REVIEW URRENT C OPINION
Factors that increase reactivity during fetal nonstress testing Sertac Esin
Purpose of review The most common method of antepartum fetal surveillance is the nonstress test (NST). Although it has satisfactory false-negative rates, dubious nonreactive results may challenge the physician. Any method or factor increasing the reactive NST results or shortening the time to attain a reactive test may be considerably useful. Recent findings Most of the studies have found no effect of maternal glucose administration on fetal heart rate and fetal activity, specificity of NST, time to reactivity and percentage of reactive NST results when compared with the control group. Maternal intake of 70% cocoa or caffeine had stimulating action on the fetal reactivity, and this effect on the fetal heart rate was more marked with high concentrations of cocoa (80%). Studies on maternal positioning during NST had equivocal results. Fetal manipulation has no impact on the NST reactivity. Vibroacoustic and halogen light stimulation may be associated with a reduction in time to reactivity. Summary These methods may increase the reactivity during a NST and may facilitate the antenatal fetal surveillance. Keywords chocolate, glucose, halogen light stimulation, nonstress test, vibroacoustic stimulation
INTRODUCTION The primary aim of antenatal fetal surveillance is to discern the vulnerable fetus that will benefit from early recognition of risk of intrauterine injury and to reduce fetal and neonatal mortality. There are different methods of fetal surveillance, and electronic fetal monitoring (EFM) has become the cornerstone. EFM has been universally available in the developed world since the early 1970s. Although it has high specificity and false-positive rate and low falsenegative rate for perinatal morbidity and mortality in low-risk populations, it has become too routine for pregnant patients to undergo EFM in developed countries [1]. EFM is based on the fetal heart rate (FHR) assessment which is highly dependent on the gestational age. The main factor regulating FHR is the autonomic nervous system (ANS). The ANS receives inputs from several receptors and systems, and modulates the FHR simultaneously. As the gestational age increases, the parasympathetic nervous system (PNS) becomes more influential on the heart than the sympathetic nervous system (SNS) and this is primarily mediated by the vagus nerve, identified
as the tenth cranial nerve. The vagus nerve acts upon the sinoatrial and the atrioventricular nodes and has two main effects: it slows down the FHR (negative chronotropic effect) and decreases FHR variability, whereas sympathetic activation of the heart results in increased FHR and variability. FHR variability is also dependent on the gestational week and it should be present after 28 weeks when PNS is fully operational. The most common method of antepartum fetal surveillance assessment by FHR interpretation is the nonstress test (NST) [2]. For multiple gestations, antepartum fetal testing is recommended in circumstances where it would normally be performed in singleton pregnancies [3]. The main assumption of the NST is that with fetal movements, the heart rate Etlik Zubeyde Hanim Women’s Health and Teaching Hospital, Department of Perinatology, Ankara, Turkey Correspondence to Sertac Esin, MD, 212 Washington Avenue, 21204 Towson, Maryland, USA. Tel: +1 215 520 2768; e-mail: sertacesin@ gmail.com Curr Opin Obstet Gynecol 2014, 26:61–66 DOI:10.1097/GCO.0000000000000050
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KEY POINTS No effect of maternal glucose administration on FHR and fetal activity, specificity of NST, time to reactivity, or the percentage of reactive NST has been found. Maternal intake of chocolate has stimulating action on the fetal reactivity and this effect increases with higher cocoa content. Studies on maternal positioning during NST had equivocal results. Fetal manipulation has no impact on the NST reactivity. Vibroacoustic and halogen light stimulation may be associated with a reduction in time to reactivity.
of a nonacidotic or neurologically normal fetus would be accelerated [4]. NST results may be categorized as reactive or nonreactive. If there are two or more FHR accelerations that peak at least 15 beats per minute (b.p.m.) above the baseline and last 15 s from baseline to baseline (before 32 gestational weeks, two or more accelerations that peak at least 10 b.p.m. above the baseline and last 10 s from baseline to baseline [5,6]) within a 20-min period with or without fetal movement discernible by the mother, the NST is considered as reactive (or normal) [4,7]. For pregnancies below 32 weeks’ gestation, an interesting study compared the 10 10 criteria (10 beats/min, 10 s) with the 15 15 (15 beats/min, 15 s) criteria, and the time to attain a reactive NST was 4 min shorter with the 10 10 criteria [8]. When there are no sufficient FHR accelerations over a 40-min period, the NST is considered as nonreactive [4]. Fifteen percent of NSTs are nonreactive in general [2]. Decelerations and reduced or absent variability may be identified during the NST, and these prompt further evaluation for possible fetal jeopardy. If the NST is nonreactive, in order to increase the positive predictive value, the observation duration may be prolonged to 120 min [9]. The reactivity of the NST is closely associated with the gestational week; before 28 weeks of gestation, 50% of the NSTs may not be reactive [10]. The false-negative rate for the NST is around 0.19% [11], which is quite low. But the problematic feature of the NST comes with the nonreactive results. The sleep cycle of the fetus is frequently associated with the loss of reactivity during NST, hence the false-positive rate of an isolated nonreactive test may be as high as 55% [12], but it may be associated with fetal hypoxemia or acidosis, as well. Other associated factors with nonreactive NST results are maternal race [13,14], fetal immaturity, maternal smoking, 62
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sepsis, maternal ingestion of certain drugs which would depress fetal cardiac activity and fetal neurological and cardiac anomalies. A diurnal NST variation may be present, and performing a NST in the evening would lead to more reactive results [15]. Mild bradycardia (100–119 b.p.m.) or mild tachycardia (161–180 b.p.m.) may also be present during the NST. In the third trimester, FHR tends to regress toward the mean, and mild bradycardia/tachycardia is not regarded as a pathologic signal in nonacute situations [16]. Abused substances and medications [17] may also affect the test results and they should not be overlooked. Given that a fetus is more likely to be healthy than compromised in the setting of a nonreactive NST result, it is more appropriate to use NST in high-risk pregnancies in which fetal death risk is higher (given below) [4]. Indications for antepartum fetal surveillance: (1) Maternal conditions (a) Antiphospholipid syndrome (b) Hyperthyroidism (poorly controlled) (c) Hemoglobinopathies [hemoglobin SS (sickle cell anemia), SC (sickle-hemoglobin C disease), or sickle beta thalassemia] (d) Cyanotic heart disease (e) Systemic lupus erythematosus (f) Chronic renal disease (g) Type 1 diabetes mellitus (h) Hypertensive disorders (2) Pregnancy-related conditions (a) Pregnancy-induced hypertension (b) Decreased fetal movement (c) Oligohydramnios (d) Polyhydramnios (e) Intrauterine growth restriction (IUGR) (f) Post-term pregnancy (g) Isoimmunization (moderate to severe) (h) Previous fetal demise (unexplained or recurrent risk) (i) Multiple gestation (with significant growth discrepancy) There is no consensus for the optimal frequency for a NST, especially in high-risk situations such as IUGR or diabetes [18,19]. When the result is nonreactive, further evaluation is usually required as a back-up test such as the biophysical profile, contraction stress test or ultrasonography. But before these steps, some ancillary interventions may be more useful than invasive or time-consuming tests and may decrease the falsepositive results. In this review, we will focus on the factors or methods which may increase reactivity during fetal NST. Volume 26 Number 2 April 2014
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Factors that increase reactivity during fetal nonstress testing Esin
MATERNAL GLUCOSE ADMINISTRATION AND MATERNAL FASTING STATUS The main source of energy of the fetus is the glucose and the transfer of glucose from maternal to fetal compartments depends on the concentration gradient between them [20]. Although the benefit is controversial, maternal glucose consumption in the form of candies, sugary beverages and chocolate is widely practiced by pregnant patients to wiggle the baby. There are a small number of studies in the literature which investigate the effect of maternal glucose consumption on FHR patterns and fetal movements. Most of the studies included a small number of patients and hence were subjected to bias. Only two studies found increased fetal activity after maternal glucose administration [21,22]; however, most of the studies have found no effect of maternal glucose administration on FHR and fetal activity [23], specificity of NST [24], time to reactivity or the incidence of reactive NST [25,26], or percentage of reactive NST results when compared with the control group [27]. A recent Cochrane review including only two studies has also concluded that maternal glucose administration was not associated with reduced nonreactive cardiotocography results [28]. Association of maternal serum glucose levels and reactivity of NST was also investigated in the literature and no correlation was found [29,30]. Effect of maternal fasting on FHR was investigated by Mirghani et al. [31] and they found that the number of large accelerations was decreased in pregnant women abstaining from water and food. Although most pregnant women consume ‘glucose loaders’ to facilitate fetal movements and this is a routine, it is interesting to find so few studies with few patients in the literature assessing the value of these practices. Well designed randomized studies with higher numbers of participants are needed to clarify this myth on ‘sweet fetal accelerators’.
