Semin Respir Crit Care Med 2017; 38(02): 174-184
DOI: 10.1055/s-0037-1602375
Review Article
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Pulmonary Infections in Pregnancy

Jyoti S. Mathad
1   Department of Medicine, Weill Cornell Medicine, Center for Global Health, New York, New York
,
Amita Gupta
2   Department of Medicine and International Health, Johns Hopkins University, Center for Clinical Global Health Education, Baltimore, Maryland
› Author Affiliations
Further Information

Publication History

Publication Date:
22 May 2017 (online)

Abstract

Pregnant women experience physiological and immunological changes that increase the risk or severity of certain pulmonary infections. These changes also affect drug disposition, which impacts treatment choices. In this article, we review the available data on (1) the physiological and immunological changes that specifically impact tuberculosis, influenza, and varicella pneumonia; (2) active and latent tuberculosis management, including drug monitoring and maternal–infant outcomes; (3) the treatment and prevention of influenza; and (4) the diagnosis and management of varicella pneumonia. Clinical trials often exclude pregnant women, but there is a consensus that treating pregnant women for tuberculosis, influenza, and varicella pneumonia improves outcomes for both the woman and her child.

 
  • References

  • 1 Robinson DP, Klein SL. Pregnancy and pregnancy-associated hormones alter immune responses and disease pathogenesis. Horm Behav 2012; 62 (03) 263-271
  • 2 Kourtis AP, Read JS, Jamieson DJ. Pregnancy and infection. N Engl J Med 2014; 370 (23) 2211-2218
  • 3 Wegmann TG, Lin H, Guilbert L, Mosmann TR. Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon?. Immunol Today 1993; 14 (07) 353-356
  • 4 Szekeres-Bartho J, Faust Z, Varga P, Szereday L, Kelemen K. The immunological pregnancy protective effect of progesterone is manifested via controlling cytokine production. Am J Reprod Immunol 1996; 35 (04) 348-351
  • 5 Hill JA, Polgar K, Anderson DJ. T-helper 1-type immunity to trophoblast in women with recurrent spontaneous abortion. JAMA 1995; 273 (24) 1933-1936
  • 6 Marzi M, Vigano A, Trabattoni D. , et al. Characterization of type 1 and type 2 cytokine production profile in physiologic and pathologic human pregnancy. Clin Exp Immunol 1996; 106 (01) 127-133
  • 7 Soldan SS, Alvarez Retuerto AI, Sicotte NL, Voskuhl RR. Immune modulation in multiple sclerosis patients treated with the pregnancy hormone estriol. J Immunol 2003; 171 (11) 6267-6274
  • 8 Tulchinsky D, Hobel CJ, Yeager E, Marshall JR. Plasma estrone, estradiol, estriol, progesterone, and 17-hydroxyprogesterone in human pregnancy. I. Normal pregnancy. Am J Obstet Gynecol 1972; 112 (08) 1095-1100
  • 9 Sicotte NL, Liva SM, Klutch R. , et al. Treatment of multiple sclerosis with the pregnancy hormone estriol. Ann Neurol 2002; 52 (04) 421-428
  • 10 Szekeres-Bartho J, Polgar B. PIBF: the double edged sword. Pregnancy and tumor. Am J Reprod Immunol 2010; 64 (02) 77-86
  • 11 Polanczyk MJ, Carson BD, Subramanian S. , et al. Cutting edge: estrogen drives expansion of the CD4+CD25+ regulatory T cell compartment. J Immunol 2004; 173 (04) 2227-2230
  • 12 Murphy K, Travers P, Walport M, Janeway C. Janeway's Immunobiology, 8th ed. New York, NY: Garland Science; 2012
  • 13 Singh N, Perfect JR. Immune reconstitution syndrome and exacerbation of infections after pregnancy. Clin Infect Dis 2007; 45 (09) 1192-1199
  • 14 Hegewald MJ, Crapo RO. Respiratory physiology in pregnancy. Clin Chest Med 2011; 32 (01) 1-13 , vii vii.
