Semin Respir Crit Care Med 2016; 37(02): 257-266
DOI: 10.1055/s-0036-1578802
Thieme Medical Publishers 333 Seventh Avenue, New York, NY 10001, USA.

Fungal, Viral, and Parasitic Pneumonias Associated with Human Immunodeficiency Virus

Joseph H. Skalski
1   Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Mayo Clinic, Rochester, Minnesota
,
Andrew H. Limper
1   Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine, Mayo Clinic, Rochester, Minnesota
› Author Affiliations
Further Information

Publication History

Publication Date:
14 March 2016 (online)

Abstract

Respiratory illness is an important cause of morbidity and mortality in patients with human immunodeficiency virus (HIV). The spectrum of pulmonary disease that can affect patients with HIV is wide and includes opportunistic infection with many fungal, viral, and parasitic organisms. This article reviews the clinical presentation; approach to diagnosis; and management of fungal, viral, and parasitic pneumonias that can develop in patients with HIV including respiratory disease caused by Aspergillus, Cryptococcus, Histoplasma, Coccidioides, Cytomegalovirus, Toxoplasma, and Strongyloides. Because clinical symptoms and radiographic patterns are often insensitive at distinguishing these pulmonary infections, this review particularly focuses on specific host risk factors and diagnostic testing to consider when approaching HIV patients with respiratory illness.

 
  • References

  • 1 Limper AH, Knox KS, Sarosi GA , et al; American Thoracic Society Fungal Working Group. An official American Thoracic Society statement: treatment of fungal infections in adult pulmonary and critical care patients. Am J Respir Crit Care Med 2011; 183 (1) 96-128
  • 2 Mylonakis E, Barlam TF, Flanigan T, Rich JD. Pulmonary aspergillosis and invasive disease in AIDS: review of 342 cases. Chest 1998; 114 (1) 251-262
  • 3 Latgé JP. Aspergillus fumigatus and aspergillosis. Clin Microbiol Rev 1999; 12 (2) 310-350
  • 4 Arnow PM, Sadigh M, Costas C, Weil D, Chudy R. Endemic and epidemic aspergillosis associated with in-hospital replication of Aspergillus organisms. J Infect Dis 1991; 164 (5) 998-1002
  • 5 Codina R, Fox RW, Lockey RF, DeMarco P, Bagg A. Typical levels of airborne fungal spores in houses without obvious moisture problems during a rainy season in Florida, USA. J Investig Allergol Clin Immunol 2008; 18 (3) 156-162
  • 6 Sharpe RA, Bearman N, Thornton CR, Husk K, Osborne NJ. Indoor fungal diversity and asthma: a meta-analysis and systematic review of risk factors. J Allergy Clin Immunol 2015; 135 (1) 110-122
  • 7 Godinho VM, Gonçalves VN, Santiago IF , et al. Diversity and bioprospection of fungal community present in oligotrophic soil of continental Antarctica. Extremophiles 2015; 19 (3) 585-596
  • 8 Nash G, Irvine R, Kerschmann RL, Herndier B. Pulmonary aspergillosis in acquired immune deficiency syndrome: autopsy study of an emerging pulmonary complication of human immunodeficiency virus infection. Hum Pathol 1997; 28 (11) 1268-1275
  • 9 Kemper CA, Hostetler JS, Follansbee SE , et al. Ulcerative and plaque-like tracheobronchitis due to infection with Aspergillus in patients with AIDS. Clin Infect Dis 1993; 17 (3) 344-352
  • 10 Jain M. Allergic bronchopulmonary aspergillosis in an HIV-infected individual. Allergy Asthma Proc 2000; 21 (6) 351-354