CHOCOLATE Chocolate is one of the most delectable treats for pregnant women, and recent evidence showed that it may have substantial health benefits, as well. Chocolate may have a protective effect against atherogenesis, and dark chocolate, which is rich in flavonoids, may be more protective than milk or white chocolate [32]. However, there are concerns about chocolate consumption during pregnancy and these stemmed from the caffeine content [33]. Although most of the studies reported beneficial effects of chocolate, [34–36,37 ], in an experimental study, possible negative impact on the wellbeing of &
offspring has been shown [38]. An interesting randomized study from Italy [39 ] evaluated the impact of supplementation with high-cocoacontent chocolate in pregnancy and found out that modest daily intake was associated with reduced glycemic levels, liver function tests and blood pressure in pregnancy. And a recent randomized doubleblind study has shown no negative impact of flavonol-rich chocolate on blood pressures in pregnancy [40]. The effect of chocolate on FHR patterns was evaluated by Buscicchio et al. [41], and the investigators found out that maternal intake of 70% cocoa or caffeine had stimulating action on fetal reactivity. Another study from the same investigators [42 ] revealed that the stimulating effect of chocolate on the FHR was more marked with high concentrations of cocoa (80%). These stimulating effects were linked to the pharmacological action of theobromine which is a methylxanthine present in cocoa. We have also investigated the effect of chocolate and orange juice on NST reactivity in a randomized controlled study [27] and have shown that orange juice and chocolate groups had similar percentage of reactive NST patterns when compared with the control group. Although the number of participants was limited, our study emphasized that repeating the test in 30 min without any intervention had similar NST results when compared with orange juice and bitter chocolate. In the future, I believe that chocolate with high flavonoid content may have a more important role in the diet of pregnant women who have placentation abnormalities. Studies particularly investigating the effect of chocolate, by means of flavonoids, on trophoblastic invasion are warranted in the future. &&
&
MATERNAL POSITION Maternal position during NST has been evaluated in a few studies. Friedman et al. [43] compared standing and left lateral recumbent positions during NST and found no difference in the number of heart rate accelerations and fetal movements. Abitbol et al. [44] compared the supine and lateral decubitus positions for NST reactivity for both low and high-risk patients and found that preference of lateral decubitus position during the test reduced the percentage of false nonreactive NST results. In another study, the semi-Fowler position was found to be superior to left lateral recumbent position for NST reactivity when the test was performed for a shortened period (10 min) [45]. Reclining, sitting and walking during NST were compared in low-risk
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pregnancies by Cito et al. [46], and fetal reactivity was more quickly observed during sitting or walking. Effect of maternal position on NST reactivity and perception of discomfort was investigated by Alus¸ et al. [47], and supine position was associated with least reactivity and greatest discomfort. In the randomized prospective study by Moffatt and van den Hof [48], the NSTs of 573 pregnant women were analyzed with computer with respect to the maternal position either as semi-Fowler’s position with 45-degree tilt to the right or left of the patient, or without lateral tilt. The researchers found no difference between groups in terms of NST reactivity rate and time to achieve a reactive NST. According to these results, we may not suggest a specific maternal position in order to increase NST reactivity, but especially after 32 gestational weeks, lateral recumbent or sitting positions may be more acceptable for the patients at least to avoid supine hypotension or maternal and possibly fetal discomfort.
FETAL MANIPULATION There is only one study in the literature investigating the effect of manual manipulation of the fetus on the NST [49]. Seven hundred and ninety pregnant patients were randomly assigned to the fetal manipulation and no fetal manipulation groups before the NST. According to this study, there was no statistically significant difference between the two groups with respect to the mean duration of testing and the ratio of reactive to nonreactive NSTs. Future studies investigating the number and timing of fetal manipulation on NST reactivity are needed to reach a conclusion on this topic.
VIBROACOUSTIC STIMULATION Brief fetal exposure to vibroacoustic stimulation (VAS) by an artificial larynx has been shown to lower the incidence of false nonreactive NSTs and reduce testing time in otherwise healthy fetuses [50]. There may possibly be an association between maternal cortisol levels and VAS, and this association may be more apparent among female than male fetuses [51]. Although the data on the safety of VAS are limited and some studies raised safety concerns [52–55], VAS does not appear to be associated with adverse fetal effects [56,57]. The only Cochrane systematic review of VAS during the antenatal period reported that VAS shortened the testing time and reduced the incidence of nonreassuring cardiotocography, but concluded that there was insufficient evidence from randomized controlled trials to recommend the 64
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routine antenatal use of VAS in the assessment of fetal wellbeing [54]. An interesting study on the VAS of anencephalic fetuses showed that the vibratory pathway may be more likely to elicit fetal response than the auditory pathway [58]. Xi et al. [59] performed a different method of antenatal VAS by clapping hands 1 cm above the maternal abdomen over the fetal vertex and they showed that such ‘improved acoustic test’ increased the specificity of NST. In another recent study [60], VAS use was associated with a reduction in time to reactivity and a reduction in the need for a biophysical profile. The effect of VAS on computerized cardiotocographic analysis was investigated by Annunziata et al. [61] and in that study, VAS increased the fetal movements both in low and high-risk pregnancies. After VAS, the increase in the short-term variability and the decrease in the approximate entropy were associated with favorable perinatal outcomes and these effects were seen only in the high-risk group [61]. When interpreting the FHR patterns after VAS, the gestational age of the fetus should also be considered [62].
