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1 FERTILITY AND STERILITY Vol. 66, No.4, October 1996 Copyright 1996 American Society for Reproductive Medicine Printed on acid~free paper in U. s. A. Antiphospholipid antibody panels and recurrent pregnancy loss: prevalence of anti cardiolipin antibodies compared with other antiphospholipid antibodies Deborah L. Yetman, B.S. William H. Kutteh, M.D., Ph.D.* The University of Tennessee, Memphis Health Science Center, Memphis, Tennessee Objective: To describe the prevalence of anti phospholipid antibodies in addition to cardiolipin in women with recurrent pregnancy loss. Design: Retrospective data analysis of test results from an anti phospholipid antibody panel. Setting: A university-based private patient referral center. Patients: Included 866 women with a history of recurrent pregnancy loss and 288 parous women without a history of reproductive problems. Interventions: None. Main Outcome Measures: Enzyme-linked immunosorbant assay, with referenced standards and known positive and negative sera on each plate, was used to measure anticardiolipin, antiphosphatidyl inositol, antiphosphatidylglycerol, antiphosphatidylserine, and antiphosphatidylethanolamine. Statistical analyses used the two-tailed Fisher's exact test. Results: Positive anticardiolipin antibodies were detected in 17.3% of patients with recurrent pregnancy loss compared with only 4% in the control population. Eighty-seven ofthe 866 women (1.1 %) were negative for anticardiolipin antibodies but had positive levels of another antiphospholipid antibody. Isolated positive antibody levels occurred most frequently in the immunoglobulin (Ig) G class of phosphatidylinositol, cardiolipin, and phosphatidylethanolamine. Isolated IgA was only found in phosphatidylethanolamine. Conclusion: In women with recurrent pregnancy loss, 15 of866 (17.3%) had positive anticardiolipin antibodies. Additionally, 87 of 866 (1.1 %) women were positive for another antiphospholipid antibody. Patient demographics were similar in both groups. We emphasize the importance of careful standardization, quality control, and interpretation of positive results. Fertil Steril 1996;66:54-6 Key Words: Recurrent pregnancy loss, antiphospholipid antibodies, anticardiolipin antibodies Received January 17,1996; revised and accepted May 22,1996. * Reprint requests: William H. Kutteh, M.D., Ph.D., Department of Obstetrics and Gynecology, 956 Court Avenue, Room D324, Memphis, Tennessee (FAX: ). Antiphospholipid antibodies, a group of autoantibodies that bind to negatively charged phospholipids, (1) have clinical significance because oftheir association with thromboembolic events and adverse pregnancy outcomes (2). Although anti phospholipid antibodies are associated with recurrent pregnancy loss, the diagnosis of the antiphospholipid syndrome can be made only if strict criteria are met. These include one clinical criterion (venous or arterial thrombosis or recurrent pregnancy loss) and one laboratory criterion (positive lupus anticoagulant or ~2 phospholipid units of immunoglobulin [Ig] G and/or IgM anticardiolipin) (3). There has been much controversy regarding the methods used to assay anti phospholipid antibodies, the phospholipids that should be evaluated, the standards used to calculate results, and the values used to report the negativepositive cutoff (4-6). In an attempt to standardize assay methods and establish definable cutoff values, several international workshops have been held (4,5). Based on the special report from the Second International Anti Cardiolipin Standardization Workshop-The Kingston Anti-Phospholipid Study Group (5), many laboratories have adopted the standards established by 54 Yetman and Kutteh Antiphospholipid antibody panels Fertility and Sterility