  • 15 Soma-Pillay P, Nelson-Piercy C, Tolppanen H, Mebazaa A. Physiological changes in pregnancy. Cardiovasc J Afr 2016; 27 (02) 89-94
  • 16 Van Thiel DH, Gavaler JS, Joshi SN, Sara RK, Stremple J. Heartburn of pregnancy. Gastroenterology 1977; 72 (4 Pt 1): 666-668
  • 17 Anderson GD. Pregnancy-induced changes in pharmacokinetics: a mechanistic-based approach. Clin Pharmacokinet 2005; 44 (10) 989-1008
  • 18 Wadelius M, Darj E, Frenne G, Rane A. Induction of CYP2D6 in pregnancy. Clin Pharmacol Ther 1997; 62 (04) 400-407
  • 19 Panel on Antiretroviral Guidelines for Adults and Adolescents. Guidelines for the use of antiretroviral agents in HIV-1-infected adults and adolescents. Department of Health and Human Services. Available at http://www.aidsinfo.nih.gov/ContentFiles/AdultandAdolescentgl.pdf . Accessed March 17, 2017
  • 20 Sheffield JS, Siegel D, Mirochnick M. , et al. Designing drug trials: considerations for pregnant women. Clin Infect Dis 2014; 59 (Suppl. 07) S437-S444
  • 21 World Health Organization. Global Tuberculosis Report 2016. Geneva, Switzerland: World Health Organization; 2016
  • 22 Sugarman J, Colvin C, Moran AC, Oxlade O. Tuberculosis in pregnancy: an estimate of the global burden of disease. Lancet Glob Health 2014; 2 (12) e710-e716
  • 23 El-Messidi A, Czuzoj-Shulman N, Spence AR, Abenhaim HA. Medical and obstetric outcomes among pregnant women with tuberculosis: a population-based study of 7.8 million births. Am J Obstet Gynecol 2016; 215 (06) 797.e1-797.e6
  • 24 Zenner D, Kruijshaar ME, Andrews N, Abubakar I. Risk of tuberculosis in pregnancy: a national, primary care-based cohort and self-controlled case series study. Am J Respir Crit Care Med 2012; 185 (07) 779-784
  • 25 Bennett DE, Courval JM, Onorato I. , et al. Prevalence of tuberculosis infection in the United States population: the national health and nutrition examination survey, 1999-2000. Am J Respir Crit Care Med 2008; 177 (03) 348-355
  • 26 Blum RN, Polish LB, Tapy JM, Catlin BJ, Cohn DL. Results of screening for tuberculosis in foreign-born persons applying for adjustment of immigration status. Chest 1993; 103 (06) 1670-1674
  • 27 Mathad JS, Gupta A. Tuberculosis in pregnant and postpartum women: epidemiology, management, and research gaps. Clin Infect Dis 2012; 55 (11) 1532-1549
  • 28 Snider D. Pregnancy and tuberculosis. Chest 1984; 86 (3, Suppl): 10S-13S
  • 29 Khilnani GC. Tuberculosis and pregnancy. Indian J Chest Dis Allied Sci 2004; 46 (02) 105-111
  • 30 Meixner FM. Pregnancy in tuberculosis. Dis Chest 1945; 11: 409-418
  • 31 Stewart DA. Pregnancy and tuberculosis : part I-the effects of pregnancy on tuberculosis. Can Med Assoc J 1922; 12 (01) 1-3
  • 32 Daniel TM. The history of tuberculosis. Respir Med 2006; 100 (11) 1862-1870
  • 33 Bennett JE, Dolin R, Blaser MJ. Mandell, Douglas and Bennett's Principles and Practices of Infectious Diseases. 8th ed. Philadelphia, PA: Elsevier Saunders; 2015
  • 34 Mathad JS, Bhosale R, Balasubramanian U. , et al. Quantitative IFN-γ and IL-2 Response Associated with Latent Tuberculosis Test Discordance in HIV-infected Pregnant Women. Am J Respir Crit Care Med 2016; 193 (12) 1421-1428
  • 35 World Health Organization. Guidelines for Intensified Tuberculosis Case Finding and Isoniazid Preventive Therapy for People Living with HIV in Resource Constrained Settings. Geneva, Switzerland: World Health Organization; 2011
