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Haemophilus influenzae serotype f purulent pericarditis: a cause of death in a child with Down syndrome
Diagnostic Microbiology and Infectious Disease 56 (2006) 87 – 89 www.elsevier.com/locate/diagmicrobio
Haemophilus influenzae serotype f purulent pericarditis: a cause of death in a child with Down syndrome Janis M. Taubea, Grover M. Hutchinsa, Karen C. Carrolla, Luca A. Vricellab, Janet Scheelc, Marc K. Halushkaa,4 a Department of Pathology, The Johns Hopkins Medical Institutions, Baltimore, MD 21287, USA Division of Cardiac Surgery, Department of Surgery, The Johns Hopkins Medical Institutions, Baltimore, MD 21287, USA c Division of Pediatric Cardiology, Department of Pediatrics, The Johns Hopkins Medical Institutions, Baltimore, MD 21287, USA Received 8 November 2005; accepted 26 January 2006 b
Abstract Purulent pericarditis is a cardiac emergency that can be difficult to diagnose and can be rapidly fatal. We report the case of a child with Down syndrome and recent atrial and ventricular septal defect repair who died from Haemophilus influenzae serotype f pericarditis. D 2006 Elsevier Inc. All rights reserved. Keywords: Haemophilus influenzae serotype f; Purulent pericarditis; Down syndrome
1. Introduction Haemophilus influenzae is a pleomorphic Gram-negative coccobacillus that is part of the normal flora of the upper respiratory tract of humans. It has been categorized according to the presence or absence of a polysaccharide capsule—the encapsulated serotypes have been named a through f, whereas those without capsules are called bnontypeableQ. Since immunizations began for the most virulent H. influenzae, serotype b (Hib), the other less virulent strains have seen a relative increase in invasive disease. In this report, we present a case of rapidly fatal H. influenzae serotype f purulent pericarditis in a child with Down syndrome and recent atrial and ventricular septal defect (ASD/VSD) repair. 2. Case report At 13 months of age, a patient with Down syndrome and congenital heart disease underwent cardiac surgery for repairs of ASD/VSD. A postoperative echocardiogram disclosed no pericardial effusion, an intact repair, and good 4 Corresponding author. Tel.: +1-410-614-8138; fax: +1-410614-7986. E-mail address: [email protected] (M.K. Halushka). 0732-8893/$ – see front matter D 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.diagmicrobio.2006.01.032
heart function. At her 2-week postoperative checkup, she had crusting mucoid discharge from her nose, but her lungs were clear. These symptoms had resolved by the time of her next appointment 10 days later. Otherwise, her course was without complication. One evening 6 weeks after her surgery, the patient became birritable and feverishQ. The next morning she was increasingly lethargic and was brought by ambulance to the pediatric emergency department (PED). At the time of PED admission, she was afebrile (temperature, 37.7 8C), but was tachycardic (pulse, 188 beats per minute), tachypneic (48 breaths per minute), and hypotensive (blood pressure of 64/54 mm Hg). Her physical examination showed crusty mucous on her nose and coarse breath sounds bilaterally with retractions and grunting, indicating severe respiratory distress. The clinical team was unable to draw blood from the patient and, therefore, no laboratory studies were available. Forty minutes later, her skin was mottled, her temperature had risen to 39.3 8C, and her pulse and blood pressure were 164 beats per minute and 79/46 mm Hg, respectively. A chest X-ray showed a possible pericardial effusion or increase in heart size when compared to a prior postoperative study. Three hours after arrival the patient clinically deteriorated. Cardiopulmonary resuscitation was performed and she was treated with intravenous epinephrine and atropine
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J.M. Taube et al. / Diagnostic Microbiology and Infectious Disease 56 (2006) 87 – 89
