Management of Critical Asthma Syndrome During Pregnancy

Abstract

One-third of pregnant asthmatics experience a worsening of their asthma that may progress to a critical asthma syndrome (CAS) that includes status asthmaticus (SA) and near-fatal asthma (NFA). Patients with severe asthma before pregnancy may experience more exacerbations, especially during late pregnancy. Prevention of the CAS includes excellent asthma control involving targeted early and regular medical care of the pregnant asthmatic, together with medication compliance. Spontaneous abortion risk is higher in pregnant women with uncontrolled asthma than in non-asthmatics. Should CAS occur during pregnancy, aggressive bronchodilator therapy, montelukast, and systemic corticosteroids can be used in the context of respiratory monitoring, preferably in an Intensive Care Unit (ICU). Systemic epinephrine should be avoided due to potential teratogenic side-effects and placental/uterine vasoconstriction. Non-invasive ventilation has been used in some cases. Intratracheal intubation can be hazardous and rapid-sequence intubation by an experienced physician is recommended. Mechanical ventilation parameters are adjusted based on changes to respiratory mechanics in the pregnant patient. An inhaled helium–oxygen gas admixture may promote laminar airflow and improve gas exchange. Permissive hypercapnea is controversial, but may be unavoidable. Sedation with propofol which itself has bronchodilating properties is preferred to benzodiazepines. Case reports delineating good outcomes for both mother and fetus despite intubation for SA suggest that multidisciplinary ICU care of the pregnant asthmatic with critical asthma are feasible especially if hypoxemia is avoided.

Introduction

Asthma per se is one of the commonest chronic medical illnesses that complicate pregnancy, occurring in up to 8.8 % of women [1, 2]. One-third of pregnant asthmatics improve, one-third remain stable, but the remaining third demonstrate a clinical worsening of their asthma [35]. Those who worsen are rendered at risk for developing a critical asthma syndrome, i.e., status asthmaticus (SA) and near-fatal asthma (NFA). Worsening during pregnancy may be related to pre-pregnancy baseline severity, with patients with moderate and severe asthma, in particular, demonstrating more exacerbations [68]. Gluck et al. [3] reported on similarities of an individual’s asthma course during the first and subsequent pregnancies. Asthma symptoms and hence worsening usually peak in the late second or early third trimester, but exacerbations are rare during labor and peripartum [3, 5, 9, 10]. The optimal management of a critically ill pregnant patient due to worsening asthma can be challenging, with both mother and fetus at risk, especially from hypoxemia. Therefore, subspecialist management within a multidisciplinary Intensive Care Unit (ICU), including intensivists, asthma specialists, neonatologists, and obstetricians experienced in high-risk pregnancies, is vital for ultimate safety and success. This approach is particularly important if non-invasive ventilation (NIV) or mechanical ventilation after intratracheal intubation becomes necessary.

Management of the Pregnant Asthmatic

The best treatment for pregnant asthmatics is excellent asthma control, including asthma education, compliance with asthma action plan, smoking cessation [11, 12], and most important, preventing exacerbations. At-risk patients should be identified early and close follow-up instituted. In fact, Maselli et al. [13] suggest that all asthmatics who become pregnant should be considered as high-risk, and followed and managed as such.

Acute Exacerbations and Indications for Admission to the ICU

Emergency department (ED) evaluation of dyspnea in an asthmatic patient must include acute exacerbation of asthma and whether a critical asthma syndrome is present, e.g., status asthmaticus (SA) or near-fatal asthma. Other causes of acute dyspnea must be excluded including pulmonary embolism, cardiogenic pulmonary edema, acute lung injury (ALI)/acute respiratory distress syndrome (ARDS), pneumonia, and pneumothorax amongst other possibilities.

CAS, once diagnosed, can be defined as an acute and severe asthma exacerbation that does not respond promptly to intensive bronchodilator therapy. It can progress to NFA, where respiratory failure has ensued [14]. Timely diagnosis and management is therefore of paramount importance because both mother and fetus are at risk for morbidity and mortality from hypoxemia. A multidisciplinary team approach as previously described should be adopted.

Overall, Cydulka et al. [15] found that 12.6 % of pregnant asthmatic women presented to the ED, and hospitalization occurred in 1.6 %. ICU admission should be considered for patients whose asthma continues to worsen despite maximal bronchodilator therapy. This includes patients whose FEV1 is <25 % predicted, or if it improves less than 10 % after treatment [13].

