AMERICAN JOURNAL OF REPRODUCTIVE IMMUNOLOGY 28:164-167 © 1992 MUNKSGAARD
Fetal Echocardiography in the Assessment of Lupus Pregnancies DEBORAH M. FRIEDMAN Pediatric Cardiology, New York University Medical Center, New York, New York
Fetal echocardiography is the most sensitive tool in detecting the earliest possible changes of the cardiovascular system related to maternal lupus. The institution of aggressive therapy at that time may still be able to reverse the process before permanent fetal cardiac injury occurs. Experience with this technique is described. (Am J Reprod Immunol. 1992; 28:164-167.) Key words: Congenital heart block, fetal echocardiography, systemic lupus erythematosus ABSTRACT:
INTRODUCTION
Fetal echocardiography is a powerful tool in assessing the fetal cardiovascular system noninvasively.' It incorporates complimentary modalities of real-time two-dimensional imaging, M-mode measurements, and Doppler blood velocity analysis. Maternal systemic lupus erythematosus can affect the fetal cardiovascular system in many ways. 2 Transplacental transfer of anti-Ro (SSA) and anti-La (SSB) antibodies may result in congenital complete heart block. Less commonly, a neonatal myocarditis or pancarditis may be seen, which can be fatal. Maternal vascular disease, including systemic hypertension, or the presence of antiphospholipid antibodies, may produce placental dysfunction and intrauterine growth retardation. The effects of various potent maternal medications are largely unknown. Routine obstetrical ultrasound can measure fetal heart rate or biophysical profile, but these changes occur late in the course of disease. Fetal echocardiography provides more complete serial data. The M-mode reflects heart motion over time and can best determine the cardiac rate and rhythm. A variety of tools can assess fetal myocardial function, including measurement of heart size; two-dimensional echocardiography can be used to detect the presence of hydrops fetalis; M-mode shortening fraction can be used to analyse systolic ventricular function, and pulsed Doppler analysis can be used to assess cardiac output or the presence of tricuspid regurgitation. Placental function is assessed by umbilical artery Doppler blood flow waveforms. Fetal echocardiography is the most sensitive tool in detecting the earliest possible changes of the cardiovascular system related to maternallupus at a time when instituting aggressive treatment such as corticosteroid therapy and plasmapheresis,3,4 may still be able to reverse the process before permanent fetal cardiac damage is established.
6-wk intervals (24 and 30 wk), or more frequently if clinically indicated. The studies are performed using a commercially available phased array duplex two-dimensional real-time echocardiographic system with capability for both pulsed and continuous wave Doppler, as well as color flow mapping. A 5- or 3-mHz transducer is used as required. Studies are recorded on 1I2-inch video tape for later analysis. Real-time sector scanning is used for orientation. Cardiac structures are identified on the basis of characteristic features." Standard views are attempted in each case, including a four-chamber and long axis view of both ventricles. The short axis view is recorded at the ventricular level, as well as at the aortic valve level. 6,7 A wide variety of congenital cardiac defects has been diagnosed in this fashion. 6,8-10 The false positive and negative rates ofthis technique are low.6,9 For functional information, the fetus is examined for evidence of hydrops fetalis, which is manifest by the presence of effusions or ascites on twodimensional study. The presence of oligohydramnios or decreased fetal activity can be qualitatively assessed. The fetal M-mode can be used to measure cardiac chamber and wall sizes or thicknesses at various gestational ages to diagnose abnormal heart size l l- 13 or systolic function.l" The M-mode technique is also invaluable in analyzing fetal cardiac rhythms, since fetal electrocardiograms are unavailable to diagnose many fetal arrhythmias. 13-17 If diagnosed, serious arrhythmias can be treated with maternal medications such as digoxin,16,17 or even attempts at fetal pacemaker insertion. 18 Doppler principles are applied to the assessment offetal cardiovascular physiology. The umbilical artery Doppler blood flow waveforms are used to analyze placental function. I9-25 This indicator is abnormal under pathological conditions such as intrauterine growth retardation, placental infarction or abruption, or h~ertensive or other vascular disorders of pregnancy.P?" 5 Doppler blood velocity waveforms can also be sampled under direct visual guidance from the fetal cerebral arteries.r'' It is possible to record Doppler blood flow velocities across all four fetal cardiac valves, as well as in major systemic arteries and veins. 27-32 Valvular dysfunction, such as tricuspid regurgitation, is an early indicator of fetal right-sided cardiac failure and hydrops fetalis. 33 It is also possible to document the unobstructed r,atency of thue foramen 6vale 28 and ductus arteriosus 4 in the normal fetus.
