De termin ation of dexamet hasone in saliva

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1 Clinical Cheniistiy 42: (1996) De termin ation of dexamet hasone in saliva Jos H.H. THIJssEN,l* CHRISTINE C. GISPEN-DE WIED,2 WINNIE VEEMAN1 GEMMA M. VAN HEESWIJK,3 and We conducted experiments to demonstrate that the determination of dexamethasone in saliva is a valuable tool to assess dexamethasone concentrations in the body after administration of this synthetic corticosteroid. After extraction of saliva, a RIA involving highly specific commercially available antibodies was established and evaluated. This RIA was easy to conduct, reliable, and sensitive enough to measure dexaniethasone until -24 h after oral administration of I mg per 7 kg of body weight. On the morning after the administration, the mean concentration in saliva was 54 pmolll. Over a large range (13_16 pmolll), plasma concentrations correlated very well with salivary concentrations; plasma contained six times more dexamethasone than saliva. INDEXING miuts: corticosteroids dexamethasone test. hypothalamo-pituitary-adrenal axis suppression Dexamethasone, a potent glucocorticosteroid, usually suppresses pituitary adrenocorticorropic hormone release, which results in the decrease of corticosteroids measured in plasma and (or) urine, thus allowing the assessment of feedback inhibition of the hypothalamo-pituitary-adrenal (HPA) axis.4 The overnight dexamethasone suppression test (DST), in which 1 mg of dexamethasone is administered orally, was introduced [1] as a very sensitive test to assess spontaneous hypercorticoidism in humans. The test is widely used in the endocrine clinic, and high-dose modifications still appear to be of great value in the differential diagnosis of Cushing syndrome [2]. Extensive clinical investigations have shown that many patients with psychiatric disorders, especially those with a diagnosis of depression, possess a relative resistance of the pituitary to the inhibiting Departments of Endocrinology and Psychiatiy, University Hospital, and Department of Medical Physiology, Faculty of Medicine, Heidelberglaan 1, 3584 CX Utrecht, The Netherlands. *Address correspondence to this author at: Department of Endocrinology, University Hospital Utrecht, P.O. Box 855, 358 GA Utrecht, The Netherlands. Fax ; Nonstandard abbreviations: HPA, hypothalamo-pituitary-adrenal; DST, dexamethasone suppression test; and BSA, bovine serum albumin. Received December ii, 1995; accepted March 2, effect of the low dose of dexamethasone. Consequently, the DST has been suggested as a biologicalmarker for depression [3], but because of a low specificity, the DST has lost its value for this purpose. The DST reflects the relative resistance of the pituitary to glucocorticosteroids. Thus, the phenomenon of dexamethasone resistance remains of interest in understanding HPA dysfunction in depression [4]. Observations on increased cortisol production and dexamethasone resistance in depressed patients have led to the assumption of a general increase in HPA activity during depression, which disappears when the patient recovers from the illness. Still unclear is whether dexamethasone nonsuppression is the result of feed-forward forces of central origin overriding feedback activity at the pituitary bevel or the result of an impaired negative feedback system [5]. Differences in dexamethasone plasma concentrations suggesting an enhanced dexamethasone metabolism and thus bower HPA activity have also reportedly contributed to the dexamethasone nonsuppression [6-1]. Therefore, measurements of plasma dexamethasone are thought to be of value when the DST is done in patients with psychiatric disorders [8] and in patients with slight disturbances in liver function [11]. More recently, improvements in the detection limits of methods for assaying cortisol have made it possible to determine the presence of cortisob at concentrations usually found in saliva. Salivary cortisol concentrations are correlated with plasma concentrations and thus have been used to study the HPA axis in depressed patients [12-14]. Furthermore, the development of a