Physiological Changes of Pregnancy

These include an increase in the transverse diameter of the chest, and the subcostal angle widens from 68° to 103°. The diaphragm also ultimately rises by 4 cm due to an enlarging uterus. These changes result in a decrease of residual volume (RV) by 20 % but only a 5 % decrease in total lung capacity (TLC). Chest wall compliance and hence total respiratory compliance decreases by about 30 %, but lung compliance per se remains unchanged [1618].

Ventilatory Management

Non-invasive ventilation may be an alternative under the right clinical circumstance, and may support ventilation whilst corticosteroids and maximal bronchodilator therapy take effect [9, 19]. The use of NIV is however controversial, and the case report that Dalar et al. [19] described involved a 28-year-old female in her 16th week of pregnancy with preceding influenza, the development of lobar pneumonia, and reported worsening of asthma with hypoxemic respiratory failure (PaO2/FiO2 ratio 250, APACHE II score 20). NIV administration was found to be successful in this patient. Caution regarding gastric distension whilst on NIV needs to be emphasized, especially if subsequent intubation takes place [9].

Progressive or unremitting hypoxemia, respiratory acidosis, maternal fatigue, alteration in mental status, and other causes for increased work of breathing despite maximal bronchodilator therapies and NIV are indications for intubation and mechanical ventilation (MV) [13]. Amelioration or indeed prevention of continued hypoxia to the mother and especially the fetus remains of paramount priority and importance [14].

Intubation, if indicated, in the pregnant asthmatic may be up to eight times more difficult when compared to non-pregnant women secondary to soft tissue edema [20]. In a recent study in the UK, the failure rate incidence for tracheal intubation in obstetric cases was 1 in 224 (95 % CI 179–281) with univariate analysis showing index cases to be both older and heavier with a higher body-mass index, and a Mallampati score >1. The laryngeal mask airway was the most commonly used airway in 39 of 57 cases, and gastric aspiration occurred in 4 % or 8 % index cases [20]. Reduced functional residual capacity (FRC) and increased oxygen consumption with diminished oxygen reserve can cause alarmingly rapid desaturation when the pregnant patient is apneic. Therefore, skilled intensivists or anesthesiologists should ideally perform the intubation procedure in these challenging cases. Adequate preoxygenation avoiding severe respiratory alkalosis and aerophagia is helpful [13]. Rapid-sequence protocols should be utilized [14, 21]. This may include use of non-depolarizing neuromuscular blocking agents such as rocuronium, and sedatives such as etomidate or ketamine [14]. Intratracheal intubation via the oral route should be favored over the nasal route because of hyperemia from capillary engorgement of the upper respiratory tract resulting in a narrower airway. A smaller-sized endotracheal tube may be necessary [22, 23].

Mechanical ventilation can be initiated with a target tidal volume (TV) of 6–10 ml/kg once the pregnant asthmatic patient is intubated. However, a TV of 12 ml/kg in intubated asthmatics did not show any increased complication rates [24]. Ideally an alveolar plateau pressure of 30 cm H2O is not exceeded with any increase in TV [17]. The priority is to maintain adequate maternal oxygenation with a PaO2 of approximately 65 mm Hg [25]. Permissive hypercapnia together with a reduction in dynamic hyperinflation have likely contributed to the improvement in mortality for status asthmaticus patients [9, 26] although the concept of permissive hypercapnea in a pregnant patient with status asthmaticus is controversial, with minimal data available regarding its use in the intubated pregnant asthmatic. Indeed a high pCO2 can have deleterious effects on uterine blood flow [27]. In addition, permissive hypercapnea may shift the fetal oxyhemoglobin dissociation curve to the right with impaired oxygenation of fetal hemoglobin and contribute to fetal respiratory acidosis [6, 9, 17]. However, Elsayegh et al. [9] showed that three of four pregnant patients intubated for status asthmaticus with hypercapnia and PaCO2’s varying between 57 to 145 mm Hg had excellent pregnancy outcomes despite hypercapnia. The fourth patient elected to have termination of her pregnancy instead.

Dynamic hyperinflation in CAS can be ameliorated with prolonged expiratory times associated with a lower set respiratory rate, higher peak inspiratory flow rate and lower TVs. This may remedy the dyssynchrony between the pregnant patient and the ventilator and ameliorate volutrauma and barotrauma.