METHODS
Fetal Doppler Echocardiography Fetal echocardiograms can be performed serially beginning as early as 16-18 wk of gestation and repeated at Submitted for publication June 2,1992; accepted June 6, 1992. Address reprint requests to Deborah M. Friedman, Pediatric Cardiology, First Avenue, New York, NY 10016.
550
EXPERIENCE WITH LUPUS AND RELATED PREGNANCIES
Neonatal lupus" may take the form of transient newborn rashes, or hematologic abnormalities, including hemolytic anemia, thrombocytopenia, or lymphopenia. Recently, a neonatal hepatitis has been described. Of most concern is the development of cardiac disease. Permanent complete heart block may appear even as early as the late second trimester of pregnancy, but has also
FETAL ECHOCARDIOGRAPHY IN LUPUS PREGNANCIES
165
A
B Fig. 1. The two-dimensionally directed fetal M-Mode tracing through the level of the aortic valve of (A) A normal 16-wk fetus with synchronous atrial and ventricular rates at 150 beats per min and (B) a 32-wk fetus with complete heart block, an atrial rate of 136 and ventricular
rate of 66 beats per min. Atrial wall motion reflects the atrial activation rate (P wave) and aortic valve motion reflects the ventricular activation rate (QRS). Time markers on the abcissa reflect 0.5 second intervals.
been described as progressing from second to third degree block.i'" and, therefore, the process may appear in an incomplete form. This conduction system disease may be associated with a more generalized myocarditis, with rare cases reported of hydrops and early mortality. Pathology of the heart includes inflammation and fibrosis of the conduction system with evidence of antibody binding. Treatment has been proposed to avert these disasters prenatally by administering maternal corticosteroids or using plasmapheresis.i''" Our experience using fetal echocardiography with
maternal autoimmunity has included 36 patients seen over a 9-year period of time. Pregnant patients with known lupus were referred on 29 occasions. One had previously given birth to a child with complete heart block and a fatal myocarditis. Therefore, in the face of very high serum 88B/La titers, she was treated with corticosteroids and plasmapheresis, resulting in the birth of a normal baby. Two other women with prior histories of neonatal lupus in their offspring were not treated and also had unaffected neonates. Two other pregnancies involving lupus showed Doppler evidence of placental dys-
166
FRIEDMAN
function at 27 and 34 wk of gestation, but these findings resolved within 1 and 4 wk, respectively. Another woman with lupus gave birth to unaffected, normal twins. Three patients were referred during pregnancies complicated by Sjogren's Syndrome, but had unaffected fetuses. There were four patients referred for overt fetal bradycardias. One was studied serially from presentation at 37 wk with complete heart block and a fetal heart rate of 43 beats per min. The asymptomatic mother was found to have autoimmune antibodies against SSA/Ro and SSB/La, and a neonatal pacemaker insertion was necessary. A second woman, also asymptomatic but with similar autoimmune antibodies, was found to be carrying a fetus with complete heart block but with rates always greater than 60 beats per min (Fig. IB). No immediate therapy was necessary, despite a rash of neonatal lupus in early infancy. An additional woman with known lupus and hemolytic anemia presented at 22 wk gestation, carrying a fetus with apparently complete heart block at a rate of70. She was treated with dexamethasone and delivered a child with only second degree heart block, which later progressed to complete heart block. Finally, a curious case was seen at 18 wk of gestation with an apparent 2:1 heart block and a fetal ventricular rate of 72 beats per min. However, the arrhythmia completely resolved spontaneously within 1 wk and resulted in a normal outcome. CONCLUSIONS
Serial fetal echocardiography for pregnancies affected by maternal lupus or related antibodies is useful in several ways. The fetal heart rate and rhythm can be assessed by M-mode techniques in lieu of a fetal electrocardiogram to detect heart block or other arrhythmias. Hemodynamic function is measured by chamber enlargement or systolic ejection indices by two-dimensional or M-mode techniques, to detect myocarditis or the effects of dysrhythmias. Structural abnormalities can be diagnosed by these methods, which is important in light of some reports suggesting an increased incidence of patent ductus arteriosus and atrial septal defect in lupus pregnancies.P'v" Such analyses may form the basis for determining the earliest indications for treatment. In the presence of risk factors for neonatal lupus, particularly with a history of previous congenital complete heart block or high titers of SSAlRo and SSB/La antibodies, serial fetal echocardiograms should be performed beginning at 16 wk of pregnancy. This is the earliest point of good visualization of the heart and probably corresponds to the window of susceptibility of placentally acquired maternal antibodies. This early, frequent and sensitive monitoring may allow one to predict, follow the course of, and possibly treat fetal passive immune-mediated myocarditis and prevent the development of permanent congenital complete heart block. REFERENCES 1. Friedman DM. Fetal echocardiography and Doppler blood flow studies. In: Filkins K, Russo JF, eds. Human Prenatal Diagnosis, 2nd Ed. New York: Marcel Dekker, 1990:407-423. 2. Petri M, Watson R, Hochberg MC. Anti-Ro antibodies and neonatal lupus. Rheum Dis Clin North Am. 1989; 15:335-360. 3. Buyon J, Roubey R, Swersky S, Pompeo L, Parke A, Baxi L, Winchester R. Complete congenital heart block: Risk of occurrence and therapeutic approach to prevention. J Rheumatol. 1988; 15:1104.
