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From the Department of Anaesthesia, Intensive Care, The Chinese University of Hong Kong, Prince of Wales Hospital, Shatin, Nt, Hong Kong, China.
Address correspondence to: Dr. Anna Lee, Department of Anaesthesia and Intensive Care, The Chinese University of Hong Kong, Prince of Wales Hospital, Shatin, NT, Hong Kong, China. Phone: +852 2632 2735; Fax: +852 2637 2422; E-mail: annalee{at}cuhk.edu.hk
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Abstract |
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Source: Randomized, controlled trials obtained through MEDLINE, EMBASE, the Cochrane Controlled Trials Registry, contact with leading experts, and a reference list of published articles were analyzed. The following keywords were utilized: spinal anesthesia, hypotension, Cesarean section, pregnancy complications, pregnancy outcome, fetal outcome, neonatal outcome, umbilical blood cord gases, vasopressor and ephedrine. Clinical trials were considered if they compared prophylactic ephedrine, given by any dose or route, vs control.
Principal findings: The 14 clinical trials identified included data from a total of 641 patients. Ephedrine was more effective than control for preventing hypotension (relative risk [RR], 0.73; 95% confidence interval [CI], 0.63 to 0.86). Most importantly, there was no difference in the risk of fetal acidosis, defined as umbilical arterial pH < 7.2 (RR, 1.36; 95% CI, 0.55 to 3.35) or the incidence of low Apgar scores (< 7 or < 8) at one minute (RR, 0.77; 95% CI, 0.29 to 2.06) and five minutes (RR, 0.72; 95% CI, 0.24 to 2.19).
Conclusions: Prophylactic ephedrine is more effective than control for preventing hypotension during spinal anesthesia for elective Cesarean delivery but a clinically relevant positive effect on neonatal outcome was not observed. Therefore, the routine use of prophylactic ephedrine to prevent any adverse effects of maternal hypotension following spinal anesthesia for Cesarean delivery is not supported by the current systematic review.
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Introduction |
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TOPAbstractIntroductionMaterials and methodsResultsMaternal outcomesDiscussionReferences |
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Lateral uterine displacement and iv prehydration are commonly used to prevent hypotension but these have limited efficacy and a vasopressor drug is often required.2,4 Although vasopressors unquestionably have a role in the treatment of hypotension,2 their prophylactic use is more controversial. Some studies have shown no significant reduction of maternal hypotension associated with the prophylactic use of ephedrine when compared with control.5,6 In other studies, women given ephedrine before or during induction of spinal anesthesia had a lower incidence of maternal hypotension compared with those not given a vasopressor.1,4,7
To identify evidence-based recommendations for clinical practice and further areas of research, we conducted a systematic review of randomized controlled trials (RCTs) of prophylactic vasopressor use in obstetrics. Because the main drug that has been investigated in this context is ephedrine, other drugs were excluded in this review. The purpose of the current systematic review was to compare the effects and consequences of ephedrine vs controls of placebo or no ephedrine for the prevention of hypotension during spinal anesthesia during Cesarean delivery.
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Materials and methods |
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Data extraction
The selection of trials for inclusion in the systematic review was performed independently by the reviewers (A.L. and W.N.) after using the search strategy described above. Trials were examined for duplicate data. Data were abstracted independently by A.L. and W.N. using a standardized data collection form. There was no attempt to blind the reviewers (A.L. and W.N.) to the authors or results of the relevant trials. Details of anesthetic technique, study population, prehydration, uterine displacement and definition of maternal hypotension were collected. Where appropriate, the primary author of a RCT was contacted for clarification of data. Discrepancies were resolved by discussion, or advice was sought from a third party (T.G.).
The quality of the eligible trials was assessed independently. The level of allocation concealment, defined as the process used to prevent the foreknowledge of group assignment in a RCT, was graded as A (adequate), B (unclear), or C (inadequate), as previously described.9 Blinding, losses to follow-up and whether the authors did a sample size calculation before trial commencement were recorded. The reasons for trial exclusion from the review were recorded.
