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Agglutinating Antibody Titers to Members of the Family Reacting Antibodies to Pseudomonas Aeruginosa

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Agglutinating Antibody Titers to Members of the Family Reacting Antibodies to Pseudomonas Aeruginosa JOURNAL OF CLINICAL MICROBIOLOGY, June 1984, P. 757-762 Vol. 19, No. 6 0095-1137/84/060757-06$02.00/0 Copyright C 1984, American Society for Microbiology Agglutinating Antibody Titers to Members of the Family Legionellaceae in Cystic Fibrosis Patients as a Result of Cross- Reacting Antibodies to Pseudomonas aeruginosa MICHAEL T. COLLINS,lt* JEANNETTE McDONALD, NIELS H0IBY,2 AND OLE AALUND3 Department of Microbiology and Environmental Health, Colorado State University, Fort Collins, Colorado 805231; and Statens Seruminstitut, Department of Clinical Microbiology, and Pediatric Department TG, Rigshospitalet,2 and Laboratory of Preventive Medicine, Royal Veterinary and Agriculture College,3 Copenhagen, Denmark Received 6 October 1983/Accepted 9 March 1984 The objective of this study was to evaluate the prevalence and significance of antibody titers to organisms in the family Legionellaceae in 128 serum samples collected from cystic fibrosis patients at routine examinations. Antibody titers were determined for 10 antigenic types of Legionellaceae; Legionella pneumophila serogroups 1 to 6, Fluoribacter (Legionella) bozemanae, Fluoribacter (Legionella) dumoffii, Fluoribacter (Legionella) gormanii, and Tatlockia (Legionella) micdadei. The method of antibody titer determination was the microagglutination test. Elevated titers (.1:64) to one or more antigens were found in 41.3% of cystic fibrosis patients but in only 9.7% of 103 normal control subjects (P < 0.01). Titers to 8 of the 10 antigens were directly correlated with the number ofPseudomonas aeruginosa precipitating antibodies in patient sera, as determined by crossed immunoelectrophoresis (correlation coefficients, -0.74). Cross- reactions between P. aeruginosa and L. pneumophila were substantiated by crossed immunoelectrophore- sis of hyperimmune rabbit serum as well as patient sera against P. aeruginosa and Legionellaceae antigens. Monospecific antibody to the "common antigen" of P. aeruginosa was used to demonstrate the presence of this antigen in L. pneumophila. The presence of cross-reacting antibodies in cystic fibrosis patients chronically infected with P. aeruginosa emphasizes the need for cautious interpretation of antibody titers to members of the family Legionellaceae. Bacteria in the family Legionellaceae have emerged in established as previously described (12). Serum samples recent years as important opportunistic respiratory patho- from 103 normal children and young adults were obtained gens, particularly in immunocompromised persons. Children from the serum bank of the State Serum Institute, Copenha- with cystic fibrosis (CF) have a marked susceptibility to gen, Denmark, for use as controls. The age and sex distribu- bacterial infections of the respiratory tract. Petersen et al. tions of persons included in this study are shown in Table 1. (21) have reported that 76% of exacerbations of respiratory Agglutinating antibodies to members of the family Legionel- disease in 116 CF patients were associated with bacteria, laceae. The microagglutination (MA) test of Farshy et al. (6) most frequently Pseudomonas aeruginosa. Of the exacerba- was used with minor modifications as described in a previ- tions of respiratory disease, 20% were associated with ous report from our laboratory (3). The initial serum dilution viruses, mycoplasma, or chlamydia, although bacteria were used in this study was 1:2 instead of 1:4, 1:8, or 1:10 as also present in most of these cases, and no etiology was described in other reports (7, 18, 23). Antigens for each established in 18% of the exacerbations. Studies by Katz and strain of Legionella, Fluoribacter, and Tatlockia were grown Holsclaw (16) and Efthimiou et al. (Sa) have reported that on buffered charcoal-yeast extract agar (20). Carbol-fuchsin CF patients have a higher than normal prevalence of anti- (final concentration, 0.002%) was used instead of safranin to body to Legionella pneumophila, using the indirect fluoues- increase the visibility of the agglutination reaction. All serum cent antibody test, and suggested that CF patients acquire samples were tested against the six serogroups (SG) of L. Legionella infections more often than normal persons. The pneumophila (SG 1, Philadelphia 1 strain; SG 2, Togus 1 purpose of the present study was to evaluate the prevelance strain; SG 3, Bloomington 2 strain; SG 4, Los Angeles 1 and specificity of antibodies to members of the family strain; SG 5, Dallas 1E strain; SG 6, Chicago 2 strain) and Legionellaceae in serum samples from 128 CF patients by Fluoribacter (Legionella) bozemanae Wiga, Fluoribacter use of a different serological test and a broader range of (Legionella) dumoffii NY-23, Fluoribacter (Legionella) gor- antigens from Legionellaceae than in the previous studies. manii LA 12-13, and Tatlockia (Legionella) micdadei Tat- lock. MATERIALS AND METHODS Precipitating antibodies to P. aeruginosa. All CF patient Serum specimens. Serum specimens from 128 CF patients serum