4. Buyon JP, Swersky SH, Fox HE, Bierman FZ, Winchester RJ. Intrauterine therapy for presumptive fetal myocarditis with acquired heart block due to systemic lupus erythematosus. Experience in a mother with a predominance of SS-B (La) antibodies. Arthritis Rheum. 1987; 30:449. 5. Reed KL, Anderson CF, Shenkar L. Fetal Echocardiography. An Atlas. New York: Alan R. Liss, Inc., 1988:1-135. 6. Silverman NH, Golbus MS. Echocardiographic techniques for assessing normal and abnormal fetal cardiac anatomy. J Am Coli Cardiol. 1985; 5:20s-29s. 7. Lange LW, Sahn DJ, Allen HF, Goldberg SJ, Anderson C, Giles H. Qualitative real-time cross-sectional echocardiographic imaging of the human fetus during the second half of pregnancy. Circulation. 1980; 62:799-806. 8. Kleinman CS, Hobbins JC, Jaffe CC, Lynch DC, Talner NS. Echocardiographic studies of the human fetus: Prenatal diagnosis of congenital heart disease and cardiac dysrhythmia. Pediatrics. 1980; 65:1059-1067. 9. Wladimiroff JW, Steward PA, Vosters RPL. Fetal cardiac structure and function as studied by ultrasound. Clin Cardiol. 1984; 7: 239-253. 10. Friedman DM. Prenatal diagnosis of single ventricle by echocardiography. Report of two survivors. J Cardiovasc Ultrasonogr. 1988; 7:151-156. 11. Sahn DJ, Lange LW, Allen HD, Goldberg SJ, Anderson C, Giles H, Haber K. Quantitative real-time cross-sectional echocardiography in the developing normal human fetus and newborn. Circulation. 1980; 62:588-597. 12. Allan LD, Joseph MC, Boyd EGCA, Campbell S, Tynan M. M-mode echocardiography in the developing human fetus. Br Heart J. 1982; 47:573-583. 13. St. John Sutton M, Gewitz MH, Shah B, Cohen A, Reichek M, Gabbe S, HuffDS. Quantitative assessment of growth and function of the cardiac chambers in the normal human fetus: A prospective longitudinal echocardiographic study. Circulation. 1984; 69:645-654. 14. Kleinman CD, Donnerstein RL. Ultrasonic assessment of cardiac function in the intact human fetus. J Am Coli Cardiol. 1985; 5:84s-94s. 15. Kleinman CS, Donnerstein RL, Jaffee CC, DeVore GR, Weinstein EM, Lynch DC, Talner NS, Berkowitz RL, Hobbins JC. Fetal echocardiography. A tool for evaluation of in utero cardiac arrhythmias and monitoring of in utero therapy: Analysis of 71 patients. AmJ Cardiol.1983; 51:237-243. 16. Crowley DC, Dick M, Rayburn WF, Rosenthal A. Two-dimensional and M-mode echocardiographic evaluation of fetal arrhythmia. Clin Cardiol. 1985; 8:1-10. 17. Kleinman CS, Copel JA, Weinstein EM, Santulli TV Jr., Hobbins JC. In utero diagnosis and treatment of fetal supraventricular tachycardia. Semin Perinatol.1985; 9:113-129. 18. Carpenter RJ, Strasburger JF, Garson A, Smith RT, Deter RL, Engelhardt HT. Fetal ventricular pacing for hydrops secondary to complete atrioventricular block.J Am Coli CardioI.1986; 8:1434-1436. 19. Gosling RG, King DH. Continuous wave ultrasound as an alternative and compliment to x-rays in vascular examinations. In: Reneman RS, ed. Cardiovascular Application of Ultrasound. New York:N orth Holland!American Elsevier, 1974:266-282. 