HALOGEN LIGHT STIMULATION Halogen light has also been used to stimulate the fetus in a similar manner to VAS. In the randomized study by Caridi et al. [63], pregnant patients who received transabdominal light stimulation had more rapid reactive NST results when compared with no light. Bolnick et al. [64] compared VAS and halogen light stimulation with a control group. The reactive NST results were similar in the groups, but patients in the vibroacoustic and halogen light stimulation groups had more rapid FHR response and hence a shorter time to reactive NSTs. A similar study by Rahimikian et al. [65] concluded that both vibroacoustic and halogen light stimulation were safe and efficient in fetal wellbeing assessment units. The results of these studies are promising, but further studies are needed.
CONCLUSION As a conclusion, above-mentioned factors may increase the reactivity during a NST. These procedures and techniques may be particularly useful in order to prevent an undesired early delivery following a nonreactive NST result. Nonreactive NST results should be interpreted cautiously by the physicians given that in the setting of a nonreactive NST result, the fetus is more likely to be healthy than compromised. In the absence of decelerations, a more representative view of the fetus may be achieved by prolongation of test duration or by Volume 26 Number 2 April 2014
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Factors that increase reactivity during fetal nonstress testing Esin
repeating the test which may help us to exclude the physiologic causes. In contemporary practice, the physician should not rely on NST as a sole method of antenatal surveillance; in case, back-up tests such as biophysical profile, contraction stress test or ultrasonography are available. The use of multiple fetal surveillance tests in an algorithm may improve the prediction of adverse fetal outcomes and help delivery before permanent damage occurs. Acknowledgements None. Conflicts of interest There is no conflict of interest.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. Malcus P. Antenatal fetal surveillance. Curr Opin Obstet Gynecol 2004; 16:123–128. 2. Walton JR, Peaceman AM. Identification, assessment and management of fetal compromise. Clin Perinatol 2012; 39:753–768. 3. DeJesus Allison SO, Javitt MC, Glanc P, et al. ACR Appropriateness Criteria1 Multiple gestations. Ultrasound Q 2012; 28:149–155. 4. ACOG Practice Bulletin. Antepartum fetal surveillance. Number 9, October 1999 (replaces Technical Bulletin Number 188, January 1994). Clinical management guidelines for obstetrician-gynecologists. Int J Gynaecol Obstet 2000; 68:175–185. 5. Electronic fetal heart rate monitoring: research guidelines for interpretation. National Institute of Child Health and Human Development Research Planning, Workshop. Am J Obstet Gynecol 1997; 177:1385–1390. 6. Macones GA, Hankins GD, Spong CY, et al. The 2008 National Institute of Child Health and Human Development workshop report on electronic fetal monitoring: update on definitions, interpretation, and research guidelines. Obstet Gynecol 2008; 112:661–666. 7. Evertson LR, Gauthier RJ, Schifrin BS, Paul RH. Antepartum fetal heart rate testing. I. Evolution of the nonstress test. Am J Obstet Gynecol 1979; 133:29–33. 8. Cousins LM, Poeltler DM, Faron S, et al. Nonstress testing at 32.0 weeks’ gestation: a randomized trial comparing different assessment criteria. Am J Obstet Gynecol 2012; 207:311.e311–311.e317. 9. Brown R, Patrick J. The nonstress test: how long is enough? Am J Obstet Gynecol 1981; 141:646–651. 10. Bishop EH. Fetal acceleration test. Am J Obstet Gynecol 1981; 141:905– 909. 11. Freeman RK, Anderson G, Dorchester W. A prospective multiinstitutional study of antepartum fetal heart rate monitoring. II. Contraction stress test versus nonstress test for primary surveillance. Am J Obstet Gynecol 1982; 143:778–781. 12. Freeman RK, Anderson G, Dorchester W. A prospective multiinstitutional study of antepartum fetal heart rate monitoring. I. Risk of perinatal mortality and morbidity according to antepartum fetal heart rate test results. Am J Obstet Gynecol 1982; 143:771–777. 13. Paine LL, Strobino DM, Witter FR, Johnson TR. Population differences affect nonstress test reactivity. J Perinatol 1991; 11:41–45. 14. Johnson MJ, Paine LL, Mulder HH, et al. Population differences of fetal biophysical and behavioral characteristics. Am J Obstet Gynecol 1992; 166:138–142. 15. Babazadeh R, Abdali K, Lotfalizadeh M, et al. Diurnal nonstress test variations in the human fetus at risk. Int J Gynaecol Obstet 2005; 90:189–192. 16. Park YS, Hoh JK, Park MI. Fetal heart rate regresses toward the mean in the third trimester. J Korean Med Sci 2012; 27:794–798. 17. Kopel E, Hill WC. The effect of abused substances on antenatal and intrapartum fetal testing and well being. Clin Obstet Gynecol 2013; 56:154–165. 18. Miailhe G, Le Ray C, Timsit J, Lepercq J. Factors associated with urgent cesarean delivery in women with type 1 diabetes mellitus. Obstet Gynecol 2013; 121:983–989.
19. Thompson JL, Kuller JA, Rhee EH. Antenatal surveillance of fetal growth restriction. Obstet Gynecol Surv 2012; 67:554–565. 20. Teng CC, Tjoa S, Fennessey PV, et al. Transplacental carbohydrate and sugar alcohol concentrations and their uptakes in ovine pregnancy. Exp Biol Med (Maywood) 2002; 227:189–195. 21. Aladjem S, Feria A, Rest J, et al. Effect of maternal glucose load on fetal activity. Am J Obstet Gynecol 1979; 134:276–280. 22. Gelman SR, Spellacy WN, Wood S, et al. Fetal movements and ultrasound: effect of maternal intravenous glucose administration. Am J Obstet Gynecol 1980; 137:459–461. 23. Bocking A, Adamson L, Carmichael L, et al. Effect of intravenous glucose injection on human maternal and fetal heart rate at term. Am J Obstet Gynecol 1984; 148:414–420. 24. Richardson B, Briggs ML, Toomey C, et al. The effect of maternal glucose administration on the specificity of the nonstress test. Am J Obstet Gynecol 1983; 145:141–146. 25. McCarthy KE, Narrigan D. Is there scientific support for the use of juice to facilitate the nonstress test? J Obstet Gynecol Neonatal Nurs 1995; 24:303– 306. 26. Druzin ML, Foodim J. Effect of maternal glucose ingestion compared with maternal water ingestion on the nonstress test. Obstet Gynecol 1986; 67:425–426. 27. Esin S, Baser E, Cakir C, et al. Chocolate or orange juice for nonreactive nonstress test (NST) patterns: a randomized prospective controlled study. J Matern Fetal Neonatal Med 2013; 26:915–919. 28. Tan KH, Sabapathy A. Maternal glucose administration for facilitating tests of fetal wellbeing. Cochrane Database Syst Rev 2001; CD003397. 29. Phelan JP, Kester R, Labudovich ML. Nonstress test and maternal serum glucose determinations. Obstet Gynecol 1982; 60:437–439. 