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A rare cause of pericarditis
CORRESPONDENCE A rare cause of pericarditis Non-typhoid salmonella infections are 20±100 times more common in patients infected with the human immunode®ciency virus (HIV) than in the immunocompetent population [1]. In Spain, Salmonella is the second most common cause of bacterial diarrhea in HIV-infected patients after Mycobacterium avium complex. The most frequently isolated species is Salmonella enterica serovar Enteritidis [2,3]. Bacteremia caused by nontyphoid Salmonella is most common in HIV patients, and constitutes 7±35% of the total cases of bacteremia in this group of patients [4]. Nevertheless, purulent pericarditis caused by non-typhoid Salmonella is exceptional, and there have been no more than 15 cases reported in the last 15 years [5±8]. Since the introduction of highly active antiretroviral therapy (HAART), the incidence of infection with non-typhoid Salmonella has decreased, although it may appear in cases of severe immunode®ciency and in patients not taking HAART. However, despite the capacity for recurrence of non-typhoid Salmonella bacteremia (3±8%) [3,9,10], there is no de®nitive consensus on the duration of antibiotic therapy at the acute stage of this process. A 37-year-old male with a history of intravenous drug use (IVDU) was diagnosed with HIV infection 9 months before admission, during which time he had Pneumocystis carinii pneumonia, oral candidiasis and perianal abscess. He had a CD4 count of 12 cells/mL3 and a viral load of 38 000 HIV RNA copies. He did not begin HAART at that time. Four months previously, the patient had developed bacteremic gastroenteritis caused by Salmonella derby, and was treated with cipro¯oxacin, which he stopped on his own accord after 7 days. He returned to the hospital 3 months later, complaining of weakness, anorexia and weight loss. During the 3 days before the second admission, he had a cough, dyspnea, and edema of both legs. A physical examination revealed a temperature of 35 8C, a blood pressure of 140/60 mmHg, and a heart rate of 130 beats/min. He was conscious but disoriented, pale and sweaty, and showed signs of low peripheral perfusion. This was accompanied by an elevation of jugular vein pressure. A cardiopulmonary examination revealed tachyarrhythmia, pericardial friction rub, and crepitations in
both pulmonary bases. The abdomen showed no abnormalities, but the patient had edema of both legs. The results of hematology and biochemistry analyses were normal, with the exception of hyperglycemia and a creatinine level of 8.8 mg/ dL. A new immunologic study showed a CD4 count of 9 cells/mL3 and 75 000 HIV RNA copies of viral load. A chest X-ray revealed increased cardiac size. The ECG showed atrial ®brillation with a ventricular rate of 130 beats/min and low voltage. The ultrasound scan (Figure 1A) revealed severe pericardial effusion with no signs of tamponade. Pericardiocentesis was performed, and 700 mL of thick ¯uid was obtained. This ¯uid had 31 000 leukocytes/mL3 (98% polymorphonuclear leukocytes), a glucose level of 167 mg/dL (plasma glucose 295 mg/dL), a lactate dehydrogenase level of 2453 mg/dL, and a pH of 7.012. Drainage was maintained for 72 h (Figure 1B). Salmonella derby grew on cultures of pericardial ¯uid, and had the same microbiological characteristics as the strain obtained from a blood culture on a previous admission. Serotype identi®cation of Salmonella was done with the Bacto-Salmonella O antisera set A-I and Bacto-Salmonella H antisera Spicer±Edwards set (DIFCO Laboratories; Detroit, MI, USA). The patient developed a septic syndrome with hypotension, severe peripheral hypoperfusion, a low level of consciousness and renal failure; this was controlled with the use of plasma expanders and continuous perfusion of dopamine. Amiodarone was needed to restore sinusal rhythm in a few hours. The patient completed treatment with levo¯oxacin for 21 days, and started HAART, with progressive clinical, radiologic and echocardiographic improvement. One year after discharge from hospital, he was asymptomatic. Pericarditis is not unusual in association with HIV infection, although the majority of cases are minor and asymptomatic. They usually appear in advanced stages of AIDS [11,12]. Pericardial effusion and cardiac tamponade are exceptional [13,14]. The reported etiology of these effusions includes neoplasm (Kaposi sarcoma, lymphoma, etc.) and several infections (bacterial, viral, fungal and protozoal) [11,12,14]. Purulent pericarditis caused by Salmonella spp. is an exceptional ®nding in the general population, and there are no more than 15 reported cases in the medical literature [5±8]. In these series, cardiac tamponade developed in approximately 50% of
ß 2003 Copyright by the European Society of Clinical Microbiology and Infectious Diseases
1262 Clinical Microbiology and Infection, Volume 9 Number 12, December 2003
Figure 1 (A) Pericardial effusion on admission. (B) Important reduction after pericardiocentesis and microbial therapy.
