Journal of Infection (t99o) zo, 231-236
CASE REPORTS Metastatic pneumococcal endophthalmitis: report of two cases and review of literature John S. Cheesbrough,* Craig L. Williams,* Rana R u s t o m , t Roger C. Bucknallt and Roger B. T r i m b l e ,
* Departments of Microbiology and ~fRheumatology, Royal Liverpool Hospital and ~ St Paul's Eye Hospital, Liverpool, U.K. Accepted for publication 29 December I989 Summary Two patients with pneumococcal bacteraemia complicated by endophthalmitis are described. While this condition appears to have been relatively common in the preantibiotic era, a review of the literature since I95O only identified six additional case reports. Analysis of these eight cases reveals two patterns: unilateral disease in six patients and bilateral disease with simultaneous onset in two patients. The potential pathogenic mechanisms- direct bacterial invasion or immunologically mediated processes- are discussed in relation to these clinical presentations. The critical importance of seeking ophthalmological advice early in the course of the disease is emphasised, as the risk of visual loss with systemic antimicrobials alone is very high, particularly if the infective process involves the vitreous humour.
Introduction Bacterial endophthalmitis is a devastating disease of the eye frequently resulting in loss of useful vision. Early diagnosis and adequate t r e a t m e n t are essential if the eye is to be saved, t T h e diagnosis is usually reached quickly w h e n features of intra-ocular inflammation follow penetrating injury or surgery to the eye. If, however, infection is secondary to bacteraemia the diagnosis m a y not be initially considered and the ocular s y m p t o m s m a y be incorrectly attributed to another cause. We report two cases of endophthalmitis secondary to pneumococcal bacteraemia.
Case reports Case
1
A 64-year-old male A f r o - C a r i b b e a n presented with a I-week history of rigors and myalgia and a I - d a y history of pain in the left eye and right hand. O n examination, he was pyrexial with a temperature of 38"5 °C. T h e proximal and distal interphalangeal joints of the right little finger were red, swollen and ~: Address for correspondence: J. S. Cheesbrough, Department of Medical Microbiology, Duncan Building, Royal Liverpool Hospital, P.O. Box I47, Liverpool L69 3BX, U.K. oi63-4453/9o/o3o23I +o6 $o2.oo/o
© r99o The British Society for the Study of Infection
232
J. S. CHEESBROUGH E T A L .
tender. Rales were present at the left base. T h e left eye was red with an irregular constricted pupil. T h e red reflex was decreased but visual acuity normal. A clinical diagnosis of septicaemia, respiratory infection and possible septic arthritis with septic embolism to the left eye was made. There were no cardiac m u r m u r s or cutaneous manifestations of endocarditis. Haematological investigation revealed a WBC of 2o × lO9/1 (with 75 % neutrophils), an E S R of 87 m m / h and a negative sickle-cell test. T h e chest X-ray showed slight shadowing in the left lower zone. Blood cultures grew Streptococcus pneumoniae. Aspiration of the involved joints yielded no growth. T r e a t m e n t was commenced with intravenous ampicillin 5 o o m g and erythromycin 500 mg, both given intravenously 6-hourly, and switched to benzylpenicillin 3 M U 6-hourly after the blood culture result was known. While his general condition improved and the p n e u m o n i a and arthritis resolved there was a rapid deterioration in vision of the left eye with progressive panophthalmitis. He remains blind in this eye but otherwise well at follow-up 6 m o n t h s later. Case 2
A 47-year-old Caucasian female was admitted with a 2-day history of nausea, vomiting, headache and photophobia. In I98I a diagnosis of systemic lupus erythematosus had been made, and in I983 she had required a splenectomy for an associated haemolytic anaemia. In I986 she was found to have nephrotic syndrome with active lupus, despite maintenance on prednisolone 40 mg daily. On examination she was febrile, with a temperature of 39"5 °C, and had a widespread purpuric rash and marked neck stiffness. Haematological studies confirmed disseminated intravascular coagulation and cerebrospinal fluid examination revealed a WBC count of 217 m m 3 (90% neutrophils) and numerous Gram-positive diplococci. Benzylpenicillin 4 M U 4-hourly by vein was commenced. Blood and C S F cultures grew Streptococcus pneumoniae. T w o days after admission her vision became grossly impaired. An ophthalmic opinion was sought and a diagnosis of severe bilateral anterior iridocyclitis without involvement of the posterior segment was made. She was treated with local steroids (Bemosol drops 2-hourly) and atropine eye drops. Her vision progressively improved over the next ro weeks and on follow-up 9 m o n t h s later she has normal visual acuity. Discussion
Metastatic bacterial endophthalmitis appears to have been relatively c o m m o n in the pre-antibiotic era. An extensive review published in I9232 cites 342 cases; the disease was bilateral in IO9 and bacteria were isolated in I I9 cases. Beta-haemolytic streptococci and pneumococci were the most frequent pathogens. In reports from more recent literature Gram-negative organisms and yeasts have predominated. 3'~ T h e risk of endophthalmitis per episode of bacteraemia is unknown. Axenfeld (cited in Seguini) z estimated that 3"5% of patients with postpuerperal sepsis developed endophthalmitis prior to the availability of antimicrobial agents. In I98I Henderson et al. 4 reported finding candida