30. Miller FC, Skiba H, Klapholz H. The effect of maternal blood sugar levels on fetal activity. Obstet Gynecol 1978; 52:662–665. 31. Mirghani HM, Weerasinghe S, Al-Awar S, et al. The effect of intermittent maternal fasting on computerized fetal heart tracing. J Perinatol 2005; 25:90–92. 32. Ferna´ndez-Murga L, Tarı´n JJ, Garcı´a-Perez MA, Cano A. The impact of chocolate on cardiovascular health. Maturitas 2011; 69:312–321. 33. Vik T, Bakketeig LS, Trygg KU, et al. High caffeine consumption in the third trimester of pregnancy: gender-specific effects on fetal growth. Paediatr Perinat Epidemiol 2003; 17:324–331. 34. Ra¨ikko¨nen K, Pesonen AK, Ja¨rvenpa¨a¨ AL, Strandberg TE. Sweet babies: chocolate consumption during pregnancy and infant temperament at six months. Early Hum Dev 2004; 76:139–145. 35. Triche EW, Grosso LM, Belanger K, et al. Chocolate consumption in pregnancy and reduced likelihood of preeclampsia. Epidemiology 2008; 19:459– 464. 36. Saftlas AF, Triche EW, Beydoun H, Bracken MB. Does chocolate intake during pregnancy reduce the risks of preeclampsia and gestational hypertension? Ann Epidemiol 2010; 20:584–591. 37. Erkkola M, Nwaru BI, Kaila M, et al. Risk of asthma and allergic outcomes in & the offspring in relation to maternal food consumption during pregnancy: a Finnish birth cohort study. Pediatr Allergy Immunol 2012; 23:186–194. An interesting study which shows that low maternal chocolate consumption is associated with increased risk of allergic rhinitis in the offspring. 38. Zhang ZY, Zeng JJ, Kjaergaard M, et al. Effects of a maternal diet supplemented with chocolate and fructose beverage during gestation and lactation on rat dams and their offspring. Clin Exp Pharmacol Physiol 2011; 38:613– 622. 39. Di Renzo GC, Brillo E, Romanelli M, et al. Potential effects of chocolate on && human pregnancy: a randomized controlled trial. J Matern Fetal Neonatal Med 2012; 25:1860–1867. This study found out that modest daily intake of high-cocoa-content chocolate in pregnancy was associated with reduced glycemic levels, liver function tests and blood pressure in pregnancy. 40. Mogollon JA, Bujold E, Lemieux S, et al. Blood pressure and endothelial function in healthy, pregnant women after acute and daily consumption of flavanol-rich chocolate: a pilot, randomized controlled trial. Nutr J 2013; 12:41. 41. Buscicchio G, Piemontese M, Gentilucci L, et al. The effects of maternal caffeine and chocolate intake on fetal heart rate. J Matern Fetal Neonatal Med 2012; 25:528–530. 42. Buscicchio G, Lorenzi S, Tranquilli AL. The effects of different concentrations & of cocoa in the chocolate intaken by the mother on fetal heart rate. J Matern Fetal Neonatal Med 2013; 26:1465–1467. The stimulating action of chocolate on fetal reactivity is more marked with high concentrations (80%) of cocoa. 43. Friedman M, Divon MY, Zimmer EZ, et al. Nonstress test in standing and lying women. Early Hum Dev 1983; 8:317–322. 44. Abitbol MM, Monheit AG, Poje J, Baker MA. Nonstress test and maternal position. Obstet Gynecol 1986; 68:310–316. 45. Nathan EB, Haberman S, Burgess T, Minkoff H. The relationship of maternal position to the results of brief nonstress tests: a randomized clinical trial. Am J Obstet Gynecol 2000; 182:1070–1072. 46. Cito G, Luisi S, Mezzesimi A, et al. Maternal position during nonstress test and fetal heart rate patterns. Acta Obstet Gynecol Scand 2005; 84:335–338.
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www.co-obgyn.com
65
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Maternal–fetal medicine 47. Alus¸ M, Okumus¸ H, Mete S, Gu¨c¸lu¨ S. The effects of different maternal positions on nonstress test: an experimental study. J Clin Nurs 2007; 16:562–568. 48. Moffatt FW, van den Hof M. Semi-Fowler’s positioning, lateral tilts, and their effects on nonstress tests. J Obstet Gynecol Neonatal Nurs 1997; 26:551– 557. 49. Druzin ML, Gratacos J, Paul RH, et al. Antepartum fetal heart rate testing. XII. The effect of manual manipulation of the fetus on the nonstress test. Am J Obstet Gynecol 1985; 151:61–64. 50. Smith CV, Phelan JP, Platt LD, et al. Fetal acoustic stimulation testing. II. A randomized clinical comparison with the nonstress test. Am J Obstet Gynecol 1986; 155:131–134. 51. Glynn LM, Sandman CA. Sex moderates associations between prenatal glucocorticoid exposure and human fetal neurological development. Dev Sci 2012; 15:601–610. 52. Zimmer EZ, Chao CR, Guy GP, et al. Vibroacoustic stimulation evokes human fetal micturition. Obstet Gynecol 1993; 81:178–180. 53. Ingemarsson I, Arulkumaran S. Reactive fetal heart rate response to vibroacoustic stimulation in fetuses with low scalp blood pH. Br J Obstet Gynaecol 1989; 96:562–565. 54. Tan KH, Smyth R. Fetal vibroacoustic stimulation for facilitation of tests of fetal wellbeing. Cochrane Database Syst Rev 2001; CD002963. 55. Laventhal NT, Dildy GA, Belfort MA. Fetal tachyarrhythmia associated with vibroacoustic stimulation. Obstet Gynecol 2003; 101:1116–1118. 56. Ohel G, Horowitz E, Linder N, Sohmer H. Neonatal auditory acuity following in utero vibratory acoustic stimulation. Am J Obstet Gynecol 1987; 157:440– 441.
66
www.co-obgyn.com
57. Marden D, McDuffie RS, Allen R, Abitz D. A randomized controlled trial of a new fetal acoustic stimulation test for fetal well being. Am J Obstet Gynecol 1997; 176:1386–1388. 58. Park YJ, Park SH, Kim YJ, et al. Computerized fetal heart rate monitoring after vibroacoustic stimulation in the anencephalic fetus. Early Hum Dev 2010; 86:569–572. 59. Xi Q, Du J, Liu X, Shao L. Clinical study on detecting false nonreactive of nonstress test by improved acoustic stimulation. Arch Gynecol Obstet 2011; 284:271–274. 60. Turitz AL, Bastek JA, Sammel MD, et al. Can vibroacoustic stimulation improve the efficiency of a tertiary care antenatal testing unit? J Matern Fetal Neonatal Med 2012; 25:2645–2650. 61. Annunziata ML, Scala M, Giuliano N, et al. Fetal vibroacoustic stimulation in computerized cardiotocographic analysis: the role of short-term variability and approximate entropy. J Pregnancy 2012; 2012:814987. 62. Hoh JK, Park YS, Cha KJ, Park MI. Fetal heart rate after vibroacoustic stimulation. Int J Gynaecol Obstet 2009; 106:14–18. 63. Caridi BJ, Bolnick JM, Fletcher BG, Rayburn WF. Effect of halogen light stimulation on nonstress testing. Am J Obstet Gynecol 2004; 190:1470– 1472. 64. Bolnick JM, Garcia G, Fletcher BG, Rayburn WF. Cross-over trial of fetal heart rate response to halogen light and vibroacoustic stimulation. J Matern Fetal Neonatal Med 2006; 19:215–219. 65. Rahimikian F, Rahiminia T, Modarres M, Mehran A. Comparison of halogen light and vibroacoustic stimulation on nonreactive fetal heart rate pattern. Iran J Nurs Midwifery Res 2013; 18:112–116.