to stimulate her heart rate. An echocardiogram was performed, and a large, circumferential pericardial effusion was noted. Pericardiocentesis produced 50–60 mL of frank pus from the pericardial sac that was sent for culture. After pericardiocentesis, the patient’s condition failed to improve. A repeat echocardiogram revealed no reaccumulation of fluid. Despite continued resuscitative efforts, the patient expired shortly after the pericardiocentesis, 4 hours after admission to the PED, and less than 24 h after the onset of symptoms. A complete autopsy excluding the central nervous system (brain and spinal cord) was performed per the family’s request. The patient had external features consistent with Down syndrome. Thoracic cavity examination showed moderate adhesions between the pericardium, lungs, and diaphragm. Opening of the pericardial sac revealed a thick fibrinopurulent epicardial exudate, that is, a purulent pericarditis (Fig. 1). There were also multiple dense adhesions between the visceral and parietal pericardium along the anterior surface of the heart secondary to her cardiac surgery. The myocardium was unremarkable macroscopically. The ASD/VSD repairs were identified and both were intact and well-healed. Histologic examination showed a thick fibrinopurulent exudate involving the full thickness of the visceral and parietal pericardium. The right upper lobe of the lung showed an early developing pneumonia. Gram stain of the pericardial fluid revealed moderate polymorphonuclear cells and rare Gram-negative bacilli. Cultures of the pericardial fluid showed moderate to heavy growth after overnight incubation at 37 8C in 5% CO2 on chocolate agar of a pleomorphic, Gram-negative coccobacillus. The organism lacked hemolysis and was X factor- and V factor-positive as determined on BBL Hemo(Haemophilus) ID Quad media (Becton Dickinson, Sparks, MD). The organism was identified as H. influenzae. h-Lactamase testing was performed using the Cefinase disk test (BBL, Sparks, MD) and the results were negative. The organism was susceptible to ampicillin,
Fig. 1. Purulent pericarditis. The parietal pericardium has been reflected back to reveal a shaggy, fibrinopurulent exudate covering the epicardial surface of the heart. Normal lung is seen to the right of the pericardial sac in this autopsy image.
ceftriaxone, tetracycline, trimethoprim–sulfamethoxazole, and gatifloxacin. It was sent to the Maryland State Department of Health and Mental Hygiene Microbiology Laboratory where it was identified as serotype f using Difco H. influenzae type f antisera (Voight Global Distribution, Catalog no. 227921). 3. Discussion Purulent pericarditis is characterized by gross pus in the pericardium or by a microscopic purulent effusion and is most commonly associated with bacterial infection. Infections caused by mycoplasma or viruses are rarely macroscopically or microscopically purulent, but cause a sanguineous or serosanguineous effusion (Kenney et al., 1993). At the beginning of the 20th century, purulent pericarditis was predominantly a disease of healthy children and young adults who contracted a fulminant pneumococcal pneumonia. The incidence fell dramatically after the advent of antibiotic therapy, and the affected shifted to those with an underlying medical condition such as septicemia, perforating injury to the chest wall from surgery or trauma, endocarditis, or osteomyelitis (Klacsmann et al., 1977). A greater percentage of disease was also caused by a broader range of pathogens including Staphylococcus sp., Mycobacterium tuberculosis, and Gram-negative organisms, including Hib. The spectrum of causative agents may be changing again. Effective widespread immunization against Hib has led to a dramatic decrease in the amount of invasive disease due to this organism. Hib immunization, however, does not confer protection against the other encapsulated (a, c, d, e, f) or unencapsulated strains of H. influenzae. In 1989, before immunization against Hib, H. influenzae serotype f (Hif) accounted for only 1% of all invasive H. influenzae disease; after implementation of the vaccine, there has been a relative increase to 17% (Urwin et al., 1996). As Hib-related morbidity decreases, Hif infections have become of greater clinical interest. In the most extensive compilation to date, Urwin et al. collected