  • 11 Addrizzo-Harris DJ, Harkin TJ, McGuinness G, Naidich DP, Rom WN. Pulmonary aspergilloma and AIDS. A comparison of HIV-infected and HIV-negative individuals. Chest 1997; 111 (3) 612-618
  • 12 Wallace JM, Lim R, Browdy BL , et al; Pulmonary Complications of HIV Infection Study Group. Risk factors and outcomes associated with identification of Aspergillus in respiratory specimens from persons with HIV disease. Chest 1998; 114 (1) 131-137
  • 13 Antinori S, Nebuloni M, Magni C , et al. Trends in the postmortem diagnosis of opportunistic invasive fungal infections in patients with AIDS: a retrospective study of 1,630 autopsies performed between 1984 and 2002. Am J Clin Pathol 2009; 132 (2) 221-227
  • 14 Lortholary O, Meyohas MC, Dupont B , et al; French Cooperative Study Group on Aspergillosis in AIDS. Invasive aspergillosis in patients with acquired immunodeficiency syndrome: report of 33 cases. Am J Med 1993; 95 (2) 177-187
  • 15 Mylonakis E, Paliou M, Sax PE, Skolnik PR, Baron MJ, Rich JD. Central nervous system aspergillosis in patients with human immunodeficiency virus infection. Report of 6 cases and review. Medicine (Baltimore) 2000; 79 (4) 269-280
  • 16 Panel on Opportunistic Infections in HIV-Infected Adults and Adolescents. Guidelines for the prevention and treatment of opportunistic infections in HIV-infected adults and adolescents: recommendations from the Centers for Disease Control and Prevention, the National Institutes of Health, and the HIV Medicine Association of the Infectious Diseases Society of America. Available at: http://aidsinfo.nih.gov/contentfiles/lvguidelines/adult_oi.pdf . Accessed August 2015
  • 17 Marukutira T, Huprikar S, Azie N, Quan SP, Meier-Kriesche HU, Horn DL. Clinical characteristics and outcomes in 303 HIV-infected patients with invasive fungal infections: data from the Prospective Antifungal Therapy Alliance registry, a multicenter, observational study. HIV AIDS (Auckl) 2014; 6: 39-47
  • 18 Cox JN, di Dió F, Pizzolato GP, Lerch R, Pochon N. Aspergillus endocarditis and myocarditis in a patient with the acquired immunodeficiency syndrome (AIDS). A review of the literature. Virchows Arch A Pathol Anat Histopathol 1990; 417 (3) 255-259
  • 19 Halpern M, Szabo S, Hochberg E , et al. Renal aspergilloma: an unusual cause of infection in a patient with the acquired immunodeficiency syndrome. Am J Med 1992; 92 (4) 437-440
  • 20 Miller Jr WT, Sais GJ, Frank I, Gefter WB, Aronchick JM, Miller WT. Pulmonary aspergillosis in patients with AIDS. Clinical and radiographic correlations. Chest 1994; 105 (1) 37-44
  • 21 Pursell KJ, Telzak EE, Armstrong D. Aspergillus species colonization and invasive disease in patients with AIDS. Clin Infect Dis 1992; 14 (1) 141-148
  • 22 De Pauw B, Walsh TJ, Donnelly JP , et al; European Organization for Research and Treatment of Cancer/Invasive Fungal Infections Cooperative Group; National Institute of Allergy and Infectious Diseases Mycoses Study Group (EORTC/MSG) Consensus Group. Revised definitions of invasive fungal disease from the European Organization for Research and Treatment of Cancer/Invasive Fungal Infections Cooperative Group and the National Institute of Allergy and Infectious Diseases Mycoses Study Group (EORTC/MSG) Consensus Group. Clin Infect Dis 2008; 46 (12) 1813-1821