2 -- the Harris Phospholipid Association, Incorporated. These standards are based on phospholipid units defined as the cardiolipin-binding activity of 1 flg/ml of an affinity-purified IgG and IgM anticardiolipin preparation from a standard serum (4). Some laboratories have reported results as standard deviation units from the mean, but it has been proposed that the multiples of the median method of reporting be used because the distribution of anti phospholipid antibody results in a patient population is not normal (7). Several investigators across the country have advocated a panel of anti phospholipid antibodies to screen for antiphospholipid antibody syndrome (8, 9). This panel of tests includes not only cardiolipin but also phosphatidylinositol, phosphatidylglycerol, phosphatidylserine, and phosphatidylethanolamine. Controversy has arisen as to the significance ofthese antibodies and whether treatment should be based on positive results of anticardiolipin only or based on any of the other antiphospholipid antibodies. We have analyzed 866 different samples from women with a history of recurrent pregnancy loss for the prevalence of positivity in five different antiphospholipid antibodies. We include an analysis of isolated positive anti phospholipid antibodies and encourage caution in the interpretation of these results. A comparison of clinical and laboratory demographics is provided for women with pregnancy loss and positive anticardiolipin antibodies versus other positive antiphospholipid antibodies. These results emphasize the importance of careful standardization, quality control, and interpretation of positive anti phospholipid antibody results. Patients MATERIALS AND METHODS We evaluated 866 different women with a history of recurrent pregnancy loss. For this study, only women with a history of at least two consecutive pregnancy losses fathered by the same individual were included. All women with recurrent pregnancy loss were encouraged to have a complete evaluation that included a history and physical examination, karyotype on both partners, hysterosalpingogram or hysteroscopy, midluteal P or late-luteal endometrial biopsy, PRL, thyroid-stimulating hormone, lupus anticoagulant (partial thromboplastin time, dilute Russell viper venom time [drvvt], and platelet neutralization), and cervical cultures for mycoplasma, ureaplasma, and chlamydia. Additionally, the control population consisted of 288 nonpregnant, reproductive-aged, parous women who had no history of reproductive problems (1). This study was ap- Vol. 66, No.4, October 1996 proved by the Institutional Review Board of the University of Texas Southwestern Medical Center. Enzyme-Linked Immunosorbant Assay All women selected were evaluated for the presence of antiphospholipid antibodies using the ELISA method as described by Harris (11). Briefly, individual 96-well microtiter plates (Immulon-2; Dynatech Labs, Chantilly, VA) were coated with 3 fll of either cardiolipin, phosphatidylinositol, phosphatidylglycerol, phosphatidylserine, or phosphatidylethanolamine (Sigma Chemical Co., St. Louis, MO) at a concentration of 45 flg/ml (cardiolipin) in ethanol and 5 flg/ml (all other phospholipids) in methanol. The plates air dried overnight at 4 C, were blocked with 2 fll of 1% fetal calf serum (GIBCO, Long Island, NY) in Ix phosphate-buffered saline (PBS; GIBCO), washed, and incubated at 37 C for 2 hours with 5 fll of patients' sera diluted 1:5 in 1% fetal calf serum in PBS. Each unknown sample was run in triplicate. The plates then were washed to remove unbound antibody and proteins, and a secondary antibody, alkaline-phosphatase-conjugated antihuman IgG (Caltag Labs, South San Francisco, CA), IgM (Biosource; Tago Immunologicals, Camarillo, CA), or IgA (Calbiochem, La Jolla, CA) was added to the plate. After incubation and washing, p-nitrophenyl phosphate substrate (no. 14; Sigma) was added and used to measure indirectly the level of anti phospholipid antibodies in a patient's serum. The optical density ofthe samples, caused by the cleavage of the substrate by the enzyme, was determined at 45 nm by a BioRad Microplate Reader Model 45 (BioRad Laboratories, Richmond, CA) and was used to quantitate the amount of anti phospholipid antibodies in the sera. Every assay plate also included a known high-positive anticardiolipin sample (> 1 G phospholipid units [GPL]) run in triplicate. Plates were incubated until the high-positive wells achieved an optical density> 1.; typically, this required an incubation of 2 to 3 minutes. Referenced standard sets for cardiolipin (Louisville APL Diagnostics, Louisville, KY) and known negative sera were used on every plate. All results were defined in phospholipid units for IgG and IgM (MPL) as follows: < 1 units, negative; 1 to 19 units borderline; 2 to 8 units, positive; and >8 units, high positive. Results for IgA were defined in phospholipid units for IgA (APL) as follows: <3 units, negative; ~3 units, positive. Phosphatidylinositol, phosphatidyl glycerol, and phosphatidylserine values were interpreted based on the anticardiolipin standards of Harris (11). For phosphatidylethanolamine, the multiples of the median method was used for standardization as described previously (12). Briefly, phospholipid units Yetman and Kutteh Antiphospholipid antibody panels 541