dexamethasone challenge test for the assessment of growth hormone secretion [15] may requireinformationon its concentration in the human body. Especially in children, the noninvasive monitoring of the relevant cortisol concentrations without repeated venipuncture or indwelling intravenous catheters is very helpful. Measurement of the concentration of dexamethasone still requires blood sampling. Because dexamethasone does not bind to cortisol-binding globulin in plasma, its protein-bound fraction is bow [16], and thus dexamethasone may well be measurable in saliva. We have conducted experiments to demonstrate that the determination of dexamethasone in saliva is a valuable tool for assessing the dexamethasone concentration after oral administration and thus can easily replace blood measurements. 1238

2 Clinical Chemistry 42, No. 8, Materials and Methods Samples. Samples of saliva were collected from patients and volunteers undergoing a DST; 1 mg of dexamethasone per 7 kg of body weight was administered orally at 2. After stimulation with a few crystals of citric acid, at beast 1 ml of saliva was collected in a small glass container, and the samples were frozen at -2 #{176}C and stored until determination. On some occasions, at the same time that blood samples were collected in heparinor EDTA-containing tubes, plasma was obtained after centrifugation and stored at -2 #{176}C. Before assay, plasma and saliva samples were thawed at 4 #{176}C and centrifuged for 5 mm, and the supernatant was used for analysis. Additional samples of plasma and saliva were collected from patients who received corticosteroid-pulse therapy with high doses of dexamethasone, 2 mg via intravenous infusions [17]. Reagents. Dexamethasone was obtained from Sigma Chemical Co. (St. Louis, MO). The antiserum against dexamethasone (IgG-Dex-l) was purchased from IgG Corp. (Nashville, TN), and the [1,2,4,6,7-3Hldexamethasone [specific activity 3.33 TBq (9 Ci)/mmol] was purchased from Amersham Life Sciences (Houten, The Netherlands). Other reagents include bovine serum albumin (BSA) (Boserab; Organon Teknika, Boxtel, The Netherlands), sodium dihydrogen phosphate (Riedel de Haen, Seelze, Germany), charcoal (reinst; Merck, Darmstadt, Germany), dextran T-7 (Pharmacia Biotech, Uppsala, Sweden), diethyl ether (Rathburn, Walkerburn, UK), and scintillation fluid (Ultima Gold; Packard, Meriden, CT). Water was purified with the Milli-Q system (Miblipore, Mobsheim, France). The buffer used consisted of.1 moljl phosphate-buffered saline containing 1 g/l BSA. The antiserum as supplied by the manufacturer was diluted with this buffer until.1 ml contained the amount of antiserum needed for one assay tube, according to the information from the manufacturer. Radioactive dexamethasone was diluted with ethanol and stored at 4 #{176}C recovery was 64%. All individual results have been corrected for at a concentration of 37 MBq (1 mci)/l ethanol; before use, the losses during extraction. amount needed was evaporated under nitrogen and dissolved in buffer at a concentration of MBq (5 MCi)/L, as used in the assay. Dextran-coated charcoal was prepared at least 16 h before use by suspending 1 mg of charcoal plus 5 mg of dextran T-7 in 1 ml of phosphate buffer without BSA and stirring overnight at 4 #{176}C. Liquid scintillation counting was done with a Tri-Carb 4 Series Minaxi from United Technologies Packard Instrument Co. (Downers Grove, IL). Dexamethasone extraction and assay. Before extraction,.1 ml of buffer containing -37 Bq (1 nci) of [3H]dexamethasone was added to at beast.5 ml of saliva, and the mixture was allowed to stand at room temperature for 3 mm with occasional, gentle manual stirring to avoid the formation of foam. Dexamethasone was extractedwith 6 ml of diethybetherand gentleswinging to avoid formation of emulsions.afterwards, the water layer was frozen in ethanol containing dry ice, and the ether layer was decanted into clean glass tubes and evaporated under a stream of air at temperatures <4 #{176}C. The residue was dissolved in.4 ml of buffer by careful mixing and leaving the tubes for 3 mm at room temperature. Of this