A Qualitative Assessm ent o f Biotinidase D eficien cy*
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1 ANNALS OF CLINICAL AND LABORATORY SCIENCE, Vol. 17, No. 6 Copyright 1987, Institute for Clinical Science, Inc. A Qualitative Assessm ent o f Biotinidase D eficien cy* D A N IEL D. BANKSON, P H.D.,t RANDOLPH P. MARTIN, B.A.,t and DONALD T. FORM AN, P H.D.fi University o f North Carolina School o f Medicine, North Carolina Memorial Hospital, Departments of fhospital Laboratories, $Pathology, and Biochemistry and Nutrition, Chapel Hill, NC ABSTRACT Screening program s for late-onset, biotin-responsive, m ultiple carboxylase deficiency (LM CD) detect colormetrically the presence of biotinidase activity in dried samples of whole-blood spotted on filter-papers as used in the neonatal screening of phenylketonuria. A sensitive and stable qualitative technique is described using 10 (xl of serum that avoids problem s associated with poor sample collection, im proper drying of blood-spots and transient color developm ent. The m odified assay is tim ely and suitable for th e clinical laboratory not involved in mass screening program s. Introduction Patients initially characterized as having late-onset biotin-responsive m ultiple carboxylase deficiency w ere shown by W olf and colleagues in to have a deficiency of the enzym e biotinidase (b io tin a m id e a m id o h y d ro la s e, E C ) in serum. This enzym e catalyzes the removal and release of free biotin which is recycled from biocytin (e-nbiotinyl-l-lysine) or from biotinylated peptides produced by the norm al degradation of b io tin -d e p e n d e n t carboxyl * Address reprints to: Daniel D. Bankson, Ph.D., Clinical Chem istry Laboratories, North Carolina M em orial H ospital, 1071 PST, C hapel Hill, NC ases12 (figure 1). B iotin is covalently bound through lysine to the carboxylases and functions as the C 0 2 recep to r in enzymatic carboxylation reactions. The four hum an carboxylases are crucial in fatty acid biosynthesis, gluconeogenesis, leucine m etabolism and propionic acid oxidation.8 A deficiency of biotinidase activity is in h e rite d as an au to so m al-recessiv e trait.1 Deficient infants usually begin to show clinical signs several months after birth (onset at three to six months, but may be delayed up to 24 months).7 The untreated child may ultim ately develop a variety of derm atologic, neurologic, m etabolic, and im m unologic abnorm alities followed by coma or death (table I). The neurologic or cutaneous signs may occur in the absence of m etabolic acidosis or /87/ $00.90 Institute for Clinical Science, Inc.
2 SERUM BIOTINIDASE B io t in a m id e A in id o h v d r o ía s e ( B i o t i n i d a s e ) (EC ) B i o t i n i d a s e e - N - b i o t i n y l - L - l y s i n e ( p e p t i d e s )- - > b i o t i n + l y s i n e ( p e p t i d e s ) ph 6. 0 F ig u r e 1. Biotinidase specifically cleaves th e amide bond betw een the epsilon am ino group of lysine and th e carboxyl group of biotin. detectable organic aciduria.14 Therefore, definitive diagnosis requires th e dem onstration of the enzym e deficiency. The purpose of our paper is to present a sim ple, rapid diagnostic test for biotinidase deficiency which utilizes 1 0 jjli of serum in place of dried, blood-saturated paper disks currently used in pediatric and neonatal screening program s. M aterials and Methods T he biotinidase assay involves incubation of 10 jjli of patient sera, standards, and positive controls in 30 (xl of potassium phosphate buffer [(50 mmol per 1, p H 6.0) contain in g 54 m g p e r I (140 H-mol per 1) of synthetic substrate N-biotinyl-p-am inobenzoate (or biotin-4-amidobenzoic acid*), 250 mg per 1 (3.6 (xrnol p er 1) bovine serum albumin, and 1.85 g p er 1 (5.0 mmol p er 1) disodium ethylenediam ine tetraacetic acid (EDTA)] at 37 C for four to 24 h r (table II). The incubations are carried out in a w ater bath using floating polystyrene reaction traysf containing 20 dim ple wells each with 750 (xl capacity and sealed with an adhesive covering to p re v e n t evaporation. Sera from at least four patients can be ru n in duplicate w ith controls and reagent blanks. O ur m ethod for serum biotinidase is a modification of a procedure described by H eard et al4 that used a three mm bloodspot p