  • 23 Pfeiffer CD, Fine JP, Safdar N. Diagnosis of invasive aspergillosis using a galactomannan assay: a meta-analysis. Clin Infect Dis 2006; 42 (10) 1417-1427
  • 24 Narreddy S, Chandrasekar PH. False-positive Aspergillus galactomannan (GM) assay in histoplasmosis. J Infect 2008; 56 (1) 80-81
  • 25 Mikulska M, Furfaro E, Del Bono V , et al. Piperacillin/tazobactam (Tazocin™) seems to be no longer responsible for false-positive results of the galactomannan assay. J Antimicrob Chemother 2012; 67 (7) 1746-1748
  • 26 Orlopp K, von Lilienfeld-Toal M, Marklein G , et al. False positivity of the Aspergillus galactomannan Platelia ELISA because of piperacillin/tazobactam treatment: does it represent a clinical problem?. J Antimicrob Chemother 2008; 62 (5) 1109-1112
  • 27 Schelenz S, Barnes RA, Barton RC , et al; British Society for Medical Mycology. British Society for Medical Mycology best practice recommendations for the diagnosis of serious fungal diseases. Lancet Infect Dis 2015; 15 (4) 461-474
  • 28 Lin SJ, Schranz J, Teutsch SM. Aspergillosis case-fatality rate: systematic review of the literature. Clin Infect Dis 2001; 32 (3) 358-366
  • 29 Park BJ, Wannemuehler KA, Marston BJ, Govender N, Pappas PG, Chiller TM. Estimation of the current global burden of cryptococcal meningitis among persons living with HIV/AIDS. AIDS 2009; 23 (4) 525-530
  • 30 Kielstein P, Hotzel H, Schmalreck A, Khaschabi D, Glawischnig W. Occurrence of Cryptococcus spp. in excreta of pigeons and pet birds. Mycoses 2000; 43 (1–2) 7-15
  • 31 Brizendine KD, Baddley JW, Pappas PG. Pulmonary cryptococcosis. Semin Respir Crit Care Med 2011; 32 (6) 727-734
  • 32 Khawcharoenporn T, Apisarnthanarak A, Mundy LM. Non-neoformans cryptococcal infections: a systematic review. Infection 2007; 35 (2) 51-58
  • 33 Chen SC, Meyer W, Sorrell TC. Cryptococcus gattii infections. Clin Microbiol Rev 2014; 27 (4) 980-1024
  • 34 Perfect JR, Dismukes WE, Dromer F , et al. Clinical practice guidelines for the management of cryptococcal disease: 2010 update by the Infectious Diseases Society of America. Clin Infect Dis 2010; 50 (3) 291-322
  • 35 Mirza SA, Phelan M, Rimland D , et al. The changing epidemiology of cryptococcosis: an update from population-based active surveillance in 2 large metropolitan areas, 1992-2000. Clin Infect Dis 2003; 36 (6) 789-794
  • 36 Chechani V, Kamholz SL. Pulmonary manifestations of disseminated cryptococcosis in patients with AIDS. Chest 1990; 98 (5) 1060-1066
  • 37 Chang WC, Tzao C, Hsu HH , et al. Pulmonary cryptococcosis: comparison of clinical and radiographic characteristics in immunocompetent and immunocompromised patients. Chest 2006; 129 (2) 333-340
  • 38 Baddley JW, Perfect JR, Oster RA , et al. Pulmonary cryptococcosis in patients without HIV infection: factors associated with disseminated disease. Eur J Clin Microbiol Infect Dis 2008; 27 (10) 937-943
  • 39 Connolly Jr JE, McAdams HP, Erasmus JJ, Rosado-de-Christenson ML. Opportunistic fungal pneumonia. J Thorac Imaging 1999; 14 (1) 51-62
  • 40 Sider L, Westcott MA. Pulmonary manifestations of cryptococcosis in patients with AIDS: CT features. J Thorac Imaging 1994; 9 (2) 78-84
  • 41 Lindsley MD, Mekha N, Baggett HC , et al. Evaluation of a newly developed lateral flow immunoassay for the diagnosis of cryptococcosis. Clin Infect Dis 2011; 53 (4) 321-325