3 for IgG and IgM were calculated for each serum sample, and the median value was determined from the non-gaussian distribution. The cutoff value in phospholipid units for each antiphospholipid antibody was then determined by using the 99th percentile of the normal population, approximately 3. times the median value. All values reported as positive were the mean of triplicate determinations with background absorbance obtained from wells prepared without the coating phospholipid subtracted. Any values with standard error> 1% were discarded and reassayed. Interassay variation was <8% and intra-assay variation was <6%. Statistical Analysis Statistical analyses were performed using the twotailed Fisher's exact test and the X 2 test. The Academic Computing Services ofthe University of Texas Southwestern Medical Center at Dallas were used. RESULTS Abnormal Findings in Women With Recurrent Pregnancy Loss All women with recurrent pregnancy loss were encouraged to undergo a complete evaluation as described in Materials and Methods; however, only 83% had a complete evaluation as described. For example, of the couples who had a karyotype analysis, 2.6% (191721) had an abnormal parental chromosome thought to be compatible with pregnancy loss. More than 7 women were evaluated for luteal phase defect, uterine abnormality, and cervical infection as described above. Approximately, 8% of women were found to have an abnormal test after hormonal evaluation, 14% had an abnormal hysterosalpingogram or hysteroscopy, and 6% had a positive cervical culture. In each case, if multiple abnormal findings were identified concurrently, appropriate treatment for each problem was initiated. For example, women with luteal phase deficiency were supplemented with 5 mg vaginal P two times per day. Women with abnormal findings on hysterosalpingogram were counseled to have a hysteroscopy and corrective procedures as indicated. Women with positive cervical cultures for mycoplasma, ureaplasma, or chlamydia were treated with a 1-day course of doxycycline and, in most cases, their partner was treated simultaneously. Antiphospholipid Antibodies in Women With Recurrent Pregnancy Loss Versus Controls Blood samples from 866 women with recurrent pregnancy loss and 288 control women were tested by ELISA for anti phospholipid antibodies. Immuno- 542 Yetman and Kutteh Antiphospholipid antibody panels Table 1 Positive Antiphospholipid Anttibodies in Control Women Versus Women With Recurrent Pregnancy Loss* Recurrent pregnancy Antiphospholipid Controls loss Isotype antibodies (n = 288) (n = 866) Significance IgM Cardiolipin 3 (1.) 19 (2.2) t IgG Cardiolipin 12 (4.2) 135 (15_6) <.1 IgM Phosphatidylinositol 2 (.7) 18 (2.1) IgG Phosphatidylinositol 12 (4.2) 125 (14.4).1 IgM Phosphatidylglycerol 3 (1.) 37 (4.3).8 IgG Phosphatidylglycerol 7 (2.4) 97 (11.2) <.1 IgM Phosphatidylserine 5 (1.7) 14 (1.6) IgG Phosphatidylserine 6 (2.1) 64 (7.4).1 IgM Phosphatidylethanolamine 6 (2.1) 28 (3.2) IgG Phosphatidylethanolamine 8 (2.8) 59 (6.8).18 * Values in parentheses are percentages. t, not significant. globulin G anti phospholipid antibodies of each phospholipid were more prevalent in the women with recurrent pregnancy loss than in the control individuals (Table 1). Overall, 12 of288 (4%) different individuals from the control group were positive for anticardiolipin antibodies, whereas 15 different women of 866 (17.3%) with a history of recurrent pregnancy loss were positive for IgG and/or IgM anticardiolipin antibodies (P <.1). Although IgM anti phospholipid antibodies were found more frequently in women with recurrent pregnancy loss compared with the control women, these differences were only significant when considering phosphatidylglycerol (P =.8). Many women had positive antibodies in more than one category; therefore, the number of different women with any positive antibody present included 237 of 866 (27.4%). Anticardiolipin Antibodies Negative but Other Antiphospholipid Antibodies Positive in Women With Recurrent Pregnancy Loss To determine if any women with negative anticardiolipin