the disrupted brush border.4 United States,32 the Navajo have villous atrophy with vacuolation of the Although it is possible that repeated thrived with a growth rate as high as surface enterocytes; periodic acid- hospitalizations and chronic illness 4% per year,33 making them the Schiff staining was increased in the may account for the delayed develop- largest Native American population in apical cytoplasm of the enterocytes. In ment noted in these patients (Table II), the United States.34 The remote loca- 2 of the patients disaccharidase analy- the cause is unknown and will require tion of the Navajo nation has caused sis revealed severe generalized disac- further study to determine whether it the population to remain geographi- charidase deficiency. Electron mi- is a previously unrecognized manifes- cally and genetically isolated. This croscopy revealed an increased tation of MID. scenario of a population “bottleneck” number of secretory granules in the The exact mode of inheritance of followed by genetic isolation and apical cytoplasm of the enterocytes, MID in the Navajo is unknown, but rapid growth are ideal conditions vacuolation of the surface enterocytes the presence of unaffected parents and under which a founder effect might with apical inclusions containing mi- disease in both males and females develop. This hypothesis is also sup- crovilli, and an absence of the brush strongly suggests an autosomal reces- ported by the finding of a number of border consistent with the diagnosis of sive inheritance. A previous study of other rare autosomal recessive illness- MID (Fig). Biopsy specimens of the children from the United Kingdom es found among the Navajo nation in- esophagus, stomach, and colon were with protracted diarrhea in infancy of cluding Navajo neuropathy, severe normal. One patient (no. 2) was treat- an unknown cause has shown an auto- combined immunodeficiency syn- ed with somatostatin and did not show somal recessive pattern and an inci- drome, and metachromatic leukodys- a favorable response to therapy. The dence of 1 in 200,000. However, these trophy.35-37 clinical course and outcome are shown patients had normal findings on jejunal Presuming that MID in the Navajo in Table II. biopsy by light microscopy.19 The find- is the result of a founder effect, then it 104 THE JOURNAL OF PEDIATRICS POHL ET AL VOLUME 134, NUMBER 1 Table I. Summary of characteristics of 5 Navajo patients with microvillous inclusion disease Stool Stool electrolytes output Birth Gestational Age at (mEq/L) (mL/kg/day) Patient weight age onset of No. Sex (kg) (wk) diarrhea (d) Na K Cl Fed Fasting 1 Male 3.5 39 6 110 7 85 175 95 2 Male 2.6 38 6 81 2 44 250 135-165 3 Male 3.3 36 6 115 5 96 150-175 125-175 4 Female 3.16 39 4 107 18 84 200-250 150-200 5 Female 2.7 37 4 6 27 150-250 100 Table II.
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