Invasive Hemodynamic Monitoring

Hemodynamic monitoring via a pulmonary artery catheter in the pregnant asthmatic is not usually indicated. If utilized however, the incidence of complications may be reduced due to younger age and lack of comorbid illnesses [22, 28]. Table 1 outlines the expected hemodynamic findings in a patient during late pregnancy. In the pregnant state, a decrease in systemic vascular resistance and pulmonary vascular resistance with a concomitant higher heart rate and stroke volume and hence an increased cardiac output are noted. The pulmonary capillary wedge pressure remained unchanged when compared to the non-pregnant state [22, 29]. Body surface area nomograms in pregnancy may not be routinely available, and hence hemodynamic data corrected for body surface area may not be applicable [22, 30].

Table 1 Normal hemodynamic parameters in the third trimester, giving mean (± standard deviation) values and the change relative to values in the non-pregnant state (From Lapinsky et al. [22])

Bronchodilator Therapy

Asthma drugs themselves may also impact the risk of congenital anomalies. Schatz et al. [31] studied 824 pregnant asthmatics exposed to oral corticosteroids, and found that pre-eclampsia rates were increased twofold. No increase in fetal congenital malformations was noted. In addition, no data linking inhaled steroids to adverse effects on the fetus have been noted [17]. Montelukast also did not appear to increase the baseline rate of major fetal malformations in a multicenter prospective comparative study of infant outcomes [32]. A matched cohort study based on the United Kingdom’s General Practice Research database also found that asthma drugs overall did not increase the risk of fetal congenital abnormalities, when taken during the first trimester of pregnancy. The prevalence of a congenital anomaly among pregnant women not exposed to asthma drugs, and those exposed was 27.8 (95 % CI 25.4–30.6/1,000 pregnancies and 31.3 (95 % CI 27.7–35.5/1,000 pregnancies) respectively (RR 1.1, 95 % CI 1.0–1.3) [33]. However, some increased risk of specific abnormalities were found in association with specific asthma drugs, for example cleft lip or palate associated with long-acting beta-agonists. These findings were, however, not statistically significant, as they were based on small numbers (Table 2). Of note, systemic administration of epinephrine, a combined alpha and beta agonist, is not recommended because of potential teratogenic effects and placental or uterine vasoconstriction. Terbutaline, a pure beta-2 agonist, may be given subcutaneously instead as a means of systemic delivery [13, 14].

Table 2 Relative Risks of various anomalies according to maternal use of asthma drug during early pregnancya (From Vasilakis-Scaramozza C. et al. [33])

Bronchodilators remain the cornerstone of treatment in the acutely ill pregnant asthmatic in the ED and ICU. Such patients will likely benefit from continuous aerosolized delivery of beta-agonists by nebulizer (0.5 m–1.0 mg/h); as this can be associated with a more rapid clinical improvement versus intermittent nebulization at 2.5 mg every 2–4 h. Such drug delivery may be augmented with Heliox as the carrier gas at 70:30 or 80:20 helium–oxygen gas mixture. Helium per se lowers gas density and increases its viscosity, helping to convert turbulent airflow to laminar flow with a concomitant decrease in the Reynolds number to a value less than 2,000, above which turbulent airflow is thought to occur [14, 27, 34]. These effects of a helium–oxygen mixture can therefore decrease airway resistance to airflow especially in the more distal airways, decrease peak inspiratory pressures and improve gas exchange. Helium, as an inert gas, is not absorbed across the respiratory tract and is therefore not expected to have toxic effects on the mother or fetus. George et al. [27] described the first case report describing the successful use of a helium-oxygen mixture for mechanical ventilation in a 15-year-old girl with a second trimester intrauterine pregnancy with status asthmaticus and ARDS. The patient was discharged home 5 days after extubation, and subsequently delivered a full-term healthy male infant.

The effectiveness of concomitant inhaled ipratropium (category B) with nebulized albuterol in status asthmaticus in adults remains unclear. However, Louie et al. suggest that it may benefit critically ill asthmatics with chronic obstructive pulmonary disease (COPD) physiology and a forced expiratory volume in 1 s (FEV1) of <50 % by increasing FEV1 to an increased degree when compared to albuterol alone, and also by decreasing the hospitalization rate [14, 35].

Systemic corticosteroids, administered orally or intravenously, can reduce mortality. For example intravenous (iv) methylprednisolone 60 mg every 6 h reduces the incidence of fatal asthma [14]. Intravenous montelukast, a leukotriene receptor antagonist, may allow patients with acute asthma to receive less beta agonists and demonstrate fewer treatment failures when compared to placebo without unexpected adverse events. The intravenous preparation of montelukast is however currently not available in the USA [14, 36].