unched from a phenylketonuria (P K U ) s c re e n in g c a rd (c o n ta in in g * Sigma Chemical Co., St. Louis, MO t Abbott Diagnostics, N. Chicago, IL, approximately three fxl of blood). In the blood-spot procedure, the reaction trays are covered and incubated in a hum idified cham ber for 16 hr. In ou r ex p erien ce, th e final color was tra n sien tly d etectable for approxim ately 30 min. In the present procedure after incubation of sera and substrate, the reaction was stopped by adding to each reaction well 30 fxl of 30 percent (1.84 mol per 1) trichloroacetic acid. For color developm ent, the following reagents w ere added sequentially with a dispensing pipet at three m inute intervals: 30 jjli of 1.0 g per 1 (14.5 mmol/1) sodium nitrate, 30 (jli of 5.0 g per 1 (43.8 mmol per 1) ammonium sulfamate, and 30 xl of 1.0 g p er 1 (3.86 m m ol p e r 1) N -l-n a p th y le th y le n e d i- am ine dihydrochloride (table III). Color developm ent was com plete w ithin five m inutes following addition of the last reag en t. Those sam ples th at becam e pink-purple w ere considered to have biotinidase activity; those that rem ained TABLE I Clinical Findings in Biotinidase Deficiency O n s e t: Three to six months (may be delayed up to 24 months or longer) D e r m a to l o g ic a l: Skin rash Alopecia, Ke ratoconjunc tivi ti s N e u r o l o g i c a l : Seizures and myoclonis Hypotonia and tremor Developmental delay Hearing loss Optic atrophy M e ta b o l ic a n d Im m u n o lo g ic : Acidosis and organic aciduria Immune defects (candidiasis, recurrent infections)
3 4 2 6 BANKSON, MARTIN, AND FORMAN T A B L E II Incubation Procedure for Biotinidase Assay* Serum, Control or P A B A Standard (Hi) Subs tra te (B-PABA) (ìli) P h o s p h a te Buffer (Ul) Patient _ Serum Patient S e r u m Blank Positive Control Control Blank PABA Standard Reagent 40 B l a n k *After all the reagents are dispensed, the tray wells are covered w i t h adhesive covering, a g i t a t e d for 30 seconds, a n d incubated at 37*0 f r o m 4 to 24 hours. See table 3 for developing reaction. P A B A = para-aminobenzoic acid B-PABA = biotinyl-para-aminobenzoic acid clear or straw-colored were considered to have little or none. The final color was stable for at least 48 hr at 4 C. R esults and Discussion Biotinidase catalyzes the cleavage of biotinyl-p-am inobenzoate to biotin and para-am inobenzoate (PABA). After stopping th e reaction w ith trichloroacetic acid, the amino group of PABA released via the action of biotinidase is diazotized and coupled with N -l-naphthyethylenediam ine h y drochloride. The azo dye form ed (pink-purple) is clearly visible to the eye. The final reaction color is stable and can be visually graded (table IV) or followed spectrophotom etrically at 546 nm to give sem i-quantitative results. A fter incubation and developm ent, sam ples are classified either as norm al (having biotinidase activity) or abnormal, based on th e color of the reaction mixture. Abnormal samples are subclassified in to th r e e g ro u p s, d e p e n d in g on w h e th e r th e reaction m ixture is palepurple, very pale-purple, or straw-colored. If an abnorm al result is obtained w ith a second repeat of the sam ple, a n ew seru m sam p le is o b ta in e d and tested. If an abnormal result is obtained again, a fresh sam ple is pro cu red for quantitative determ ination of biotinidase activity. Several quantitative procedures are available using fluorescence d etectio n,10 high perform ance liquid chrom a tography w ith fluorescent detection,3 or radioassay using 15N-biotinyl-para-am i- n o b e n z o a te o r 14C -b io c y tin as th e la b e le d s u b s tr a te.913 B oth kinds of assays have been found useful for quantitative m easurem ent of biotinidase activity in norm al p erip h eral blood leukocytes and fibroblasts. E v a l u a t io n o f t h e S c r e e n in g M e t h o d A reliable screening test should detect all affected individuals without false-positives. In general, false-positive tests have a smaller impact than do false-negative results. The econom ic and em o tional costs of follow-up testing are small com pared with failure to detect an infant or child with this disorder. The overall ra te of o c c u rre n c e o f fa lse -p o sitiv e results (those req u irin g a second confirming assay) as reported by H eard et al5 was 0.09 percent. This rate compares favorably w ith false-positive rates (0.005 T A B L E I I I Post-Incubation Development Procedure R e a g e n t Time I n t e r v a l 3 0 il 1. 