  • 36 Gupta A, Chandrasekhar A, Gupte N. , et al; Byramjee Jeejeebhoy Medical College–Johns Hopkins University Study Group. Symptom screening among HIV-infected pregnant women is acceptable and has high negative predictive value for active tuberculosis. Clin Infect Dis 2011; 53 (10) 1015-1018
  • 37 Hoffmann CJ, Variava E, Rakgokong M. , et al. High prevalence of pulmonary tuberculosis but low sensitivity of symptom screening among HIV-infected pregnant women in South Africa. PLoS One 2013; 8 (04) e62211
  • 38 LaCourse SM, Cranmer LM, Matemo D. , et al. Tuberculosis case finding in HIV-infected pregnant women in Kenya reveals poor performance of symptom screening and rapid diagnostic tests. J Acquir Immune Defic Syndr 2016; 71 (02) 219-227
  • 39 Gounder CR, Wada NI, Kensler C. , et al. Active tuberculosis case-finding among pregnant women presenting to antenatal clinics in Soweto, South Africa. J Acquir Immune Defic Syndr 2011; 57 (04) e77-e84
  • 40 Sheriff FG, Manji KP, Manji MP, Chagani MM. Pulmonary tuberculosis among pregnant mothers in Tanzania. Dar Es Salaam Medical Student J 2010; 16 (01) 5-9
  • 41 Mtei L, Matee M, Herfort O. , et al. High rates of clinical and subclinical tuberculosis among HIV-infected ambulatory subjects in Tanzania. Clin Infect Dis 2005; 40 (10) 1500-1507
  • 42 Bloch AB. Screening for tuberculosis and tuberculosis infection in high-risk populations. Recommendations of the Advisory Council for the Elimination of Tuberculosis. MMWR Recomm Rep 1995; 44 (RR-11): 19-34
  • 43 Geiter LJ, Gordin FM, Hershfield E. , et al; American Thoracic Society. Targeted tuberculin testing and treatment of latent tuberculosis infection. MMWR Recomm Rep 2000; 49 (RR-6): 1-51
  • 44 World Health Organization. Strategic and Technical Advisory Group (STAG-TB). Geneva, Switzerland: World Health Organization; 2010
  • 45 Mathad JS, Bhosale R, Sangar V. , et al. Pregnancy differentially impacts performance of latent tuberculosis diagnostics in a high-burden setting. PLoS One 2014; 9 (03) e92308
  • 46 LaCourse SM, Cranmer LM, Matemo D. , et al. Effect of pregnancy on interferon gamma release-assay and tuberculin skin test detection of latent TB infection among HIV-infected women in a high burden setting. J Acquir Immune Defic Syndr 2017
  • 47 Gupta A, Mathad JS, Abdel-Rahman SM. , et al. Toward earlier inclusion of pregnant and postpartum women in tuberculosis drug trials: consensus statements from an international expert panel. Clin Infect Dis 2016; 62 (06) 761-769
  • 48 Kaplan JE, Benson C, Holmes KK, Brooks JT, Pau A, Masur H. ; Centers for Disease Control and Prevention (CDC); National Institutes of Health; HIV Medicine Association of the Infectious Diseases Society of America. Guidelines for prevention and treatment of opportunistic infections in HIV-infected adults and adolescents: recommendations from CDC, the National Institutes of Health, and the HIV Medicine Association of the Infectious Diseases Society of America. MMWR Recomm Rep 2009; 58 (RR-4): 1-207 , quiz CE1–CE4
  • 49 Palacios E, Dallman R, Muñoz M. , et al. Drug-resistant tuberculosis and pregnancy: treatment outcomes of 38 cases in Lima, Peru. Clin Infect Dis 2009; 48 (10) 1413-1419
  • 50 Centers for Disease Control and Prevention. Latent tuberculosis infection: a guide for primary health care providers. Atlanta, GA: Centers for Disease Control and Prevention, National Center for HIV/AIDS, Viral Hepatitis, STD, and TB Prevention, Division of Tuberculosis Elimination; 2013