Statistical analysis
The main outcome was prevention of maternal hypotension by ephedrine vs control. We used the specific definition of hypotension that was used in each individual trial and made no attempt at standardization. Consequences associated with the use of ephedrine that we assessed were reactive hypertension, maternal heart rate, low Apgar scores (< 7 or < 8 as defined by trial authors) and fetal acidosis which we defined as umbilical arterial pH < 7.20).10 In RCTs 4,11 with more than one ephedrine treatment arm, we combined the data from each treatment arm for dichotomous outcomes (hypotension, hypertension, nausea and/or vomiting and Apgar scores). For continuous data (umbilical arterial and venous pH and standard base excess), the greatest ephedrine dose treatment arm was used as it was not possible to combine data from all ephedrine arms when only summary group means were reported.
The DerSimonian and Laird random-effects model was used to combine data for both continuous and dichotomous outcomes, because the treatment and conditions in these studies were expected to be heterogeneous. This model incorporates both between-study (different treatment effects) and within-study (sampling error) variability.12 The pooled relative risk (RR) and 95% confidence interval (95% CI) were calculated for dichotomous data. The weighted mean difference (WMD) method was used to pool continuous data. Heterogeneity was analyzed using the Q-statistic with a threshold for the P < 0.10. Where heterogeneity (inter-study variation) was found, the studies that seemed to be the major contributors to the heterogeneity were evaluated in an attempt to discover the reasons. All meta-analyses were done using Arcus Quickstat software (version 1.2; Addison Wesley Longman Ltd, Cambridge, UK).
Sensitivity analyses for hypotension were done to estimate the robustness of results according to allocation concealment (adequate vs unclear/inadequate), blinding (double-blinding vs single-blinding) and intervention type (ephedrine given before hypotension vs ephedrine given when a small decrease in arterial pressure was detected).
A funnel plot (plot of treatment effect against trial precision) was used to detect bias in the meta-analysis of prophylactic ephedrine trials on preventing hypotension. In the presence of bias which will usually lead to an over-estimate of the treatment effect, the funnel plot will be skewed and asymmetrical. The degree of asymmetry was measured by Egger's method13 using EasyMa software (version 2000, Michel Cucherat, Lyon, France). Sources of asymmetry in funnel plots can be due to selection bias (publication bias, English language bias, citation bias, multiple publication bias), true heterogeneity, data irregularities, choice of effect measure and chance.13
To judge whether therapy was worthwhile for an individual, the absolute magnitude of benefit was estimated by calculating the numbers-needed-to-treat (NNT). As a NNT derived from meta-analysis can be sensitive to factors that change the baseline risk, a more useful NNT was estimated by applying the pooled relative risk to a relevant baseline risk.14 We chose 80%2 as the baseline risk to calculate a clinically useful NNT.
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Results |
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There were 13 articles describing 14 RCTs of ephedrine vs placebo or no ephedrine (n = 641; Table
). Trials were conducted between 1976 and 2001. There was one trial that had two vasopressor arms (ephedrine, angiotensin) and a control arm.21 One study described two separate ephedrine dose-response trials: iv bolus (trial 1) and continuous iv infusion (trial 2).11 Multiple ephedrine groups were used in several trials.4,5,11(trial 1, trial 2),22
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). In all trials, the women were described as healthy or were graded as ASA physical status I or II. There were no reports of trials recruiting women undergoing emergency Cesarean delivery, and therefore, we have assumed that all trials included in this systematic review involved women undergoing elective Cesarean delivery. Drugs used for spinal anesthesia included tetracaine,7,21,22 bupivacaine,5,6,27 and hyperbaric bupivacaine.1,4,11,23–26 The combined spinal-epidural anesthesia technique was used in two trials.1,26 All trials specified the use of uterine displacement. Iv fluid prehydration was given in all trials except one in which the ephedrine group was not given prehydration.25
There was adequate allocation concealment (A) in four trials.1,4,5,26 Despite attempts to contact the primary author, we were uncertain whether randomization occurred in the earliest trial7 but the groups appeared comparable. All other trials were classified as having unclear allocation concealment (B) because the randomization procedure was not described. There was double-blinding in seven trials.1,4–7,24,26 There was no blinding in three trials.21,11 (trial 1, trial 2) All other trials were single-blinded. Details about withdrawals from the trial were given in three trials.1,4,23 Sample size calculations were done in three recent trials.4,6,26
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Maternal outcomes |
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The mean baseline risk of hypotension in the control group was 69% (95% CI, 63% to 75%) in the 11 trials. Disregarding the dose of ephedrine used, data pooled from 12 trials (n = 571) were homogeneous (Q statistic = 13.94, df = 11, P = 0.24) and showed that ephedrine was more effective for preventing hypotension than control (RR, 0.73; 95% CI, 0.63 to 0.86; Figure 1). There was no evidence of bias in this meta-analysis as shown by the symmetry in the funnel plot (intercept = 0.53, 90% CI, -0.48 to 1.54, P = 0.41; Figure 2).
