Laboratory Evaluation o f the A drenogenital Syndrom e
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1 ANNALS O F CLINICAL A N D LABORATORY SCIENCE, Vol. 15, No. 2 Copyright 1985, Institute for Clinical Science, Inc. Laboratory Evaluation o f the A drenogenital Syndrom e SHESHADRI NARAYANAN, P h.d. Department of Pathology, New York Medical College Metropolitan Hospital Center, New York, NY ABSTRACT The adrenogenital syndrom e is a result of the deficiency of one of the enzymes involved in the pathway leading to the synthesis of cortisol by the adrenal cortex. Laboratory evaluation of the adrenogenital syndrome involves m easurem ent of horm ones and metabolites accum ulated prior to the enzymic block as well as hormones whose synthesis is affected by deficiency of a specific enzyme. Laboratory m easurem ents of horm one metabolites in urine, because of their nonspecificity, lack of sensitivity, and m ultiple assay steps resulting in poor yield, have been supplanted by specific and sensitive radioimmunoassays of steroid hormones in plasma. In the laboratory evaluation of the adrenogenital syndrom e, problem s involved in some of the immunoassays of selected hormones should be addressed. Variables owing to specimen collection, storage and handling, and the assay itself should be minimized and controlled. Introduction The adrenogenital syndrom e results from the lack or deficiency of one of the many enzymes involved in the synthesis of cortisol by the adrenal cortex. The laboratory evaluation of the adrenogenital syndrome requires m easurem ent of p recursors or their m etabolites prior to the enzymatic step that is affected and also establishing the deficiency or excess of key biochem ical constituents resulting from a specific enzym atic defect. Characteristics of the A drenogenital Syndrom e T here are six varieties of th e adrenogenital syndrome, all of which lead to the dev elo p m en t of congen ital ad ren al hyperplasia. Ninety five percent of the cases of adrenogenital syndrom e rep o rted in the literatu re resu lt from a deficiency of the enzym e 2 1 -hydroxylase, 7 which can be either partial or complete. The adrenogenital syndrom e resulting from a partial deficiency of the enzyme 2 1 -hydroxylase leads to a sim ple virilizing form of congenital adrenal hyperplasia. The partial deficiency of 21-hydroxylase leads to lowered cortisol levels and an in creased ad ren o co rtico tro p ic h o r mone (ACTH) because of the feed-back effect of cortisol on ACTH. The increase in ACTH is of a m agnitude to restore levels of cortisol to normal. The increase in ACTH, coupled w ith th e p artial deficiency of 2 1 -hydroxylase, leads to /85/ $00.90 Institute for Clinical Science, Inc.
2 160 NARAYANAN increased accum ulation of cortisol p re cursors, such as 17-hydroxyprogesterone, progesterone and 2 1 -deoxycortisol. The accum ulation of 17-hydroxyprogesterone and progesterone would tend to result in loss of sodium. Sodium loss leads to increased renin synthesis and, since 2 1 -hydroxylase deficiency is p a r tial, aldosterone synthesis is increased to twice the normal levels stim ulated by the renin-angiotensin system. Thus, loss of sodium does not occur in the simple virilizing form of congenital adrenal h y p erplasia caused by a partial deficiency of 2 1 -hydroxylase, since increase in aldosterone counteracts the sodium losing te n dency. In creased ACTH leads to in creased synthesis of adrenal androgens, such as androstenedione; although not itse lf a p o te n t androgen, it is n e v e r theless partially converted to the potent androgen testosterone in the circulation. Increases in testosterone levels lead to virilization in the patient with a partial deficiency of 21-hydroxylase. Com plete deficiency of 2 1 -hydroxylase precludes the synthesis of both cortisol and aldosterone. Because of the accumulation of cortisol precursors and absence of aldosterone, sodium loss through diarrhea, vomiting, and dehydration occurs. There is also an in creased synthesis of adrenal an d ro gens. The third and more common form of adrenogenital syndrom e is the hypertensive form resulting from a deficiency of the enzyme 11-3-hydroxylase. In this condition, there is an accumulation