clinical and epidemiologic information of 91 cases of invasive Hif infection as part of a population-based active surveillance program from 1989 to 1994. They found that invasive Hif infection in adults most often results in pneumonia (75% of cases), whereas in children under 5 years of age, both pneumonia (40% of cases) and meningitis (40% of cases) are common. Other diseases caused by invasive Hif include septicemia, otitis media, sinusitis, and epiglottitis (Urwin et al., 1996). There is only a single case report of Hif causing purulent pericarditis, and this was as the initial presentation of a 46-year-old patient with systemic lupus erythematosus (Yeh et al., 2004). In contrast to Hib, research on invasive Hif indicates that approximately three-quarters of adults and between one-quarter and one-half of children have an underlying lung disease or a chronic medical condition that predisposes them to this less virulent
J.M. Taube et al. / Diagnostic Microbiology and Infectious Disease 56 (2006) 87 – 89
pathogen. Among adults, 30% had chronic obstructive pulmonary disease and more than 50% had a history of smoking (Urwin et al., 1996; Nitta et al., 1995). Similarly, 63% of children had a recent history of an upper respiratory tract infection. Primary or secondary immunodeficiencies were also reported in many of the children including humoral immunodeficiency, subacute combined immunodeficiency, AIDS, sickle cell disease, cancer, or cerebrospinal fluid leaks (Urwin et al., 1996; Nitta et al., 1995). Patients with Down syndrome are at a general increased risk of infections, especially those with cardiopathies (Ribeiro et al., 2003), and this is the second case of invasive Hif disease in a Down syndrome patient (Urwin et al., 1996). The source and full extent of our patient’s Hif infection remains unknown. The pericardium is rarely a primary site of bacterial infection; rather, it is thought to become involved by either direct extension or hematogenous spread of disease. Her symptoms were suggestive of septic shock and bacteremia cannot be excluded as a cause of her heart failure. The early pneumonia seen histologically was minimal compared to the significant pericarditis and was not thought to be the primary source of infection. The patient had mucous crusting on her nose when she first presented to the PED, which was not Gram stained or cultured, preventing our determination of a rhinitis as a putative source. Because of autopsy consent limitations, we were unable to inspect the central nervous system for evidence of meningitis. In a study of 14 patients who died of purulent pericarditis after thoracic surgery, all had signs of fever and leukocytosis with the postoperative interval to death ranging from 3 to 152 days (average, 37 days) (Bulkley et al., 1977b). We found no evidence that Hif was seeded at the time of surgery, although this cannot be entirely excluded. Zacharisen et al. reported a case of rapidly fatal Hif sepsis in a 4-year-old immunocompetent child. The case was similar to ours in that she experienced a rapidly fatal clinical course (36 h between initial symptoms and her death) and, most notably, she had no upper respiratory tract symptoms or other identifiable focus of infection (Zacharisen et al., 2003). Antemortem diagnosis of purulent pericarditis is difficult and is often delayed until the signs and symptoms of cardiac tamponade manifest. Once diagnosed, treatment includes pericardial drainage and antibiotic treatment. An accurate diagnosis was rendered in this case, and pericardiocentesis was performed; however, the heart did not resume a normal rhythm after pericardiocentesis. Because of the rapid course of events after diagnosis, antibiotics had not yet been administered. Although the patient’s Hif infection was unrelated to the previous surgery, her rapid
89
