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Obstetrics & Gynecology 2006;107:293-299
© 2006 by The American College of Obstetricians and Gynecologists
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ORIGINAL RESEARCH

Early Risk Factors for Pregnancy Loss in Lupus

Megan E. B. Clowse, MD, MPH1, Laurence S. Magder, PhD2, Frank Witter, MD3 and Michelle Petri, MD, MPH4

From the 1Department of Medicine, Division of Rheumatology, Duke University Medical Center, Durham, North Carolina; 2Department of Biostatistics, University of Maryland School of Medicine, Baltimore, and 3Departments of Gynecology and Obstetrics, and 4Medicine, Division of Rheumatology, Johns Hopkins University School of Medicine, Baltimore, Maryland.


   ABSTRACT
TOP
ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
OBJECTIVE: To identify early risk factors for pregnancy loss in lupus pregnancies.

METHODS: We conducted a cohort study of all pregnancies seen in the first trimester in lupus patients followed from 1987 to 2002 at the Hopkins Lupus Center. At each visit, vital signs, a complete blood count, a urinalysis, and a 24-hour urine collection for total protein, if the dipstick revealed proteinuria, were obtained. Proteinuria was defined as protein greater than 500 mg in a 24-hour urine collection. Secondary antiphospholipid syndrome was diagnosed by using the Sapporo criteria. Thrombocytopenia was defined as platelets under 150,000. Hypertension was defined as blood pressure over 140/90 mm Hg during the first trimester. Pregnancies electively terminated were excluded from this study.

RESULTS: One hundred sixty-six pregnancies in 125 women were followed in the Hopkins Lupus Cohort from the first trimester onward. Twenty-seven pregnancies (16%) ended with a loss. Pregnancy loss was increased 2.6 times in women with first-trimester proteinuria (P = .04). A diagnosis of secondary antiphospholipid syndrome led to a 3.1-fold increase in pregnancy loss, predominantly after 20 weeks of gestation (P = .004). Thrombocytopenia in the first trimester led to an increase in pregnancy loss by 3.3 fold (P ≤ .001). First-trimester hypertension led to a 2.4-fold increase in pregnancy loss (P = .027). Each risk factor was independent in raising pregnancy loss risk.

CONCLUSION: The acronym PATH can help remind clinicians to monitor for Proteinuria, Antiphospholipid syndrome, Thrombocytopenia, and Hypertension early in pregnancy. Close observation, with frequent laboratory analysis and appropriate therapy, is important to pregnancy success in women with lupus.

LEVEL OF EVIDENCE: II-2

As care for systemic lupus erythematosus (SLE) improves, more women with this disease are healthy enough to conceive and carry successful pregnancies. The majority of pregnancies in women with SLE are successful, although many are delivered prematurely. Few long-term effects of lupus are found in these offspring.4 Lasting maternal disability secondary to lupus activity during pregnancy is also rare.3,5,6

Not all pregnancies in women with SLE will result in a live birth, however. Previously identified risk factors for poor pregnancy outcome include the presence of antiphospholipid syndrome and increased lupus activity in the 6 months preceding or during pregnancy.3,7–10 We have reviewed a large cohort of lupus pregnancies to identify risk factors, measurable in the first trimester, that are predictive for pregnancy loss.


   MATERIALS AND METHODS
TOP
ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
The Hopkins Lupus Pregnancy Cohort has accrued consecutive lupus pregnancies that were seen in the Hopkins Lupus Center since 1987. This study includes pregnancies up until 2002. The Johns Hopkins institutional review board approved the collection of data into the Hopkins Lupus Pregnancy Cohort. Each woman signed informed consent paperwork before being enrolled in the cohort. Data were collected prospectively, and pregnancy outcomes were obtained from interview with the mother and/or obstetric records soon after delivery. All women were diagnosed with SLE either before or during the reported pregnancy. Only pregnancies in which the woman was seen in the Lupus Center were included in this study. The 6 pregnancies that ended in an elective abortion for reasons other than the health of the mother or the condition of the fetus were excluded.