8 m o l / 1 0 m i n T r i c h l o r o a c e t a t e 3 0 ill m m o l / 1 3 m i n S o d i u m n i t r i t e 30 ill m m o l / 1 3 m i n A m m o n i u m s u l f a m a t e 30 ul 3. 9 m m o l / 1 3 m i n * N N a p thy e t h y l e n e d i a m i n e - d i h y d r o c h l o r i d e * P i n k -purple c o l o r : N o r m a l b i o t i n i d a s e a c t i v i t y. C l e a r t o s t r a w - c o l o r e d : a c t i v i t y. D e f i c i e n t b i o t i n i d a s e
4 SERUM BIOTINIDASE TABLE IV Sensitivity and Qualitative Grading of Biotinidase Activity Using Para-aminobenzoic Acid Para-aminoJoenzoic A c i d * (nmoles) Intensity G r a d e f / *Para-am inobenzoic a c id added p e r tr a y w e ll. ^Qualitative grading o f the c o lo r produced by the Br a t t o n - M a r s h a l l reaction (Bratton, A.C. and Marshall, E. K. : J. Biol. Chem. 125: , 1939). percent to 0.52 percent) for other inborn errors of m etabolism.6 The biotinidase screening test appears quite discrim inating. In our laboratory, after 70 assays, false-negative results were not apparent. These data com pare favorably with laboratories using th e blood-disk m ethod.4 C oncern regarding transplacental passage of m aternal biotinidase as a cause for false-negative results in the early neonatal p e rio d has not proven ju stifiable. For example, no blood biotinidase activity was detectable in a biotinidased e fic ie n t infant w ith a heterozygous m other.4 Thus, it is unlikely that falsenegative results will be a consequence of m aternal biotinidase transfer to the new born. However, transplacental transfer is an im p o rta n t co n sid eratio n for o th er inborn errors, such as phenylketonuria w here a m etabolite can rem ain elevated for several days after birth. False-negative results are m ore likely to occur as a result of drug interferences. For exam ple, sulfonam ide antibiotics react w ith the developing reagent to produce a pink-purple color.2 Therefore, an affected child receiving sulfonamides m ight appear as having enzyme activity. Fortunately, the presence of interfering compounds can be readily detected by running a blank serum in buffer without added substrate. This latter procedure is a routine com ponent of our procedure. Since th ere w ere no false-negative results, it can be concluded tentatively th a t th e sen sitiv ity of th e te st m ust approach 100 percent. The specificity is defined as the probability that the test will be negative when the disease is not present. By these criteria, the specificity after screening and repeat screening is greater than percent. Problem s associated with poor blood spot collection tech n iq u e, including in co m p lete satu ratio n of a section of punched filter paper disk, are avoided using serum. Likewise, H eard et al have also reported some inconsistent results from disks dried im properly.5 C o s t o f T e s t in g The cost p er test per child is relatively inexpensive since the laboratory technologist requires approximately one hour to com plete four assays in duplicate. Using mass screening m ethods and punched disks, H eard et al5 have calculated costs at $0.24 per child assayed including analysis, reagent preparation, and com m unicating with the physician. Sum m ary B io tin id a s e d e fic ie n c y is re a d ily dem onstrable by colorim etric assay of the enzym e in serum using a synthetic substrate, N -biotinyl-p-am inobenzoic acid. This direct, functional assay has been modified and adapted in a low-cost screening m ethod for neonates and children. The procedure can be com pleted in from four to 24 hr. Biotinidase deficiency testing fits the accepted criteria fo r in c lu s io n in r o u tin e m e ta b o lic screening program s since it has significant incidence (1:40,000), excellent sensitivity (100 p e rcen t), and specificity (>99.99 percent). The deficiency usually rem ains unrecognized clinically until serious symptoms occur; it is life-threatening, and early treatm ent with biotin is effective.14