samples were tested for the number of precipitins were obtained during routine visits to the Danish Cystic against sonicated whole-cell antigens of P. aeruginosa by Fibrosis Center, Copenhagen, Denmark, in 1980, regardless crossed immunoelectrophoresis (XIE) as described by of the clinical history of the patient. Diagnosis of CF was H0iby and Axelsen (12). Serum samples from normal per- sons in this study were not tested for P. aeruginosa precipi- * Corresponding author. tins since previous studies have documented that no precipi- t Present address: Department of Pathobiological Sciences, tating antibodies to P. aeruginosa occur in the sera of School of Veterinary Medicine, University of Wisconsin, Madison, children up to the age of puberty, and only one precipitin WI 53706. was found in only 6% of adult sera (8, 11, 15). 757 758 COLLINS ET AL. J. CLIN. MICROBIOL. TABLE 1. Age and sex distribution of CF patients and normal of serum P. aeruginosa precipitins. A total of 56, 26, 17, and persons included in the study 27 CF patients had 0 to 1, 2 to 10, 11 to 20, and >20 P. No. with the following ages (yr) Median aeruginosa precipitins, respectively. Mean MA titers for each group are depicted in Fig. 1. Mean MA titers to 5 of 10 <5 6-10 11-20 20-30 agea Legionellaceae antigens were significantly higher than nor- CF mal in CF patients with .11 P. aeruginosa precipitins (P < Male 14 22 21 9 10 0.01). The magnitude of the titers was directly correlated to Female 27 12 18 5 8 the number of P. aeruginosa precipitins for 8 of 10 antigens (correlation coefficients, .0.74). Correlation coefficients be- Normal F. or T. micdadei and Male 6 5 31 14 12 tween the mean MA titers to dumoffii Female 7 8 14 18 14 the mean numbers of P. aeruginosa precipitins for each group of CF patients was 1.00. a Total median age for CF patients was 9 years, and the total Antibody titers to F. bozemanae were elevated most median age for normal subjects was 13 years. dramatically in CF patients, with all P. aeruginosa precipitin groups having mean MA titers higher than normal (P < 0.01). The correlation coefficient between MA titers and P. Immunoelectrophoretic methods for analysis of cross-reac- aeruginosa precipitins for this antigen was 0.91. The group tions between P. aeruginosa and L. pneumophila. XIE was of CF patients with >20 P. aeruginosa precipitins had a performed with intermediate gels as described previously (1, mean MA titer to F. bozemanae equal to eight times that of 26). Intermediate gels contained either saline (0.154 M), the normal controls (mean MA titer of 92.7 versus 20.3). patient serum, or purified rabbit immunoglobulins. Rabbit Two CF patients with 31 and 37 P. aeruginosa precipitins immunoglobulins specific for the "common antigen" of P. had MA titers to F. bozemanae of 1:1,024. aeruginosa were obtained from a previous study reported Cross-reaction between P. aeruginosa and L. pneumo- from our laboratory (25). The antigen-antibody XIE refer- phila was substantiated by XIE of the L. pneumophila ence system employed for P. aeruginosa was described reference system with CF patient sera or purified immuno- previously by H0iby (9). An analogous XIE reference sys- globulins to P. aeruginosa in the intermediate gels (Fig. 2A, tem for L. pneumophila SG 1 developed in our laboratory C, and E). Figure 2C illustrates that a CF patient with was also used (2). precipitating antibodies to >20 P. aeruginosa antigens also Electrophoresis was performed in 1% agarose (depth, 1.5 precipitated antigen 66 of L. pneumophila. Purified immuno- mm) on glass slides (5 by 7 cm). Litex type LSM agarose globulins from rabbits immunized to P. aeruginosa reacted (Litex, Copenhagen, Denmark), with a relative endosmosis similarly, precipitating antigen 66 plus at least five additional value of 0.17 ± 0.01 and a gelling temperature of 35 to 37°C, L. pneumophila antigens (Fig. 2E). Precipitation of antigen was employed. Barbital buffer (pH 8.6; ionic strength, 0.02) 66 by heterologous antibody caused a separation of the was used for agarose preparation and as the running buffer precipitin arch into two components, indicating some hetero- during all electrophoretic procedures. First-dimension elec- geneity of this antigen as previously described (2). trophoresis was performed at 12°C, applying 10 V/cm until a Reciprocal cross-reactions were evaluated by use of the P. bromphenol blue-labeled human albumin marker migrated 35 aeruginosa XIE reference system with CF patient serum or mm (approximately 45 min). Second-dimension electropho- resis was performed at 12°C, applying 1.5 V/cm for 18 h. Patient serum or purified rabbit immunoglobulins were in- TABLE 2. Distribution of MA titers against Legionella species, corporated into the intermediate gels at 18.6 pA/cm2. The Fluoribacter species, and Tatlockia species in sera from CF agarose gels were stained with Coomassie brilliant blue. patients and normal persons Statistical methods. CF patients were grouped by the Antigen and serogroup in % with a titer of: number ofPseudomonas precipitins in their sera. Geometric the following subjects: s_8 16 32 64 128 .256 mean titers to each antigen for each CF patient group were CF (n = 128) calculated and plotted.
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