Methylxanthines, either theophylline or aminophylline (both category C), are drugs with narrow therapeutic windows, and lack proven additional efficacy. They are therefore not routinely employed in the critically ill pregnant asthmatic [14].

Magnesium sulfate (category A) likely bronchodilates by inhibiting bronchial smooth muscle calcium channels and by blocking parasympathetic tone in the tracheobronchial tree [14]. Intravenous magnesium sulfate, also commonly used to treat preeclampsia, reduced hospitalizations in severe asthmatics when compared to placebo in the emergency department [37]. Newborns may show signs of magnesium toxicity, however, in terms of respiratory and/or neuromuscular depression.

Inhaled general anesthetics such as isoflurane (category C) and sevoflurane (category B) can provide further bronchodilation in asthmatic patients with progressive CAS despite maximal bronchodilator therapy. Therefore these agents are used under extreme circumstances only, with the more popular choice of propofol as an intravenous sedative but also with bronchodilator properties.

Ketamine (category B) is a dissociative anesthetic that causes bronchorrhea and bronchodilatation, and hence may be useful especially in NFA. However, its side effects of hallucinations may require concurrent benzodiazepine administration (category D/X), and other side effects of tachycardia and hypertension require close observation and management as clinically indicated [14].

Other ICU Medications

Asthma drugs notwithstanding, the critically ill pregnant asthmatic often requires sedation and sometimes paralysis. The safety of continuous sedation in pregnant patients is unclear. Nevertheless, propofol, a sedative-hypnotic, is category B and was used by Elsayegh et al. in their intubated pregnant asthmatic patients as their main form of sedation [9]. The authors noted that hypotension, a common side effect of propofol would risk decreasing uteroplacental blood flow, and that higher doses might lead to a reduction in uterine muscle tone [38]. However, no teratogenic effects were seen [39]. The potential bronchodilating effects of propofol confer an added advantage to its use in the pregnant asthmatic patient [14].

Benzodiazepines as sedatives in the ICU cross the placenta and are category D (there is positive evidence of human fetal risk based on adverse reaction data from investigational or marketing experience or studies in humans, but potential benefits may warrant use of the drug in pregnant women despite potential risks). They are associated with an increased risk of preterm birth and low birth weight and may have a tentative association with pylorostenosis and alimentary tract atresia [40] late trimester use of benzodiazepines may be associated with the neonatal withdrawal syndrome (i.e., floppy infant syndrome) [9, 41]. Therefore, benzodiazepine use in a pregnant asthmatic patient is best avoided if possible.

The use of opioids as analgesics in the ICU is often unavoidable, despite its category C/D classification. They cross the placenta, and may affect the neonate neurologically [9, 42]. Caution regarding the daily necessity of opioids use is advised.

Neuromuscular paralysis is sometimes indicated in the intubated pregnant asthmatic because of continued agitation despite maximal sedation. Cisatracurium (category B) has been used by some authors [9] with success, over the short term without untoward effect. However, long-term fetal pharmacological paralysis can be associated with arthrogryposis [43]. Such neuromuscular paralysis should be minimized and removed as soon as clinically indicated, as prolonged weakness may result from its use especially in conjunction with corticosteroids over a prolonged time period [4446].

Table 3 shows a list of asthma medications and select drugs used in the ICU as classified for safety in pregnancy by the United States Food and Drug Administration (FDA).

Table 3 US FDA pregnancy category classification of ashtma medications and select drugs used in the ICU (Adapted and updated from Maselli et al. [13])

Other Treatments in the Critically Ill Pregnant Asthmatic

Pumpless extra-corporeal carbon dioxide (CO2) removal may be a useful adjunct in NFA where severe hypercapnea and metabolic acidosis persist despite maximal aggressive therapies being given. Elliot et al. [47] reported on the use of a low-resistance, pumpless, gas exchange membrane that relied on an arteriovenous shunt and a sweep flow of oxygen to effect membrane diffusion of oxygen and carbon dioxide in two patients with life-threatening asthma. Successful weaning from mechanical ventilation and a full recovery were noted in both patients, but the utility of this in a pregnant patient is uncertain. However, King et al. [48] reported on the use of extra-corporeal membrane oxygenation (ECMO) utilizing bypass in a pregnant patient with pneumonia, asthma and respiratory failure. The patient was successfully weaned and extubated a few days later, and subsequently, delivered a healthy baby.

Complications

Elevated intrathoracic pressures and hyperinflation may contribute to barotrauma manifesting as pneumomediastinum, subcutaneous air, pneumothorax, and/or pericardial air. Worsening severity of such complications may lead to tension pneumothorax or even cardiac tamponade. Life-saving decompressive measures including chest tube thoracostomy in the case of the former diagnosis may become necessary [14].