Metastatic Pneumococcal Endophthalmitis
z33
endophthalmitis in 9"9 % of I3I patients receiving total parenteral nutrition. T h e incidence among patients with pneumococcaemia is uncertain but clearly very low; there were no cases recorded among 1377 patients with pneumococcal bacteraemia recorded in four series compiled during the antibiotic era. 5-s A search of the literature since I95o has revealed only six cases of metastatic pneumococcal endophthalmitis. 9-1a T h e salient features of these and the current cases are summarised in the table. T w o of the six patients died from pneumoccoccal disease involving other organs and in one endophthalmitis was only observed immediately before death. Intra-ocular cultures were negative in all six patients in which they were obtained but in every case the cultures were only taken after the administration of beta-lactam antibiotics. Good residual vision was retained only in those patients without posterior segment involvement. Reports from the I93os invariably culminated in surgical enucleation of the infected eye which persistently yielded pneumococci on culture. TM 1~ Inspection of the Table shows that other extra-pulmonary loci of infection frequently co-exist with endophthalmitis (Table I). T h r e e patients had had prior splenectomy and two of these (cases 6 and 8) had bacteraemia associated with disseminated intravascular coagulation. It is interesting that both of these patients had bilateral endophthalmitis of simultaneous onset while the remainder had unilateral disease. This raises the possibility that different pathogenic mechanisms may be operating in bilateral and unilateral disease. If it is assumed that metastatic endophthalmitis is a consequence of infective embolism in the ocular vessels it may be reasonable to expect a greater chance of bilateral disease in patients with the high-grade bacteiaemia characteristic of post-splenectomy pneumococcaemia. Alternatively, it may be that only in the asplenic patient will capsular polysaccharide, or some other soluble component of the pneumococcus, reach a sufficiently high plasma concentration to provoke an inflammatory response in the aqueous humour without the local presence of viable organisms. I m m u n e complexes, which can be demonstrated in many cases of pneumococcal disease 16 and have occasionally been implicated as a cause of post-pneumonic glomerulonephritis, ~7 may also play a role. Walker and Fenwick implicated pathogenic mechanisms of this nature in a case of bilateral endophthalmitis related to Lancefield Group A beta-haemolytic streptococcal bacteraemia. 18 Our second patient did not develop endophthalmitis until 3 days after the start of effective chemotherapy. Although this would seem to fit with an immunologically mediated process, circulating immune complexes were not detected during the peak of her iritis. Since the nature of the initial eye symptoms is nonspecific the diagnosis depends upon having a high index of suspicion. T h e isolation of pneumococci from blood or a distant focus should alert the clinician and initiate a referral for an urgent ophthalmological opinion. While the diagnosis can only be made definitively by culture of intra-ocular material intravenous antimicrobial treatment should never be withheld while collection of such samples is arranged, as delay increases the risk of visual loss. T h e beta-lactam antimicrobials, generally accepted as the agents of choice in the treatment of pneumococcal disease, only reach adequate concentrations in
234
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M e t a s t a t i c Pneumococcal E n d o p h t h a l m i t i s
235
t h e a n t e r i o r c h a m b e r o f t h e e y e w h e n g i v e n i n t r a v e n o u s l y in h i g h doses. W h i l e p e r i o c u l a r i n j e c t i o n will i n c r e a s e t h e s e levels s u b s t a n t i a l l y , n e i t h e r r o u t e will e n s u r e reliable c o n c e n t r a t i o n s in t h e v i t r e o u s . 19 C h l o r a m p h e n i c o l a n d t r i m e t h o p r i m c a n p e n e t r a t e t h e v i t r e o u s b e t t e r , b u t lack t h e r a p i d b a c t e r i o c i d a l a c t i v i t y o f t h e b e t a - l a c t a m s . 19 I n v i e w o f this t h e m a n a g e m e n t o f v i t r e o u s i n f e c t i o n m u s t at least i n c l u d e d i r e c t i n t r a - v i t r e a l i n j e c t i o n o f a n a n t i m i c r o b i a l ( p e n i c i l l i n in p n e u m o c o c c a l disease), a n d m a n y o p h t h a l m o l o g i s t s w o u l d recommend immediate vitrectomy. T h e b e n e f i c i a l role o f s t e r o i d s in this c o n d i t i o n is u n c e r t a i n . C l e a r l y t h e y s h o u l d o n l y b e u s e d in c o n j u n c t i o n w i t h a d e q u a t e a n t i m i c r o b i a l t r e a t m e n t . I n bilateral disease with simultaneous onset which may be immunologically mediated they may be particularly useful. (We thank Mrs Pauline Olsen for secretarial support.)