Volume 26 Number 2 April 2014
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Factors that increase reactivity during fetal nonstress testing Sertac Esin
Purpose of review The most common method of antepartum fetal surveillance is the nonstress test (NST). Although it has satisfactory false-negative rates, dubious nonreactive results may challenge the physician. Any method or factor increasing the reactive NST results or shortening the time to attain a reactive test may be considerably useful. Recent findings Most of the studies have found no effect of maternal glucose administration on fetal heart rate and fetal activity, specificity of NST, time to reactivity and percentage of reactive NST results when compared with the control group. Maternal intake of 70% cocoa or caffeine had stimulating action on the fetal reactivity, and this effect on the fetal heart rate was more marked with high concentrations of cocoa (80%). Studies on maternal positioning during NST had equivocal results. Fetal manipulation has no impact on the NST reactivity. Vibroacoustic and halogen light stimulation may be associated with a reduction in time to reactivity. Summary These methods may increase the reactivity during a NST and may facilitate the antenatal fetal surveillance. Keywords chocolate, glucose, halogen light stimulation, nonstress test, vibroacoustic stimulation
INTRODUCTION The primary aim of antenatal fetal surveillance is to discern the vulnerable fetus that will benefit from early recognition of risk of intrauterine injury and to reduce fetal and neonatal mortality. There are different methods of fetal surveillance, and electronic fetal monitoring (EFM) has become the cornerstone. EFM has been universally available in the developed world since the early 1970s. Although it has high specificity and false-positive rate and low falsenegative rate for perinatal morbidity and mortality in low-risk populations, it has become too routine for pregnant patients to undergo EFM in developed countries [1]. EFM is based on the fetal heart rate (FHR) assessment which is highly dependent on the gestational age. The main factor regulating FHR is the autonomic nervous system (ANS). The ANS receives inputs from several receptors and systems, and modulates the FHR simultaneously. As the gestational age increases, the parasympathetic nervous system (PNS) becomes more influential on the heart than the sympathetic nervous system (SNS) and this is primarily mediated by the vagus nerve, identified
as the tenth cranial nerve. The vagus nerve acts upon the sinoatrial and the atrioventricular nodes and has two main effects: it slows down the FHR (negative chronotropic effect) and decreases FHR variability, whereas sympathetic activation of the heart results in increased FHR and variability. FHR variability is also dependent on the gestational week and it should be present after 28 weeks when PNS is fully operational. The most common method of antepartum fetal surveillance assessment by FHR interpretation is the nonstress test (NST) [2]. For multiple gestations, antepartum fetal testing is recommended in circumstances where it would normally be performed in singleton pregnancies [3]. The main assumption of the NST is that with fetal movements, the heart rate Etlik Zubeyde Hanim Women’s Health and Teaching Hospital, Department of Perinatology, Ankara, Turkey Correspondence to Sertac Esin, MD, 212 Washington Avenue, 21204 Towson, Maryland, USA. Tel: +1 215 520 2768; e-mail: sertacesin@ gmail.com Curr Opin Obstet Gynecol 2014, 26:61–66 DOI:10.1097/GCO.0000000000000050
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KEY POINTS No effect of maternal glucose administration on FHR and fetal activity, specificity of NST, time to reactivity, or the percentage of reactive NST has been found. Maternal intake of chocolate has stimulating action on the fetal reactivity and this effect increases with higher cocoa content. Studies on maternal positioning during NST had equivocal results. Fetal manipulation has no impact on the NST reactivity. Vibroacoustic and halogen light stimulation may be associated with a reduction in time to reactivity.
of a nonacidotic or neurologically normal fetus would be accelerated [4]. NST results may be categorized as reactive or nonreactive. If there are two or more FHR accelerations that peak at least 15 beats per minute (b.p.m.) above the baseline and last 15 s from baseline to baseline (before 32 gestational weeks, two or more accelerations that peak at least 10 b.p.m. above the baseline and last 10 s from baseline to baseline [5,6]) within a 20-min period with or without fetal movement discernible by the mother, the NST is considered as reactive (or normal) [4,7]. For pregnancies below 32 weeks’ gestation, an interesting study compared the 10 10 criteria (10 beats/min, 10 s) with the 15 15 (15 beats/min, 15 s) criteria, and the time to attain a reactive NST was 4 min shorter with the 10 10 criteria [8]. When there are no sufficient FHR accelerations over a 40-min period, the NST is considered as nonreactive [4]. Fifteen percent of NSTs are nonreactive in general [2]. Decelerations and reduced or absent variability may be identified during the NST, and these prompt further evaluation for possible fetal jeopardy. If the NST is nonreactive, in order to increase the positive predictive value, the observation duration may be prolonged to 120 min [9]. The reactivity of the NST is closely associated with the gestational week; before 28 weeks of gestation, 50% of the NSTs may not be reactive [10]. The false-negative rate for the NST is around 0.19% [11], which is quite low. But the problematic feature of the NST comes with the nonreactive results. The sleep cycle of the fetus is frequently associated with the loss of reactivity during NST, hence the false-positive rate of an isolated nonreactive test may be as high as 55% [12], but it may be associated with fetal hypoxemia or acidosis, as well. Other associated factors with nonreactive NST results are maternal race [13,14], fetal immaturity, maternal smoking, 62
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sepsis, maternal ingestion of certain drugs which would depress fetal cardiac activity and fetal neurological and cardiac anomalies. A diurnal NST variation may be present, and performing a NST in the evening would lead to more reactive results [15]. Mild bradycardia (100–119 b.p.m.) or mild tachycardia (161–180 b.p.m.) may also be present during the NST. In the third trimester, FHR tends to regress toward the mean, and mild bradycardia/tachycardia is not regarded as a pathologic signal in nonacute situations [16]. Abused substances and medications [17] may also affect the test results and they should not be overlooked. Given that a fetus is more likely to be healthy than compromised in the setting of a nonreactive NST result, it is more appropriate to use NST in high-risk pregnancies in which fetal death risk is higher (given below) [4]. Indications for antepartum fetal surveillance: (1) Maternal conditions (a) Antiphospholipid syndrome (b) Hyperthyroidism (poorly controlled) (c) Hemoglobinopathies [hemoglobin SS (sickle cell anemia), SC (sickle-hemoglobin C disease), or sickle beta thalassemia] (d) Cyanotic heart disease (e) Systemic lupus erythematosus (f) Chronic renal disease (g) Type 1 diabetes mellitus (h) Hypertensive disorders (2) Pregnancy-related conditions (a) Pregnancy-induced hypertension (b) Decreased fetal movement (c) Oligohydramnios (d) Polyhydramnios (e) Intrauterine growth restriction (IUGR) (f) Post-term pregnancy (g) Isoimmunization (moderate to severe) (h) Previous fetal demise (unexplained or recurrent risk) (i) Multiple gestation (with significant growth discrepancy) There is no consensus for the optimal frequency for a NST, especially in high-risk situations such as IUGR or diabetes [18,19]. When the result is nonreactive, further evaluation is usually required as a back-up test such as the biophysical profile, contraction stress test or ultrasonography. But before these steps, some ancillary interventions may be more useful than invasive or time-consuming tests and may decrease the falsepositive results. In this review, we will focus on the factors or methods which may increase reactivity during fetal NST. Volume 26 Number 2 April 2014
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Factors that increase reactivity during fetal nonstress testing Esin
MATERNAL GLUCOSE ADMINISTRATION AND MATERNAL FASTING STATUS The main source of energy of the fetus is the glucose and the transfer of glucose from maternal to fetal compartments depends on the concentration gradient between them [20]. Although the benefit is controversial, maternal glucose consumption in the form of candies, sugary beverages and chocolate is widely practiced by pregnant patients to wiggle the baby. There are a small number of studies in the literature which investigate the effect of maternal glucose consumption on FHR patterns and fetal movements. Most of the studies included a small number of patients and hence were subjected to bias. Only two studies found increased fetal activity after maternal glucose administration [21,22]; however, most of the studies have found no effect of maternal glucose administration on FHR and fetal activity [23], specificity of NST [24], time to reactivity or the incidence of reactive NST [25,26], or percentage of reactive NST results when compared with the control group [27]. A recent Cochrane review including only two studies has also concluded that maternal glucose administration was not associated with reduced nonreactive cardiotocography results [28]. Association of maternal serum glucose levels and reactivity of NST was also investigated in the literature and no correlation was found [29,30]. Effect of maternal fasting on FHR was investigated by Mirghani et al. [31] and they found that the number of large accelerations was decreased in pregnant women abstaining from water and food. Although most pregnant women consume ‘glucose loaders’ to facilitate fetal movements and this is a routine, it is interesting to find so few studies with few patients in the literature assessing the value of these practices. Well designed randomized studies with higher numbers of participants are needed to clarify this myth on ‘sweet fetal accelerators’.