Acute resuscitation of the pregnant asthmatic, including cardiopulmonary resuscitation (CPR) involves attention to body position as the gravid uterus in the supine position can mechanically diminish venous return. Left lateral decubitus positioning of the mother may ameliorate maternal cardiac output and hence blood pressure, and improve placental blood flow. Elevation of the right hip by 15° may help [17, 49]. A body angle of inclination of 27° on an inclined board allows 80 % of the maximal force for chest compression delivery and yet allows significant mechanical relief to venous return [50]. Perimortem Cesarean section at 24–26 weeks of gestation may be necessary if CPR fails. This extreme option may also reverse aorto-caval compromise and allow a satisfactory outcome for both mother and fetus [22, 51].

Tata et al. [52] did show that pregnant women with asthma when compared to pregnant women without asthma had no difference in stillbirths or therapeutic abortions overall. However, the miscarriage risk was higher in the former group (odds ratio (OR), 1.10; 95 % confidence interval (CI), 1.06–1.13). In addition to miscarriage, the risk of depression and cesarean section were moderately increased in pregnant women with severe asthma and previous asthma exacerbation. Blais et al. [53] found that pregnant women with severe or uncontrolled asthma were at higher risk for spontaneous abortions. (OR = 1.41; 95 % CI 1.33–1.49) and a decreased risk of induced abortions (OR = 0.92; 0.88–0.97). Uncontrolled asthma per se increased the spontaneous abortion risk by 26 % (95 % CI 14–41 %) and the risk of induced abortions by 11 % (95 % CI 1–21 %).

Conclusion

Successful outcomes for both mother and fetus in the management of critical asthma in the pregnant patient are very feasible as demonstrated by Elsayegh et al. [9]. Attention has to be paid to early and aggressive bronchodilator therapy in ameliorating both maternal and fetal hypoxemia, rapid sequence techniques if intubation becomes necessary, ventilator adjustments based on mechanical changes in the pregnant mother, consideration of helium-oxygen, maternal positioning, or controversially permissive hypercapnea as just a few factors when compared to the non-pregnant patient. These goals are best achieved using a multidisciplinary team approach. However the emphasis must still be on prevention of severe acute asthma exacerbations and their progression to one of the critical asthma syndromes, either SA or NFA. This includes access to appropriate subspecialist care both in an early and regular manner to assess asthma control and prevent exacerbations.

References

  1. 1.

    Murphy VE, Gibson P, Talbot PI, Clifton VL (2005) Severe asthma exacerbations during pregnancy. Obstet Gynecol 106:1046–1054

    PubMed  Article  Google Scholar 

  2. 2.

    Kwon HL, Triche EW, Belanger K, Bracken MB (2006) The epidemiology of asthma during pregnancy: prevalence, diagnosis, and symptoms. Immunol Allergy Clin N Am 26:29–62

    Article  Google Scholar 

  3. 3.

    Gluck JC, Gluck PA (2006) The effect of pregnancy on the course of asthma. Immunol Allergy Clin N Am 26:63–80

    Article  Google Scholar 

  4. 4.

    Schatz M, Dombrowski MP, Wise R, Thom EA, Landon M, Mabie W, Newman RB, Hauth JC, Lindheimer M, Caritis SN, Leveno KJ, Meis P, Miodovnik M, Wapner RJ, Paul RH, Varner MW, O'Sullivan MJ, Thurnau GR, Conway D, McNellis D (2003) Asthma morbidity during pregnancy can be predicted by severity classification. J Allergy Clin Immunol 112:283–288

    PubMed  Article  Google Scholar 

  5. 5.

    McCallister JW (2013) Asthma in pregnancy: management strategies. Curr Opin Pulm Med 19:13–17

    CAS  PubMed  Article  Google Scholar 

  6. 6.

    Hanania NA, Belfort MA (2005) Acute asthma in pregnancy. Crit Care Med 33:S319–S324

    PubMed  Article  Google Scholar 

  7. 7.

    Dombrowski MP (2006) Asthma and pregnancy. Obstet Gynecol 108:667–681

    PubMed  Article  Google Scholar 

  8. 8.

    Belanger K, Hellenbrand ME, Holford TR, Bracken M (2010) Effect of pregnancy on maternal asthma symptoms and medication use. Obstet Gynecol 115:559–567

    PubMed Central  PubMed  Article  Google Scholar 

  9. 9.