antibodies were positive for one of the other antiphospholipid antibodies, results for IgM, IgG, and IgA antibodies against phosphatidylinositol, phosphatidylglycerol, phosphatidylserine, and phosphatidylethanolamine were evaluated. As demonstrated in Table 2, a number of women with recurrent pregnancy loss were positive for an anti phospholipid antibody but completely negative for IgM, IgG, and/or IgA anticardiolipin antibodies. In all, 87 of866 (1.1%) women with recurrent pregnancy loss were negative for anticardiolipin antibodies and positive for one of the other antiphospholipid antibodies, considering patients with more than one positive immunoglobulin only once. Fertility and Sterility
4 Table 2 Anticardiolipin Antibodies Negative and Other Antiphospholipid Antibodies Positive in Women With Recurrent Pregnancy Loss* IgM IgG IgA Phosphatidylinositol 4 (.46) 34 (3.9) 1 (.12) Phosphatidylglycerol 12 (1.4) 9 (1.) 1 (.12) Phosphatidylserine 2 (.23) 8 (.92) 2 (.23) Phosphatidylethanolamine 11 (1.3) 2 (2.3) 3 (.35) * Numbers represent patients with the indicated isotype positive regardless of other positive results. Values in parentheses are percentages based on 866 different patients. Isolated Positive Antiphospholipid Antibody Test Results This study identified the prevalence of a single, isolated positive antibody on the panel of 15 antiphospholipid antibodies (Table 3). The most frequent isolated positive antibody excluding cardiolipin was phosphatidylethanolamine, which occurred in 21 of 866 patients (2.5%) with IgG and IgM isotopes distributed approximately equally. Isolated positive phosphatidylinositol was found only in the IgG isotype in 2 of 866 women (2.3%) with recurrent pregnancy loss. Isolated positive phosphatidylglycerol occurred in 1 of866 patients (1.1 %) and was primarily the IgM isotype. Only 1 of 866 women (.12%) with recurrent pregnancy loss had isolated positive IgM phosphatidylserine. Isolated IgA of any phospholipid was extremely rare and was identified only in antiphosphatidylethanolamine in 2 of 866 patients (.23%). Demographics of Women With Recurrent Pregnancy Loss Women with recurrent pregnancy loss and positive anticardiolipin antibodies were compared with women with recurrent pregnancy loss and negative anticardiolipin antibodies but with another antiphospholipid antibody positive (Table 4). Complete clinical history confirmed by medical records was available in 66 of 15 women with positive anticardiolipin antibodies and 38 of 87 women with other positive anti phospholipid antibodies. As shown, no significant differences existed in the age of the women at entry, numbers of prior pregnancies, numbers of prior pregnancy losses, or the number of prior livebirths in both groups of women. Both groups had similar levels ofigg and IgM antiphospholipid antibodies, 46.4 ± 3.5 (mean ± SD; range 2.2 to 133) phospholipid units versus 3.9 ± 1.8 (range 2.2 to 58.7) phospholipid units, respectively. Although the average levels of IgG anticardiolipin (48.2 ± 31.4) were higher than the average levels of IgG against other phospholipids (39.9 ± 29), these differences Vol. 66, No.4, October 1996 were not significant. It is important to realize that anticardiolipin antibodies were negative ( < 1 GPL) in all women with other phospholipids positive as presented in Tables 2, 3, and 4. Differences were noted in the estimated gestational age at the time of loss and the frequently distribution of IgG and IgM isotopes in the two groups. The estimated gestational age at the time of loss for the anticardiolipin positive group of women was 9.3 ± 6.1 weeks, whereas the estimated gestational age at the time of loss for the group with another antiphospholipid antibody positive was earlier, 6.4 ± 4.3 weeks (P =.1). Immunoglobulin G class antibodies were found more frequently in both the cardiolipin group (92.7%) as well as the other antiphospholipid antibodies-positive group (72.5%); however, these differences were significant (P =.5). DISCUSSION In this study, only 4% of control women had a positive result for anticardiolipin antibodies, agreeing with previous reports of 1 % to 4% (13, 14). Additionally, our results indicate 17.3% of women with recurrent pregnancy loss had positive anticardiolipin antibodies. These data correlate with several different investigations that found a range of 8% to 42% of recurrent pregnancy loss samples