CHOCOLATE Chocolate is one of the most delectable treats for pregnant women, and recent evidence showed that it may have substantial health benefits, as well. Chocolate may have a protective effect against atherogenesis, and dark chocolate, which is rich in flavonoids, may be more protective than milk or white chocolate [32]. However, there are concerns about chocolate consumption during pregnancy and these stemmed from the caffeine content [33]. Although most of the studies reported beneficial effects of chocolate, [34–36,37 ], in an experimental study, possible negative impact on the wellbeing of &
offspring has been shown [38]. An interesting randomized study from Italy [39 ] evaluated the impact of supplementation with high-cocoacontent chocolate in pregnancy and found out that modest daily intake was associated with reduced glycemic levels, liver function tests and blood pressure in pregnancy. And a recent randomized doubleblind study has shown no negative impact of flavonol-rich chocolate on blood pressures in pregnancy [40]. The effect of chocolate on FHR patterns was evaluated by Buscicchio et al. [41], and the investigators found out that maternal intake of 70% cocoa or caffeine had stimulating action on fetal reactivity. Another study from the same investigators [42 ] revealed that the stimulating effect of chocolate on the FHR was more marked with high concentrations of cocoa (80%). These stimulating effects were linked to the pharmacological action of theobromine which is a methylxanthine present in cocoa. We have also investigated the effect of chocolate and orange juice on NST reactivity in a randomized controlled study [27] and have shown that orange juice and chocolate groups had similar percentage of reactive NST patterns when compared with the control group. Although the number of participants was limited, our study emphasized that repeating the test in 30 min without any intervention had similar NST results when compared with orange juice and bitter chocolate. In the future, I believe that chocolate with high flavonoid content may have a more important role in the diet of pregnant women who have placentation abnormalities. Studies particularly investigating the effect of chocolate, by means of flavonoids, on trophoblastic invasion are warranted in the future. &&
&
MATERNAL POSITION Maternal position during NST has been evaluated in a few studies. Friedman et al. [43] compared standing and left lateral recumbent positions during NST and found no difference in the number of heart rate accelerations and fetal movements. Abitbol et al. [44] compared the supine and lateral decubitus positions for NST reactivity for both low and high-risk patients and found that preference of lateral decubitus position during the test reduced the percentage of false nonreactive NST results. In another study, the semi-Fowler position was found to be superior to left lateral recumbent position for NST reactivity when the test was performed for a shortened period (10 min) [45]. Reclining, sitting and walking during NST were compared in low-risk
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pregnancies by Cito et al. [46], and fetal reactivity was more quickly observed during sitting or walking. Effect of maternal position on NST reactivity and perception of discomfort was investigated by Alus¸ et al. [47], and supine position was associated with least reactivity and greatest discomfort. In the randomized prospective study by Moffatt and van den Hof [48], the NSTs of 573 pregnant women were analyzed with computer with respect to the maternal position either as semi-Fowler’s position with 45-degree tilt to the right or left of the patient, or without lateral tilt. The researchers found no difference between groups in terms of NST reactivity rate and time to achieve a reactive NST. According to these results, we may not suggest a specific maternal position in order to increase NST reactivity, but especially after 32 gestational weeks, lateral recumbent or sitting positions may be more acceptable for the patients at least to avoid supine hypotension or maternal and possibly fetal discomfort.
FETAL MANIPULATION There is only one study in the literature investigating the effect of manual manipulation of the fetus on the NST [49]. Seven hundred and ninety pregnant patients were randomly assigned to the fetal manipulation and no fetal manipulation groups before the NST. According to this study, there was no statistically significant difference between the two groups with respect to the mean duration of testing and the ratio of reactive to nonreactive NSTs. Future studies investigating the number and timing of fetal manipulation on NST reactivity are needed to reach a conclusion on this topic.
VIBROACOUSTIC STIMULATION Brief fetal exposure to vibroacoustic stimulation (VAS) by an artificial larynx has been shown to lower the incidence of false nonreactive NSTs and reduce testing time in otherwise healthy fetuses [50]. There may possibly be an association between maternal cortisol levels and VAS, and this association may be more apparent among female than male fetuses [51]. Although the data on the safety of VAS are limited and some studies raised safety concerns [52–55], VAS does not appear to be associated with adverse fetal effects [56,57]. The only Cochrane systematic review of VAS during the antenatal period reported that VAS shortened the testing time and reduced the incidence of nonreassuring cardiotocography, but concluded that there was insufficient evidence from randomized controlled trials to recommend the 64
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routine antenatal use of VAS in the assessment of fetal wellbeing [54]. An interesting study on the VAS of anencephalic fetuses showed that the vibratory pathway may be more likely to elicit fetal response than the auditory pathway [58]. Xi et al. [59] performed a different method of antenatal VAS by clapping hands 1 cm above the maternal abdomen over the fetal vertex and they showed that such ‘improved acoustic test’ increased the specificity of NST. In another recent study [60], VAS use was associated with a reduction in time to reactivity and a reduction in the need for a biophysical profile. The effect of VAS on computerized cardiotocographic analysis was investigated by Annunziata et al. [61] and in that study, VAS increased the fetal movements both in low and high-risk pregnancies. After VAS, the increase in the short-term variability and the decrease in the approximate entropy were associated with favorable perinatal outcomes and these effects were seen only in the high-risk group [61]. When interpreting the FHR patterns after VAS, the gestational age of the fetus should also be considered [62].
HALOGEN LIGHT STIMULATION Halogen light has also been used to stimulate the fetus in a similar manner to VAS. In the randomized study by Caridi et al. [63], pregnant patients who received transabdominal light stimulation had more rapid reactive NST results when compared with no light. Bolnick et al. [64] compared VAS and halogen light stimulation with a control group. The reactive NST results were similar in the groups, but patients in the vibroacoustic and halogen light stimulation groups had more rapid FHR response and hence a shorter time to reactive NSTs. A similar study by Rahimikian et al. [65] concluded that both vibroacoustic and halogen light stimulation were safe and efficient in fetal wellbeing assessment units. The results of these studies are promising, but further studies are needed.