solution, 1 ML was used to measure the recovery of the added [3H]dexamethasone, and twice, 1 ML was transferred into assay tubes; 1 ML of the antiserum and 1 ML of the tracer were added. Tubes containing dexamethasone calibrators were treated identically, and all tubes were incubated overnight at 4-6 #{176}C. Separation of free and bound dexamethasone was done by addition of I ml of dextran-coated charcoal suspension and incubation for 3 mm in an icebath.the charcoalwas spun down by centrifugation at a temperature of <5 #{176}C. The supernatant was decanted into counting vials, 3 ml of scintillation fluid was added, and the vials were counted in a liquid scintillation counter for 1 mm. Similarly the recovery was measured. The amount of dexamethasone in unknown samples was estimated by comparing the percentage of binding in these samples with the percentages obtained for the calibrators, as usual. The concentration was calculated from these amounts, taking into account the recovery. Because of the overnight incubation, total assay time was -24 h. For the determination of dexamethasone in plasma, an identical procedure was followed, except for the volume;.25 ml of plasma was used routinely. Results The assay procedure as described was capable of measuring the concentration of dexamethasone in saliva. The following results demonstrate the validity of the determination. E,ctraction. The composition of saliva did show variations between individual subjects. This resulted in small but significant changes in calibration curves of dexamethasone, made directly in saliva. To avoid these so-called matrix effects, the described extractionprocedure with diethyletherwas used throughout all additional investigations. The extraction resulted in recoveries that ranged from 5% to 8% for individual samples; the mean Linearity.Extraction of different quantities ( ml) of salivary samples yielded a linear relation between the volume of saliva used and the amount of dexamethasone measured. In seven samples with dexamethasone concentrations between 9 and 113 pmol/l, the slope was 1.4 ±.3 with a negligible intercept; the correlation coefficient was.999. Recovery. Addition of 4 to 5 pmol/l resulted in nearly quantitative recoveries; the results are shown in Table I. Sensitivity. With 1 ml of saliva, the lowest detectable concentration of dexamethasone was calculatedto be 1 pmol/l. The Table 1. Recovery of added dexamethasone. Concentration added, pniol/l Recovery, % ± SD No. of experiments ± 99 ± ± ±1 7

3 124 Thijssen et al.: Salivary dexamethasone calculationwas based on measurement of the variationin binding without dexamethasone; 3 SD of zero concentration yielded 7 pmol/l. In addition, 2 salivary samples of subjects who had not takendexamethasone allhad concentrationsof<1 pmol/l. The amount of dexamethasone required to reduce B, by 5% is 15-2 pg/tube,equivalentto -25 pmob/l. Specificity. The antiserum used shows a very high specificity; cortisol shows.4% and 11-deoxycortisol.7%, and other physiologically occurring steroids show <.1% cross-reactivity. Only some other synthetic corticosteroids such as J3-methasone (1%), triamcinolone (.27%), and prednisobone (.14%) have significant cross-reactions. Additional evidence for the specificity of the determination was obtained by extracting two salivary samples (9 and 18 pmol/l) and subjectingthe evaporated extractsto thin-layer chromatography in the system chboroform:ethanol(8:2by vol), followed by immunoassay of eluted fractions from the chromatogram. In saliva, only material with a mobility identical to authentic dexamethasone could be demonstrated, as shown in Fig. I;the totalrecovery in these fractionswas >9%. Table 2. Betw een-assay reproducibility. Concentration, pmoi/l (mean ± SD) CV, % No. of experiments 41± ± ± ± Correlation with blood concentrations. Comparison of the dexamethasone concentrations in simultaneously collected plasma and saliva samples gave the results presented in Fig. 2. Over a very large range (plasma concentrationsof pmob/l), a good correlation between the concentrations in these two body fluidswas found;r was.998 forlog-transformedand.993 for untransformed concentrations.dexamethasone concentrations in saliva were six times lower than in plasma; the slope of the regression line was.165. In the smaller concentration range, usually observed after ingestion of 1 mg of dexamethasone, the ratio between the concentrations in plasma and salivaranged from 6 to 11. Reproducibility. Between-assay variability was testedby repeated analysis of the same salivary samples on different occasions. The CV at different dexamethasone concentrations is shown in Table 2. Within-assay variation ranged from 11% at 4 pmob/l to 5.1% at 1 pmol/l (n = 1). 