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The level of allocation concealment did not affect the overall summary effect size. In restricting the meta-analysis to only trials that had adequate allocation concealment 1,4,5,26 the overall RR was 0.69 (95% CI, 0.58 to 0.83) with no evidence of heterogeneity (Q statistic = 2.04, df = 3, P = 0.56). In trials where allocation concealment was unclear,6,7,11,21,24,25,27 the overall RR was 0.76 (95% CI, 0.59 to 0.99) with no evidence of heterogeneity (Q statistic = 11.50; df = 7; P = 0.12).
Meta-analysis of double-blinded studies1,4–7,24,26 showed that ephedrine was significantly associated with a smaller risk of hypotension compared with control (RR, 0.70; 95% CI, 0.57 to 0.87). In contrast, this association was not significant in single-and open-blinded studies (RR, 0.79; 95% CI, 0.58 to 1.08).11(trial 1, trial 2),21,25,27
Hypertension
The authors of eight trials recorded data on reactive hypertension.4,6,7,11 (trial 1, trial 2),22,24,26 Although hypertension was defined specifically in many trials, it was not standardized. Gutsche7 and Tsen6 reported a nil incidence of hypertension in both ephedrine and control groups without giving a specific definition. When we restricted the analysis to trials in which specific definitions of reactive hypertension were given,4,11 (trial 1, trial 2),22,24,26 there was no evidence that ephedrine was associated with reactive hypertension (RR, 1.63; 95% CI, 0.93 to 2.84).
Abnormal maternal heart rate
Maternal tachycardia was defined in one trial24 as heart rate > 120 and there was no difference in the incidence between ephedrine (14/20) and placebo (13/20) groups. Maternal bradycardia was defined in one trial by Vercauteren et al.1 as heart rate < 30% of baseline; in this trial the incidence of bradycardia was small in both ephedrine (0/24) and placebo (1/24) groups. In another trial,26 bradycardia (heart rate < 60 beats•min-1) did not occur in either ephedrine or placebo groups. Combining these two trials showed that ephedrine was not associated with bradycardia (RR, 0.52; 95% CI, 0.04 to 5.96).
Nausea and vomiting
There was no difference in the incidence of nausea (RR, 0.82; 95% CI, 0.57 to 1.18),1,11(trial 1, trial 2),23 vomiting (RR, 0.73; 95% CI, 0.35 to 1.52)1,11(trial 1, trial 2),23 or nausea and vomiting (RR, 0.71; 95% CI, 0.37 to 1.37)4,7,21,22,25,27 between the ephedrine and control groups.
Uterine vasculature
The uterine vasculature was assessed in a subgroup of patients (n = 11) in one trial using Doppler ultrasound.25 There was no difference in the uterine artery pulsatility index between ephedrine and fluid control groups.25
Neonatal outcomes
APGAR SCORES
The Apgar scores were recorded at one minute and five minutes in all trials. A low Apgar score at one minute was defined as < 7 in all trials except Webb (1998)24 and Kang (1982)22 in which it was defined as < 8. With the exception of one trial,1 all neonates had an Apgar score at one minute above the threshold. There was no difference between ephedrine and control groups in the incidence of low Apgar score at one minute (RR, 0.77; 95% CI, 0.29 to 2.06). A low Apgar score at five minutes was defined as < 8 in three trials,1,7,24 and in all other trials it was defined as < 7. No neonates had low Apgar score at five minutes. The overall effect size suggested that there was no difference in low Apgar score at five minutes between ephedrine and control groups (RR, 0.72; 95% CI, 0.24 to 2.19).