terminal clinical course may have been. In this case the patient had multiple dense adhesions between the pericardium and the epicardium secondary to heart surgery. The pericardial sac can normally distend to hold large volumes of fluid; however, her pericardium would have been less able to expand to hold the rapidly developing exudate, possibly leading to an earlier, more significant tamponade effect (Bulkley et al., 1977a). 4. Conclusion The pathogens that cause purulent pericarditis have changed after antibiotic therapy and the Hib vaccine. But what has remained constant is the high mortality associated with this disease. With the advent of a Hib vaccine, there has been a relative emergence of H. influenzae non-type b strains causing severe and sometimes fatal infections. This case highlights an unfortunate outcome of a H. influenzae serotype f infection in a child with multiple risk factors. Acknowledgments The authors thank Dr Frederic Askin for helpful discussions and Jon Christofersen for assistance with photography. References Bulkley BH, Humphries JO, Hutchins GM (1977a) Clinical pathologic conference. Purulent pericarditis with asymmetric cardiac tamponade: a cause of death months after coronary artery bypass surgery. Am Heart J 93:776 – 783. Bulkley BH, Klacsmann PG, Hutchins GM (1977b) A clincopathologic study of post-thoracotomy purulent pericarditis. J Thorac Cardiovasc Surg 73:408 – 412. Kenney RT, Ki JS, Clyde WA, et al. (1993) Mycoplasmal pericarditis: evidence of invasive disease. Clin Infect Dis (Suppl 1):s58 – s62. Klacsmann PG, Bulkley BH, Hutchins GM (1977) The changed spectrum of purulent pericarditis: an 86 year autopsy experience in 200 patients. Am J Med 63:666 – 673. Nitta DM, Jackson MA, Burry VF, Olson LC (1995) Invasive Haemophilus influenzae type f disease. Pediatr Infect Dis J 14:157 – 160. Ribeiro LM, Jacob CM, Pastorino AC, et al. (2003) Evaluation of factors associated with recurrent and/or severe infections in patients with Down’s syndrome. J Pediatr (Rio J) 79:141 – 148. Urwin G, Krohn JA, Deaver-Robinson K, Wenger JD, Farley MM (1996) Invasive disease due to Haemophilus influenzae serotype f: clinical and epidemiologic characteristics in the H. influenzae serotype b vaccine era. The Haemophilus influenzae Study Group. Clin Infect Dis 22:1069 – 1076. Yeh YH, Chu PH, Yeh CH, et al. (2004) Haemophilus influenzae pericarditis with tamponade as the initial presentation of systemic lupus erythematosus. Int J Clin Pract 58:1045 – 1047. Zacharisen MC, Watters SK, Edwards J (2003) Rapidly fatal Haemophilus influenzae serotype f sepsis in a healthy child. J Infect 46:194 – 196.
Haemophilus influenzae serotype f purulent pericarditis: a cause of death in a child with Down syndrome Janis M. Taubea, Grover M. Hutchinsa, Karen C. Carrolla, Luca A. Vricellab, Janet Scheelc, Marc K. Halushkaa,4 a Department of Pathology, The Johns Hopkins Medical Institutions, Baltimore, MD 21287, USA Division of Cardiac Surgery, Department of Surgery, The Johns Hopkins Medical Institutions, Baltimore, MD 21287, USA c Division of Pediatric Cardiology, Department of Pediatrics, The Johns Hopkins Medical Institutions, Baltimore, MD 21287, USA Received 8 November 2005; accepted 26 January 2006 b
Abstract Purulent pericarditis is a cardiac emergency that can be difficult to diagnose and can be rapidly fatal. We report the case of a child with Down syndrome and recent atrial and ventricular septal defect repair who died from Haemophilus influenzae serotype f pericarditis. D 2006 Elsevier Inc. All rights reserved. Keywords: Haemophilus influenzae serotype f; Purulent pericarditis; Down syndrome
1. Introduction Haemophilus influenzae is a pleomorphic Gram-negative coccobacillus that is part of the normal flora of the upper respiratory tract of humans. It has been categorized according to the presence or absence of a polysaccharide capsule—the encapsulated serotypes have been named a through f, whereas those without capsules are called bnontypeableQ. Since immunizations began for the most virulent H. influenzae, serotype b (Hib), the other less virulent strains have seen a relative increase in invasive disease. In this report, we present a case of rapidly fatal H. influenzae serotype f purulent pericarditis in a child with Down syndrome and recent atrial and ventricular septal defect (ASD/VSD) repair. 2. Case report At 13 months of age, a patient with Down syndrome and congenital heart disease underwent cardiac surgery for repairs of ASD/VSD. A postoperative echocardiogram disclosed no pericardial effusion, an intact repair, and good 4 Corresponding author. Tel.: +1-410-614-8138; fax: +1-410614-7986. E-mail address: [email protected] (M.K. Halushka). 0732-8893/$ – see front matter D 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.diagmicrobio.2006.01.032