20. Friedman DM, Rutkowski M, Snyder JR, Lustig-Gillman I, Young BK. Doppler blood velocity waveforms in the umbilical artery as an indicator offetal well-being. JCD. 1985; 13:161-165. 21. Friedman DM, Rutkowski M. Umbilical artery Doppler waveforms in severe pre-eclampsia. J Cardiovasc Ultrasonogr. 1985; 4:83-86. 22. Friedman DM, Ehrlich P, Hoskins IA. Umbilical artery Doppler blood velocity waveforms in normal and abnormal gestations. J Ultrasound Med. 1989; 8:375-380. 23. Stuart B, Drumm J, Fitzgerald DE, Duignan NM. Fetal blood velocity waveforms in normal pregnancy. Br J Obstet Gynaecol. 1980; 87:780-785. 24. Giles WB, Trudinger BJ, Cook CM. Fetal umbilical artery velocity waveforms (abstract). J Ultrasound Moo. 1982; 1 (suppl):98. 25. McCallum WD, Williams CS, Napel S, Daigle RE: Fetal blood velocity waveforms. Am J Obstet Gynecol. 1978; 132:425-429. 26. WladimiroffJW, Tonge HM, Stewart PA. Doppler ultrasound assessment of cerebral blood flow in the human fetus. Br J Obstet Gynaecol. 1986; 93:471-475. 27. Reid MH, Mackay RS, Lantz BMT. Noninvasive measurement of fetal and neonatal blood flow. Acta Radiol (Diag), 1980; 21:197-202. 28. Maulik D, Nanda NC, Saini VD. Fetal Doppler echocardiography: Methods and characterization of normal and abnormal hemodynamics. Am J Cardiol. 1984; 53:572-578. 29. Reed KL, Meijboom EJ, Sahn DJ, Scagnelli SA, Valdes-Cruz LM, Shenker L. Cardiac Doppler flow velocities in human fetuses. Circulation. 1986; 73:41-46.
FETAL ECHOCARDIOGRAPHY IN LUPUS PREGNANCIES 30. Reed KL, Sahn DJ, Scagnelli S, Anderson CD, Shenker L. Doppler echocardiographic studies of diastolic function in the human fetal heart: Changes during gestation. J Am Coli Cardio!' 1986; 8:391395. 31. Kenny JF, Plappert T, Doublilet P, Saltzman DH, Cartier M, Zollars L, Leatherman GF, St. John Sutton MG. Changes in intracardiac blood flow velocities and right and left ventricular stroke volumes with gestational age in the normal human fetus: A prospective Doppler echocardiographic study. Circulation. 1986; 74:12081216. 32. DeSmedt MCH, Visser GHA, Meijboom EJ. Fetal cardiac output estimated by Doppler echocardiography during mid and late gestation. Am J Cardio!' 1987; 60:338-342. 33. Silverman NH, Kleinman CS, Rudolph AM, Copel JA, Weinstein EM, Enderlein MA, Golbus M. Fetal atrioventricular valve insufficiency associated with nonimmune hydrops: A two-dimensional
167
echocardiographic and pulsed Doppler ultrasound study. Circulation. 1985; 72:825-832. 34. Huhta JC, Moise KJ, Fisher DJ, Sharif DS, Wasserstrum N, Martin C. Detection and quantitation of constriction of the fetal ductus arteriosus by Doppler echocardiography. Circulation. 1987; 75: 406-412. 35. Geggel RL, Tucker L, Szer I. Postnatal progression from second to third degree heart block in neonatal lupus syndrome. J Pediatr. 1988; 113:1049-1052. 36. Stephenson 0, Cleland WP, Hallide-Smith K. Congenital complete heart block and persistent ductus arteriosus associated with maternal systemic lupus erythematosus. Br Heart J. 1981; 46: 104-106. 37. Ho SY, Esscher E, Anderson RH, Michaelsson M. Anatomy of congenital complete heart block and relation to maternal anti-Ro antibodies. Am J Cardio!' 1986; 58:291-294.