Umbilical pH and fetal acidosis
The authors reported umbilical arterial pH in eight trials1,4,11 (trial 1, trial 2),21–23,25 (n = 301) but these trials were heterogeneous (Q statistic = 15.99, df = 7, P = 0.03). The mean umbilical arterial pH in the control groups ranged from 7.2325 to 7.29.1,23 The incidence of fetal acidosis (umbilical arterial pH < 7.2) was available in six trials (n = 350).1,4,11 (trial 1, trial 2),21,23, There was no difference in the risk of fetal acidosis between ephedrine and control groups (RR, 1.36; 95% CI, 0.55 to 3.35). Seven trials1,4,21,22,24–26 (n = 292) reported umbilical venous pH. However, these trials were heterogeneous (Q statistic = 18.60, df = 6, P < 0.01).
Standard base excess
Four trials 21–23,25 (n = 136) showed that there was no significant difference between ephedrine and control for arterial standard base excess (WMD = -0.85, 95% CI = -2.32 to 0.61). The range of arterial standard base excess in the placebo or control groups was -1.8 21 to -5.9.25 Three trials21,22,25 (n = 110) were heterogeneous (Q statistic = 6.91, df = 2, P = 0.03) when venous standard base excess was analyzed.
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Discussion |
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TOPAbstractIntroductionMaterials and methodsResultsMaternal outcomesDiscussionReferences |
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To apply the results of this meta-analysis to a clinical setting so that anesthesiologists can judge whether prophylactic ephedrine is worthwhile for an individual, we calculated the NNT. If our results were applied to a baseline risk of 80%,2 the NNT would be 4.6 (95% CI, 3.4 to 8.9) meaning that for every 100 women who receive ephedrine, 22 (95% CI, 11 to 30) will not develop hypotension who would have done so had they not received ephedrine. Therefore, the overall benefit of prophylactic ephedrine for the prevention of maternal hypotension during spinal anesthesia is small; this implies that clinical practice may be better focused on treatment after hypotension has occurred.
There was wide variation in the ephedrine regimens used in the trials included in our review. This most likely reflects regional differences in practice around the world and between individual anesthesiologists. It is important to note that our meta-analysis did not discriminate between doses, precise timing or routes of administration of ephedrine. Meta-regression,28 a statistical technique to assess whether specific factors (such as timing and routes of administration of ephedrine) influence the overall treatment effect was not carried out because of the small number of trials available in this systematic review.
As there was no standardized dose of ephedrine used across trials, this systematic review did not answer the question about what dose should be used to prevent maternal hypotension. Intuitively, one would expect that all investigators would have given an adequate and effective prophylactic dose of ephedrine. Although ephedrine has a small benefit, this may be due to an inadequate dose of ephedrine used in some trials or that ephedrine has limited effectiveness.
Therefore, to determine the relative effects of dose, timing and route of ephedrine administration, it is necessary to refer to the results of individual RCTs. For example, in a previous dose-finding RCT, we found that the efficacy of prophylactic ephedrine for the prevention of hypotension, when given as an iv bolus one minute after intrathecal injection, was dose-dependent.4 Furthermore, our meta-analysis was limited to ephedrine as there was insufficient data on other vasopressors given prophylactically at the time we performed the search for RCTs. However, we note that a recent RCT showed that prophylactic im phenylephrine 4 mg was associated with a twofold decrease in developing hypotension compared with control (RR = 2.00, 95% CI, 1.10 to 3.57).26 These findings suggest that further work to determine the optimal technique of prophylactic ephedrine administration and trials of other prophylactic vasopressors are warranted.
The efficacy of crystalloid bolus in the management of hypotension associated with spinal anesthesia for Cesarean delivery has been examined.29,30 In a non-blinded study that used a sequential analysis design, a preload of 20 mL•kg-1 lactated Ringer's solution reduced the incidence of hypotension from 71% to 55% but did not affect neonatal outcome or ephedrine requirement.29 After this, a randomized blinded trial showed no beneficial effect of 1000 mL crystalloid.30 In this systematic review, only one trial compared prophylactic ephedrine infusion with fluid preloading.25 Although the incidence of moderate hypotension (20% reduction in SBP) was similar, there was a lower incidence of severe hypotension (30% reduction in SBP) in the ephedrine group (35%) compared with the fluid group (65%).25 The reason why crystalloid bolus has only limited efficacy can be attributed to its rapid redistribution out of the intravascular space, which results in a relatively small augmentation of circulating volume.
