Original Research
4 August 2015

Predictors of Pregnancy Outcomes in Patients With Lupus: A Cohort Study

Publication: Annals of Internal Medicine
Volume 163, Number 3

Abstract

Background:

Because systemic lupus erythematosus (SLE) affects women of reproductive age, pregnancy is a major concern.

Objective:

To identify predictors of adverse pregnancy outcomes (APOs) in patients with inactive or stable active SLE.

Design:

Prospective cohort.

Setting:

Multicenter.

Patients:

385 patients (49% non-Hispanic white; 31% with prior nephritis) with SLE in the PROMISSE (Predictors of Pregnancy Outcome: Biomarkers in Antiphospholipid Antibody Syndrome and Systemic Lupus Erythematosus) study. Exclusion criteria were urinary protein–creatinine ratio greater than 1000 mg/g, creatinine level greater than 1.2 mg/dL, prednisone use greater than 20 mg/d, and multifetal pregnancy.

Measurements:

APOs included fetal or neonatal death; birth before 36 weeks due to placental insufficiency, hypertension, or preeclampsia; and small-for-gestational-age (SGA) neonate (birthweight below the fifth percentile). Disease activity was assessed with the Systemic Lupus Erythematosus Pregnancy Disease Activity Index and the Physician's Global Assessment (PGA).

Results:

APOs occurred in 19.0% (95% CI, 15.2% to 23.2%) of pregnancies; fetal death occurred in 4%, neonatal death occurred in 1%, preterm delivery occurred in 9%, and SGA neonate occurred in 10%. Severe flares in the second and third trimesters occurred in 2.5% and 3.0%, respectively. Baseline predictors of APOs included presence of lupus anticoagulant (LAC) (odds ratio [OR], 8.32 [CI, 3.59 to 19.26]), antihypertensive use (OR, 7.05 [CI, 3.05 to 16.31]), PGA score greater than 1 (OR, 4.02 [CI, 1.84 to 8.82]), and low platelet count (OR, 1.33 [CI, 1.09 to 1.63] per decrease of 50 × 109 cells/L). Non-Hispanic white race was protective (OR, 0.45 [CI, 0.24 to 0.84]). Maternal flares, higher disease activity, and smaller increases in C3 level later in pregnancy also predicted APOs. Among women without baseline risk factors, the APO rate was 7.8%. For those who either were LAC-positive or were LAC-negative but nonwhite or Hispanic and using antihypertensives, the APO rate was 58.0% and fetal or neonatal mortality was 22.0%.

Limitation:

Patients with high disease activity were excluded.

Conclusion:

In pregnant patients with inactive or stable mild/moderate SLE, severe flares are infrequent and, absent specific risk factors, outcomes are favorable.

Primary Funding Source:

National Institutes of Health.

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Information & Authors

Information

Published In

cover image Annals of Internal Medicine
Annals of Internal Medicine
Volume 163Number 34 August 2015
Pages: 153 - 163