    Elsayegh D, Shapiro JM (2008) Management of the obstetric patient with status asthmaticus. J Intensive Care Med 23:396–402

    PubMed  Article  Google Scholar 

  10. 10.

    Mabie WC, Barton JR, Wasserstrum N, Baha MS (1992) Clinical Observations on Asthma in Pregnancy. J Maternal Fetal Med 1:45–50

    Article  Google Scholar 

  11. 11.

    Salihu HM, Wilson RE (2007) Epidemiology of prenatal smoking and perinatal outcomes. Early Hum Dev 83:713–720

    CAS  PubMed  Article  Google Scholar 

  12. 12.

    McCoy K, Shade DM, Irvin CG, Mastronarde JG, Hanania NA, Castro M, Anthonisen NR (2006) Predicting episodes of poor asthma control in treated patients with asthma. J Allergy Clin Immunol 118:1226–1233

    PubMed  Article  Google Scholar 

  13. 13.

    Maselli DJ, Adams SG, Peters JI, Levine SM (2012) Management of asthma during pregnancy. Ther Adv Respir Dis 7:87–100

    PubMed  Article  Google Scholar 

  14. 14.

    Louie S, Morrissey BM, Kenyon NJ, Albertson TE, Avdalovic M (2012) The critically ill asthmatic–from ICU to discharge. Clin Rev Allergy Immunol 43:30–44

    CAS  PubMed  Article  Google Scholar 

  15. 15.

    Cydulka RK, Emerman CL, Schreiber D, Molander KH, Woodruff PG, Camargo CA Jr (1999) Acute asthma among pregnant women presenting to the emergency department. Am J Respir Crit Care Med 160:887–892

    CAS  PubMed  Article  Google Scholar 

  16. 16.

    Marx GF, Murthy PK, Orkin LR (1970) Static compliance before and after vaginal delivery. Br J Anaesth 42:1100–1104

    CAS  PubMed  Article  Google Scholar 

  17. 17.

    Campbell LA, Klocke RA (2001) Implications for the pregnant patient. Am J Respir Crit Care Med 163:1051–1054

    CAS  PubMed  Article  Google Scholar 

  18. 18.

    Cruickshank DP, Wigton TR, Hays PM (1996) Maternal physiology in pregnancy. In: Gabbe SG, Neibyl JR, Simpson JL (eds) Obstetrics: Normal and Problem Pregnancies, ed. Churchchill Livingstone, New York, NY, pp 91–109

    Google Scholar 

  19. 19.

    Dalar L, Caner H, Eryuksel E, Kosar F (2013) Application of non-invasive mechanical ventilation in an asthmatic pregnant woman in respiratory failure: a case report. J Thorac Dis 5:97–100

    PubMed Central  PubMed  Google Scholar 

  20. 20.

    Quinn AC, Milne D, Columb M, Gorton H, Knight M (2013) Failed tracheal intubation in obstetric anaesthesia: 2 yr national case–control study in the UK. Br J Anaesth 110:74–80

    CAS  PubMed  Article  Google Scholar 

  21. 21.

    Hodder R, Lougheed MD, FitzGerald JM, Rowe BH, Kaplan AG, McIvor RA (2010) Management of acute asthma in adults in the emergency department: assisted ventilation. CMAJ 182:265–272

    PubMed Central  PubMed  Article  Google Scholar 

  22. 22.

    Lapinsky SE, Kruczynski K, Slutsky AS (1995) Critical care in the pregnant patient. Am J Respir Crit Care Med 152:427–455

    CAS  PubMed  Article  Google Scholar 

  23. 23.

    Cheek TG, Gutsche BB (1993) Maternal Physiology Changes During Pregnancy. In: Schnider SM, Levinson G (eds) Anesthesia for Obstetrics, 3rd edn. Willians & Wilkins, Baltimore, pp 3–13

    Google Scholar 

  24. 24.

    Peters JI, Stupka JE, Singh H, Rossrucker J, Angel LF, Melo J, Levine SM (2012) Status asthmaticus in the medical intensive care unit: a 30-year experience. Respir Med 106:344–348

    PubMed  Article  Google Scholar 

  25. 25.

    Siddiqui AK, Gouda H, Multz AS, Steinberg H, Kamholz SL (2005) Ventilator strategy for status asthmaticus in pregnancy: a case-based review. J Asthma 42:159–162

    PubMed  Google Scholar 

  26. 26.