References
i. Forster RK, Zachary IG, Cottingham AJ, Norton EWD. Further observations on the diagnosis, cause, and treatment of endophthalmitis. Am J Ophthalmol I976; 8I: 52-56. 2. Seguini A. Corodite meastatica. Annali di Ottalmologiae cliniea occulistica I923; 7: 3oi-393 • 3. Liu YC, Cheng DL, Liu CL. Klebsiella pnemoniae. Liver abscess associated with septic endophthalmitis. Arch Intern Med I986; x46: I913-I916. 4. Henderson DK, Edwards JE, Montgomery JZ. Hematogenous Candida endophthalmitis in patients receiving parenteral hyperalimentation fluids. J Infect Dis I98I ; 143 : 655-66I. 5. Austrian R, Gold J. Pneumococcal bacteraemia with especial reference to bacteraemic pneumococcal pneumonia. Ann Intern Nled i964; 6o: 759-776. 6. Gruer LD, McKendrick MW, Geddes AM. Pneumococcal bacteraemia: a continuing challenge. Q J Med i984; zio: 259---270. 7. Gramsden WR, Eyken SJ, Phillips I. Pneumoccal bacteraemia: 325 episodes diagnosed at St Thomas's Hospital. Br Med J (Clin Res) I985; 290: 5o5-508. 8. Burman LA, Norrby R, Trollfors B. Invasive pneumococcal infection; incidence, predisposing factors, and prognosis. Rev Infect Dis I985 ; 7: I33-I42. 9. Almeda EM. Metastatic pneumococcal endophthalmitis. Am J Ophthalmol I96o; 49: 353-355. Io. Macoul KL. Pneumococcal septicaemia presenting as a hypopyon. Arch Ophthalmol I968 ; 8, : I44-I45. i i. Jarret WH, Wells JA, Hyman BN. Metastatic endophthalmitis : A report of three cases in proven septicaemia. South Med J I97I ; 64 : I94-I98. i2. Gregg CR, Tucker WS. Acute endogenous endophthalmitis after splenectomy..7 Tenn Med Assoc I985; 78: 25--26. I3. Farber BP, Weinbaum DL, Dummen JS. Metastatic bacterial endophthalmitis. Arch Intern Med I985 ; I45: 62-64. I4. Lawson LJ. Metastatic panophthalmitis following pneumococcic otitis media, f f A M A I933 ; , o r : 599. I5. MeKee SH. Metastatic ophthalmia in a patient with pneumonia : Bacteriologic observations. Am J Ophthalmol I935; I8: II45-II46. I6. Mellencamp MA, Preheim LC, McDonald TL. Isolation and characterization of circulating immune complexes from patients with pneumococcal pneumonia. Infect Immun r987; 55: I737-I742. r 7. Rytel MW, Dee T H , Ferstenfeld JE et al. Possible pathogenic role of capsular antigens in fulminant pneumococcal disease with disseminated intravascular coagulation (DIC). Am J Med I974; 57: 889-898.
236
J. s. CHEESBROUGH E T A L .
I8. Walker CB, Fenwick P. Bilateral fulminating endophthalmitis with streptococal septicaemia. Br ff Ophthalmol 1962; 46: 281-284. I9. Barza M. Treatment of bacterial infections ofthe eye. In: Remington JS, Swartz MN, Eds. Current clinical topics in infectious disease z. New York: McGraw-Hill, I98O: 158-194.