Fetal Echocardiography in the Assessment of Lupus Pregnancies DEBORAH M. FRIEDMAN Pediatric Cardiology, New York University Medical Center, New York, New York
Fetal echocardiography is the most sensitive tool in detecting the earliest possible changes of the cardiovascular system related to maternal lupus. The institution of aggressive therapy at that time may still be able to reverse the process before permanent fetal cardiac injury occurs. Experience with this technique is described. (Am J Reprod Immunol. 1992; 28:164-167.) Key words: Congenital heart block, fetal echocardiography, systemic lupus erythematosus ABSTRACT:
INTRODUCTION
Fetal echocardiography is a powerful tool in assessing the fetal cardiovascular system noninvasively.' It incorporates complimentary modalities of real-time two-dimensional imaging, M-mode measurements, and Doppler blood velocity analysis. Maternal systemic lupus erythematosus can affect the fetal cardiovascular system in many ways. 2 Transplacental transfer of anti-Ro (SSA) and anti-La (SSB) antibodies may result in congenital complete heart block. Less commonly, a neonatal myocarditis or pancarditis may be seen, which can be fatal. Maternal vascular disease, including systemic hypertension, or the presence of antiphospholipid antibodies, may produce placental dysfunction and intrauterine growth retardation. The effects of various potent maternal medications are largely unknown. Routine obstetrical ultrasound can measure fetal heart rate or biophysical profile, but these changes occur late in the course of disease. Fetal echocardiography provides more complete serial data. The M-mode reflects heart motion over time and can best determine the cardiac rate and rhythm. A variety of tools can assess fetal myocardial function, including measurement of heart size; two-dimensional echocardiography can be used to detect the presence of hydrops fetalis; M-mode shortening fraction can be used to analyse systolic ventricular function, and pulsed Doppler analysis can be used to assess cardiac output or the presence of tricuspid regurgitation. Placental function is assessed by umbilical artery Doppler blood flow waveforms. Fetal echocardiography is the most sensitive tool in detecting the earliest possible changes of the cardiovascular system related to maternallupus at a time when instituting aggressive treatment such as corticosteroid therapy and plasmapheresis,3,4 may still be able to reverse the process before permanent fetal cardiac damage is established.
6-wk intervals (24 and 30 wk), or more frequently if clinically indicated. The studies are performed using a commercially available phased array duplex two-dimensional real-time echocardiographic system with capability for both pulsed and continuous wave Doppler, as well as color flow mapping. A 5- or 3-mHz transducer is used as required. Studies are recorded on 1I2-inch video tape for later analysis. Real-time sector scanning is used for orientation. Cardiac structures are identified on the basis of characteristic features." Standard views are attempted in each case, including a four-chamber and long axis view of both ventricles. The short axis view is recorded at the ventricular level, as well as at the aortic valve level. 6,7 A wide variety of congenital cardiac defects has been diagnosed in this fashion. 6,8-10 The false positive and negative rates ofthis technique are low.6,9 For functional information, the fetus is examined for evidence of hydrops fetalis, which is manifest by the presence of effusions or ascites on twodimensional study. The presence of oligohydramnios or decreased fetal activity can be qualitatively assessed. The fetal M-mode can be used to measure cardiac chamber and wall sizes or thicknesses at various gestational ages to diagnose abnormal heart size l l- 13 or systolic function.l" The M-mode technique is also invaluable in analyzing fetal cardiac rhythms, since fetal electrocardiograms are unavailable to diagnose many fetal arrhythmias. 13-17 If diagnosed, serious arrhythmias can be treated with maternal medications such as digoxin,16,17 or even attempts at fetal pacemaker insertion. 18 Doppler principles are applied to the assessment offetal cardiovascular physiology. The umbilical artery Doppler blood flow waveforms are used to analyze placental function. I9-25 This indicator is abnormal under pathological conditions such as intrauterine growth retardation, placental infarction or abruption, or h~ertensive or other vascular disorders of pregnancy.P?" 5 Doppler blood velocity waveforms can also be sampled under direct visual guidance from the fetal cerebral arteries.r'' It is possible to record Doppler blood flow velocities across all four fetal cardiac valves, as well as in major systemic arteries and veins. 27-32 Valvular dysfunction, such as tricuspid regurgitation, is an early indicator of fetal right-sided cardiac failure and hydrops fetalis. 33 It is also possible to document the unobstructed r,atency of thue foramen 6vale 28 and ductus arteriosus 4 in the normal fetus.