  • 51 Saukkonen JJ, Cohn DL, Jasmer RM. , et al; ATS (American Thoracic Society) Hepatotoxicity of Antituberculosis Therapy Subcommittee. An official ATS statement: hepatotoxicity of antituberculosis therapy. Am J Respir Crit Care Med 2006; 174 (08) 935-952
  • 52 Ouyang DW, Shapiro DE, Lu M. , et al. Increased risk of hepatotoxicity in HIV-infected pregnant women receiving antiretroviral therapy independent of nevirapine exposure. AIDS 2009; 23 (18) 2425-2430
  • 53 Lyons F, Hopkins S, Kelleher B. , et al. Maternal hepatotoxicity with nevirapine as part of combination antiretroviral therapy in pregnancy. HIV Med 2006; 7 (04) 255-260
  • 54 Huntington S, Thorne C, Anderson J. , et al. Does pregnancy increase the risk of ART-induced hepatotoxicity among HIV-positive women?. J Int AIDS Soc 2014; 17 (04) (Suppl. 03) 19486
  • 55 Jana N, Vasishta K, Jindal SK, Khunnu B, Ghosh K. Perinatal outcome in pregnancies complicated by pulmonary tuberculosis. Int J Gynaecol Obstet 1994; 44 (02) 119-124
  • 56 Jana N, Vasishta K, Saha SC, Ghosh K. Obstetrical outcomes among women with extrapulmonary tuberculosis. N Engl J Med 1999; 341 (09) 645-649
  • 57 Bjerkedal T, Bahna SL, Lehmann EH. Course and outcome of pregnancy in women with pulmonary tuberculosis. Scand J Respir Dis 1975; 56 (05) 245-250
  • 58 Bothamley G. Drug treatment for tuberculosis during pregnancy: safety considerations. Drug Saf 2001; 24 (07) 553-565
  • 59 Pillay T, Khan M, Moodley J. , et al. The increasing burden of tuberculosis in pregnant women, newborns and infants under 6 months of age in Durban, KwaZulu-Natal. S Afr Med J 2001; 91 (11) 983-987
  • 60 Khan M, Pillay T, Moodley JM, Connolly CA. ; Durban Perinatal TB HIV-1 Study Group. Maternal mortality associated with tuberculosis-HIV-1 co-infection in Durban, South Africa. AIDS 2001; 15 (14) 1857-1863
  • 61 Gupta A, Bhosale R, Kinikar A. , et al; Six Week Extended-Dose Nevirapine (SWEN) India Study Team. Maternal tuberculosis: a risk factor for mother-to-child transmission of human immunodeficiency virus. J Infect Dis 2011; 203 (03) 358-363
  • 62 Gomes VF, Andersen A, Wejse C. , et al. Impact of tuberculosis exposure at home on mortality in children under 5 years of age in Guinea-Bissau. Thorax 2011; 66 (02) 163-167
  • 63 Harris JW. Influenza occurring in pregnant women: A statistical study of thirteen hundred and fifty cases. JAMA 1919; 72: 978-980
  • 64 Freeman DW, Barno A. Deaths from Asian influenza associated with pregnancy. Am J Obstet Gynecol 1959; 78: 1172-1175
  • 65 Jamieson DJ, Honein MA, Rasmussen SA. , et al; Novel Influenza A (H1N1) Pregnancy Working Group. H1N1 2009 influenza virus infection during pregnancy in the USA. Lancet 2009; 374 (9688): 451-458
  • 66 Callaghan WM, Creanga AA, Jamieson DJ. Pregnancy-Related Mortality Resulting From Influenza in the United States During the 2009-2010 Pandemic. Obstet Gynecol 2015; 126 (03) 486-490
  • 67 Widelock D, Csizmas L, Klein S. Influenza, pregnancy, and fetal outcome. Public Health Rep 1963; 78: 1-11
  • 68 Eickhoff TC. Immunization against influenza: rationale and recommendations. J Infect Dis 1971; 123 (04) 446-454
  • 69 Siston AM, Rasmussen SA, Honein MA. , et al; Pandemic H1N1 Influenza in Pregnancy Working Group. Pandemic 2009 influenza A(H1N1) virus illness among pregnant women in the United States. JAMA 2010; 303 (15) 1517-1525