CASE REPORTS Metastatic pneumococcal endophthalmitis: report of two cases and review of literature John S. Cheesbrough,* Craig L. Williams,* Rana R u s t o m , t Roger C. Bucknallt and Roger B. T r i m b l e ,
* Departments of Microbiology and ~fRheumatology, Royal Liverpool Hospital and ~ St Paul's Eye Hospital, Liverpool, U.K. Accepted for publication 29 December I989 Summary Two patients with pneumococcal bacteraemia complicated by endophthalmitis are described. While this condition appears to have been relatively common in the preantibiotic era, a review of the literature since I95O only identified six additional case reports. Analysis of these eight cases reveals two patterns: unilateral disease in six patients and bilateral disease with simultaneous onset in two patients. The potential pathogenic mechanisms- direct bacterial invasion or immunologically mediated processes- are discussed in relation to these clinical presentations. The critical importance of seeking ophthalmological advice early in the course of the disease is emphasised, as the risk of visual loss with systemic antimicrobials alone is very high, particularly if the infective process involves the vitreous humour.
Introduction Bacterial endophthalmitis is a devastating disease of the eye frequently resulting in loss of useful vision. Early diagnosis and adequate t r e a t m e n t are essential if the eye is to be saved, t T h e diagnosis is usually reached quickly w h e n features of intra-ocular inflammation follow penetrating injury or surgery to the eye. If, however, infection is secondary to bacteraemia the diagnosis m a y not be initially considered and the ocular s y m p t o m s m a y be incorrectly attributed to another cause. We report two cases of endophthalmitis secondary to pneumococcal bacteraemia.
Case reports Case
1
A 64-year-old male A f r o - C a r i b b e a n presented with a I-week history of rigors and myalgia and a I - d a y history of pain in the left eye and right hand. O n examination, he was pyrexial with a temperature of 38"5 °C. T h e proximal and distal interphalangeal joints of the right little finger were red, swollen and ~: Address for correspondence: J. S. Cheesbrough, Department of Medical Microbiology, Duncan Building, Royal Liverpool Hospital, P.O. Box I47, Liverpool L69 3BX, U.K. oi63-4453/9o/o3o23I +o6 $o2.oo/o
© r99o The British Society for the Study of Infection
232
J. S. CHEESBROUGH E T A L .
tender. Rales were present at the left base. T h e left eye was red with an irregular constricted pupil. T h e red reflex was decreased but visual acuity normal. A clinical diagnosis of septicaemia, respiratory infection and possible septic arthritis with septic embolism to the left eye was made. There were no cardiac m u r m u r s or cutaneous manifestations of endocarditis. Haematological investigation revealed a WBC of 2o × lO9/1 (with 75 % neutrophils), an E S R of 87 m m / h and a negative sickle-cell test. T h e chest X-ray showed slight shadowing in the left lower zone. Blood cultures grew Streptococcus pneumoniae. Aspiration of the involved joints yielded no growth. T r e a t m e n t was commenced with intravenous ampicillin 5 o o m g and erythromycin 500 mg, both given intravenously 6-hourly, and switched to benzylpenicillin 3 M U 6-hourly after the blood culture result was known. While his general condition improved and the p n e u m o n i a and arthritis resolved there was a rapid deterioration in vision of the left eye with progressive panophthalmitis. He remains blind in this eye but otherwise well at follow-up 6 m o n t h s later. Case 2
A 47-year-old Caucasian female was admitted with a 2-day history of nausea, vomiting, headache and photophobia. In I98I a diagnosis of systemic lupus erythematosus had been made, and in I983 she had required a splenectomy for an associated haemolytic anaemia. In I986 she was found to have nephrotic syndrome with active lupus, despite maintenance on prednisolone 40 mg daily. On examination she was febrile, with a temperature of 39"5 °C, and had a widespread purpuric rash and marked neck stiffness. Haematological studies confirmed disseminated intravascular coagulation and cerebrospinal fluid examination revealed a WBC count of 217 m m 3 (90% neutrophils) and numerous Gram-positive diplococci. Benzylpenicillin 4 M U 4-hourly by vein was commenced. Blood and C S F cultures grew Streptococcus pneumoniae. T w o days after admission her vision became grossly impaired. An ophthalmic opinion was sought and a diagnosis of severe bilateral anterior iridocyclitis without involvement of the posterior segment was made. She was treated with local steroids (Bemosol drops 2-hourly) and atropine eye drops. Her vision progressively improved over the next ro weeks and on follow-up 9 m o n t h s later she has normal visual acuity. Discussion
Metastatic bacterial endophthalmitis appears to have been relatively c o m m o n in the pre-antibiotic era. An extensive review published in I9232 cites 342 cases; the disease was bilateral in IO9 and bacteria were isolated in I I9 cases. Beta-haemolytic streptococci and pneumococci were the most frequent pathogens. In reports from more recent literature Gram-negative organisms and yeasts have predominated. 3'~ T h e risk of endophthalmitis per episode of bacteraemia is unknown. Axenfeld (cited in Seguini) z estimated that 3"5% of patients with postpuerperal sepsis developed endophthalmitis prior to the availability of antimicrobial agents. In I98I Henderson et al. 4 reported finding candida