heart function. At her 2-week postoperative checkup, she had crusting mucoid discharge from her nose, but her lungs were clear. These symptoms had resolved by the time of her next appointment 10 days later. Otherwise, her course was without complication. One evening 6 weeks after her surgery, the patient became birritable and feverishQ. The next morning she was increasingly lethargic and was brought by ambulance to the pediatric emergency department (PED). At the time of PED admission, she was afebrile (temperature, 37.7 8C), but was tachycardic (pulse, 188 beats per minute), tachypneic (48 breaths per minute), and hypotensive (blood pressure of 64/54 mm Hg). Her physical examination showed crusty mucous on her nose and coarse breath sounds bilaterally with retractions and grunting, indicating severe respiratory distress. The clinical team was unable to draw blood from the patient and, therefore, no laboratory studies were available. Forty minutes later, her skin was mottled, her temperature had risen to 39.3 8C, and her pulse and blood pressure were 164 beats per minute and 79/46 mm Hg, respectively. A chest X-ray showed a possible pericardial effusion or increase in heart size when compared to a prior postoperative study. Three hours after arrival the patient clinically deteriorated. Cardiopulmonary resuscitation was performed and she was treated with intravenous epinephrine and atropine
88
J.M. Taube et al. / Diagnostic Microbiology and Infectious Disease 56 (2006) 87 – 89
to stimulate her heart rate. An echocardiogram was performed, and a large, circumferential pericardial effusion was noted. Pericardiocentesis produced 50–60 mL of frank pus from the pericardial sac that was sent for culture. After pericardiocentesis, the patient’s condition failed to improve. A repeat echocardiogram revealed no reaccumulation of fluid. Despite continued resuscitative efforts, the patient expired shortly after the pericardiocentesis, 4 hours after admission to the PED, and less than 24 h after the onset of symptoms. A complete autopsy excluding the central nervous system (brain and spinal cord) was performed per the family’s request. The patient had external features consistent with Down syndrome. Thoracic cavity examination showed moderate adhesions between the pericardium, lungs, and diaphragm. Opening of the pericardial sac revealed a thick fibrinopurulent epicardial exudate, that is, a purulent pericarditis (Fig. 1). There were also multiple dense adhesions between the visceral and parietal pericardium along the anterior surface of the heart secondary to her cardiac surgery. The myocardium was unremarkable macroscopically. The ASD/VSD repairs were identified and both were intact and well-healed. Histologic examination showed a thick fibrinopurulent exudate involving the full thickness of the visceral and parietal pericardium. The right upper lobe of the lung showed an early developing pneumonia. Gram stain of the pericardial fluid revealed moderate polymorphonuclear cells and rare Gram-negative bacilli. Cultures of the pericardial fluid showed moderate to heavy growth after overnight incubation at 37 8C in 5% CO2 on chocolate agar of a pleomorphic, Gram-negative coccobacillus. The organism lacked hemolysis and was X factor- and V factor-positive as determined on BBL Hemo(Haemophilus) ID Quad media (Becton Dickinson, Sparks, MD). The organism was identified as H. influenzae. h-Lactamase testing was performed using the Cefinase disk test (BBL, Sparks, MD) and the results were negative. The organism was susceptible to ampicillin,
Fig. 1. Purulent pericarditis. The parietal pericardium has been reflected back to reveal a shaggy, fibrinopurulent exudate covering the epicardial surface of the heart. Normal lung is seen to the right of the pericardial sac in this autopsy image.