  • 42 Kaplan JE, Vallabhaneni S, Smith RM, Chideya-Chihota S, Chehab J, Park B. Cryptococcal antigen screening and early antifungal treatment to prevent cryptococcal meningitis: a review of the literature. J Acquir Immune Defic Syndr 2015; 68 (Suppl. 03) S331-S339
  • 43 Kralovic SM, Rhodes JC. Utility of routine testing of bronchoalveolar lavage fluid for cryptococcal antigen. J Clin Microbiol 1998; 36 (10) 3088-3089
  • 44 Malabonga VM, Basti J, Kamholz SL. Utility of bronchoscopic sampling techniques for cryptococcal disease in AIDS. Chest 1991; 99 (2) 370-372
  • 45 Vail GM, Mocherla S, Wheat LJ , et al. Cellular immune response in HIV-infected patients with histoplasmosis. J Acquir Immune Defic Syndr 2002; 29 (1) 49-53
  • 46 Antinori S, Magni C, Nebuloni M , et al. Histoplasmosis among human immunodeficiency virus-infected people in Europe: report of 4 cases and review of the literature. Medicine (Baltimore) 2006; 85 (1) 22-36
  • 47 Chu JH, Feudtner C, Heydon K, Walsh TJ, Zaoutis TE. Hospitalizations for endemic mycoses: a population-based national study. Clin Infect Dis 2006; 42 (6) 822-825
  • 48 Murray JF, Mills J. Pulmonary infectious complications of human immunodeficiency virus infection. Part II. Am Rev Respir Dis 1990; 141 (6) 1582-1598
  • 49 McKinsey DS, Spiegel RA, Hutwagner L , et al. Prospective study of histoplasmosis in patients infected with human immunodeficiency virus: incidence, risk factors, and pathophysiology. Clin Infect Dis 1997; 24 (6) 1195-1203
  • 50 Wheat LJ, Connolly-Stringfield PA, Baker RL , et al. Disseminated histoplasmosis in the acquired immune deficiency syndrome: clinical findings, diagnosis and treatment, and review of the literature. Medicine (Baltimore) 1990; 69 (6) 361-374
  • 51 Sarosi GA, Johnson PC. Disseminated histoplasmosis in patients infected with human immunodeficiency virus. Clin Infect Dis 1992; 14 (Suppl. 01) S60-S67
  • 52 Arango-Bustamante K, Restrepo A, Cano LE, de Bedout C, Tobón AM, González A. Diagnostic value of culture and serological tests in the diagnosis of histoplasmosis in HIV and non-HIV Colombian patients. Am J Trop Med Hyg 2013; 89 (5) 937-942
  • 53 Baddley JW, Sankara IR, Rodriquez JM, Pappas PG, Many Jr WJ. Histoplasmosis in HIV-infected patients in a southern regional medical center: poor prognosis in the era of highly active antiretroviral therapy. Diagn Microbiol Infect Dis 2008; 62 (2) 151-156
  • 54 Wheat LJ, Kohler RB, Tewari RP. Diagnosis of disseminated histoplasmosis by detection of Histoplasma capsulatum antigen in serum and urine specimens. N Engl J Med 1986; 314 (2) 83-88
  • 55 Hage CA, Ribes JA, Wengenack NL , et al. A multicenter evaluation of tests for diagnosis of histoplasmosis. Clin Infect Dis 2011; 53 (5) 448-454
  • 56 Nguyen C, Barker BM, Hoover S , et al. Recent advances in our understanding of the environmental, epidemiological, immunological, and clinical dimensions of coccidioidomycosis. Clin Microbiol Rev 2013; 26 (3) 505-525
  • 57 Edwards PQ, Palmer CE. Prevalence of sensitivity to coccidioidin, with special reference to specific and nonspecific reactions to coccidioidin and to histoplasmin. Dis Chest 1957; 31 (1) 35-60