5 4 2 8 liankson. MAHÏÏN, ANI) KOIIMAN R eferences 1. B a u m g a r t n e r, E. R., S u o r m a l a, T., W ic k, 11., B a u s c h, J., and B o n j o u r, J. P.: Biotinidase deficiency: Factors responsible for the increased biotin requirem ent. J. Inherit. M etab. Dis. S(Suppl. l):59-64, B r a t t o n, A. C. and M a r s h a l l, E. K.: A new coupling component for sulfanilamide determ i nation. J. Biol. Chem. 128: , H a y a k a w a, K. and O i z u m i, J.: Determination of biotinidase activity by liquid chromatography w ith fluorim etric detection. J. Chrom atogr. 383: , H e a r d, G. S., S e c o r M c V o y, J. R., and W o l f, B.: A screening m ethod for biotinidase deficiency in newborns. Clin. Chem. 30: , H e a r d, G. S., W o l f, B., J e f f e r s o n, L. G., W e is s b e c k e r, K. A., N a n c e, W. E., S e c o r M c V o y, J. R., N a p o l it a n o, A., M i t c h e l l, P. L., L a m b e r t, F. W., and L in y e a r, A. S.: Neonatal screening for biotinidase deficiency: R esults of a 1 year pilot study. J. Pediatr. 108:40-46, M a c h il l, G. and K n a p p, A.: Organization and cost-benefit analysis of screening for metabolic disorders in G.D.R. Neonatal Screening. Naru se, H. and Irie, M., eds. A m sterdam : Excerpta Medica, 1983, pp Pa c k m a n, S., S w e e t m a n, L., Yo s h i n o, M., B a k e r, H., and C o w a n, M.: Biotin-responsive m ultiple carboxylase deficiency of infantile onset. J. Pediatr..9.9: , S w is e t m a n, L. and N y h a n, W. L.: Inheritable biotin-treatable disorders and associated phenomena. Annu. Rev. Nutr. 6: , T h u y, L. P, Z ie l in s k a, B., S w e e t m a n, L., and N y h a n, W. L.: D eterm ination of biotinidase activity in human plasma using [14C]biocytin as substrate. Ann. N Y Acad. Sci. 447:434, W a s t e l l, H., D a l e, G., and B a r t l e t t, K.: A sensitive fluorimetric rate assay for biotinidase using a new derivative of biotin, biotinyl-6- aminoquinoline. Anal. Biochem. 140:69-73, W o l f, B., G r ie r, R. E., A l l e n, R. J., G o o d m a n, S. I., and K i e n, C. L.: Biotinidase deficiency: The enzymatic defect in late-onset multiple carboxylase deficiency. Clin. Chim. Acta 131: , W o l f, B., G r ie r, R. E., S e c o r M c V oy, J. R., a n d H e a r d, G. S.: B io tin id a s e d e fic ie n c y. A n o v e l v i t a m i n r e c y c l i n g d e f e c t. J. I n h e r i t. M e ta b. D is. 8 (S u p p l. 1):53 58, W o l f, B. and S e c o r M c V oy, J.: A sensitive radioassay for biotinidase activity in tissues of serum biotindase-deficient individuals. Clin. Chim. Acta 135: , W o l f, B., H e a r d, G. S., J e f f e r s o n, L. G., P r o u d, V. K., N a n c e, W. E., and W e i s s b e c k e r, K. A.: Clinical findings in four children with biotinidase deficiency detected through a statew ide neonatal screening program. New Engl. J. Med. 313:16-19, STATEMENT OF OWNERSHIP. MANAGEMENT AND CIRCULATION (Act of October 23, I«62. Section Title 39. United States Code) Date of Filing September 30, 1987 Title of Publication ANNALS OF CLINICAL AND LABORATORY SCIENCE Frequency of Issue Bimonthly Location of Known Office of Publication 230 N. Broad St. Philadelphia. RA Location of the Headquarters or General Business Offices of the Publisher Same us al>ove Publisher Institute for Clinical Sciences, Inc. Editor F. William Sunderman, M.D., Ph.D. Managing Editor Same as above Owner Institute for Clinical Sciences, Inc. Known Bondholders, Mortgagees, and Other Security Holders Owing or Holding 1 Percent or More of Total Amount of BmuU. Mortgage» or Other Securities None Average No. Copies Each Issue During. Preceding 12 Months Actual Number of Copies of Single Issue Published Nearest to Filing Date A. Total No. Copies Printed {Net Press finn) B. Paid Circulation I. Sales Through Deaters and Carriers. Street Vendors and Counter Sales None None 2. Mail Subscriptions L(K C. Total Paid Circulation D. Free Distribution by Mail, Carrier or Other Means, Samples, Complimentary, and Other Free Copies E. Total Distribution (Sum o f C and D) F. Copies not Distributed 1. Office Use, Left-over. Unaccounted Spoiled After Printing Returns from News Agents None None G. Total (Sum o f E and F should equal net press run xhoicn in A) certify that the statements made by me are correct and complete F. WILLIAM SUNDERMAN, M I), Ph.D.
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