patients, and this correlated with better survival rates, and early diagnosis and therapy. Moreover, the authors [5] consider that pericardiocentesis and effective parenteral antibiotics are the main therapeutic measures to be adopted, and do not consider intrapericardic instillation of antibiotics to be necessary. Our patient had no signs of cardiac tamponade, although he developed cardiac failure and septic shock. Pericardial drainage for 72 h and prolonged intravenous antibiotic therapy were suf®cient to achieve clinical improvement. Non-typhoid Salmonella bacteremia has been reported as the ®rst manifestation of HIV infection in 10±50% of cases, and 15±60% of these had diarrhea on diagnosis [15]. The rate at which these bacteremias recur ranges from 12% to 83% [3,9]. This bacteremia appears in cases of severe immunode®ciency [9], and decreases in frequency after secondary prophylaxis with co-trimoxazole and/or the use of HAART [15,16].
Immunologic identi®cation tests of the Salmonella spp. strain obtained from a blood culture taken at the ®rst admission con®rmed that the same strain of Salmonella derby was isolated from pericardial ¯uid on the second admission. There are studies showing that relapses of Salmonella spp. bacteremia are usually due to the same microorganism, which remains inside macrophages and, in severe states of immunode®ciency, reactivates to produce a new local or bacteremic infection [10,17,18]. There is no consensus about the duration of antimicrobial therapy in HIV patients with salmonella infections. This is due to the dif®culty that macrophages have in eliminating the sequestered bacilli, which makes relapses of salmonella bacteremia more likely. In these cases, we propose, as do other authors, maintaining therapy for 3 weeks [15,19] or longer (4±6 weeks) [20]. In conclusion, recurrent bacteremia caused by Salmonella spp. is not unusual in HIV infection. Nevertheless, purulent pericarditis caused by Salmonella spp. is exceptional. In HIV patients with severe immunode®ciency and salmonella infection, we recommend 3 weeks of effective antimicrobial therapy and secondary prophylaxis with co-trimoxazole, until satisfactory immune restoration is obtained with HAART. F. J. Candel, V. Roca-ArboneÂs, M. J. NuÂnÄez, C. Arroyo, A. Valdivia, M. J. TeÂllez and J. J. Picazo Department of Clinical Microbiology, C/Antonio LoÂpez, No. 67, portal 2, 15B, 28019 Madrid, Spain E-mail: [email protected] REFERENCES 1. Levine WC, Buehler JW, Bean NH, Tauxe RV. Epidemiology of nontyphoidal Salmonella bacteremia during the human inmunodeficiency virus epidemic. J Infect Dis 1991; 164: 81±7. 2. Roca V, GarcõÂa C, Coello R, GonzaÂlez JR, Romero J. Bacteriemia por Salmonella no typhi en la infeccioÂn por VIH. Estudio de 36 pacientes. Enferm Infecc Microbiol Clin 1991; 9(suppl 1): 32±7. 3. Moreno A, Gatell JM; Mensa J et al. Incidencia de enteropatoÂgenos en pacientes con infeccioÂn por el virus de la inmunodeficiencia humana. Med Clin (Barc) 1994; 102: 205±8. 4. Hickey MM, Shanson DC. Septicaemia in patients with and without AIDS at Westminster Hospital, London. J Infect 1993; 27: 243±50.