METHODS
Fetal Doppler Echocardiography Fetal echocardiograms can be performed serially beginning as early as 16-18 wk of gestation and repeated at Submitted for publication June 2,1992; accepted June 6, 1992. Address reprint requests to Deborah M. Friedman, Pediatric Cardiology, First Avenue, New York, NY 10016.
550
EXPERIENCE WITH LUPUS AND RELATED PREGNANCIES
Neonatal lupus" may take the form of transient newborn rashes, or hematologic abnormalities, including hemolytic anemia, thrombocytopenia, or lymphopenia. Recently, a neonatal hepatitis has been described. Of most concern is the development of cardiac disease. Permanent complete heart block may appear even as early as the late second trimester of pregnancy, but has also
FETAL ECHOCARDIOGRAPHY IN LUPUS PREGNANCIES
165
A
B Fig. 1. The two-dimensionally directed fetal M-Mode tracing through the level of the aortic valve of (A) A normal 16-wk fetus with synchronous atrial and ventricular rates at 150 beats per min and (B) a 32-wk fetus with complete heart block, an atrial rate of 136 and ventricular
rate of 66 beats per min. Atrial wall motion reflects the atrial activation rate (P wave) and aortic valve motion reflects the ventricular activation rate (QRS). Time markers on the abcissa reflect 0.5 second intervals.
been described as progressing from second to third degree block.i'" and, therefore, the process may appear in an incomplete form. This conduction system disease may be associated with a more generalized myocarditis, with rare cases reported of hydrops and early mortality. Pathology of the heart includes inflammation and fibrosis of the conduction system with evidence of antibody binding. Treatment has been proposed to avert these disasters prenatally by administering maternal corticosteroids or using plasmapheresis.i''" Our experience using fetal echocardiography with
maternal autoimmunity has included 36 patients seen over a 9-year period of time. Pregnant patients with known lupus were referred on 29 occasions. One had previously given birth to a child with complete heart block and a fatal myocarditis. Therefore, in the face of very high serum 88B/La titers, she was treated with corticosteroids and plasmapheresis, resulting in the birth of a normal baby. Two other women with prior histories of neonatal lupus in their offspring were not treated and also had unaffected neonates. Two other pregnancies involving lupus showed Doppler evidence of placental dys-
166
FRIEDMAN
function at 27 and 34 wk of gestation, but these findings resolved within 1 and 4 wk, respectively. Another woman with lupus gave birth to unaffected, normal twins. Three patients were referred during pregnancies complicated by Sjogren's Syndrome, but had unaffected fetuses. There were four patients referred for overt fetal bradycardias. One was studied serially from presentation at 37 wk with complete heart block and a fetal heart rate of 43 beats per min. The asymptomatic mother was found to have autoimmune antibodies against SSA/Ro and SSB/La, and a neonatal pacemaker insertion was necessary. A second woman, also asymptomatic but with similar autoimmune antibodies, was found to be carrying a fetus with complete heart block but with rates always greater than 60 beats per min (Fig. IB). No immediate therapy was necessary, despite a rash of neonatal lupus in early infancy. An additional woman with known lupus and hemolytic anemia presented at 22 wk gestation, carrying a fetus with apparently complete heart block at a rate of70. She was treated with dexamethasone and delivered a child with only second degree heart block, which later progressed to complete heart block. Finally, a curious case was seen at 18 wk of gestation with an apparent 2:1 heart block and a fetal ventricular rate of 72 beats per min. However, the arrhythmia completely resolved spontaneously within 1 wk and resulted in a normal outcome. CONCLUSIONS
Serial fetal echocardiography for pregnancies affected by maternal lupus or related antibodies is useful in several ways. The fetal heart rate and rhythm can be assessed by M-mode techniques in lieu of a fetal electrocardiogram to detect heart block or other arrhythmias. Hemodynamic function is measured by chamber enlargement or systolic ejection indices by two-dimensional or M-mode techniques, to detect myocarditis or the effects of dysrhythmias. Structural abnormalities can be diagnosed by these methods, which is important in light of some reports suggesting an increased incidence of patent ductus arteriosus and atrial septal defect in lupus pregnancies.P'v" Such analyses may form the basis for determining the earliest indications for treatment. In the presence of risk factors for neonatal lupus, particularly with a history of previous congenital complete heart block or high titers of SSAlRo and SSB/La antibodies, serial fetal echocardiograms should be performed beginning at 16 wk of pregnancy. This is the earliest point of good visualization of the heart and probably corresponds to the window of susceptibility of placentally acquired maternal antibodies. This early, frequent and sensitive monitoring may allow one to predict, follow the course of, and possibly treat fetal passive immune-mediated myocarditis and prevent the development of permanent congenital complete heart block. REFERENCES 1. Friedman DM. Fetal echocardiography and Doppler blood flow studies. In: Filkins K, Russo JF, eds. Human Prenatal Diagnosis, 2nd Ed. New York: Marcel Dekker, 1990:407-423. 2. Petri M, Watson R, Hochberg MC. Anti-Ro antibodies and neonatal lupus. Rheum Dis Clin North Am. 1989; 15:335-360. 3. Buyon J, Roubey R, Swersky S, Pompeo L, Parke A, Baxi L, Winchester R. Complete congenital heart block: Risk of occurrence and therapeutic approach to prevention. J Rheumatol. 1988; 15:1104.