At each clinic visit before and during pregnancy, laboratory testing was performed. This included complete blood count and urinalysis with a 24-hour urine for protein if there was more than 1+ protein on dipstick. Assessment of the lupus anticoagulant and anticardiolipin antibodies was made at most visits, but especially at the first visit in each pregnancy.

Secondary antiphospholipid syndrome was diagnosed according to the Sapporo criteria, fulfilling both laboratory and clinical criteria.11 Primary antiphospholipid syndrome occurs in women without other autoimmune diseases and secondary antiphospholipid syndrome occurs in patients with other diagnoses, most commonly SLE. Each woman with antiphospholipid syndrome had moderate to high positive anticardiolipin IgG and/or IgM antibodies or a positive lupus anticoagulant with positive mixing studies and confirmatory tests on 2 occasions at least 6 weeks apart. Clinical criteria for antiphospholipid syndrome included a history of thrombosis, prior pregnancy loss after 12 weeks, or 3 consecutive first-trimester pregnancy losses.

Thrombocytopenia was defined as a platelet count below 150,000 at any time during the first trimester. A 24-hour urine protein level greater than 500 mg during the first trimester constituted proteinuria.

The blood pressure was obtained as part of routine care at each clinic visit. Any measurement of the systolic blood pressure over 140 mm Hg or the diastolic blood pressure over 90 mm Hg during the first trimester was recorded as hypertension for this study. At each visit, the current medications were also recorded, allowing an assessment of the use of hypertensive medications. Despite being seen in a clinic, 3 women did not have blood pressure measurements recorded in the first trimester. One of these had a miscarriage at 11 weeks of gestation and the other 2 carried to full term.

Pregnancy loss was defined as any pregnancy that did not result in an infant that survived more than 28 days. A miscarriage was a pregnancy loss that occurred before 20 weeks of gestation. A stillbirth was defined as a pregnancy loss that occurred after 20 weeks gestation. For simplicity of presentation, the 2 infants that died soon after birth from complications of extreme prematurity were included in the stillbirth category.

Subgroups of women defined by first-trimester risk factors were compared with respect to the rates of miscarriages or stillbirths. The statistical significance of observed differences and associated confidence intervals for effects were calculated based on parameter estimates and their standard errors, derived from generalized estimating equation models12 (implemented in SAS 8.02). This approach appropriately accounts for the fact that some women in the study had multiple pregnancies.


   RESULTS
TOP
ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
One hundred sixty-six pregnancies were seen during the first trimester in 125 women. Thirty-one (19%) of the women were seen in the first 4 weeks of pregnancy, 70 (42%) were first seen in weeks 4 to 8, and 65 (39%) were first seen in the last 4 weeks of the first trimester. The majority of the women were white and the mean maternal age at delivery was 30 years (Table 1). Most women had been diagnosed with lupus several years before the pregnancy. However, 12 cases of lupus were diagnosed during the studied pregnancy. Almost half of the women had a history of lupus nephritis. A quarter of the pregnancies were to nulliparous women; the other women had had at least one pregnancy before presenting to the Hopkins Lupus Clinic.


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  		Table 1. Demographic Information for Each Risk Factor

 

Some important differences between women with each of the identified risk factors were noted. (Table 1) The ethnic composition was strikingly different with few African Americans having antiphospholipid syndrome or thrombocytopenia, but a large percentage having proteinuria. Women with antiphospholipid syndrome had more prior pregnancy losses and, as would be expected with this syndrome, an excessive number of late pregnancy losses. Women with a history of lupus nephritis were more common to have proteinuria and/or hypertension during the first trimester.

Of the 166 pregnancies, 84% produced a live birth, 15 (9%) resulted in a miscarriage and 12 (7%) resulted in a stillbirth. The timing of these pregnancy losses included 9 before 10 weeks of gestation, 6 between weeks 10 and 15, none between weeks 15 and 20, 9 between weeks 20 and 25, and 3 between weeks 25 and 30.