CONCLUSION As a conclusion, above-mentioned factors may increase the reactivity during a NST. These procedures and techniques may be particularly useful in order to prevent an undesired early delivery following a nonreactive NST result. Nonreactive NST results should be interpreted cautiously by the physicians given that in the setting of a nonreactive NST result, the fetus is more likely to be healthy than compromised. In the absence of decelerations, a more representative view of the fetus may be achieved by prolongation of test duration or by Volume 26 Number 2 April 2014
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Factors that increase reactivity during fetal nonstress testing Esin
repeating the test which may help us to exclude the physiologic causes. In contemporary practice, the physician should not rely on NST as a sole method of antenatal surveillance; in case, back-up tests such as biophysical profile, contraction stress test or ultrasonography are available. The use of multiple fetal surveillance tests in an algorithm may improve the prediction of adverse fetal outcomes and help delivery before permanent damage occurs. Acknowledgements None. Conflicts of interest There is no conflict of interest.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. Malcus P. Antenatal fetal surveillance. Curr Opin Obstet Gynecol 2004; 16:123–128. 2. Walton JR, Peaceman AM. Identification, assessment and management of fetal compromise. Clin Perinatol 2012; 39:753–768. 3. DeJesus Allison SO, Javitt MC, Glanc P, et al. ACR Appropriateness Criteria1 Multiple gestations. Ultrasound Q 2012; 28:149–155. 4. ACOG Practice Bulletin. Antepartum fetal surveillance. Number 9, October 1999 (replaces Technical Bulletin Number 188, January 1994). Clinical management guidelines for obstetrician-gynecologists. Int J Gynaecol Obstet 2000; 68:175–185. 5. Electronic fetal heart rate monitoring: research guidelines for interpretation. National Institute of Child Health and Human Development Research Planning, Workshop. Am J Obstet Gynecol 1997; 177:1385–1390. 6. Macones GA, Hankins GD, Spong CY, et al. The 2008 National Institute of Child Health and Human Development workshop report on electronic fetal monitoring: update on definitions, interpretation, and research guidelines. Obstet Gynecol 2008; 112:661–666. 7. Evertson LR, Gauthier RJ, Schifrin BS, Paul RH. Antepartum fetal heart rate testing. I. Evolution of the nonstress test. Am J Obstet Gynecol 1979; 133:29–33. 8. Cousins LM, Poeltler DM, Faron S, et al. Nonstress testing at 32.0 weeks’ gestation: a randomized trial comparing different assessment criteria. Am J Obstet Gynecol 2012; 207:311.e311–311.e317. 9. Brown R, Patrick J. The nonstress test: how long is enough? Am J Obstet Gynecol 1981; 141:646–651. 10. Bishop EH. Fetal acceleration test. Am J Obstet Gynecol 1981; 141:905– 909. 11. Freeman RK, Anderson G, Dorchester W. A prospective multiinstitutional study of antepartum fetal heart rate monitoring. II. Contraction stress test versus nonstress test for primary surveillance. Am J Obstet Gynecol 1982; 143:778–781. 12. Freeman RK, Anderson G, Dorchester W. A prospective multiinstitutional study of antepartum fetal heart rate monitoring. I. Risk of perinatal mortality and morbidity according to antepartum fetal heart rate test results. Am J Obstet Gynecol 1982; 143:771–777. 13. Paine LL, Strobino DM, Witter FR, Johnson TR. Population differences affect nonstress test reactivity. J Perinatol 1991; 11:41–45. 14. Johnson MJ, Paine LL, Mulder HH, et al. Population differences of fetal biophysical and behavioral characteristics. Am J Obstet Gynecol 1992; 166:138–142. 15. Babazadeh R, Abdali K, Lotfalizadeh M, et al. Diurnal nonstress test variations in the human fetus at risk. Int J Gynaecol Obstet 2005; 90:189–192. 16. Park YS, Hoh JK, Park MI. Fetal heart rate regresses toward the mean in the third trimester. J Korean Med Sci 2012; 27:794–798. 17. Kopel E, Hill WC. The effect of abused substances on antenatal and intrapartum fetal testing and well being. Clin Obstet Gynecol 2013; 56:154–165. 18. Miailhe G, Le Ray C, Timsit J, Lepercq J. Factors associated with urgent cesarean delivery in women with type 1 diabetes mellitus. Obstet Gynecol 2013; 121:983–989.
19. Thompson JL, Kuller JA, Rhee EH. Antenatal surveillance of fetal growth restriction. Obstet Gynecol Surv 2012; 67:554–565. 20. Teng CC, Tjoa S, Fennessey PV, et al. Transplacental carbohydrate and sugar alcohol concentrations and their uptakes in ovine pregnancy. Exp Biol Med (Maywood) 2002; 227:189–195. 21. Aladjem S, Feria A, Rest J, et al. Effect of maternal glucose load on fetal activity. Am J Obstet Gynecol 1979; 134:276–280. 22. Gelman SR, Spellacy WN, Wood S, et al. Fetal movements and ultrasound: effect of maternal intravenous glucose administration. Am J Obstet Gynecol 1980; 137:459–461. 23. Bocking A, Adamson L, Carmichael L, et al. Effect of intravenous glucose injection on human maternal and fetal heart rate at term. Am J Obstet Gynecol 1984; 148:414–420. 24. Richardson B, Briggs ML, Toomey C, et al. The effect of maternal glucose administration on the specificity of the nonstress test. Am J Obstet Gynecol 1983; 145:141–146. 25. McCarthy KE, Narrigan D. Is there scientific support for the use of juice to facilitate the nonstress test? J Obstet Gynecol Neonatal Nurs 1995; 24:303– 306. 26. Druzin ML, Foodim J. Effect of maternal glucose ingestion compared with maternal water ingestion on the nonstress test. Obstet Gynecol 1986; 67:425–426. 27. Esin S, Baser E, Cakir C, et al. Chocolate or orange juice for nonreactive nonstress test (NST) patterns: a randomized prospective controlled study. J Matern Fetal Neonatal Med 2013; 26:915–919. 28. Tan KH, Sabapathy A. Maternal glucose administration for facilitating tests of fetal wellbeing. Cochrane Database Syst Rev 2001; CD003397. 29. Phelan JP, Kester R, Labudovich ML. Nonstress test and maternal serum glucose determinations. Obstet Gynecol 1982; 60:437–439. 30. Miller FC, Skiba H, Klapholz H. The effect of maternal blood sugar levels on fetal activity. Obstet Gynecol 1978; 52:662–665. 31. Mirghani HM, Weerasinghe S, Al-Awar S, et al. The effect of intermittent maternal fasting on computerized fetal heart tracing. J Perinatol 2005; 25:90–92. 32. Ferna´ndez-Murga L, Tarı´n JJ, Garcı´a-Perez MA, Cano A. The impact of chocolate on cardiovascular health. Maturitas 2011; 69:312–321. 