4. Buyon JP, Swersky SH, Fox HE, Bierman FZ, Winchester RJ. Intrauterine therapy for presumptive fetal myocarditis with acquired heart block due to systemic lupus erythematosus. Experience in a mother with a predominance of SS-B (La) antibodies. Arthritis Rheum. 1987; 30:449. 5. Reed KL, Anderson CF, Shenkar L. Fetal Echocardiography. An Atlas. New York: Alan R. Liss, Inc., 1988:1-135. 6. Silverman NH, Golbus MS. Echocardiographic techniques for assessing normal and abnormal fetal cardiac anatomy. J Am Coli Cardiol. 1985; 5:20s-29s. 7. Lange LW, Sahn DJ, Allen HF, Goldberg SJ, Anderson C, Giles H. Qualitative real-time cross-sectional echocardiographic imaging of the human fetus during the second half of pregnancy. Circulation. 1980; 62:799-806. 8. Kleinman CS, Hobbins JC, Jaffe CC, Lynch DC, Talner NS. Echocardiographic studies of the human fetus: Prenatal diagnosis of congenital heart disease and cardiac dysrhythmia. Pediatrics. 1980; 65:1059-1067. 9. Wladimiroff JW, Steward PA, Vosters RPL. Fetal cardiac structure and function as studied by ultrasound. Clin Cardiol. 1984; 7: 239-253. 10. Friedman DM. Prenatal diagnosis of single ventricle by echocardiography. Report of two survivors. J Cardiovasc Ultrasonogr. 1988; 7:151-156. 11. Sahn DJ, Lange LW, Allen HD, Goldberg SJ, Anderson C, Giles H, Haber K. Quantitative real-time cross-sectional echocardiography in the developing normal human fetus and newborn. Circulation. 1980; 62:588-597. 12. Allan LD, Joseph MC, Boyd EGCA, Campbell S, Tynan M. M-mode echocardiography in the developing human fetus. Br Heart J. 1982; 47:573-583. 13. St. John Sutton M, Gewitz MH, Shah B, Cohen A, Reichek M, Gabbe S, HuffDS. Quantitative assessment of growth and function of the cardiac chambers in the normal human fetus: A prospective longitudinal echocardiographic study. Circulation. 1984; 69:645-654. 14. Kleinman CD, Donnerstein RL. Ultrasonic assessment of cardiac function in the intact human fetus. J Am Coli Cardiol. 1985; 5:84s-94s. 15. Kleinman CS, Donnerstein RL, Jaffee CC, DeVore GR, Weinstein EM, Lynch DC, Talner NS, Berkowitz RL, Hobbins JC. Fetal echocardiography. A tool for evaluation of in utero cardiac arrhythmias and monitoring of in utero therapy: Analysis of 71 patients. AmJ Cardiol.1983; 51:237-243. 16. Crowley DC, Dick M, Rayburn WF, Rosenthal A. Two-dimensional and M-mode echocardiographic evaluation of fetal arrhythmia. Clin Cardiol. 1985; 8:1-10. 17. Kleinman CS, Copel JA, Weinstein EM, Santulli TV Jr., Hobbins JC. In utero diagnosis and treatment of fetal supraventricular tachycardia. Semin Perinatol.1985; 9:113-129. 18. Carpenter RJ, Strasburger JF, Garson A, Smith RT, Deter RL, Engelhardt HT. Fetal ventricular pacing for hydrops secondary to complete atrioventricular block.J Am Coli CardioI.1986; 8:1434-1436. 19. Gosling RG, King DH. Continuous wave ultrasound as an alternative and compliment to x-rays in vascular examinations. In: Reneman RS, ed. Cardiovascular Application of Ultrasound. New York:N orth Holland!American Elsevier, 1974:266-282. 