  • 58 Valdivia L, Nix D, Wright M , et al. Coccidioidomycosis as a common cause of community-acquired pneumonia. Emerg Infect Dis 2006; 12 (6) 958-962
  • 59 Masannat FY, Ampel NM. Coccidioidomycosis in patients with HIV-1 infection in the era of potent antiretroviral therapy. Clin Infect Dis 2010; 50 (1) 1-7
  • 60 Singh VR, Smith DK, Lawerence J , et al. Coccidioidomycosis in patients infected with human immunodeficiency virus: review of 91 cases at a single institution. Clin Infect Dis 1996; 23 (3) 563-568
  • 61 Fish DG, Ampel NM, Galgiani JN , et al. Coccidioidomycosis during human immunodeficiency virus infection. A review of 77 patients. Medicine (Baltimore) 1990; 69 (6) 384-391
  • 62 DiTomasso JP, Ampel NM, Sobonya RE, Bloom JW. Bronchoscopic diagnosis of pulmonary coccidioidomycosis. Comparison of cytology, culture, and transbronchial biopsy. Diagn Microbiol Infect Dis 1994; 18 (2) 83-87
  • 63 Antoniskis D, Larsen RA, Akil B, Rarick MU, Leedom JM. Seronegative disseminated coccidioidomycosis in patients with HIV infection. AIDS 1990; 4 (7) 691-693
  • 64 Durkin M, Connolly P, Kuberski T , et al. Diagnosis of coccidioidomycosis with use of the Coccidioides antigen enzyme immunoassay. Clin Infect Dis 2008; 47 (8) e69-e73
  • 65 Binnicker MJ, Buckwalter SP, Eisberner JJ , et al. Detection of Coccidioides species in clinical specimens by real-time PCR. J Clin Microbiol 2007; 45 (1) 173-178
  • 66 Gago S, Buitrago MJ, Clemons KV, Cuenca-Estrella M, Mirels LF, Stevens DA. Development and validation of a quantitative real-time PCR assay for the early diagnosis of coccidioidomycosis. Diagn Microbiol Infect Dis 2014; 79 (2) 214-221
  • 67 Woods CW, McRill C, Plikaytis BD , et al. Coccidioidomycosis in human immunodeficiency virus-infected persons in Arizona, 1994-1997: incidence, risk factors, and prevention. J Infect Dis 2000; 181 (4) 1428-1434
  • 68 Klein BS, Vergeront JM, Davis JP. Epidemiologic aspects of blastomycosis, the enigmatic systemic mycosis. Semin Respir Infect 1986; 1 (1) 29-39
  • 69 Pappas PG, Pottage JC, Powderly WG , et al. Blastomycosis in patients with the acquired immunodeficiency syndrome. Ann Intern Med 1992; 116 (10) 847-853
  • 70 Witzig RS, Hoadley DJ, Greer DL, Abriola KP, Hernandez RL. Blastomycosis and human immunodeficiency virus: three new cases and review. South Med J 1994; 87 (7) 715-719
  • 71 Durkin M, Witt J, Lemonte A, Wheat B, Connolly P. Antigen assay with the potential to aid in diagnosis of blastomycosis. J Clin Microbiol 2004; 42 (10) 4873-4875
  • 72 Paniago AM, de Freitas AC, Aguiar ES , et al. Paracoccidioidomycosis in patients with human immunodeficiency virus: review of 12 cases observed in an endemic region in Brazil. J Infect 2005; 51 (3) 248-252
  • 73 Sarti EC, de Oliveira SM, dos Santos LF, de Camargo ZP, Paniago AM. Paracoccidioidal infection in HIV patients at an endemic area of paracoccidioidomycosis in Brazil. Mycopathologia 2012; 173 (2–3) 145-149
  • 74 Supparatpinyo K, Khamwan C, Baosoung V, Nelson KE, Sirisanthana T. Disseminated Penicillium marneffei infection in southeast Asia. Lancet 1994; 344 (8915) 110-113
  • 75 Duong TA. Infection due to Penicillium marneffei, an emerging pathogen: review of 155 reported cases. Clin Infect Dis 1996; 23 (1) 125-130
  • 76 Cannon MJ, Schmid DS, Hyde TB. Review of cytomegalovirus seroprevalence and demographic characteristics associated with infection. Rev Med Virol 2010; 20 (4) 202-213