2 1 Concentration of dexamethasone in saliva. After oral administration of 1 mg of dexamethasone at 2 to volunteers and to patients without a clear psychiatric diagnosis, the concentrations of dexamethasone were measured in saliva collected between 8 and 2 the next day.at 8, the concentrationshowed barge variations;95% of the valuesranged from 12 to 5 pmolil (n = 53), and the mean concentrationwas 54 ± 59 (SE) pmob/l. With similar barge variations, the concentrations decreased during the day, as illustrated in Fig. 3; after 173, the concentrations fell below the detection limit in 4 of the 53 subjects. 16 -J P E Q. 6 mobility (cm-fractions) If, C 4-, I- 4- C, C 1 1, a.,, 1$ v-1_ 1o 1O 16 mobiiity (cm-fractions) Fig. 1. Mobility of the immunoreactive material extracted from saliva of subjects pretreated with 1 mg of dexamethasone. Arrows indicate the positionofauthenticdexamethasone. plasma concentrationspmoi/l Fig. 2. Correlation between concentrations of dexamethasone in plasma and saliva taken simultaneously from healthy subjects and patients pretreated with dexamethasone.

4 ClinicalChemistiy 42, No. 8, tested in the near future, and multiple point determinations in salivatogetherwith cortisobmeasurements arebeing done inthe follow-up of children with psychiatric disorders. too 2 T I -r S ii 12 IS Il time of day h Fig. 3. Mean concentrations ± SE of dexamethasone in saliva of healthy control subjects pretreated on the preceding evening at 2 with 1 mg of dexamethasone. Discussion Since the first demonstration [18] of a very good correlation between salivaryand plasma corticosteroidconcentrations, many studies have shown that the measurement of specific steroidsand theirmetabobitesin salivaoffersa good alternative for determinations in blood. Because salivary steroids more closely reflect the biologically active free steroids than the total concentration of protein-bound plus -unbound steroids in plasma, much attention has been given to measurements of severalandrogens in saliva[19]. As pointed out above, salivary cortisolmeasurements have become more popular among pediatricians. In addition, the follow-up in patients with congenital adrenal hyperplasia under therapy can be curried out by using steroidconcentrationsin saliva[2]. For diagnostic investigations regarding the HPA feedback system, one of the most widely used synthetic corticosteroids is dexamethasone. Measurement of this steroid has been advised for use during the DST in patientswith psychiatricdisorders. To our knowledge, thisisthe firstdemonstration showing that dexamethasone can also be measured in saliva. The method involved is relativelysimple; it is easilyaccessible,involvesa commercially available antibody of very high quality, and all other reagents are rather uncomplicated. The relatively bow extraction efficiency is due to the choice of diethyb ether as the solvent.this choice was based on very practicalarguments: avoidance of emulsions and the possibility of using the very efficient freezing technique for separation of the two liquid phases. Consistent with the transportation of dexamethasone in blood only bound to albumin [16], salivary concentrations of dexamethasone show an excellent correlation with those in plasma over a very large (more than three decades) concentration range. Thus, salivary concentrations can be considered a good reflection of plasma concentrations. Furthermore, the concentrations in saliva are only about six times lower than those in plasma, in very good agreement with