of deoxycortisol (compound S), a precursor of cortisol and 1 1 -deoxycorticosterone (D O C ), a p recu rso r of co rtico stero n e (com pound B), which in tu rn is a p re cursor of aldosterone. The deficiency of cortisol resu ltin g from a lack of 1 1 -phydroxylase resu lts in an increase in ACTH and an accum ulation of cortisol p recu rso rs and adrenal androgens. Although aldosterone cannot be synthesized, sodium loss does not occur since excessive am ounts of desoxycortiosterone (D O C), w hich has salt retain in g p ro p ertie s, are p roduced. As a consequence, h y p ertensio n occurs in ll-(3- hydroxylase deficiency. Deficiency of the enzym e 17-hydroxylase results in im pairm ent of synthesis of cortisol, aldosterone, androgens and estrogens. The deficiency of aldosterone is com pensated by the increased synthesis of the sodium retaining steroid DOC. H y p ertensio n also occurs because of accum ulation of both D O C and com pound B. The deficiency of cortisol is partially compensated by an increase in levels of compound B. The hypertensive adrenogenital syndrome resulting from 17-hydroxylase deficiency is c h a ra c te r ized by am biguous m ale genitalia and infantile sexual characteristics at puberty owing to th e deficiency of sex steroids. The rem aining two forms of adrenogenital syndrome are rare. One results from a deficiency of th e enzym e 3-(3- hydroxysteroid dehydrogenase. If the enzym e deficiency is severe, th e syndrom e is lethal, resu ltin g in neonatal death. Partial deficiency of 3-(3-hydroxystero id dehydrogenase resu lts in p ro nounced sodium loss and severe adrenal insufficiency because of the deficiency of mineralocorticoids and glucocorticoids. W ith the exception of dehydroepiandrostero n e, levels of o th er androgens and estrogens are low in this form of ad ren ogenital syndrom e, which is characterized by males having ambiguous genitalia and females virtually free of the effects of masculinization. The other rare form of adrenogenital syndrome results from an enzymic block in the conversion of cholesterol to pregnenolone. The enzyme involved is 20,22- desm olase. Because of an inability to synthesize glucocorticoids, m ineralocorticoids and sex steroids, neonatal death results.
3 LABORATORY EVALUATION OF ADRENOGENITAL SYNDROME 161 Laboratory Assessment of the Adrenogenital Syndrome H y d r o x y l a s e D e f i c i e n c y As noted previously, the deficiency of this enzyme can be either partial resulting in the simple virilizing form of the adrenogenital syndrom e, or m ore com plete w hen th ere is sodium loss. Laboratory assessm ent of e ith e r variety requires m easurem ent by radioim m u noassay of plasm a ACTH and cortisol precu rso rs in plasm a p rio r to the enzymic block, such as 17-a-hydroxyprogesterone and progesterone and testostero n e, all of w hich will be elevated. Laboratories that do not have access to these radioimmunoassay procedures can still evaluate this enzym e deficiency by the m easurem ent of 17-ketosteroids in urine by the classic Z im m erm ann reaction or the m easurem ent of urine pregnanediol and prenanetriol by colorim etric or gas chromatographic procedures, or by the non-specific m easurem ent of ketogenic steroids in u rin e. In 21- hydroxylase deficiency, all of these urinary constituents will be elevated. D iscrim ination b e tw e en the sim ple virilizing form and the m ore com plete deficiency of 2 1 -hydroxylase can be made by the analysis of cortisol and aldosterone in plasm a by radioim m unoassay. Both plasm a cortisol and aldosterone levels will be drastically decreased in the more com plete deficiency of 2 1 -hydroxylase. In addition, serum sodium levels will be low because of sodium loss, and serum potassium levels will be increased. In contrast, in the simple virilizing form of congenital adrenal hyperplasia, cortisol levels are not as low as in the m ore complete deficiency of 2 1 -hydroxylase, and aldosterone levels are actually approximately twice that found in the normal range. Serum sodium level is also not reduced. Levels of urinary cortisol and its dihydro-and tetrahydroderivatives as m easured by the Porter-Silber reaction are much lower when the deficiency of 2 1 -hydroxylase is m ore com plete than w hen the enzym e deficiency is partial ( 3 - H y d r o x y l a s e D e f i c i e n c y ll- 3-Hydroxylase deficiency and the m ore com plete 2 1 -hydroxylase deficiency have in common an increase in plasma ACTH and plasma testosterone levels as m easu red by radioim m unoassay, an elevation of urinary 17-ketosteroids, as well as a reduction in plasma aldosterone and plasm a cortisol levels. T he laboratory data that allow discrim i nation b etw een 2 1 -hydroxylase d eficiency and ll-@-hydroxylase deficiency are the increase in the latter case of levels of plasm a 1 1 -deoxycorticosterone (DOC) and plasm a 11-deoxycortisol (com pound S), both of w hich are b est determ ined by radioimmunoassay. U rinary 17-hydroxycorticosteroid levels determ ined by the Porter-Silber reaction and serum sodium levels are also increased in 1 1 -fj-hydroxylase deficiency, w hereas serum potassium level is decreased H y d r o x y l a s e D e f i c i e n c y An increase in plasma ACTH, plasma 1 1 -deoxycorticosterone, plasm a aldosterone and serum sodium and a decrease in plasm a cortisone, 17-a-hydroxyprogesterone, serum potassium and urinary 17-hydroxycorticosteroids as determ ined by the Porter-Silber reaction are found in 17-hydroxylase deficiency. However, unlike 2 1 -hydroxylase and ll-(3-hydroxylase deficiency plasma testosterone and urinary 17-ketosteroid levels are d rastically reduced H y d r o x y s t e r o id D e h y d r o g e n a s e o r 2 0, D e s m o l a s e D e f i c i e n c y As n o ted previously, b o th th ese enzym e deficiencies are rare, and if the
4 162 NARAYANAN enzym e deficiency is severe, neonatal death results. A characteristic of th e partial deficiency of 3-3-hydroxysteroid dehydrogenase is the increase in plasma levels of d e h y d ro e p ian d ro ste ro n e as determ ined by radioimmunoassay and an increase in urinary 3-(3-hydroxysteroids (prim arily dehydroepiandrosterone) as determ ined by th e Z im m erm ann reaction for 17-ketosteroids, both before and after digitonin precipitation. The laboratory evaluation of 20,22- desm olase deficiency is im practicable, since cholesterol cannot be converted to corticosteroids, thus resulting in a life threatening situation due to a deficiency of gluco- and mineralo-corticoids and sex steroids. As with all the other enzyme deficiencies leading to congenital adrenal hyperplasia, ACTH levels will be greatly increased because of th e inability to synthesize cortisol. Considerations in the Choice of Laboratory Tests for the Evaluation of Adrenogenital Syndrome Laboratory tests on urine for the m easurem ent of selected hormones and their m etabolites are not only cum bersom e with num erous steps, but are also non specific. The recovery of the steroids are also n o t q u a n tita tiv e b ecau se of the num erous steps involved in the assay. In clu d ed in this category are u rin ary pregnanetriol determ inations, 3 17-ketosteroids, ketogenic steroids, 8 and the Porter-Silber reaction for 17-hydroxycorticosteroids. 9 T he tediousness of urinary steroid m easurem ents is illustrated by the fact that the assay for p regnanetriol entails hydrolysis to free the steroid from its sulfate and glucuronide conjugates in an overnight incubation step of extraction w ith toluene followed by several washing steps, evaporation of extract to dryness, extraction with benzene and elution from an alum ina colum n, and subsequent m easurem ent of pregnanetriol at 425 nm. The classical u rin ary 17-ketosteroid determ ination also involves hydrolysis, extraction, and w ashing steps prior to affecting the Zimmerm ann reaction with m -dinitrobenzene in alcoholic potassium hydroxide. Since u rin e of infants and prep u b ertal children contains non specific chromogens, the Zimmerm ann color reaction is not only m easured at its wavelength of maximal absorption at 520 nm but also at two equidistant wavelengths (480 nm and 560 nm) at which the non specific chrom ogens in u rin e absorb, thus effecting the Allen Correction. The non-specific urinary 17-ketogenic stero id s p ro ced u re th a t perm its m easu re m e n t of cortisol, 1 1 -deoxycortisol and th e ir tetra- and hexahydroderivatives (cortols and cortolones) and