    Shapiro JM, McLeroth P (2002) Status asthmaticus: a large MICU experience. Clin Intensive Care 13:89–93

    Article  Google Scholar 

  27. 27.

    George R, Berkenbosch JW, Fraser RF, Tobias JD (2001) Mechanical Ventilation During Pregnancy Using a Helium-Oxygen Mixture in a Patient With Respiratory Failure due to Status Asthmaticus. J Perinatol 21:395–398

    CAS  PubMed  Article  Google Scholar 

  28. 28.

    Wallenburg HC (1991) Invasive hemodynamic monitoring in pregnancy. Eur J Obstet Gynecol Reprod Biol 42(Suppl):S45–S51

    PubMed  Google Scholar 

  29. 29.

    Clark SL, Cotton DB, Lee W, Bishop C, Hill T, Southwick J, Pivarnik J, Spillman T, DeVore GR, Phelan J et al (1989) Central hemodynamic assessment of normal term pregnancy. Am J Obstet Gynecol 161:1439–1442

    CAS  PubMed  Article  Google Scholar 

  30. 30.

    American College of Obstetricians and Gynecologists (1993) Invasive hemodynamic monitoring in obstetrics and gynecology: ACOG technical bulletin number 175. Int J Gynecol Obstet 42:199–205

    Article  Google Scholar 

  31. 31.

    Schatz M, Zeiger RS, Harden K, Hoffman CC, Chilingar L, Petitti D (1997) The safety of asthma and allergy medications during pregnancy. J Allergy Clin Immunol 100:301–306

    CAS  PubMed  Article  Google Scholar 

  32. 32.

    Sarkar M, Koren G, Kalra S, Ying A, Smorlesi C, De Santis M, Diav-Citrin O, Avgil M, Lavigne SV, Berkovich M, Einarson A (2009) Montelukast use during pregnancy: a multicentre, prospective, comparative study of infant outcomes. Eur J Clin Pharmacol 65:1259–1264

    CAS  PubMed  Article  Google Scholar 

  33. 33.

    Vasilakis-Scaramozza C, Aschengrau A, Cabral HJ, Jick SS (2013) Asthma drugs and the risk of congenital anomalies. Pharmacotherapy 33:363–368

    CAS  PubMed  Article  Google Scholar 

  34. 34.

    Kress JP, Noth I, Gehlbach BK, Barman N, Pohlman AS, Miller A, Morgan S, Hall JB (2002) The utility of albuterol nebulized with heliox during acute asthma exacerbations. Am J Respir Crit Care Med 165:1317–1321

    PubMed  Article  Google Scholar 

  35. 35.

    Rodrigo GJ, Rodrigo C, Pollack CV, Rowe B (2003) Use of helium-oxygen mixtures in the treatment of acute asthma: a systematic review. Chest 123:891–896

    PubMed  Article  Google Scholar 

  36. 36.

    Camargo CA Jr, Gurner DM, Smithline HA, Chapela R, Fabbri LM, Green SA, Malice MP, Legrand C, Dass SB, Knorr BA, Reiss TF (2010) A randomized placebo-controlled study of intravenous montelukast for the treatment of acute asthma. J Allergy Clin Immunol 125:374–380

    CAS  PubMed  Article  Google Scholar 

  37. 37.

    Rowe BH, Bretzlaff JA, Bourdon C, Bota GW, Camargo CA Jr (2000) Intravenous magnesium sulfate treatment for acute asthma in the emergency department: a systematic review of the literature. Ann Emerg Med 36:181–190

    CAS  PubMed  Article  Google Scholar 

  38. 38.

    Cox PB, Marcus MA, Bos H (2001) Pharmacological considerations during pregnancy. Curr Opin Anaesthesiol 14:311–316

    CAS  PubMed  Article  Google Scholar 

  39. 39.

    Hudspith M (2002) Anesthesia in pregnancy. In: Collis R, Plaat F, Urquhart J (eds) Textbook of Obstetric Anaesthesia, ed. Greenwich Medical Media Ltd, London, pp 291–314

    Google Scholar 

  40. 40.

    Wikner BN, Stiller CO, Bergman U, Asker C, Kallen B (2007) Use of benzodiazepines and benzodiazepine receptor agonists during pregnancy: neonatal outcome and congenital malformations. Pharmacoepidemiol Drug Saf 16:1203–1210

    PubMed  Article  Google Scholar 

  41. 41.

    McElhatton PR (1994) The effects of benzodiazepine use during pregnancy and lactation. Reprod Toxicol 8:461–475

    CAS  PubMed  Article  Google Scholar 

  42. 42.