There was no association between the use of ephedrine and fetal acidosis in our review. This is in contrast with the observational study by Shearer16 who reported a significant association, with a threefold greater incidence of fetal acidosis in the ephedrine group compared with control (no ephedrine). The authors postulated that the decreased uteroplacental perfusion that results from hypotension may be further compromised by the 
-agonist vasoconstricting properties of ephedrine,16 but this had not been confirmed by studies that have assessed uterine vascular resistance using Doppler ultrasound.25,31 Nonetheless, further studies are required to confirm the safety and efficacy of prophylactic ephedrine in cases where there is compromised uteroplacental blood flow.
There are several limitations to the present systematic review. As there was no standard definition of hypotension in this systematic review, we chose to rely upon the definition of hypotension given by the authors of each trial. Therefore, there is some degree of clinical heterogeneity between trials. The quality of trials included in this systematic review was fair, with four trials that had both adequate allocation concealment and double-blinding. Compared with trials that have adequate allocation concealment or are double-blinded, trials with unclear allocation concealment or are not double-blinded are associated with a larger treatment effect (41% and 17% respectively).9 However, our sensitivity analyses showed that quality of the trials did not appear to influence the overall treatment effect. Finally, some caution is needed in interpreting the results of this meta-analysis which is based on results of many small trials as subsequent large trials have disagreed with meta-analyses 10% to 23% of the time.32 Nevertheless, in the absence of a large multi-centered trial on this issue, the best strategy for appraising the available evidence is the use of meta-analysis. We believe that the findings from this systematic review are robust, as there was no evidence of bias from the funnel plot.
In summary, there is evidence that prophylactic ephedrine has limited efficacy for the prevention of hypotension during spinal anesthesia for Cesarean delivery. The optimal route, dose and timing are undetermined and we found no evidence that ephedrine was associated with improved neonatal outcome.
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Acknowledgments |
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Revision received January 16, 2002. Accepted for publication October 25, 2002.
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References |
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2 Rout CC, Rocke DA. Prevention of hypotension following spinal anesthesia for cesarean section. Int Anesthesiol Clin 1994; 32: 117–35.[Medline]
3 Wright RG, Shnider SM. Hypotension and regional anesthesia. In: Shnider SM, Levinson G. (Eds.). Anesthesia for Obstetrics, 3rd ed. Baltimore: Williams & Wilkins, 1993: 397–406.
4
Ngan Kee WD, Khaw KS, Lee BB, Lau TK, Gin T. A dose-response study of prophylactic intravenous ephedrine for the prevention of hypotension during spinal anesthesia for cesarean delivery. Anesth Analg 2000; 90: 1390–5.
5 King SW, Rosen MA. Prophylactic ephedrine and hypotension associated with spinal anesthesia for cesarean delivery. Int J Obstet Anesth 1998; 7: 18–22.
6 Tsen LC, Boosalis P, Segal S, Datta S, Bader AM. Hemodynamic effects of simultaneous administration of intravenous ephedrine and spinal anesthesia for cesarean delivery. J Clin Anesth 2000; 12: 378–82.[Medline]
7 Gutsche BB. Prophylactic ephedrine preceding spinal analgesia for cesarean section. Anesthesiology 1976; 45: 462–5.[Medline]
8 Egger M, Davey Smith G, Altman DG. Systematic Reviews in Health Care: Meta-Analysis in Context, 2nd ed. London: British Medical Journal Publishing Group, 2001.
9 Schulz KF, Chalmers I, Hayes RJ, Altman DG. Empirical evidence of bias. Dimensions of methodological quality associated with estimates of treatment effects in controlled trials. JAMA 1995; 273: 408–12.[Abstract]
10 Roberts SW, Leveno KJ, Sidawi JE, Lucas MJ, Kelly MA. Fetal acidemia associated with regional anesthesia for elective cesarean delivery. Obstet Gynecol 1995; 85: 79–83.[Abstract]
11 Carvalho JCA, Cardoso MMSC, Capelli EL, Amaro AR, Rosa MCR. Prophylactic ephedrine during cesarean delivery spinal anesthesia. Dose-response study of bolus and continuous infusion administration (Portugese). Rev Bras Anestesiol 1999; 49: 309–14.
12 Mosteller F, Colditz GA. Understanding research synthesis (meta-analysis). Ann Rev Public Health 1996; 17: 1–23.[Medline]
13
Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ 1997; 315: 629–34.