Metastatic Pneumococcal Endophthalmitis
z33
endophthalmitis in 9"9 % of I3I patients receiving total parenteral nutrition. T h e incidence among patients with pneumococcaemia is uncertain but clearly very low; there were no cases recorded among 1377 patients with pneumococcal bacteraemia recorded in four series compiled during the antibiotic era. 5-s A search of the literature since I95o has revealed only six cases of metastatic pneumococcal endophthalmitis. 9-1a T h e salient features of these and the current cases are summarised in the table. T w o of the six patients died from pneumoccoccal disease involving other organs and in one endophthalmitis was only observed immediately before death. Intra-ocular cultures were negative in all six patients in which they were obtained but in every case the cultures were only taken after the administration of beta-lactam antibiotics. Good residual vision was retained only in those patients without posterior segment involvement. Reports from the I93os invariably culminated in surgical enucleation of the infected eye which persistently yielded pneumococci on culture. TM 1~ Inspection of the Table shows that other extra-pulmonary loci of infection frequently co-exist with endophthalmitis (Table I). T h r e e patients had had prior splenectomy and two of these (cases 6 and 8) had bacteraemia associated with disseminated intravascular coagulation. It is interesting that both of these patients had bilateral endophthalmitis of simultaneous onset while the remainder had unilateral disease. This raises the possibility that different pathogenic mechanisms may be operating in bilateral and unilateral disease. If it is assumed that metastatic endophthalmitis is a consequence of infective embolism in the ocular vessels it may be reasonable to expect a greater chance of bilateral disease in patients with the high-grade bacteiaemia characteristic of post-splenectomy pneumococcaemia. Alternatively, it may be that only in the asplenic patient will capsular polysaccharide, or some other soluble component of the pneumococcus, reach a sufficiently high plasma concentration to provoke an inflammatory response in the aqueous humour without the local presence of viable organisms. I m m u n e complexes, which can be demonstrated in many cases of pneumococcal disease 16 and have occasionally been implicated as a cause of post-pneumonic glomerulonephritis, ~7 may also play a role. Walker and Fenwick implicated pathogenic mechanisms of this nature in a case of bilateral endophthalmitis related to Lancefield Group A beta-haemolytic streptococcal bacteraemia. 18 Our second patient did not develop endophthalmitis until 3 days after the start of effective chemotherapy. Although this would seem to fit with an immunologically mediated process, circulating immune complexes were not detected during the peak of her iritis. Since the nature of the initial eye symptoms is nonspecific the diagnosis depends upon having a high index of suspicion. T h e isolation of pneumococci from blood or a distant focus should alert the clinician and initiate a referral for an urgent ophthalmological opinion. While the diagnosis can only be made definitively by culture of intra-ocular material intravenous antimicrobial treatment should never be withheld while collection of such samples is arranged, as delay increases the risk of visual loss. T h e beta-lactam antimicrobials, generally accepted as the agents of choice in the treatment of pneumococcal disease, only reach adequate concentrations in
234
J . s . CHEESBROUGH
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M e t a s t a t i c Pneumococcal E n d o p h t h a l m i t i s
235
t h e a n t e r i o r c h a m b e r o f t h e e y e w h e n g i v e n i n t r a v e n o u s l y in h i g h doses. W h i l e p e r i o c u l a r i n j e c t i o n will i n c r e a s e t h e s e levels s u b s t a n t i a l l y , n e i t h e r r o u t e will e n s u r e reliable c o n c e n t r a t i o n s in t h e v i t r e o u s . 19 C h l o r a m p h e n i c o l a n d t r i m e t h o p r i m c a n p e n e t r a t e t h e v i t r e o u s b e t t e r , b u t lack t h e r a p i d b a c t e r i o c i d a l a c t i v i t y o f t h e b e t a - l a c t a m s . 19 I n v i e w o f this t h e m a n a g e m e n t o f v i t r e o u s i n f e c t i o n m u s t at least i n c l u d e d i r e c t i n t r a - v i t r e a l i n j e c t i o n o f a n a n t i m i c r o b i a l ( p e n i c i l l i n in p n e u m o c o c c a l disease), a n d m a n y o p h t h a l m o l o g i s t s w o u l d recommend immediate vitrectomy. T h e b e n e f i c i a l role o f s t e r o i d s in this c o n d i t i o n is u n c e r t a i n . C l e a r l y t h e y s h o u l d o n l y b e u s e d in c o n j u n c t i o n w i t h a d e q u a t e a n t i m i c r o b i a l t r e a t m e n t . I n bilateral disease with simultaneous onset which may be immunologically mediated they may be particularly useful. (We thank Mrs Pauline Olsen for secretarial support.)