Four first-trimester risk factors, proteinuria, secondary antiphospholipid syndrome, thrombocytopenia, and hypertension, each led to a several-fold increase in pregnancy loss (Table 2). This rate of pregnancy loss was elevated for both miscarriages and stillbirths in pregnancies affected by these risks. The presence of proteinuria in the first trimester led to a 2.6-fold increase in pregnancy loss (P = .04) and a 4.1-fold increase in miscarriage (P = .02). Antiphospholipid syndrome increased the risk of pregnancy loss by 3.1-fold (P = .004) and for stillbirths by 5-fold (P = .001). A low platelet count in the first trimester was associated with a 3.3-fold increase in pregnancy loss (P < .001) and a significant increase in both miscarriages and stillbirths. First-trimester hypertension increased the pregnancy loss rate by 2.4-fold (P = .03) and increased the stillbirth rate by 3.2-fold (P = .03).


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  		Table 2. Pregnancy Loss for Each First-Trimester Predictor

 

Both SLE and antiphospholipid syndrome can be associated with thrombocytopenia. In this cohort, thrombocytopenia was found in 30% of women with secondary antiphospholipid syndrome but in only 10% of those without secondary antiphospholipid syndrome. The rate of pregnancy loss was higher for patients with low platelet counts, regardless of antiphospholipid syndrome status. Among women with thrombocytopenia in the first trimester, 5 of 15 (33%) pregnancies without antiphospholipid syndrome ended in pregnancy loss and 4 of 6 (66%) with antiphospholipid syndrome ended with a loss.

Patients with a history of renal disease had a 4.3-fold increased risk for first-trimester proteinuria (14% versus 3%, 95% confidence interval [CI] for risk ratio 1.6–16.4, P = .007).

Women with laboratory findings consistent with antiphospholipid syndrome, but without prior thrombosis or pregnancy loss, did not have an increased risk of pregnancy loss. Of 66 pregnancies in such women, 8 (12%) resulted in pregnancy loss. This was significantly less than those with secondary antiphospholipid syndrome (40% pregnancy loss, risk ratio 3.3, 95% CI 1.5–8.0, P = .006) and similar to that of patients without the laboratory findings (15% pregnancy loss).

The combination of heparin and aspirin was used during 17 pregnancies with secondary antiphospholipid syndrome, 5 (29%) of which were lost. Each of the 3 pregnancies in women with secondary antiphospholipid syndrome that were not treated with this combination was lost (one had no treatment, one had aspirin only, one had heparin only).

Women who took antihypertensive medications that maintained normal blood pressure readings appeared to have improved pregnancy outcomes over women who had hypertension, although the difference did not meet statistical significance. Twelve women took effective doses of antihypertensive medications, and none of them suffered a pregnancy loss. Thirteen women took ineffective doses of antihypertensive medications and had 5 pregnancy losses (38%), and 16 women had hypertension without first-trimester treatment and had 4 (25%) losses.

Ethnicity and pregnancy history do not appear to be as good predictors of pregnancy loss in this cohort. Of 48 pregnancies to African-American women, 6 (12.5%) ended with a loss and of 112 pregnancies of white women, 21 (18.75%) ended with a loss. In this cohort, the vast majority of women with antiphospholipid syndrome are white. If women with antiphospholipid syndrome are removed from the ethnicity analysis, the rate of pregnancy loss between African-American and white women is almost identical (13% versus 14%).

Of 125 pregnancies preceded by at least one pregnancy, 69 (55%) had had a loss. Twenty percent of the current pregnancies resulted in a loss, while 16% of pregnancies without a prior loss ended with a miscarriage or stillbirth. If women with antiphospholipid syndrome are removed from this analysis, the difference in pregnancy loss based on pregnancy history becomes less (15% loss if prior loss versus 17% loss if no prior loss). The number of pregnancies in this cohort does not provide the power to detect a significant difference between these rates.