33. Vik T, Bakketeig LS, Trygg KU, et al. High caffeine consumption in the third trimester of pregnancy: gender-specific effects on fetal growth. Paediatr Perinat Epidemiol 2003; 17:324–331. 34. Ra¨ikko¨nen K, Pesonen AK, Ja¨rvenpa¨a¨ AL, Strandberg TE. Sweet babies: chocolate consumption during pregnancy and infant temperament at six months. Early Hum Dev 2004; 76:139–145. 35. Triche EW, Grosso LM, Belanger K, et al. Chocolate consumption in pregnancy and reduced likelihood of preeclampsia. Epidemiology 2008; 19:459– 464. 36. Saftlas AF, Triche EW, Beydoun H, Bracken MB. Does chocolate intake during pregnancy reduce the risks of preeclampsia and gestational hypertension? Ann Epidemiol 2010; 20:584–591. 37. Erkkola M, Nwaru BI, Kaila M, et al. Risk of asthma and allergic outcomes in & the offspring in relation to maternal food consumption during pregnancy: a Finnish birth cohort study. Pediatr Allergy Immunol 2012; 23:186–194. An interesting study which shows that low maternal chocolate consumption is associated with increased risk of allergic rhinitis in the offspring. 38. Zhang ZY, Zeng JJ, Kjaergaard M, et al. Effects of a maternal diet supplemented with chocolate and fructose beverage during gestation and lactation on rat dams and their offspring. Clin Exp Pharmacol Physiol 2011; 38:613– 622. 39. Di Renzo GC, Brillo E, Romanelli M, et al. Potential effects of chocolate on && human pregnancy: a randomized controlled trial. J Matern Fetal Neonatal Med 2012; 25:1860–1867. This study found out that modest daily intake of high-cocoa-content chocolate in pregnancy was associated with reduced glycemic levels, liver function tests and blood pressure in pregnancy. 40. Mogollon JA, Bujold E, Lemieux S, et al. Blood pressure and endothelial function in healthy, pregnant women after acute and daily consumption of flavanol-rich chocolate: a pilot, randomized controlled trial. Nutr J 2013; 12:41. 41. Buscicchio G, Piemontese M, Gentilucci L, et al. The effects of maternal caffeine and chocolate intake on fetal heart rate. J Matern Fetal Neonatal Med 2012; 25:528–530. 42. Buscicchio G, Lorenzi S, Tranquilli AL. The effects of different concentrations & of cocoa in the chocolate intaken by the mother on fetal heart rate. J Matern Fetal Neonatal Med 2013; 26:1465–1467. The stimulating action of chocolate on fetal reactivity is more marked with high concentrations (80%) of cocoa. 43. Friedman M, Divon MY, Zimmer EZ, et al. Nonstress test in standing and lying women. Early Hum Dev 1983; 8:317–322. 44. Abitbol MM, Monheit AG, Poje J, Baker MA. Nonstress test and maternal position. Obstet Gynecol 1986; 68:310–316. 45. Nathan EB, Haberman S, Burgess T, Minkoff H. The relationship of maternal position to the results of brief nonstress tests: a randomized clinical trial. Am J Obstet Gynecol 2000; 182:1070–1072. 46. Cito G, Luisi S, Mezzesimi A, et al. Maternal position during nonstress test and fetal heart rate patterns. Acta Obstet Gynecol Scand 2005; 84:335–338.
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65
Copyright © Lippincott Williams & Wilkins. Unauthorized reproduction of this article is prohibited.
Maternal–fetal medicine 47. Alus¸ M, Okumus¸ H, Mete S, Gu¨c¸lu¨ S. The effects of different maternal positions on nonstress test: an experimental study. J Clin Nurs 2007; 16:562–568. 48. Moffatt FW, van den Hof M. Semi-Fowler’s positioning, lateral tilts, and their effects on nonstress tests. J Obstet Gynecol Neonatal Nurs 1997; 26:551– 557. 49. Druzin ML, Gratacos J, Paul RH, et al. Antepartum fetal heart rate testing. XII. The effect of manual manipulation of the fetus on the nonstress test. Am J Obstet Gynecol 1985; 151:61–64. 50. Smith CV, Phelan JP, Platt LD, et al. Fetal acoustic stimulation testing. II. A randomized clinical comparison with the nonstress test. Am J Obstet Gynecol 1986; 155:131–134. 51. Glynn LM, Sandman CA. Sex moderates associations between prenatal glucocorticoid exposure and human fetal neurological development. Dev Sci 2012; 15:601–610. 52. Zimmer EZ, Chao CR, Guy GP, et al. Vibroacoustic stimulation evokes human fetal micturition. Obstet Gynecol 1993; 81:178–180. 53. Ingemarsson I, Arulkumaran S. Reactive fetal heart rate response to vibroacoustic stimulation in fetuses with low scalp blood pH. Br J Obstet Gynaecol 1989; 96:562–565. 54. Tan KH, Smyth R. Fetal vibroacoustic stimulation for facilitation of tests of fetal wellbeing. Cochrane Database Syst Rev 2001; CD002963. 55. Laventhal NT, Dildy GA, Belfort MA. Fetal tachyarrhythmia associated with vibroacoustic stimulation. Obstet Gynecol 2003; 101:1116–1118. 56. Ohel G, Horowitz E, Linder N, Sohmer H. Neonatal auditory acuity following in utero vibratory acoustic stimulation. Am J Obstet Gynecol 1987; 157:440– 441.
66
www.co-obgyn.com
57. Marden D, McDuffie RS, Allen R, Abitz D. A randomized controlled trial of a new fetal acoustic stimulation test for fetal well being. Am J Obstet Gynecol 1997; 176:1386–1388. 58. Park YJ, Park SH, Kim YJ, et al. Computerized fetal heart rate monitoring after vibroacoustic stimulation in the anencephalic fetus. Early Hum Dev 2010; 86:569–572. 59. Xi Q, Du J, Liu X, Shao L. Clinical study on detecting false nonreactive of nonstress test by improved acoustic stimulation. Arch Gynecol Obstet 2011; 284:271–274. 60. Turitz AL, Bastek JA, Sammel MD, et al. Can vibroacoustic stimulation improve the efficiency of a tertiary care antenatal testing unit? J Matern Fetal Neonatal Med 2012; 25:2645–2650. 61. Annunziata ML, Scala M, Giuliano N, et al. Fetal vibroacoustic stimulation in computerized cardiotocographic analysis: the role of short-term variability and approximate entropy. J Pregnancy 2012; 2012:814987. 62. Hoh JK, Park YS, Cha KJ, Park MI. Fetal heart rate after vibroacoustic stimulation. Int J Gynaecol Obstet 2009; 106:14–18. 63. Caridi BJ, Bolnick JM, Fletcher BG, Rayburn WF. Effect of halogen light stimulation on nonstress testing. Am J Obstet Gynecol 2004; 190:1470– 1472. 64. Bolnick JM, Garcia G, Fletcher BG, Rayburn WF. Cross-over trial of fetal heart rate response to halogen light and vibroacoustic stimulation. J Matern Fetal Neonatal Med 2006; 19:215–219. 65. Rahimikian F, Rahiminia T, Modarres M, Mehran A. Comparison of halogen light and vibroacoustic stimulation on nonreactive fetal heart rate pattern. Iran J Nurs Midwifery Res 2013; 18:112–116.
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