14
Smeeth L, Haines A, Ebrahim S. Numbers needed to treat derived from meta-analyses-sometimes informative, usually misleading. BMJ 1999; 318: 1548–51.
15 Datta S, Alper MH, Ostheimer GW, Weiss JB. Method of ephedrine administration and nausea and hypotension during spinal anesthesia for cesarean section. Anesthesiology 1982; 56: 68–70.[Medline]
16 Shearer VE, Ramin SM, Wallace DH, Dax JS, Gilstrap III LC. Fetal effects of prophylactic ephedrine and maternal hypotension during regional anesthesia for cesarean section. J Matern Fetal Med 1996; 5: 79–84.[Medline]
17 Haruta M, Funato T, Saeki N, Naka Y, Shinkai T. Ephedrine administration for cesarean section under spinal anesthesia (Japanese). Nippon Sanka Fujinka Gakkai Zasshi 1987; 39: 207–14.[Medline]
18 Rout CC, Rocke DA, Brijball R, Koovarjee RV. Prophylactic intramuscular ephedrine prior to caesarean section. Anaesth Intensive Care 1992; 20: 448–52.[Medline]
19 Ramanathan S, Grant GJ. Vasopressor therapy for hypotension due to epidural anesthesia for cesarean section. Acta Anaesthesiol Scand 1988; 32: 559–65.[Medline]
20 Yokoyama H, Kubota N, Toda K. Continuous infusion of dopamine to maintain stable arterial pressure during spinal anaesthesia for caesarean section. Eur J Anaesthesiol 1997; 14: 72–3.
21 Ramin SM, Ramin KD, Cox K, Magness RR, Shearer VE, Gant NF. Comparison of prophylactic angiotensin II versus ephedrine infusion for prevention of maternal hypotension during spinal anesthesia. Am J Obstet Gynecol 1994; 171: 734–9.[Medline]
22
Kang YG, Abouleish E, Caritis S. Prophylactic intravenous ephedrine infusion during spinal anesthesia for cesarean section. Anesth Analg 1982; 61: 839–42.
23 Olsen KS, Feilberg VL, Hansen CL, Rudkjøbing O, Pedersen T, Kyst A. Prevention of hypotension during spinal anaesthesia for caesarean section. Int J Obstet Anesth 1994; 3: 20–4.
24
Webb AA, Shipton EA. Re-evaluation of im ephedrine as prophylaxis against hypotension associated with spinal anaesthesia for caesarean section. Can J Anaesth 1998; 45: 367–9.
25 Chan WS, Irwin MG, Tong WN, Lam YH. Prevention of hypotension during spinal anaesthesia for caesarean section: ephedrine infusion versus fluid preload. Anaesthesia 1997; 52: 896–913.[Medline]
26
Ayorinde BT, Buczkowski P, Brown J, Shah J, Buggy DJ. Evaluation of pre-emptive intramuscular phenylephrine and ephedrine for reduction of spinal anaesthesia-induced hypotension during caesarean section. Br J Anaesth 2001; 86: 372–6.
27 Kangas-Saarela T, Hollmén AI, Tolonen U, et al. Does ephedrine influence newborn neurobehavioural responses and spectral EEG when used to prevent maternal hypotension during caesarean section? Acta Anaesthesiol Scand 1990; 34: 8–16.[Medline]
28 Berlin JA, Antman EM. Advantages and limitations of metaanalytic regressions of clinical trials data. Online J Curr Clin Trials 1994; Doc No 134.
29 Rout CC, Rocke DA, Levin J, Gouws E, Reddy D. A reevaluation of the role of crystalloid preload in the prevention of hypotension associated with spinal anesthesia for elective cesarean section. Anesthesiology 1993; 79: 262–9.[Medline]
30
Jackson R, Reid JA, Thorburn J. Volume preloading is not essential to prevent spinal-induced hypotension at caesarean section. Br J Anaesth 1995; 75: 262–5.
31 Ngan Kee WD, Lau TK, Khaw KS, Lee BB. Comparison of metaraminol and ephedrine infusions for maintaining arterial pressure during spinal anesthesia for elective cesarean section. Anesthesiology 2001; 95: 307–13.[Medline]
32
Ioannidis JPA, Cappelleri JC, Lau J. Issues in comparisons between meta-analyses and large trials. JAMA 1998; 279: 1089–3.
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