History

Published online: 4 August 2015
Published in issue: 4 August 2015

Keywords

Authors

Affiliations

Jill P. Buyon, MD
From New York University School of Medicine, Hospital for Special Surgery, Albert Einstein College of Medicine, and Weill Cornell Medical College, New York, New York; University of Utah Health Sciences Center and Intermountain Healthcare, Salt Lake City, Utah; Oestfold Hospital Trust, Fredrikstad, Norway; University of Toronto, Toronto, Ontario, Canada; Oklahoma Medical Research Foundation and the University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma;
Johns Hopkins University School of Medicine, Baltimore, Maryland; and University of Illinois at Chicago, Chicago, Illinois.
Mimi Y. Kim, ScD
From New York University School of Medicine, Hospital for Special Surgery, Albert Einstein College of Medicine, and Weill Cornell Medical College, New York, New York; University of Utah Health Sciences Center and Intermountain Healthcare, Salt Lake City, Utah; Oestfold Hospital Trust, Fredrikstad, Norway; University of Toronto, Toronto, Ontario, Canada; Oklahoma Medical Research Foundation and the University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma;
Johns Hopkins University School of Medicine, Baltimore, Maryland; and University of Illinois at Chicago, Chicago, Illinois.
Marta M. Guerra, MS
From New York University School of Medicine, Hospital for Special Surgery, Albert Einstein College of Medicine, and Weill Cornell Medical College, New York, New York; University of Utah Health Sciences Center and Intermountain Healthcare, Salt Lake City, Utah; Oestfold Hospital Trust, Fredrikstad, Norway; University of Toronto, Toronto, Ontario, Canada; Oklahoma Medical Research Foundation and the University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma;
Johns Hopkins University School of Medicine, Baltimore, Maryland; and University of Illinois at Chicago, Chicago, Illinois.
Carl A. Laskin, MD
From New York University School of Medicine, Hospital for Special Surgery, Albert Einstein College of Medicine, and Weill Cornell Medical College, New York, New York; University of Utah Health Sciences Center and Intermountain Healthcare, Salt Lake City, Utah; Oestfold Hospital Trust, Fredrikstad, Norway; University of Toronto, Toronto, Ontario, Canada; Oklahoma Medical Research Foundation and the University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma;
Johns Hopkins University School of Medicine, Baltimore, Maryland; and University of Illinois at Chicago, Chicago, Illinois.
Michelle Petri, MD, MPH
From New York University School of Medicine, Hospital for Special Surgery, Albert Einstein College of Medicine, and Weill Cornell Medical College, New York, New York; University of Utah Health Sciences Center and Intermountain Healthcare, Salt Lake City, Utah; Oestfold Hospital Trust, Fredrikstad, Norway; University of Toronto, Toronto, Ontario, Canada; Oklahoma Medical Research Foundation and the University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma;
Johns Hopkins University School of Medicine, Baltimore, Maryland; and University of Illinois at Chicago, Chicago, Illinois.
Michael D. Lockshin, MD
From New York University School of Medicine, Hospital for Special Surgery, Albert Einstein College of Medicine, and Weill Cornell Medical College, New York, New York; University of Utah Health Sciences Center and Intermountain Healthcare, Salt Lake City, Utah; Oestfold Hospital Trust, Fredrikstad, Norway; University of Toronto, Toronto, Ontario, Canada; Oklahoma Medical Research Foundation and the University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma;
Johns Hopkins University School of Medicine, Baltimore, Maryland; and University of Illinois at Chicago, Chicago, Illinois.
Lisa Sammaritano, MD
From New York University School of Medicine, Hospital for Special Surgery, Albert Einstein College of Medicine, and Weill Cornell Medical College, New York, New York; University of Utah Health Sciences Center and Intermountain Healthcare, Salt Lake City, Utah; Oestfold Hospital Trust, Fredrikstad, Norway; University of Toronto, Toronto, Ontario, Canada; Oklahoma Medical Research Foundation and the University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma;