    Cohen IL, Gallagher TJ, Pohlman AS, Dasta JF, Abraham E, and Papadokos PJ (2002) The management of the agitated ICU patient. Crit Care Med. 30, S97-123; quiz S124-125.

  43. 43.

    Guay J, Grenier Y, Varin F (1998) Clinical pharmacokinetics of neuromuscular relaxants in pregnancy. Clin Pharmacokinet 34:483

    CAS  PubMed  Article  Google Scholar 

  44. 44.

    Griffin D, Fairman N, Coursin D, Rawsthorne L, Grossman JE (1992) Acute myopathy during treatment of status asthmaticus with corticosteroids and steroidal muscle relaxants. Chest 102:510–514

    CAS  PubMed  Article  Google Scholar 

  45. 45.

    Road J, Mackie G, Jiang TX, Stewart H, Eisen A (1997) Reversible paralysis with status asthmaticus, steroids, and pancuronium: clinical electrophysiological correlates. Muscle Nerve 20:1587–1590

    CAS  PubMed  Article  Google Scholar 

  46. 46.

    Shee CD (1990) Risk factors for hydrocortisone myopathy in acute severe asthma. Respir Med 84:229–233

    CAS  PubMed  Article  Google Scholar 

  47. 47.

    Elliot SC, Paramasivam K, Oram J, Bodenham AR, Howell SJ, Mallick A (2007) Pumpless extracorporeal carbon dioxide removal for life-threatening asthma. Crit Care Med 35:945–948

    PubMed  Article  Google Scholar 

  48. 48.

    King PT, Rosalion A, McMillan J, Buist M, Holmes PW (2000) Extracorporeal membrane oxygenation in pregnancy. Lancet 356:45–46

    CAS  PubMed  Article  Google Scholar 

  49. 49.

    (1997), American Heart Association. Special resuscitation situations. In: Advanced cardiac life support ed. Cummins R, ed. American Heart Association, Dallas, TX, p. 11-11-11-19.

  50. 50.

    Rees GA, Willis BA (1988) Resuscitation in late pregnancy. Anaesthesia 43:347–349

    CAS  PubMed  Article  Google Scholar 

  51. 51.

    Oates S, Williams GL, Rees GA (1988) Cardiopulmonary resuscitation in late pregnancy. BMJ 297:404–405

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  52. 52.

    Tata LJ, Lewis SA, McKeever TM, Smith CJ, Doyle P, Smeeth L, West J, Hubbard RB (2007) A comprehensive analysis of adverse obstetric and pediatric complications in women with asthma. Am J Respir Crit Care Med 175:991–997

    PubMed  Article  Google Scholar 

  53. 53.

    Blais L, Kettani FZ, Forget A (2013) Relationship between maternal asthma, its severity and control and abortion. Hum Reprod 28:908–915

    PubMed  Article  Google Scholar 

  54. 54.

    Gluck PA, Gluck JC (2005) A review of pregnancy outcomes after exposure to orally inhaled or intranasal budesonide. Curr Med Res Opin 21:1075–1084

    CAS  PubMed  Article  Google Scholar 

  55. 55.

    Bakhireva LN, Schatz M, Chambers CD (2007) Effect of maternal asthma and gestational asthma therapy on fetal growth. J Asthma 44:71–76

    CAS  PubMed  Article  Google Scholar 

  56. 56.

    Daily Med. U.S. National Library of Medicine, National Institutes of Health, Health & Human Services http://dailymed.nlm.nih.gov/. [June 13, 2013].

  57. 57.

    Agarwal HS, Nanavati RN, Bhagwat MS, Kabra NS, Udani RH (1998) Transplancental aminophylline toxicity. Indian Pediatr 35:467–470

    CAS  PubMed  Google Scholar 

  58. 58.

    Broussard CS, Rasmussen SA, Reefhuis J, Friedman JM, Jann MW, Riehle-Colarusso T, Honein MA (2011) Maternal treatment with opioid analgesics and risk for birth defects. Am J Obstet Gynecol 204(314):e311–311

    Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Andrew L. Chan.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Chan, A.L., Juarez, M.M., Gidwani, N. et al. Management of Critical Asthma Syndrome During Pregnancy. Clinic Rev Allerg Immunol 48, 45–53 (2015). https://doi.org/10.1007/s12016-013-8397-4

Download citation

Keywords

  • Asthma
  • Pregnancy
  • Intensive care
  • Status asthmaticus
  • Near-fatal asthma