ceftriaxone, tetracycline, trimethoprim–sulfamethoxazole, and gatifloxacin. It was sent to the Maryland State Department of Health and Mental Hygiene Microbiology Laboratory where it was identified as serotype f using Difco H. influenzae type f antisera (Voight Global Distribution, Catalog no. 227921). 3. Discussion Purulent pericarditis is characterized by gross pus in the pericardium or by a microscopic purulent effusion and is most commonly associated with bacterial infection. Infections caused by mycoplasma or viruses are rarely macroscopically or microscopically purulent, but cause a sanguineous or serosanguineous effusion (Kenney et al., 1993). At the beginning of the 20th century, purulent pericarditis was predominantly a disease of healthy children and young adults who contracted a fulminant pneumococcal pneumonia. The incidence fell dramatically after the advent of antibiotic therapy, and the affected shifted to those with an underlying medical condition such as septicemia, perforating injury to the chest wall from surgery or trauma, endocarditis, or osteomyelitis (Klacsmann et al., 1977). A greater percentage of disease was also caused by a broader range of pathogens including Staphylococcus sp., Mycobacterium tuberculosis, and Gram-negative organisms, including Hib. The spectrum of causative agents may be changing again. Effective widespread immunization against Hib has led to a dramatic decrease in the amount of invasive disease due to this organism. Hib immunization, however, does not confer protection against the other encapsulated (a, c, d, e, f) or unencapsulated strains of H. influenzae. In 1989, before immunization against Hib, H. influenzae serotype f (Hif) accounted for only 1% of all invasive H. influenzae disease; after implementation of the vaccine, there has been a relative increase to 17% (Urwin et al., 1996). As Hib-related morbidity decreases, Hif infections have become of greater clinical interest. In the most extensive compilation to date, Urwin et al. collected clinical and epidemiologic information of 91 cases of invasive Hif infection as part of a population-based active surveillance program from 1989 to 1994. They found that invasive Hif infection in adults most often results in pneumonia (75% of cases), whereas in children under 5 years of age, both pneumonia (40% of cases) and meningitis (40% of cases) are common. Other diseases caused by invasive Hif include septicemia, otitis media, sinusitis, and epiglottitis (Urwin et al., 1996). There is only a single case report of Hif causing purulent pericarditis, and this was as the initial presentation of a 46-year-old patient with systemic lupus erythematosus (Yeh et al., 2004). In contrast to Hib, research on invasive Hif indicates that approximately three-quarters of adults and between one-quarter and one-half of children have an underlying lung disease or a chronic medical condition that predisposes them to this less virulent
J.M. Taube et al. / Diagnostic Microbiology and Infectious Disease 56 (2006) 87 – 89
pathogen. Among adults, 30% had chronic obstructive pulmonary disease and more than 50% had a history of smoking (Urwin et al., 1996; Nitta et al., 1995). Similarly, 63% of children had a recent history of an upper respiratory tract infection. Primary or secondary immunodeficiencies were also reported in many of the children including humoral immunodeficiency, subacute combined immunodeficiency, AIDS, sickle cell disease, cancer, or cerebrospinal fluid leaks (Urwin et al., 1996; Nitta et al., 1995). Patients with Down syndrome are at a general increased risk of infections, especially those with cardiopathies (Ribeiro et al., 2003), and this is the second case of invasive Hif disease in a Down syndrome patient (Urwin et al., 1996). The source and full extent of our patient’s Hif infection remains unknown. The pericardium is rarely a primary site of bacterial infection; rather, it is thought to become involved by either direct extension or hematogenous spread of disease. Her symptoms were suggestive of septic shock and bacteremia cannot be excluded as a cause of her heart failure. The early pneumonia seen histologically was minimal compared to the significant pericarditis and was not thought to be the