ß 2003 Copyright by the European Society of Clinical Microbiology and Infectious Diseases, CMI, 9, 1261±1263
Correspondence 1263
5. Cohen JL, Bartlett JA, Corey GR. Extra-intestinal manifestations of Salmonella infections. Medicine 1987; 66: 349±88. 6. Canut A, Brezmes MF, Antolin MI, YaguÈe A, Arribas A. Infecciones focales por Salmonella no typhi: revisioÂn de nuestra casuõÂstica y comparacioÂn con otras series. Rev Clin Esp 1992; 191: 71±5. 7. Perera CU, Luo NP, Zumla A. Bacteraemias in HIVpositive patients. Lancet 1990; 336: 877±8. 8. Kiuchi K, Endo T, Nejima J et al. Purulent pericarditis with tamponade caused by Salmonella enteritidis. Jpn Circul J 1998; 62: 139±41. 9. Nelson MR, Shanson DC, Hawkins DA, Gazzard BG. Salmonella, Campylobacter and Shigella in HIVseropositive patients. AIDS 1992; 6: 1495±8. 10. Fica AE, Horowitz HW, Lior H, Cabello FC. Demonstration of persistence of Salmonella typhimurium in an AIDS patient by molecular methods. J Clin Mibrobiol 1994; 32: 2327±30. 11. Rerkpattanapipat P, Wongpraparut N, Jacobs LE, Kotler MN. Cardiac manifestations of acquired immunodeficiency syndrome. Arch Intern Med 2000; 160: 602±8. 12. Chen Y, Brennessel D, Walters J, Johnson M, Rosner F, Raza M. Human immunodeficiency virus-associated pericardial effusion. Report of 40 cases and review of the literature. Am Heart J 1999; 137: 516±21. 13. Heidenreich PA, Eisemberg MJ, Kee LL et al. Pericardial effusion in AIDS: incidence and survival. Circulation 1995; 92: 3229±34.
14. Scerpella EG, Fatmi AA, Brito; MA. Bacterial pericarditis and cardiac tamponade in patients infected with human immunodeficiency virus type I: case report and review. Clin Infect Dis 1995; 21: 1518±19. 15. Ramos JM, FernaÂndez Guerrero ML. Salmonelosis no tifoidea e infeccioÂn por el virus de la inmunodeficiencia humana. Med Clin (Barc) 1997; 108: 349±55. 16. Casado J, Valdezate S, Caleron C et al. Zidovudine therapy protects against Salmonella bacteremia recurrence in HIV-infected patients. J Infect Dis 1999; 179: 1553±6. 17. Mayer KH, Hanson E. Recurrent Salmonella infection with a single strain in the acquired immunodeficiency syndrome. Confirmation by plasmid finger printing. Diagn Microbiol Infect Dis 1986; 4: 71±6. 18. Aguado; JM, Obeso G, Cabanillas JJ, Fernandez Guerrero ML, AleÂs J. Pleuropulmonay infections due to nontyphoid strains of Salmonella. Arch Intern Med 1990; 150: 54±6. 19. Roca V, GarcõÂa-Aguado C, PeÂrez-Cecilia E, Romero J, GonzaÂlez-Lahoz JM, Picazo JJ. Ciprofloxacin: results of treatment and prevention of relapses of Salmonella spp bacteremia in HIV-infected patients [abstract 35]. In: 32nd Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC). Anaheim, CA: American Society for Microbiology, 1992: 14 (oral communication). 20. Hohmann EL. Nontyphoidal Salmonellosis. Clin Infect Dis 2001; 32: 263±9.