Johns Hopkins University School of Medicine, Baltimore, Maryland; and University of Illinois at Chicago, Chicago, Illinois.
D. Ware Branch, MD
From New York University School of Medicine, Hospital for Special Surgery, Albert Einstein College of Medicine, and Weill Cornell Medical College, New York, New York; University of Utah Health Sciences Center and Intermountain Healthcare, Salt Lake City, Utah; Oestfold Hospital Trust, Fredrikstad, Norway; University of Toronto, Toronto, Ontario, Canada; Oklahoma Medical Research Foundation and the University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma;
Johns Hopkins University School of Medicine, Baltimore, Maryland; and University of Illinois at Chicago, Chicago, Illinois.
T. Flint Porter, MD, MPH
From New York University School of Medicine, Hospital for Special Surgery, Albert Einstein College of Medicine, and Weill Cornell Medical College, New York, New York; University of Utah Health Sciences Center and Intermountain Healthcare, Salt Lake City, Utah; Oestfold Hospital Trust, Fredrikstad, Norway; University of Toronto, Toronto, Ontario, Canada; Oklahoma Medical Research Foundation and the University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma;
Johns Hopkins University School of Medicine, Baltimore, Maryland; and University of Illinois at Chicago, Chicago, Illinois.
Allen Sawitzke, MD
From New York University School of Medicine, Hospital for Special Surgery, Albert Einstein College of Medicine, and Weill Cornell Medical College, New York, New York; University of Utah Health Sciences Center and Intermountain Healthcare, Salt Lake City, Utah; Oestfold Hospital Trust, Fredrikstad, Norway; University of Toronto, Toronto, Ontario, Canada; Oklahoma Medical Research Foundation and the University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma;
Johns Hopkins University School of Medicine, Baltimore, Maryland; and University of Illinois at Chicago, Chicago, Illinois.
Joan T. Merrill, MD
From New York University School of Medicine, Hospital for Special Surgery, Albert Einstein College of Medicine, and Weill Cornell Medical College, New York, New York; University of Utah Health Sciences Center and Intermountain Healthcare, Salt Lake City, Utah; Oestfold Hospital Trust, Fredrikstad, Norway; University of Toronto, Toronto, Ontario, Canada; Oklahoma Medical Research Foundation and the University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma;
Johns Hopkins University School of Medicine, Baltimore, Maryland; and University of Illinois at Chicago, Chicago, Illinois.
Mary D. Stephenson, MD, MSc
From New York University School of Medicine, Hospital for Special Surgery, Albert Einstein College of Medicine, and Weill Cornell Medical College, New York, New York; University of Utah Health Sciences Center and Intermountain Healthcare, Salt Lake City, Utah; Oestfold Hospital Trust, Fredrikstad, Norway; University of Toronto, Toronto, Ontario, Canada; Oklahoma Medical Research Foundation and the University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma;
Johns Hopkins University School of Medicine, Baltimore, Maryland; and University of Illinois at Chicago, Chicago, Illinois.
Elisabeth Cohn, BA
From New York University School of Medicine, Hospital for Special Surgery, Albert Einstein College of Medicine, and Weill Cornell Medical College, New York, New York; University of Utah Health Sciences Center and Intermountain Healthcare, Salt Lake City, Utah; Oestfold Hospital Trust, Fredrikstad, Norway; University of Toronto, Toronto, Ontario, Canada; Oklahoma Medical Research Foundation and the University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma;
Johns Hopkins University School of Medicine, Baltimore, Maryland; and University of Illinois at Chicago, Chicago, Illinois.
Lamya Garabet, MD