  • 77 Dieterich DT, Rahmin M. Cytomegalovirus colitis in AIDS: presentation in 44 patients and a review of the literature. J Acquir Immune Defic Syndr 1991; 4 (Suppl. 01) S29-S35
  • 78 Jabs DA, Van Natta ML, Kempen JH , et al. Characteristics of patients with cytomegalovirus retinitis in the era of highly active antiretroviral therapy. Am J Ophthalmol 2002; 133 (1) 48-61
  • 79 Kotton CN, Kumar D, Caliendo AM , et al; Transplantation Society International CMV Consensus Group. Updated international consensus guidelines on the management of cytomegalovirus in solid-organ transplantation. Transplantation 2013; 96 (4) 333-360
  • 80 Miles PR, Baughman RP, Linnemann Jr CC. Cytomegalovirus in the bronchoalveolar lavage fluid of patients with AIDS. Chest 1990; 97 (5) 1072-1076
  • 81 Millar AB, Patou G, Miller RF , et al. Cytomegalovirus in the lungs of patients with AIDS. Respiratory pathogen or passenger?. Am Rev Respir Dis 1990; 141 (6) 1474-1477
  • 82 Bozzette SA, Arcia J, Bartok AE , et al. Impact of Pneumocystis carinii and cytomegalovirus on the course and outcome of atypical pneumonia in advanced human immunodeficiency virus disease. J Infect Dis 1992; 165 (1) 93-98
  • 83 Wallace JM, Hannah J. Cytomegalovirus pneumonitis in patients with AIDS. Findings in an autopsy series. Chest 1987; 92 (2) 198-203
  • 84 Rodriguez-Barradas MC, Stool E, Musher DM , et al. Diagnosing and treating cytomegalovirus pneumonia in patients with AIDS. Clin Infect Dis 1996; 23 (1) 76-81
  • 85 Hayner CE, Baughman RP, Linnemann Jr CC, Dohn MN. The relationship between cytomegalovirus retrieved by bronchoalveolar lavage and mortality in patients with HIV. Chest 1995; 107 (3) 735-740
  • 86 McGuinness G, Scholes JV, Garay SM, Leitman BS, McCauley DI, Naidich DP. Cytomegalovirus pneumonitis: spectrum of parenchymal CT findings with pathologic correlation in 21 AIDS patients. Radiology 1994; 192 (2) 451-459
  • 87 Bower M, Barton SE, Nelson MR , et al. The significance of the detection of cytomegalovirus in the bronchoalveolar lavage fluid in AIDS patients with pneumonia. AIDS 1990; 4 (4) 317-320
  • 88 Waxman AB, Goldie SJ, Brett-Smith H, Matthay RA. Cytomegalovirus as a primary pulmonary pathogen in AIDS. Chest 1997; 111 (1) 128-134
  • 89 Huang L, Schnapp LM, Gruden JF, Hopewell PC, Stansell JD. Presentation of AIDS-related pulmonary Kaposi's sarcoma diagnosed by bronchoscopy. Am J Respir Crit Care Med 1996; 153 (4, Pt 1) 1385-1390
  • 90 Wolff SD, Kuhlman JE, Fishman EK. Thoracic Kaposi sarcoma in AIDS: CT findings. J Comput Assist Tomogr 1993; 17 (1) 60-62
  • 91 Davis SD, Henschke CI, Chamides BK, Westcott JL. Intrathoracic Kaposi sarcoma in AIDS patients: radiographic-pathologic correlation. Radiology 1987; 163 (2) 495-500
  • 92 Naidich DP, Tarras M, Garay SM, Birnbaum B, Rybak BJ, Schinella R. Kaposi's sarcoma. CT-radiographic correlation. Chest 1989; 96 (4) 723-728
  • 93 Carson PJ, Goldsmith JC. Atypical pulmonary diseases associated with AIDS. Chest 1991; 100 (3) 675-677
  • 94 Baras L, Farber CM, Van Vooren JP, Parent D. Herpes simplex virus tracheitis in a patient with the acquired immunodeficiency syndrome. Eur Respir J 1994; 7 (11) 2091-2093