pregn an etrio l as 17-ketosteroids req u ires reduction with sodium borohydride and oxidation w ith sodium b ism u th ate or m etap erio d ate p rio r to m easuring the resulting 17-ketosteroids by the Z im m erm ann reaction. The P o rter-s ilb er reaction for th e m easurem ent of 17-hydroxycorticosteroids in u rin e re q u ire s hydrolysis and extraction steps prior to reaction with phen y lh y d razin e in alcoholic sulfuric acid to yield a yellow color that is m easu re d at 410 nm. A lthough sem i-autom ated m ethods for the m easurem ent of 17-hydroxycorticosteroids in urine by the P o rter-s ilb er reaction are cu rren tly available, th e p ro ced u re is su b ject to interference by some of the commonly used drugs. 14 Gas chrom atographic procedures for the m easurem ent of urinary pregnanetriol and androgen m etabolites (17-ketosteroids) in urine, although m ore sensitive and specific than the colorim etric procedures just described, are still time consum ing and not totally q u a n tita tive. 11,13 Because of their tediousness, lack of
5 LABORATORY EVALUATION OF ADRENOGENITAL SYNDROME 163 quantitative recovery and nonspecificity, urinary steroid m easurem ents are now m ade by sensitive radioim m unoassay procedures originally used for m easurem ent of specific horm ones in plasma. In spite of their sensitivity, some of the m ethods of horm one assays by radioim m unoassay have th eir problem s. M easurem ent of ACTH which is the single substance elev ated in all form s of th e ad ren o g en ital syndrom e is a case in p o in t. 4 A d renocorticotropic horm one, w hich is p re se n t only in picogram amounts, is susceptible to attack by proteolytic enzym es. In the absence of a proteolytic enzyme inhibitor in the assay system and th e blood collection tu b e, ACTH levels are overestim ated because of damage to the horm one in plasma and also to the radiolabelled ACTH during the long incubation step of the assay. It has been show n th a t plasm a o b tain ed from blood collected in tubes with EDTA and th e p ro teo ly tic enzym e in h ib ito r aprotinin had a 1 2 percent reduction in ACTH levels com pared to plasm a obtained from blood collected in tubes containing only ethylenediam inetetraacetic acid (EDTA ). 2 Adrenocortictropic horm one is also strongly ab so rb ed by glass. Blood specimens should therefore be immediately centrifuged, preferably in a refrig e rate d cen trifu g e, and the plasm a rem oved and tra n sfe rre d to a plastic tu b e. A lternatively, blood sam ples may be collected in a plastic syringe and transferred to plastic tubes containing EDTA and preferably also aprotinin. The tubes should be chilled and cen trifuged w ith o u t delay p referab ly in a refrigerated centrifuge. Plasm a should be transfered to polystyrene tubes containing m ercaptoethanol and stored at 70 C u n til ready for analysis. E ven w ith plastic surfaces th e re is some adsorption of ACTH which can be m inim ized by using album in-containing buffers and low tem peratures during specim en preparation and handling. In the radioim m unoassay m easu rem ent of progesterone or 17-a-hydroxyprogesterone, displacem ent of hormone from protein binding sites w ith eith er D anazol at ph 7.4, or 8 anilino-1- naphthalene sulfonic acid at ph 4.0 prior to assay is more precise and technically convenient compared to extraction of the horm one from serum and su b seq u en t radioimmunoassay m easurem ent. 10 Radioimmunoassay for free cortisol is a better indicator of adrenocortical status than total plasma cortisol. 1 M e a s u re m e n t. of free testo ste ro n e obtained by ultrafiltration of serum and su b seq u e n t m easu rem ent by rad io im m unoassay is preferred to the m easurem en t of th e co n cen tratio n of th e total horm one in serum since the latter shows a considerable overlap betw een normal and hirsute w om en. 12 Consideration should also be given to th e m atrix in w hich the standards are prepared. The use of standards prepared with steroid-free plasma resulted in an overestim ation of aldosterone in a radioim m unoassay p ro c e d u re. 6 This effect was overcome by adding to plasma used for preparation of aldosterone standards a m ixture of cortisol, co rtico sterone and deoxycorticosterone to m aintain a constant stero id to aldosterone ratio. In adrenogenital syndromes that have a tendency towards sodium loss, plasma renin activity m easurem ent by radioim m unoassay may be of value. 