From New York University School of Medicine, Hospital for Special Surgery, Albert Einstein College of Medicine, and Weill Cornell Medical College, New York, New York; University of Utah Health Sciences Center and Intermountain Healthcare, Salt Lake City, Utah; Oestfold Hospital Trust, Fredrikstad, Norway; University of Toronto, Toronto, Ontario, Canada; Oklahoma Medical Research Foundation and the University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma;
Johns Hopkins University School of Medicine, Baltimore, Maryland; and University of Illinois at Chicago, Chicago, Illinois.
Jane E. Salmon, MD
From New York University School of Medicine, Hospital for Special Surgery, Albert Einstein College of Medicine, and Weill Cornell Medical College, New York, New York; University of Utah Health Sciences Center and Intermountain Healthcare, Salt Lake City, Utah; Oestfold Hospital Trust, Fredrikstad, Norway; University of Toronto, Toronto, Ontario, Canada; Oklahoma Medical Research Foundation and the University of Oklahoma Health Sciences Center, Oklahoma City, Oklahoma;
Johns Hopkins University School of Medicine, Baltimore, Maryland; and University of Illinois at Chicago, Chicago, Illinois.
Financial Support: The PROMISSE study and all authors except Drs. Sawitzke and Garabet were supported by RO1 AR49772 from the National Institute of Arthritis and Musculoskeletal and Skin Diseases of the National Institutes of Health. Drs. Lockshin and Salmon received additional support from the Mary Kirkland Center for Lupus Research, and Dr. Salmon also received support from Rheuminations. Dr. Petri received additional support from the National Institutes of Health (NIH AR43727).
Disclosures: Dr. Buyon reports grants from the National Institutes of Health and the National Institute of Arthritis and Musculoskeletal and Skin Diseases during the conduct of the study. Dr. Kim reports grants from the National Institutes of Health and the National Institute of Arthritis and Musculoskeletal and Skin Diseases during the conduct of the study. Ms. Guerra reports grants from the National Institutes of Health and the National Institute of Arthritis and Musculoskeletal and Skin Diseases during the conduct of the study. Dr. Laskin reports grants from the National Institutes of Health and the National Institute of Arthritis and Musculoskeletal and Skin Diseases during the conduct of the study. Dr. Petri reports grants from the National Institutes of Health and the National Institute of Arthritis and Musculoskeletal and Skin Diseases during the conduct of the study. Dr. Lockshin reports grants from the National Institutes of Health and the National Institute of Arthritis and Musculoskeletal and Skin Diseases during the conduct of the study. Dr. Sammaritano reports grants from the National Institutes of Health and the National Institute of Arthritis and Musculoskeletal and Skin Diseases during the conduct of the study. Dr. Branch reports grants from the National Institutes of Health and the National Institute of Arthritis and Musculoskeletal and Skin Diseases during the conduct of the study. Dr. Porter reports grants from the National Institutes of Health and the National Institute of Arthritis and Musculoskeletal and Skin Diseases during the conduct of the study. Dr. Merrill reports grants from the National Institutes of Health and the National Institute of Arthritis and Musculoskeletal and Skin Diseases and a subcontract from the principal investigator's funding from the National Institutes of Health during the conduct of the study. Dr. Stephenson reports grants from the National Institutes of Health and the National Institute of Arthritis and Musculoskeletal and Skin Diseases during the conduct of the study. Ms. Cohn reports grants from the National Institutes of Health and the National Institute of Arthritis and Musculoskeletal and Skin Diseases during the conduct of the study. Dr. Salmon reports grants from the National Institutes of Health, the National Institute of Arthritis and Musculoskeletal and Skin Diseases, and Rheuminations during the conduct of the study. Authors not named here have disclosed no conflicts of interest. Disclosures can also be viewed at www.acponline.org/authors/icmje/ConflictOf InterestForms.do?msNum=M14-2235.