primary source of infection. The patient had mucous crusting on her nose when she first presented to the PED, which was not Gram stained or cultured, preventing our determination of a rhinitis as a putative source. Because of autopsy consent limitations, we were unable to inspect the central nervous system for evidence of meningitis. In a study of 14 patients who died of purulent pericarditis after thoracic surgery, all had signs of fever and leukocytosis with the postoperative interval to death ranging from 3 to 152 days (average, 37 days) (Bulkley et al., 1977b). We found no evidence that Hif was seeded at the time of surgery, although this cannot be entirely excluded. Zacharisen et al. reported a case of rapidly fatal Hif sepsis in a 4-year-old immunocompetent child. The case was similar to ours in that she experienced a rapidly fatal clinical course (36 h between initial symptoms and her death) and, most notably, she had no upper respiratory tract symptoms or other identifiable focus of infection (Zacharisen et al., 2003). Antemortem diagnosis of purulent pericarditis is difficult and is often delayed until the signs and symptoms of cardiac tamponade manifest. Once diagnosed, treatment includes pericardial drainage and antibiotic treatment. An accurate diagnosis was rendered in this case, and pericardiocentesis was performed; however, the heart did not resume a normal rhythm after pericardiocentesis. Because of the rapid course of events after diagnosis, antibiotics had not yet been administered. Although the patient’s Hif infection was unrelated to the previous surgery, her rapid
89
terminal clinical course may have been. In this case the patient had multiple dense adhesions between the pericardium and the epicardium secondary to heart surgery. The pericardial sac can normally distend to hold large volumes of fluid; however, her pericardium would have been less able to expand to hold the rapidly developing exudate, possibly leading to an earlier, more significant tamponade effect (Bulkley et al., 1977a). 4. Conclusion The pathogens that cause purulent pericarditis have changed after antibiotic therapy and the Hib vaccine. But what has remained constant is the high mortality associated with this disease. With the advent of a Hib vaccine, there has been a relative emergence of H. influenzae non-type b strains causing severe and sometimes fatal infections. This case highlights an unfortunate outcome of a H. influenzae serotype f infection in a child with multiple risk factors. Acknowledgments The authors thank Dr Frederic Askin for helpful discussions and Jon Christofersen for assistance with photography. References Bulkley BH, Humphries JO, Hutchins GM (1977a) Clinical pathologic conference. Purulent pericarditis with asymmetric cardiac tamponade: a cause of death months after coronary artery bypass surgery. Am Heart J 93:776 – 783. Bulkley BH, Klacsmann PG, Hutchins GM (1977b) A clincopathologic study of post-thoracotomy purulent pericarditis. J Thorac Cardiovasc Surg 73:408 – 412. Kenney RT, Ki JS, Clyde WA, et al. (1993) Mycoplasmal pericarditis: evidence of invasive disease. Clin Infect Dis (Suppl 1):s58 – s62. Klacsmann PG, Bulkley BH, Hutchins GM (1977) The changed spectrum of purulent pericarditis: an 86 year autopsy experience in 200 patients. Am J Med 63:666 – 673. Nitta DM, Jackson MA, Burry VF, Olson LC (1995) Invasive Haemophilus influenzae type f disease. Pediatr Infect Dis J 14:157 – 160. Ribeiro LM, Jacob CM, Pastorino AC, et al. (2003) Evaluation of factors associated with recurrent and/or severe infections in patients with Down’s syndrome. J Pediatr (Rio J) 79:141 – 148. Urwin G, Krohn JA, Deaver-Robinson K, Wenger JD, Farley MM (1996) Invasive disease due to Haemophilus influenzae serotype f: clinical and epidemiologic characteristics in the H. influenzae serotype b vaccine era. The Haemophilus influenzae Study Group. Clin Infect Dis 22:1069 – 1076. Yeh YH, Chu PH, Yeh CH, et al. (2004) Haemophilus influenzae pericarditis with tamponade as the initial presentation of systemic lupus erythematosus. Int J Clin Pract 58:1045 – 1047. Zacharisen MC, Watters SK, Edwards J (2003) Rapidly fatal Haemophilus influenzae serotype f sepsis in a healthy child. J Infect 46:194 – 196.