20. Friedman DM, Rutkowski M, Snyder JR, Lustig-Gillman I, Young BK. Doppler blood velocity waveforms in the umbilical artery as an indicator offetal well-being. JCD. 1985; 13:161-165. 21. Friedman DM, Rutkowski M. Umbilical artery Doppler waveforms in severe pre-eclampsia. J Cardiovasc Ultrasonogr. 1985; 4:83-86. 22. Friedman DM, Ehrlich P, Hoskins IA. Umbilical artery Doppler blood velocity waveforms in normal and abnormal gestations. J Ultrasound Med. 1989; 8:375-380. 23. Stuart B, Drumm J, Fitzgerald DE, Duignan NM. Fetal blood velocity waveforms in normal pregnancy. Br J Obstet Gynaecol. 1980; 87:780-785. 24. Giles WB, Trudinger BJ, Cook CM. Fetal umbilical artery velocity waveforms (abstract). J Ultrasound Moo. 1982; 1 (suppl):98. 25. McCallum WD, Williams CS, Napel S, Daigle RE: Fetal blood velocity waveforms. Am J Obstet Gynecol. 1978; 132:425-429. 26. WladimiroffJW, Tonge HM, Stewart PA. Doppler ultrasound assessment of cerebral blood flow in the human fetus. Br J Obstet Gynaecol. 1986; 93:471-475. 27. Reid MH, Mackay RS, Lantz BMT. Noninvasive measurement of fetal and neonatal blood flow. Acta Radiol (Diag), 1980; 21:197-202. 28. Maulik D, Nanda NC, Saini VD. Fetal Doppler echocardiography: Methods and characterization of normal and abnormal hemodynamics. Am J Cardiol. 1984; 53:572-578. 29. Reed KL, Meijboom EJ, Sahn DJ, Scagnelli SA, Valdes-Cruz LM, Shenker L. Cardiac Doppler flow velocities in human fetuses. Circulation. 1986; 73:41-46.
FETAL ECHOCARDIOGRAPHY IN LUPUS PREGNANCIES 30. Reed KL, Sahn DJ, Scagnelli S, Anderson CD, Shenker L. Doppler echocardiographic studies of diastolic function in the human fetal heart: Changes during gestation. J Am Coli Cardio!' 1986; 8:391395. 31. Kenny JF, Plappert T, Doublilet P, Saltzman DH, Cartier M, Zollars L, Leatherman GF, St. John Sutton MG. Changes in intracardiac blood flow velocities and right and left ventricular stroke volumes with gestational age in the normal human fetus: A prospective Doppler echocardiographic study. Circulation. 1986; 74:12081216. 32. DeSmedt MCH, Visser GHA, Meijboom EJ. Fetal cardiac output estimated by Doppler echocardiography during mid and late gestation. Am J Cardio!' 1987; 60:338-342. 33. Silverman NH, Kleinman CS, Rudolph AM, Copel JA, Weinstein EM, Enderlein MA, Golbus M. Fetal atrioventricular valve insufficiency associated with nonimmune hydrops: A two-dimensional
167
echocardiographic and pulsed Doppler ultrasound study. Circulation. 1985; 72:825-832. 34. Huhta JC, Moise KJ, Fisher DJ, Sharif DS, Wasserstrum N, Martin C. Detection and quantitation of constriction of the fetal ductus arteriosus by Doppler echocardiography. Circulation. 1987; 75: 406-412. 35. Geggel RL, Tucker L, Szer I. Postnatal progression from second to third degree heart block in neonatal lupus syndrome. J Pediatr. 1988; 113:1049-1052. 36. Stephenson 0, Cleland WP, Hallide-Smith K. Congenital complete heart block and persistent ductus arteriosus associated with maternal systemic lupus erythematosus. Br Heart J. 1981; 46: 104-106. 37. Ho SY, Esscher E, Anderson RH, Michaelsson M. Anatomy of congenital complete heart block and relation to maternal anti-Ro antibodies. Am J Cardio!' 1986; 58:291-294.