ß 2003 Copyright by the European Society of Clinical Microbiology and Infectious Diseases, CMI, 9, 1261±1263
both pulmonary bases. The abdomen showed no abnormalities, but the patient had edema of both legs. The results of hematology and biochemistry analyses were normal, with the exception of hyperglycemia and a creatinine level of 8.8 mg/ dL. A new immunologic study showed a CD4 count of 9 cells/mL3 and 75 000 HIV RNA copies of viral load. A chest X-ray revealed increased cardiac size. The ECG showed atrial ®brillation with a ventricular rate of 130 beats/min and low voltage. The ultrasound scan (Figure 1A) revealed severe pericardial effusion with no signs of tamponade. Pericardiocentesis was performed, and 700 mL of thick ¯uid was obtained. This ¯uid had 31 000 leukocytes/mL3 (98% polymorphonuclear leukocytes), a glucose level of 167 mg/dL (plasma glucose 295 mg/dL), a lactate dehydrogenase level of 2453 mg/dL, and a pH of 7.012. Drainage was maintained for 72 h (Figure 1B). Salmonella derby grew on cultures of pericardial ¯uid, and had the same microbiological characteristics as the strain obtained from a blood culture on a previous admission. Serotype identi®cation of Salmonella was done with the Bacto-Salmonella O antisera set A-I and Bacto-Salmonella H antisera Spicer±Edwards set (DIFCO Laboratories; Detroit, MI, USA). The patient developed a septic syndrome with hypotension, severe peripheral hypoperfusion, a low level of consciousness and renal failure; this was controlled with the use of plasma expanders and continuous perfusion of dopamine. Amiodarone was needed to restore sinusal rhythm in a few hours. The patient completed treatment with levo¯oxacin for 21 days, and started HAART, with progressive clinical, radiologic and echocardiographic improvement. One year after discharge from hospital, he was asymptomatic. Pericarditis is not unusual in association with HIV infection, although the majority of cases are minor and asymptomatic. They usually appear in advanced stages of AIDS [11,12]. Pericardial effusion and cardiac tamponade are exceptional [13,14]. The reported etiology of these effusions includes neoplasm (Kaposi sarcoma, lymphoma, etc.) and several infections (bacterial, viral, fungal and protozoal) [11,12,14]. Purulent pericarditis caused by Salmonella spp. is an exceptional ®nding in the general population, and there are no more than 15 reported cases in the medical literature [5±8]. In these series, cardiac tamponade developed in approximately 50% of
ß 2003 Copyright by the European Society of Clinical Microbiology and Infectious Diseases
1262 Clinical Microbiology and Infection, Volume 9 Number 12, December 2003
Figure 1 (A) Pericardial effusion on admission. (B) Important reduction after pericardiocentesis and microbial therapy.
patients, and this correlated with better survival rates, and early diagnosis and therapy. Moreover, the authors [5] consider that pericardiocentesis and effective parenteral antibiotics are the main therapeutic measures to be adopted, and do not consider intrapericardic instillation of antibiotics to be necessary. Our patient had no signs of cardiac tamponade, although he developed cardiac failure and septic shock. Pericardial drainage for 72 h and prolonged intravenous antibiotic therapy were suf®cient to achieve clinical improvement. Non-typhoid Salmonella bacteremia has been reported as the ®rst manifestation of HIV infection in 10±50% of cases, and 15±60% of these had diarrhea on diagnosis [15]. The rate at which these bacteremias recur ranges from 12% to 83% [3,9]. This bacteremia appears in cases of severe immunode®ciency [9], and decreases in frequency after secondary prophylaxis with co-trimoxazole and/or the use of HAART [15,16].
Immunologic identi®cation tests of the Salmonella spp. strain obtained from a blood culture taken at the ®rst admission con®rmed that the same strain of Salmonella derby was isolated from pericardial ¯uid on the second admission. There are studies showing that relapses of Salmonella spp. bacteremia are usually due to the same microorganism, which remains inside macrophages and, in severe states of immunode®ciency, reactivates to produce a new local or bacteremic infection [10,17,18]. There is no consensus about the duration of antimicrobial therapy in HIV patients with salmonella infections. This is due to the dif®culty that macrophages have in eliminating the sequestered bacilli, which makes relapses of salmonella bacteremia more likely. In these cases, we propose, as do other authors, maintaining therapy for 3 weeks [15,19] or longer (4±6 weeks) [20]. In conclusion, recurrent bacteremia caused by Salmonella spp. is not unusual in HIV infection. Nevertheless, purulent pericarditis caused by Salmonella spp. is exceptional. In HIV patients with severe immunode®ciency and salmonella infection, we recommend 3 weeks of effective antimicrobial therapy and secondary prophylaxis with co-trimoxazole, until satisfactory immune restoration is obtained with HAART. F. J. Candel, V. Roca-ArboneÂs, M. J. NuÂnÄez, C. Arroyo, A. Valdivia, M. J. TeÂllez and J. J. Picazo Department of Clinical Microbiology, C/Antonio LoÂpez, No. 67, portal 2, 15B, 28019 Madrid, Spain E-mail: [email protected] REFERENCES 1. Levine WC, Buehler JW, Bean NH, Tauxe RV. Epidemiology of nontyphoidal Salmonella bacteremia during the human inmunodeficiency virus epidemic. J Infect Dis 1991; 164: 81±7. 2. Roca V, GarcõÂa C, Coello R, GonzaÂlez JR, Romero J. Bacteriemia por Salmonella no typhi en la infeccioÂn por VIH. Estudio de 36 pacientes. Enferm Infecc Microbiol Clin 1991; 9(suppl 1): 32±7. 3. Moreno A, Gatell JM; Mensa J et al. Incidencia de enteropatoÂgenos en pacientes con infeccioÂn por el virus de la inmunodeficiencia humana. Med Clin (Barc) 1994; 102: 205±8. 4. Hickey MM, Shanson DC. Septicaemia in patients with and without AIDS at Westminster Hospital, London. J Infect 1993; 27: 243±50.