A generalized estimating equation model, adjusting for each of the four identified first-trimester risk factors, suggests the independence of each of these risk factors (Table 3). Adjusted for the other predictors, each risk factor increased the risk for pregnancy loss by 2.1 to 4.4 fold. The sample size is relatively small compared with the number of variables in the adjustment, leading to the need for some skepticism in interpreting the P values of this model. It does show, however, that each of these risk factors alone, not only in combination, may put a pregnancy at increased risk.


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  		Table 3. Adjusted Odds Ratio for Prediction of Pregnancy Loss

 


   DISCUSSION
TOP
ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The majority of pregnancies in women with SLE result in a live birth. However, lupus pregnancies have a higher risk of loss and preterm birth than those in healthy women. We have identified four risk factors for pregnancy loss that can be determined by routine testing early in pregnancy. We suggest the acronym PATH (Proteinuria, Antiphospholipid syndrome, Thrombocytopenia, and Hypertension) to easily remember these important risk factors. These data suggest that each of these risk factors independently increases the risk of pregnancy loss several fold over other pregnant women with lupus. Each can, and should, be ascertained as soon as possible after pregnancy is diagnosed in a woman with lupus. (Table 4)


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  		Table 4. PATH: Early Risk Factors for Pregnancy Loss in Lupus

 

Proteinuria in the first trimester, defined as a 24-hour urine protein collection of more than 500 mg, is often an indication of lupus nephritis. First-trimester proteinuria would not occur from preeclampsia. We recommend that women with lupus have a urinalysis monthly during pregnancy. If the protein dipstick is elevated (≥ 1+), then a 24-hour urine protein or a spot urine protein:creatinine ratio should be obtained to quantify the degree of proteinuria.13 Some increase in baseline proteinuria can be expected during pregnancy. Lupus nephritis comes in several forms, ranging from more benign mesangial lesions to more severe diffuse proliferative glomerulonephritis. In a nonpregnant patient, a renal biopsy would be used to determine the severity of the renal disease and dictate therapy. During pregnancy, however, renal biopsy may carry additional risks. In our multivariate model, proteinuria appears to double the risk of pregnancy loss, although this difference is not statistically significant. Because it can be an important indication of lupus activity, we continue to emphasize the importance of frequent assessment of proteinuria and treatment when high levels are found.

Antiphospholipid syndrome is a syndrome of antiphospholipid antibodies, hypercoagulability, and recurrent pregnancy loss. If left untreated, up to 90% of pregnancies in women with antiphospholipid syndrome will end in miscarriage or stillbirth.14 Although it was previously thought that the etiology for pregnancy loss was thrombosis in the placenta, a murine model has now suggested that complement activation at the uteroplacental interface is responsible. Current therapy for antiphospholipid syndrome during pregnancy is the combination of daily low-dose aspirin and low-molecular-weight heparin.18 On this regimen, pregnancy loss rates drop to between 15% and 35%.

Our analysis of this cohort demonstrated that the presence of anticardiolipin antibodies and/or the lupus anticoagulant without the clinical criteria for secondary antiphospholipid syndrome did not increase the risk for pregnancy loss among lupus patients.

In SLE, platelet-specific antibodies can cause thrombocytopenia. Many lupus patients will have a moderate degree of thrombocytopenia (that is, 50,000–150,000). A smaller proportion will have severe thrombocytopenia requiring urgent therapy. Antiphospholipid syndrome can also cause thrombocytopenia, independently of SLE. In this study, women with both thrombocytopenia and secondary antiphospholipid syndrome experienced more pregnancy loss than either risk factor alone. Finally, pregnancy itself can be associated with thrombocytopenia. However, we thought it unlikely that the first-trimester thrombocytopenia seen in this study would be secondary to pregnancy alone.

Hypertension during pregnancy has been identified as an important risk factor for pregnancy loss and complications in lupus patients, as well as otherwise healthy women.6,24–27 In this cohort of lupus pregnancies, the presence of hypertension during the first trimester placed the pregnancy at increased risk of stillbirth. The proportion of pregnancies lost in women with hypertension taking antihypertensive medications versus those not taking antihypertensive medications was similar. Women with well-controlled hypertension, however, had improved pregnancy survival. Therefore, we recommend continuing needed antihypertensive medications during pregnancy in women with SLE, although angiotensin-converting enzyme inhibitors must be discontinued.