Editors' Disclosures: Christine Laine, MD, MPH, Editor in Chief, reports that she has no financial relationships or interests to disclose. Darren B. Taichman, MD, PhD, Executive Deputy Editor, reports that he has no financial relationships or interests to disclose. Cynthia D. Mulrow, MD, MSc, Senior Deputy Editor, reports that she has no relationships or interests to disclose. Deborah Cotton, MD, MPH, Deputy Editor, reports that she has no financial relationships or interest to disclose. Jaya K. Rao, MD, MHS, Deputy Editor, reports that she has stock holdings/options in Eli Lilly and Pfizer. Sankey V. Williams, MD, Deputy Editor, reports that he has no financial relationships or interests to disclose. Catharine B. Stack, PhD, MS, Deputy Editor for Statistics, reports that she has stock holdings in Pfizer.
Reproducible Research Statement: Study protocol and data set: Because the investigative team is still analyzing the data for biomarkers and genetics, at this time, the authors are not willing to make the protocol or data public except for what is currently published at ClinicalTrials.gov (NCT00198068). Statistical code: Not available.
Corresponding Author: Jill P. Buyon, MD, NYU/Langone Medical Center, 550 First Avenue, MSB 607, New York, NY 10016, or Jane E. Salmon, MD, Hospital for Special Surgery, 535 East 70th Street, New York, NY 10021.
Current Author Addresses: Dr. Buyon: NYU/Langone Medical Center, 550 First Avenue, MSB 607, New York, NY 10016.
Dr. Kim: Albert Einstein College of Medicine, 1300 Morris Park Avenue, Belfer Building, Room 1303, Bronx, NY 10461.
Ms. Guerra and Drs. Lockshin, Sammaritano, and Salmon: Hospital for Special Surgery, 535 East 70th Street, New York, NY 10021.
Dr. Laskin: LifeQuest Centre for Reproductive Medicine, 655 Bay Street, Suite 1800, Toronto, Ontario M5G 2K4, Canada.
Dr. Petri: Division of Rheumatology, Johns Hopkins University School of Medicine, 1830 East Monument Street, Suite 7500, Baltimore, MD 21205.
Dr. Branch: University of Utah Health Sciences Center, 30 North 1900 East, Room 2B200 SOM, Salt Lake City, UT 84132.
Dr. Porter: University Hospital, 50 North Medical Drive, Salt Lake City, UT 84132.
Dr. Sawitzke: University of Utah Health Sciences Center, 30 North 1900 East, SOM 4B200, Salt Lake City, UT 84132.
Dr. Merrill: Oklahoma Medical Research Foundation, 825 NE 13th Street, MS 22, Oklahoma City, OK 73104.
Dr. Stephenson: Department of Obstetrics and Gynecology, University of Illinois College of Medicine, 820 South Wood Street, MC 808, Chicago, IL 60612.
Ms. Cohn: 1219 South Lamar Boulevard, Austin, TX 78704.
Dr. Garabet: Oestfold Hospital Trust, Cicignongata 19, 1603 Fredrikstad, Norway.
Author Contributions: Conception and design: J.P. Buyon, M.Y. Kim, M.M. Guerra, M. Petri, M.D. Lockshin, L. Sammaritano, T.F. Porter, J.E. Salmon.
Analysis and interpretation of the data: J.P. Buyon, M.Y. Kim, M.M. Guerra, M. Petri, M.D. Lockshin, L. Sammaritano, D.W. Branch, A. Sawitzke, J.T. Merrill, J.E. Salmon.
Drafting of the article: J.P. Buyon, M.Y. Kim, M.M. Guerra, M. Petri, M.D. Lockshin, T.F. Porter, L. Garabet, J.E. Salmon.
Critical revision of the article for important intellectual content: J.P. Buyon, M.Y. Kim, M.M. Guerra, C.A. Laskin, M. Petri, M.D. Lockshin, L. Sammaritano, T.F. Porter, J.T. Merrill, J.E. Salmon.
Final approval of the article: J.P. Buyon, M.Y. Kim, M.M. Guerra, C.A. Laskin, M. Petri, M.D. Lockshin, L. Sammaritano, D.W. Branch, T.F. Porter, A. Sawitzke, J.T. Merrill, M.D. Stephenson, L. Garabet, J.E. Salmon.
Provision of study materials or patients: J.P. Buyon, C.A. Laskin, M. Petri, M.D. Lockshin, L. Sammaritano, D.W. Branch, T.F. Porter, A. Sawitzke, J.T. Merrill, M.D. Stephenson.
Statistical expertise: M.Y. Kim.
Obtaining of funding: T.F. Porter, J.E. Salmon.
Administrative, technical, or logistic support: M.M. Guerra, T.F. Porter, J.T. Merrill, J.E. Salmon.
Collection and assembly of data: J.P. Buyon, M.M. Guerra, M. Petri, M.D. Lockshin, L. Sammaritano, D.W. Branch, A. Sawitzke, E. Cohn, L. Garabet, J.E. Salmon.
This article was published online first at www.annals.org on 23 June 2015.

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