5 In considering renin m easurem ent, practical considerations related to sample collection and assay variables should be addressed. Blood specim ens collected in ED TA tubes should be chilled immediately and centrifuged prom ptly in a refrigerated centrifuge and the plasma rem oved and stored at 20 C prior to assay. The addition of the proteolytic enzyme inhibitor ap ro tin in to th e blood collection tu b e containing EDTA has a stabilizing effect on ren in activity m e a su rem e n ts. 2 The
6 164 NARAYANAN assay system should contain inhibitors of angiotensin-converting enzyme and angiotensinase (phenylm ethylsulfonyl chloride and EDTA). Angiotensin generation during radioimmunoassay should also be blocked w ith pepstatin-a. Conclusion Specific and sensitive immunoassays of plasma hormones have replaced cum bersome and non-specific urine total horm one-m etabolite assays in the laboratory evaluation of th e adrenogenital syndrome. Awareness of sample instability and technical pitfalls in specific im m u noassays of horm ones perm its m inim izing these variables. Stabilizing labile ho r mones during blood collection and assay is an approach to im proving the usefulness of the laboratory evaluation of the adrenogenital syndrom e. References 1. C l e r i c o, A., D e l C h i c c a, M. G., Z u c c h e l l i, G., B a r t o l o m e i, C., and R i c c i o n i, N.: Free-cortisol assay by immunoextraction: comparison with an equilibrium dialysis procedure. Clin. Chem. 28: , E c h e m e n d i a, E., V a n H e e r t u m, R. L., G u z m a n, L., N a r a y a n a n, S., and I n c e, G. : The stabilizing effect of aprotinin on selected hormone assays. Clin. Chem. 30:1051, F o t h e r b y, K., and L o v e, D. N.: A m odified m ethod for the estim ation of pregnanetriol in urine. J. Endocrinol. 20: , G u t o w s k a, J., J u l e s z, J., S t. L o u i s, J., and G e n e s t, J.: Radioimmunoassay of corticotropin from plasma. Clin. Chem. 28: , I k e d a, I., I i n u m a, K., T a k a i, M., Y a m a g a w a, Y., K u r a t a, K., O g i h a r a, T., and K u m a h a r a, Y.: Measurement of plasma renin activity by a simple solid phase radioim m unoassay. J. Clin. Endocrinol. Metab. 54: , L u n, S., E s p i n e r, E. A., N i c h o l l s, M. G., and Y a n d l e, T. G.: A direct radioimmunoassay for aldosterone in plasma. Clin. Chem. 29: , M i g e o n, C. J.-. Diagnosis and m anagem ent of congenital adrenal hyperplasia. Hosp. Pract. 12: , N o r y m b e r s k i, J. K., S t u b b s, R. D., and W e s t, H. F.: Assessment of adrenocortical activity by assay of 17-Ketogenic steroids in urine. Lancet i: , P o r t e r, C. C. and S i l b e r, R. H. : A quantitative color reaction for cortisone and related 17, 21- d ih ydroxy-20-k etosteroids. J. B iol. C hem. 285: , R a t c l i f f e, W. A., C o r b i e, J. E. T., D a l z i e l, A. H., and M a c p h e r s o n, J. S.: Direct 123I-radioligand assays for serum progesterone compared with assays involving extraction of serum. Clin. Chem. 28: , V a n d e n H e u v e l, W. J. A., C r e e c h, B. G., and H o r n i n g, E. C. : Separation and estim ation of the principal human urinary 17-ketosteroids as trimethylsilylethers. Anal. Biochem. 4: , V l a h o s, I., M a c M a h o k, W., S g o u t a s, D., B o w e r s B., T h o m p s o n, J., and T r a w i c k, W.: An improved ultrafiltration method for determining free testo stero n e in serum. C lin. C hem. 28: , W o t i z, H. H.: Steroid metabolism X V. Rapid determ ination of urinary pregnanediol by gas cheom atography. B iochem. B iophys. Acta 69: , Y a e, Y., I s h i i, N., M o r i, T., O k o c h i, K., and N a r a y a n a n, S.: Semiautomated determination of urinary 17-hydroxycorticosteroids as porter-silber chromogens. Clin. Chem. 29: , Z i m m e r m a n n, W.: Eine farbrekation der sexual hormone und ihre anwendung zur quantitoven colorimetrischen bestimmung. Hoppe Seylers Z. Physiol. Chem. 233: , 1935.
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