were positive for anticardiolipin antibodies (1, 15-17). This study emphasizes the importance of standardization of ELISA, quality control, and careful interpretation of positive results. Retrospective analysis of 866 samples from different women with a history of recurrent pregnancy loss revealed 17.3% (15/866) of these samples were positive for IgM, IgG, or IgA anticardiolipin antibodies. An additional 1.1 % (87/866) were positive for other antiphospholipid antibodies, whereas anticardiolipin antibodies remained negative. If any of the other antiphospholipid antibodies are indeed significant, these data suggest that 1.1% of women evaluated for anticardiolipin antibodies exclusively would not be identified unless the other antibodies were evaluated. Table 3 Isolated Positive Antiphospholipid Antibodies in Women With Recurrent Pregnancy Loss* IgM IgG Cardiolipin 17 (2.) Phosphatidylinositol 2 (2.3) Phosphatidylglycerol 9 (1.) 1 (.12) Phosphatidylserine 1 (.12) Phosphatidylethanolamine 8 (.9) 11 (1.3) IgA 2 (.23) * Numbers represent patients with the indicated isolated isotype positive. Values in parentheses are percentages based on 866 different patients. Yetman and Kutteh Antiphospholipid antibody panels 543
5 1 Table 4 Demographics of Women With Pregnancy Loss and Anticardiolipin Antibodies Versus Those With Negative Anticardiolipin Antibodies and Another Antiphospholipid Antibody Positive Cardiolipin positive (n = 66) Other phospholipids positive (n = 38) Significancet Age at entry (y) Prior pregnancies per patient Prior live births per patient Total prior losses per patient Prior losses < 2 weeks (%) Prior losses 2: 2 weeks (%) Age at loss (wk) IgG antibodies only (%) IgM antibodies only (%) IgG antiphospholipid antibody level per patient:j: IgM anti phospholipid antibody level per patient:j: 33 :!: 6.6* 3.7:!: 1.7.8:!:.8 3.:!: :!: :!: 31.4 (2.2 to 133) 28.4:!: 4.5 (24.1 to 31.4) 34 :!: :!: 1.4.8:!:.9 2.8:!: :!: :!: 29 (2.2 to 58.7) 29.2 :!: 1.6 (2.5 to 49.3) * Values are means:!: SD with ranges in parentheses. t, not significant. The t-test and Fisher's two-tailed exact test were used to calculate P values. :j: Antiphospholipid antibodies are defined in phospholipid units. Therefore, with strict standardization, 27.4% ( ) of women with recurrent pregnancy loss were positive for any of the five antiphospholipid antibodies. Considerable attention has been directed to recent investigations that reported positive antiphospholipid antibodies in 59% of women with recurrent pregnancy loss (8) and in >6% of samples from women with a history of infertility (18). Another group, also using a panel of antiphospholipid antibodies, found that >6% of recurrent pregnancy loss samples were positive for an antiphospholipid antibody other than cardiolipin (9). These very high positive rates of anti phospholipid antibodies must be considered in context of the reported prevalence of 25% to 42% of patients diagnosed with systemic lupus erythematosus and fetal loss have positive anticardiolipin antibodies (19-22). Therefore, one must seek other explanations for the investigations that concluded approximately 6% of women with recurrent pregnancy loss or infertility problems had positive antiphospholipid antibodies (23). Although the ELISA used in our laboratory includes a similar panel of antiphospholipid antibodies used by these investigators (8, 9), many differences exist because of various methods of standardization, normal controls, and the cutoff values used to determine positive results. Our laboratory currently implements a full set of standards as well as a positive and negative control on each assay plate. Conversely, several commercially available kits provide only a single standard or a dilution of standards. Furthermore, in our assay, standards and unknown samples were evaluated in triplicate and values with standard errors> 1% were reassayed. Moreover, a known high-positive anticardiolipin sample was assayed on each plate and plates were incubated until optical densities were> 1.. Intra-assay varia- 544 Yetman and Kutteh Antiphospholipid antibody panels tion in this assay is <6%. Positive and negative samples routinely are frozen at -7 C and re-evaluated to ascertain intra-assay variation that is <8%. The normal controls used in our analysis were strictly women of reproductive age with at least one child and no history of pregnancy loss. Other