its protein-bound fraction of 18% [16]. No cross-reacting metabolites of dexamethasone were found in the saliva. Clinicaluse of dexamethasone measurements in salivawillbe In conclusion, we have demonstrated that the quantitative determination of dexamethasone in saliva is a good alternative to plasma measurements afteroral administration of this synthetic corticosteroid. References 1. Liddle GW. Tests of pituitary-adrenal suppressibility in the diagnosis of Cushing s syndrome. J Clin Endocrinol Metab 196;2: Dichek HL, Nieman LK, Oldfield EH, Pass HI, Malley JD, Cutler GB. A comparison of the standard high dose dexamethasone suppression test and the overnight 8-mg dexamethasone suppression test for the differential diagnosis of adrenocorticotropin-dependent Cushing s syndrome. J Clin Endocrinol Metab 1994;78: CarrollBi. The dexamethasone suppression testformelancholia. Br J Psychiatry 1982:14: Gispen-de Wied CC, D Haenen H, Verhoeven WMA, Wynne Hi, Westenberg HGM, Thijssen JHH, et al. Inhibition of the pituitaryadrenal axis with dexamethasone and cortisol in depressed patients and healthy subjects: a dose-response study. Psychoneuroendocrinology 1993:18: Holsboer F, Von Bardeleben U, Wiedeman K, Muller OA, Stalla GK. Serial assessment of corticotropin-releasing hormone response after dexamethasone in depression. Implications for pathophysiology of DST nonsuppression. Biol Psychiatry 1987:22: Arana GW, Workman RJ, Baldessarini Ri. Association between low plasma levels of dexamethasone and elevated levels of cortisol in psychiatric patients given dexamethasone. Am J Psychiatry 1984; 141: Holsboer F, Haack D, Gerben A, Vecsei P. Plasma dexamethasone concentrations and differential suppression response of cortisol and corticosterone in depressives and controls. Biol Psychiatry 1984:19: Maguire KP, Schweitzer I, Biddle N, Bridge S, Tiller JWG. The dexamethasone suppression test: importance of dexamethasone concentrations. Biol Psychiatry 1987:22: Johnson GF, Hunt G, Kerr K, Caterson I. Dexamethasone suppression test and plasma dexamethasone levels in depressed patients. Psychiatry Res 1984;13: Meickle AW. Dexamethasone suppression tests: usefulness of simultaneous measurement of plasma cortisol and dexamethasone. Clin Endocrinol 1982;16: Kutemeyer S, Schurmeyer TH, von zur M#{252}hlen A. Effect of liver damage on the pharmacokinetics of dexamethasone. Eur J Endocrinol1994;131: Barns B, Watkins 5, Cook N, Walker RF, Read GF, Riad-Fahmy D. Comparisons of plasma and salivary cortisol determinations for the diagnostic efficacy of the dexamethasone suppression test. Biol Psychiatry 199;27: GalardR, Gallart JM, Catalan R, Schwartz 5, Arguello JM, Castellanos JM. Salivary cortisol levels and their correlations with plasma ACTH levels in depressed patients before and after the DST. Am J Psychiatry 1991;148: Woodside OB, Winter K, Fisman S. Salivary cortisol in children: correlations with serum values and effect of psychotropic drug administration. Can J Psychiatry 1991;36: Pineda J, Martul P, Casanueva FF, Dieguez C, Rica I, Loridan L. Oral dexamethasone administration: new pharmacological test for

5 1242 Thijssen et al.: Salivary dexamethasone the assessment of growth hormone secretion. Eur J Endocrinol 1994;131: Dean M, Stock B, Patterson Ri, Levy G. Serum protein binding of drugs during and after pregnancy in humans. Clin Pharmacol Ther 198O;28: Van den Brink HR, van Wijk MJG, Geertzen RGM, Bijlsma JWJ. Influence of corticosteroid-pulse therapy on the serum levels of soluble interleukin-2 receptor, interleukin-6 and interleukin-8 in patients with rheumatoid arthritis. I Rheumatol 1994;21:43O Katz FH, Shannon IL. Parotid fluid cortisol and cortisone. i CIin Invest 1969;48: Swinkels LMJW, van Hoof HJC, Ross HA, Smals AGH, Benraad Ti. Low ratio of androstenedione to testosterone in plasma and saliva of hirsute women. Clin Chem 1992;38: Otten Bi, Wellen ij, Rijken CJW, Stoelinga GBA, Benraad Ti. Salivary and plasma androstenedione and 17-hydroxyprogesterone levels in congenital adrenal hyperplasia. J Clin Endocrinol Metab 1983:57:115-4.

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