ß 2003 Copyright by the European Society of Clinical Microbiology and Infectious Diseases, CMI, 9, 1261±1263
Correspondence 1263
5. Cohen JL, Bartlett JA, Corey GR. Extra-intestinal manifestations of Salmonella infections. Medicine 1987; 66: 349±88. 6. Canut A, Brezmes MF, Antolin MI, YaguÈe A, Arribas A. Infecciones focales por Salmonella no typhi: revisioÂn de nuestra casuõÂstica y comparacioÂn con otras series. Rev Clin Esp 1992; 191: 71±5. 7. Perera CU, Luo NP, Zumla A. Bacteraemias in HIVpositive patients. Lancet 1990; 336: 877±8. 8. Kiuchi K, Endo T, Nejima J et al. Purulent pericarditis with tamponade caused by Salmonella enteritidis. Jpn Circul J 1998; 62: 139±41. 9. Nelson MR, Shanson DC, Hawkins DA, Gazzard BG. Salmonella, Campylobacter and Shigella in HIVseropositive patients. AIDS 1992; 6: 1495±8. 10. Fica AE, Horowitz HW, Lior H, Cabello FC. Demonstration of persistence of Salmonella typhimurium in an AIDS patient by molecular methods. J Clin Mibrobiol 1994; 32: 2327±30. 11. Rerkpattanapipat P, Wongpraparut N, Jacobs LE, Kotler MN. Cardiac manifestations of acquired immunodeficiency syndrome. Arch Intern Med 2000; 160: 602±8. 12. Chen Y, Brennessel D, Walters J, Johnson M, Rosner F, Raza M. Human immunodeficiency virus-associated pericardial effusion. Report of 40 cases and review of the literature. Am Heart J 1999; 137: 516±21. 13. Heidenreich PA, Eisemberg MJ, Kee LL et al. Pericardial effusion in AIDS: incidence and survival. Circulation 1995; 92: 3229±34.
14. Scerpella EG, Fatmi AA, Brito; MA. Bacterial pericarditis and cardiac tamponade in patients infected with human immunodeficiency virus type I: case report and review. Clin Infect Dis 1995; 21: 1518±19. 15. Ramos JM, FernaÂndez Guerrero ML. Salmonelosis no tifoidea e infeccioÂn por el virus de la inmunodeficiencia humana. Med Clin (Barc) 1997; 108: 349±55. 16. Casado J, Valdezate S, Caleron C et al. Zidovudine therapy protects against Salmonella bacteremia recurrence in HIV-infected patients. J Infect Dis 1999; 179: 1553±6. 17. Mayer KH, Hanson E. Recurrent Salmonella infection with a single strain in the acquired immunodeficiency syndrome. Confirmation by plasmid finger printing. Diagn Microbiol Infect Dis 1986; 4: 71±6. 18. Aguado; JM, Obeso G, Cabanillas JJ, Fernandez Guerrero ML, AleÂs J. Pleuropulmonay infections due to nontyphoid strains of Salmonella. Arch Intern Med 1990; 150: 54±6. 19. Roca V, GarcõÂa-Aguado C, PeÂrez-Cecilia E, Romero J, GonzaÂlez-Lahoz JM, Picazo JJ. Ciprofloxacin: results of treatment and prevention of relapses of Salmonella spp bacteremia in HIV-infected patients [abstract 35]. In: 32nd Interscience Conference on Antimicrobial Agents and Chemotherapy (ICAAC). Anaheim, CA: American Society for Microbiology, 1992: 14 (oral communication). 20. Hohmann EL. Nontyphoidal Salmonellosis. Clin Infect Dis 2001; 32: 263±9.
ß 2003 Copyright by the European Society of Clinical Microbiology and Infectious Diseases, CMI, 9, 1261±1263