investigators have included only approximately 4 men and women as their "normal controls" (8, 9). Additionally, the level or value considered as positive will influence the number of positive results (23). For example, some investigators considered antiphospholipid antibodies "detected at any concentration" significant (18) or concluded a value three standard deviations above the median positive (8, 9); therefore, using these criteria, more positive individuals would be identified. Positive samples in our study were based on Harris (11) phospholipid standards used in each assay with IgM and IgG antibodies considered positive if values were >2 phospholipid units and with IgA antibodies considered positive if values were >3 phospholipid units. For phosphatidylethanolamine, we interpreted positive values using the multiples of the median method, which determines the cutoff values by taking the 99th percentile of the normal population (3. times the median) (7). International efforts to standardize the reporting of anti phospholipid antibodies continue (24). Our study reports that 87 of 866 (1.1%) women with recurrent pregnancy loss had positive antiphospholipid antibodies other than anticardiolipin antibodies. This is much lower than previous studies, which indicated a prevalence of >6% positive antiphospholipid antibodies other than anticardiolipin antibodies (9). Their study design, which used multiple samples from the same individuals, can explain in part the greater prevalence of positive antiphospholipid antibodies. For example, 399 women were Fertility and Sterility
6 .. tested repeatedly to generate> 1,5 test results (9). The results reported in our study indicate that the prevalence of positive anti phospholipid antibodies other than cardiolipin in 866 different women is much lower. The significance of IgM anti phospholipid antibodies is unclear from this evaluation. Only when considering IgM antiphosphatidylglycerol were significant differences in prevalence identified between control women and women with recurrent pregnancy loss (P =.8). Thus, in the absence of positive IgG antibodies, caution in the interpretation of IgM positive results must be exercised. The significance of isolated findings of a single antiphospholipid antibodies from a panel of tests also is unclear and results must be interpreted with caution. It is important to note that approximately 4% of the positive antiphospholipid antibodies excluding cardiolipin occurred as an isolated finding. Generally, when positive anticardiolipin antibodies are excluded, isolated positive anti phospholipid antibodies have not been considered significant unless they have been repeated on multiple occasions and occur in high levels. The demographics of women with recurrent pregnancy loss and positive anticardiolipin antibodies versus other positive antiphospholipid antibodies in this study were tabulated, and most of the differences were not significant. This suggests that women with positive phospholipid antibodies other than cardiolipin have suffered a similar clinical course as women with anticardiolipin antibodies. Women with negative anticardiolipin antibodies and another anti phospholipid antibody positive had an estimated gestational age at the time of loss of 6.4 ± 4.3 weeks or approximately 3 weeks earlier than women with anticardiolipin antibodies positive (9.3 ± 6.1 weeks) (P =.1). This suggests that if the antiphospholipid antibodies other than cardiolipin are associated with pregnancy loss that they might exert their effects even before the detection of fetal cardiac activity. Furthermore, even though IgG antibodies were identified most frequently in both groups of women, there were significantly more women with IgM antibodies in the other positive anti phospholipid antibody group when compared with the anticardiolipin-positive group (P =.5); these were most frequently IgM antiphosphatidylglycerol. We currently are following both groups of women with a history of recurrent pregnancy loss and positive antiphospholipid antibodies. When all other diagnostic tests are negative and a couple has a clinical history of recurrent pregnancy loss with positive levels of anticardiolipin antibodies or antiphosphatidylserine antibodies on multiple occasions, we advo- cate treatment with subcutaneous heparin and aspirin throughout pregnancy (25). We hope to establish the clinical