  • 95 Fraisse P, Faller M, Rey D , et al. Recurrent varicella pneumonia complicating an endogenous reactivation of chickenpox in an HIV-infected adult patient. Eur Respir J 1998; 11 (3) 776-778
  • 96 Sans M, Gatell JM, Rafel M, Mallolas J, Soriano E. [Varicella pneumonia in adults infected by HIV-1. Presentation of 2 cases]. Enferm Infecc Microbiol Clin 1994; 12 (1) 26-30
  • 97 Kroon FP, van Dissel JT, de Jong JC, van Furth R. Antibody response to influenza, tetanus and pneumococcal vaccines in HIV-seropositive individuals in relation to the number of CD4+ lymphocytes. AIDS 1994; 8 (4) 469-476
  • 98 Rubin LG, Levin MJ, Ljungman P , et al; Infectious Diseases Society of America. 2013 IDSA clinical practice guideline for vaccination of the immunocompromised host. Clin Infect Dis 2014; 58 (3) e44-e100
  • 99 Israelski DM, Chmiel JS, Poggensee L, Phair JP, Remington JS. Prevalence of Toxoplasma infection in a cohort of homosexual men at risk of AIDS and toxoplasmic encephalitis. J Acquir Immune Defic Syndr 1993; 6 (4) 414-418
  • 100 Mathews WC, Fullerton SC. Use of a clinical laboratory database to estimate Toxoplasma seroprevalence among human immunodeficiency virus-infected patients. Overcoming bias in secondary analysis of clinical records. Arch Pathol Lab Med 1994; 118 (8) 807-810
  • 101 Walle F, Kebede N, Tsegaye A, Kassa T. Seroprevalence and risk factors for Toxoplasmosis in HIV infected and non-infected individuals in Bahir Dar, Northwest Ethiopia. Parasit Vectors 2013; 6 (1) 15
  • 102 Pappas G, Roussos N, Falagas ME. Toxoplasmosis snapshots: global status of Toxoplasma gondii seroprevalence and implications for pregnancy and congenital toxoplasmosis. Int J Parasitol 2009; 39 (12) 1385-1394
  • 103 Boyer KM, Holfels E, Roizen N , et al; Toxoplasmosis Study Group. Risk factors for Toxoplasma gondii infection in mothers of infants with congenital toxoplasmosis: Implications for prenatal management and screening. Am J Obstet Gynecol 2005; 192 (2) 564-571
  • 104 Wong B, Gold JW, Brown AE , et al. Central-nervous-system toxoplasmosis in homosexual men and parenteral drug abusers. Ann Intern Med 1984; 100 (1) 36-42
  • 105 Leport C, Chêne G, Morlat P , et al; AIDS Clinical Trial Group. Pyrimethamine for primary prophylaxis of toxoplasmic encephalitis in patients with human immunodeficiency virus infection: a double-blind, randomized trial. ANRS 005-ACTG 154 Group Members. Agence Nationale de Recherche sur le SIDA. J Infect Dis 1996; 173 (1) 91-97
  • 106 Luft BJ, Brooks RG, Conley FK, McCabe RE, Remington JS. Toxoplasmic encephalitis in patients with acquired immune deficiency syndrome. JAMA 1984; 252 (7) 913-917
  • 107 Abgrall S, Rabaud C, Costagliola D ; Clinical Epidemiology Group of the French Hospital Database on HIV. Incidence and risk factors for toxoplasmic encephalitis in human immunodeficiency virus-infected patients before and during the highly active antiretroviral therapy era. Clin Infect Dis 2001; 33 (10) 1747-1755
  • 108 Pomeroy C, Filice GA. Pulmonary toxoplasmosis: a review. Clin Infect Dis 1992; 14 (4) 863-870
  • 109 Rabaud C, May T, Lucet JC, Leport C, Ambroise-Thomas P, Canton P. Pulmonary toxoplasmosis in patients infected with human immunodeficiency virus: a French National Survey. Clin Infect Dis 1996; 23 (6) 1249-1254