  • 70 Mosby LG, Rasmussen SA, Jamieson DJ. 2009 pandemic influenza A (H1N1) in pregnancy: a systematic review of the literature. Am J Obstet Gynecol 2011; 205 (01) 10-18
  • 71 Raj RS, Bonney EA, Phillippe M. Influenza, immune system, and pregnancy. Reprod Sci 2014; 21 (12) 1434-1451
  • 72 Young BC, Stanic AK, Panda B, Rueda BR, Panda A. Longitudinal expression of Toll-like receptors on dendritic cells in uncomplicated pregnancy and postpartum. Am J Obstet Gynecol 2014; 210 (05) 445.e1-445.e6
  • 73 Gordon CL, Johnson PD, Permezel M. , et al. Association between severe pandemic 2009 influenza A (H1N1) virus infection and immunoglobulin G(2) subclass deficiency. Clin Infect Dis 2010; 50 (05) 672-678
  • 74 Zheng R, Qin X, Li Y. , et al. Imbalanced anti-H1N1 immunoglobulin subclasses and dysregulated cytokines in hospitalized pregnant women with 2009 H1N1 influenza and pneumonia in Shenyang, China. Hum Immunol 2012; 73 (09) 906-911
  • 75 Louie JK, Jamieson DJ, Rasmussen SA. 2009 pandemic influenza A (H1N1) virus infection in postpartum women in California. Am J Obstet Gynecol 2011; 204 (02) 144.e1-144.e6
  • 76 Rasmussen SA, Jamieson DJ, Macfarlane K, Cragan JD, Williams J, Henderson Z. ; Pandemic Influenza and Pregnancy Working Group. Pandemic influenza and pregnant women: summary of a meeting of experts. Am J Public Health 2009; 99 (Suppl. 02) S248-S254
  • 77 Greer LG, Sheffield JS, Rogers VL, Roberts SW, McIntire DD, Wendel Jr GD. Maternal and neonatal outcomes after antepartum treatment of influenza with antiviral medications. Obstet Gynecol 2010; 115 (04) 711-716
  • 78 Xie HY, Yasseen III AS, Xie RH. , et al. Infant outcomes among pregnant women who used oseltamivir for treatment of influenza during the H1N1 epidemic. Am J Obstet Gynecol 2013; 208 (04) 293.e1-293.e7
  • 79 Saito S, Minakami H, Nakai A, Unno N, Kubo T, Yoshimura Y. Outcomes of infants exposed to oseltamivir or zanamivir in utero during pandemic (H1N1) 2009. Am J Obstet Gynecol 2013; 209 (02) 130.e1-130.e9
  • 80 Beigi RH, Han K, Venkataramanan R. , et al; Obstetric-Fetal Pharmacology Research Units Network. Pharmacokinetics of oseltamivir among pregnant and nonpregnant women. Am J Obstet Gynecol 2011; 204 (06) (Suppl. 01) S84-S88
  • 81 Clay PG, Adiga RB, Taylor TA, Alsup R, Gerk PM, McRae M. Postpartum pharmacokinetics of peramivir in the treatment of 2009 H1N1 influenza. Obstet Gynecol 2011; 118 (2 Pt 2): 463-467
  • 82 Greer LG, Leff RD, Rogers VL. , et al. Pharmacokinetics of oseltamivir according to trimester of pregnancy. Am J Obstet Gynecol 2011; 204 (06) (Suppl. 01) S89-S93
  • 83 Centers for Disease Control and Prevention. Responding to Influenza: A Toolkit for Prenatal providers. Atlanta, GA: Centers for Disease Control and Prevention; 2011
  • 84 Wallace GD, Elm Jr JL. Transplacental transmission and neonatal infection with swine influenza virus (Hsw1N1) in swine. Am J Vet Res 1979; 40 (08) 1169-1172
  • 85 Yawn DH, Pyeatte JC, Joseph JM, Eichler SL, Garcia-Bunuel R. Transplacental transfer of influenza virus. JAMA 1971; 216 (06) 1022-1023
  • 86 Dulyachai W, Makkoch J, Rianthavorn P. , et al. Perinatal pandemic (H1N1) 2009 infection, Thailand. Emerg Infect Dis 2010; 16 (02) 343-344
  • 87 Luteijn JM, Brown MJ, Dolk H. Influenza and congenital anomalies: a systematic review and meta-analysis. Hum Reprod 2014; 29 (04) 809-823