significance, if any, of antibodies to phospholipids other than cardiolipin or phosphatidylserine. REFERENCES 1. Harris EN, Hughes GR. Thrombosis and miscarriages: the antiphospholipid antibody story. In: Atlas of science: immunology. Philadelphia: Institute of Scientific Information, 1988: Cowchock FS. The role of antiphospholipid antibodies in obstetric medicine. In: Lee RV, editor. Current obstetric medicine. St. Louis: Mosby-Yearbook, Inc., 1991: Triplett DA. Antiphospholipid antibodies and recurrent pregnancy loss. Am J Reprod Immunol 1989;2: Harris EN, Gharavi AE, Patel SP, Hughes GRV. Evaluation of the anti-cardiolipin antibody test: report of a standardization workshop held April 4th, Clin Exp Immunol1987; 68: Harris EN. The Second International Anti-Cardiolipin Standardization workshop/the Kingston Anti-Phospholipid Antibody Study (KAPS) group. Am J Clin Pathol 199;94: Peaceman AM, Silver RK, MacGregor SN, Socol MC. Interlaboratory variation in antiphospholipid antibody testing. Am J Obstet Gynecol 1992; 166: Cowchock FS, Fort J, Ingham K. Use of a population-based calculation (M.O.M.) to express ELISA results for antiphospholipid antibodies. In: Dondero F, Johnson PM, editors. Reproductive immunology. Serono Symposia Publication. New York: Raven Press, 1993: Matzner W, Chong P, Xu G, Ching W. Characterization of anti phospholipid antibodies in women with recurrent spontaneous abortions. J Reprod Med 1994;39: Gilman-Sachs A, Lubinski J, Beer AE, Brend S, Beaman KD. Patterns of antiphospholipid antibody specificities. J Clin Lab Immunol 1991;35: Kutteh WH, Pasquarette MM. Recurrent pregnancy loss. Adv Obstet GynecoI1995;2: Harris EN. Annotation: antiphospholipid antibodies. Br J Haematol 199; 74: Kutteh WH, Webster R, Kutteh CC. Multiples ofthe median: an alternative method for reporting antiphospholipid antibodies in women with recurrent pregnancy loss. Obstet Gynecol 1994;84: Lockwood CJ, Romero R, Feinberg RF, Clyne LP, Coster B, Hobbins JC. The prevalence and biological significance oflupus anticoagulant and cardiolipin antibodies in a general obstetric population. Am J Obstet Gynecol 1989; 161: Harris EN, Spinnato JA. Should anticardiolipin tests be performed in otherwise healthy pregnant women? Am J Obstet Gynecol1991; 165: Cowchock S, Smith JB, Gocial B. Antibodies to phospholipids and nuclear antigens in patients with repeated abortions. Am J Obstet GynecoI1986;155: Unander AM, Norberg R, Hahn L, Arfors L. Anticardiolipin antibody and complement in ninety-nine women with habitual abortion. Am J Obstet GynecoI1987;156: Lockwood CJ, Reece EA, Romero R, Hobbins JC. Antiphospholipid antibodies and pregnancy wastage. Lancet 1986; 1: Sher G, Feinman M, Zouves C, Kuttner G, Maassarani G, Vol. 66, No.4, October 1996 Yetman and Kutteh Antiphospholipid antibody panels 545
7 Salem R, et al. High fecundity rates following in-vitro fertilization and embryo transfer in anti-phospholipid antibody seropositive women treated with heparin and aspirin. Hum Reprod 1994;9: Alarcon-Segovia D, Deleze M, aria CO, Sanchez-Guerrerro J, Gomez-Pacheco L, Cabiedes J, et al. Antiphospholipid antibodies and antiphospholipid syndrome in systemic lupus erythematosus: a prospective analysis of 5 consecutive patients. Medicine (Baltimore) 1989;68: Qamar T, Levy R, Sammaritano L, Gharavi AE, Lockshin MD. Characteristics of high-titer IgG anti phospholipid antibody in systemic lupus erythematosus patients with and without fetal death. Arthritis Rheum 199;33: Love PR, Santoro SA. Antiphospholipid antibodies: anticardiolipin and the lupus anticoagulant in systemic lupus erythe- matosus (SLE) and in non-sle disorders. Ann Intern Med 199; 112: Kutteh WH, Lyda EC, Abraham SM, Wacholtz MC. Association of anticardiolipin antibodies and pregnancy loss in women with systemic lupus erythematosus. Fertil Steril 1993; 6: Bronson R. Editorial: Immunology and reproductive medicine. Hum Reprod 1995;1: Harris EN, Pierangeli SS, Birch D. Anticardiolipin wet workshop report: Vth International Symposium on antiphospholipid antibodies. Am J Clin Pathol 1994; 11: Kutteh WH. Antiphospholipid antibodies-associated recurrent pregnancy loss: treatment with heparin and low-dose aspirin is superior to low-dose aspirin alone. Am J Obstet Gynecol 1996; 174: Yetman and Kutteh Antiphospholipid antibody panels Fertility and Sterility
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