Other risk factors for pregnancy loss previously identified from this cohort include lupus activity in the months before pregnancy, lupus activity during pregnancy, and the combination of hypocomplementemia and lupus activity.3,28 Ethnicity and prior pregnancy loss are not good predictors of pregnancy loss in this cohort. The size of this cohort, however, precludes us from determining the statistical significance of small differences.

The ethnic differences in the four risk factor groups are reflective of typical patterns for lupus and antiphospholipid syndrome. Proteinuria was more common in the African-American women in this cohort. Prior studies also demonstrate a significantly higher prevalence of renal disease in women of African descent than in white women. Antiphospholipid syndrome may not be as prevalent in women of African descent as it is in white women.32,33

We have identified four clear risk factors for early pregnancy loss in women with lupus. The acronym PATH (Proteinuria, Antiphospholipid syndrome, Thrombocytopenia, and Hypertension) will help remind clinicians to look for these risk factors. We recommend obtaining vital signs, urinalysis, and complete blood count monthly during pregnancy in patients with lupus to monitor for proteinuria and thrombocytopenia. In women who meet the clinical criteria for secondary antiphospholipid syndrome, positive anticardiolipin antibodies, lupus anticoagulant, or anti-ß 2-glycoprotein I will clarify this diagnosis.

Early diagnosis and treatment of the PATH risk factors might reduce pregnancy loss. Each of these risk factors can be ascertained through simple testing by an obstetrician, primary care physician, or rheumatologist. Women with secondary antiphospholipid syndrome should be treated with daily low-dose aspirin and heparin during pregnancy. Women with either proteinuria or thrombocytopenia in the first trimester should be evaluated for active lupus in collaboration with a rheumatologist. Hypertension should be treated with antihypertensive medications. Additional prospective cohort studies are recommended to confirm and extend these recommendations in SLE pregnancies.


   Footnotes
 
The Hopkins Lupus Cohort and Lupus Pregnancy Center are supported by NIAMS RO1 #AR43737 and the Hopkins General Clinical Research Center MOIRR00052.

Presented at the American College of Obstetrics and Gynecology 53rd Annual Clinical Meeting, San Francisco, May 7–11, 2005.

Corresponding author: Megan E. B. Clowse, MD, MPH, Duke University Medical Center, DUMC 3535, Trent Drive, Durham, NC 27110; e-mail: meganclowse{at}hotmail.com.

doi:10.1097/01.AOG.0000194205.95870.86


   REFERENCES
TOP
ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
1. Petri M, Allbritton J. Fetal outcome of lupus pregnancy: a retrospective case-control study of the Hopkins Lupus Cohort. J Rheumatol 1993;20:650–6.[Medline]

2. Yasmeen S, Wilkins EE, Field NT, Sheikh RA, Gilbert WM. Pregnancy outcomes in women with systemic lupus erythematosus. J Matern Fetal Med 2001;10:91–6.[Medline]

3. Clowse M, Witter FR, Magder LC, Petri M. The impact of increased lupus activity on obstetrical outcomes. Arthritis Rheum 2005;52:514–21.[Medline]

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5. Georgiou PE, Politi EN, Katsimbri P, Sakka V, Drosos AA. Outcome of lupus pregnancy: a controlled study. Rheumatology (Oxford) 2000;39:1014–9.

6. Cortes-Hernandez J, Ordi-Ros J, Paredes F, Casellas M, Castillo F, Vilardell-Tarres M. Clinical predictors of fetal and maternal outcome in systemic lupus erythematosus: a prospective study of 103 pregnancies. Rheumatology (Oxford) 2002;41:643–50.

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13. Christopher-Stine L, Petri M, Astor BC, Fine D. Urine protein-to-creatinine ratio is a reliable measure of proteinuria in lupus nephritis. J Rheumatol 2004;31:1557–9.[Medline]

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