  • 110 Derouin F, Sarfati C, Beauvais B, Garin YJ, Larivière M. Prevalence of pulmonary toxoplasmosis in HIV-infected patients. AIDS 1990; 4 (10) 1036
  • 111 Schär F, Trostdorf U, Giardina F , et al. Strongyloides stercoralis: global distribution and risk factors. PLoS Negl Trop Dis 2013; 7 (7) e2288
  • 112 Walzer PD, Milder JE, Banwell JG, Kilgore G, Klein M, Parker R. Epidemiologic features of Strongyloides stercoralis infection in an endemic area of the United States. Am J Trop Med Hyg 1982; 31 (2) 313-319
  • 113 Berk SL, Verghese A, Alvarez S, Hall K, Smith B. Clinical and epidemiologic features of strongyloidiasis. A prospective study in rural Tennessee. Arch Intern Med 1987; 147 (7) 1257-1261
  • 114 Keiser PB, Nutman TB. Strongyloides stercoralis in the immunocompromised population. Clin Microbiol Rev 2004; 17 (1) 208-217
  • 115 Nucci M, Portugal R, Pulcheri W , et al. Strongyloidiasis in patients with hematologic malignancies. Clin Infect Dis 1995; 21 (3) 675-677
  • 116 WHO. Acquired immunodeficiency syndrome (AIDS): WHO/CDC case definition for AIDS. Wkly Epidemiol Rec 1986; 61: 69-73
  • 117 Lam CS, Tong MK, Chan KM, Siu YP. Disseminated strongyloidiasis: a retrospective study of clinical course and outcome. Eur J Clin Microbiol Infect Dis 2006; 25 (1) 14-18
  • 118 Gompels MM, Todd J, Peters BS, Main J, Pinching AJ. Disseminated strongyloidiasis in AIDS: uncommon but important. AIDS 1991; 5 (3) 329-332
  • 119 Celedon JC, Mathur-Wagh U, Fox J, Garcia R, Wiest PM. Systemic strongyloidiasis in patients infected with the human immunodeficiency virus. A report of 3 cases and review of the literature. Medicine (Baltimore) 1994; 73 (5) 256-263
  • 120 Jamil SA, Hilton E. The Strongyloides hyperinfection syndrome. N Y State J Med 1992; 92 (2) 67-68
  • 121 Siddiqui AA, Berk SL. Diagnosis of Strongyloides stercoralis infection. Clin Infect Dis 2001; 33 (7) 1040-1047
  • 122 Chen XM, Keithly JS, Paya CV, LaRusso NF. Cryptosporidiosis. N Engl J Med 2002; 346 (22) 1723-1731
  • 123 Moore JA, Frenkel JK. Respiratory and enteric cryptosporidiosis in humans. Arch Pathol Lab Med 1991; 115 (11) 1160-1162
  • 124 Højlyng N, Jensen BN. Respiratory cryptosporidiosis in HIV-positive patients. Lancet 1988; 1 (8585) 590-591
  • 125 Clavel A, Arnal AC, Sánchez EC , et al. Respiratory cryptosporidiosis: case series and review of the literature. Infection 1996; 24 (5) 341-346
  • 126 Shankar EM, Vignesh R, Murugavel KG , et al. Common protozoans as an uncommon cause of respiratory ailments in HIV-associated immunodeficiency. FEMS Immunol Med Microbiol 2009; 57 (2) 93-103
  • 127 Scaglia M, Gatti S, Sacchi L , et al. Asymptomatic respiratory tract microsporidiosis due to Encephalitozoon hellem in three patients with AIDS. Clin Infect Dis 1998; 26 (1) 174-176
  • 128 Mandal S, Mandal MD. Human cystic echinococcosis: epidemiologic, zoonotic, clinical, diagnostic and therapeutic aspects. Asian Pac J Trop Med 2012; 5 (4) 253-260
  • 129 Kern P, Bardonnet K, Renner E , et al; European Echinococcosis Registry. European echinococcosis registry: human alveolar echinococcosis, Europe, 1982-2000. Emerg Infect Dis 2003; 9 (3) 343-349
  • 130 Sailer M, Soelder B, Allerberger F, Zaknun D, Feichtinger H, Gottstein B. Alveolar echinococcosis of the liver in a six-year-old girl with acquired immunodeficiency syndrome. J Pediatr 1997; 130 (2) 320-323