References
i. Forster RK, Zachary IG, Cottingham AJ, Norton EWD. Further observations on the diagnosis, cause, and treatment of endophthalmitis. Am J Ophthalmol I976; 8I: 52-56. 2. Seguini A. Corodite meastatica. Annali di Ottalmologiae cliniea occulistica I923; 7: 3oi-393 • 3. Liu YC, Cheng DL, Liu CL. Klebsiella pnemoniae. Liver abscess associated with septic endophthalmitis. Arch Intern Med I986; x46: I913-I916. 4. Henderson DK, Edwards JE, Montgomery JZ. Hematogenous Candida endophthalmitis in patients receiving parenteral hyperalimentation fluids. J Infect Dis I98I ; 143 : 655-66I. 5. Austrian R, Gold J. Pneumococcal bacteraemia with especial reference to bacteraemic pneumococcal pneumonia. Ann Intern Nled i964; 6o: 759-776. 6. Gruer LD, McKendrick MW, Geddes AM. Pneumococcal bacteraemia: a continuing challenge. Q J Med i984; zio: 259---270. 7. Gramsden WR, Eyken SJ, Phillips I. Pneumoccal bacteraemia: 325 episodes diagnosed at St Thomas's Hospital. Br Med J (Clin Res) I985; 290: 5o5-508. 8. Burman LA, Norrby R, Trollfors B. Invasive pneumococcal infection; incidence, predisposing factors, and prognosis. Rev Infect Dis I985 ; 7: I33-I42. 9. Almeda EM. Metastatic pneumococcal endophthalmitis. Am J Ophthalmol I96o; 49: 353-355. Io. Macoul KL. Pneumococcal septicaemia presenting as a hypopyon. Arch Ophthalmol I968 ; 8, : I44-I45. i i. Jarret WH, Wells JA, Hyman BN. Metastatic endophthalmitis : A report of three cases in proven septicaemia. South Med J I97I ; 64 : I94-I98. i2. Gregg CR, Tucker WS. Acute endogenous endophthalmitis after splenectomy..7 Tenn Med Assoc I985; 78: 25--26. I3. Farber BP, Weinbaum DL, Dummen JS. Metastatic bacterial endophthalmitis. Arch Intern Med I985 ; I45: 62-64. I4. Lawson LJ. Metastatic panophthalmitis following pneumococcic otitis media, f f A M A I933 ; , o r : 599. I5. MeKee SH. Metastatic ophthalmia in a patient with pneumonia : Bacteriologic observations. Am J Ophthalmol I935; I8: II45-II46. I6. Mellencamp MA, Preheim LC, McDonald TL. Isolation and characterization of circulating immune complexes from patients with pneumococcal pneumonia. Infect Immun r987; 55: I737-I742. r 7. Rytel MW, Dee T H , Ferstenfeld JE et al. Possible pathogenic role of capsular antigens in fulminant pneumococcal disease with disseminated intravascular coagulation (DIC). Am J Med I974; 57: 889-898.
236
J. s. CHEESBROUGH E T A L .
I8. Walker CB, Fenwick P. Bilateral fulminating endophthalmitis with streptococal septicaemia. Br ff Ophthalmol 1962; 46: 281-284. I9. Barza M. Treatment of bacterial infections ofthe eye. In: Remington JS, Swartz MN, Eds. Current clinical topics in infectious disease z. New York: McGraw-Hill, I98O: 158-194.