  • 88 Centers for Disease Control and Prevention (CDC). Maternal and infant outcomes among severely ill pregnant and postpartum women with 2009 pandemic influenza A (H1N1)–United States, April 2009-August 2010. MMWR Morb Mortal Wkly Rep 2011; 60 (35) 1193-1196
  • 89 McNeil SA, Dodds LA, Fell DB. , et al. Effect of respiratory hospitalization during pregnancy on infant outcomes. Am J Obstet Gynecol 2011; 204 (06) (Suppl. 01) S54-S57
  • 90 Mendez-Figueroa H, Raker C, Anderson BL. Neonatal characteristics and outcomes of pregnancies complicated by influenza infection during the 2009 pandemic. Am J Obstet Gynecol 2011; 204 (06) (Suppl. 01) S58-S63
  • 91 Kim DK, Riley LE, Harriman KH, Hunter P, Bridges CB. Advisory Committee on Immunization Practices recommended immunization schedule for adults aged 19 years or older–United States, 2017. MMWR Morb Mortal Wkly Rep 2017; 66 (05) 136-138
  • 92 Zaman K, Roy E, Arifeen SE. , et al. Effectiveness of maternal influenza immunization in mothers and infants. N Engl J Med 2008; 359 (15) 1555-1564
  • 93 Thompson MG, Li DK, Shifflett P. , et al; Pregnancy and Influenza Project Workgroup. Effectiveness of seasonal trivalent influenza vaccine for preventing influenza virus illness among pregnant women: a population-based case-control study during the 2010-2011 and 2011-2012 influenza seasons. Clin Infect Dis 2014; 58 (04) 449-457
  • 94 Steinhoff MC, Omer SB, Roy E. , et al. Influenza immunization in pregnancy--antibody responses in mothers and infants. N Engl J Med 2010; 362 (17) 1644-1646
  • 95 Schlaudecker EP, McNeal MM, Dodd CN, Ranz JB, Steinhoff MC. Pregnancy modifies the antibody response to trivalent influenza immunization. J Infect Dis 2012; 206 (11) 1670-1673
  • 96 Fukushima W, Ohfuji S, Deguchi M. , et al. Effectiveness of an influenza A (H1N1) 2009 monovalent vaccine among Japanese pregnant women: a prospective observational study assessing antibody efficacy. Vaccine 2012; 30 (52) 7630-7636
  • 97 Regan AK, de Klerk N, Moore HC, Omer SB, Shellam G, Effler PV. Effect of maternal influenza vaccination on hospitalization for respiratory infections in newborns: a retrospective cohort study. Pediatr Infect Dis J 2016; 35 (10) 1097-1103
  • 98 Tapia MD, Sow SO, Tamboura B. , et al. Maternal immunisation with trivalent inactivated influenza vaccine for prevention of influenza in infants in Mali: a prospective, active-controlled, observer-blind, randomised phase 4 trial. Lancet Infect Dis 2016; 16 (09) 1026-1035
  • 99 Bridges CB, Harper SA, Fukuda K, Uyeki TM, Cox NJ, Singleton JA. ; Advisory Committee on Immunization Practices. Prevention and control of influenza. Recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep 2003; 52 (RR-8): 1-34 , quiz CE1–CE4
  • 100 Haake DA, Zakowski PC, Haake DL, Bryson YJ. Early treatment with acyclovir for varicella pneumonia in otherwise healthy adults: retrospective controlled study and review. Rev Infect Dis 1990; 12 (05) 788-798
  • 101 Harger JH, Ernest JM, Thurnau GR. , et al; National Institute of Child Health and Human Development, Network of Maternal-Fetal Medicine Units. Risk factors and outcome of varicella-zoster virus pneumonia in pregnant women. J Infect Dis 2002; 185 (04) 422-427
  • 102 Cox SM, Cunningham FG, Luby J. Management of varicella pneumonia complicating pregnancy. Am J Perinatol 1990; 7 (04) 300-301
  • 103 Brito V, Niederman MS. Pneumonia complicating pregnancy. Clin Chest Med 2011; 32 (01) 121-132 , ix
  • 104 Goodnight WH, Soper DE. Pneumonia in pregnancy. Crit Care Med 2005; 33 (10, Suppl): S390-S397