Infections Due to Group C Streptococci in Man

DAVID N. MOHR, M.D. DONALD 1. FEIST, M.D. JOHN A. WASHINGTON

II, M.D.

PAUL E. HERMANS. M.D. Rochester, Minnesota

Although a common cause of infection in animals, group C streptococci are rarely noted to he pathogenic in man. A total of 150,000 blood cultures obtained at the Mayo Clinic fkom 1968 to 1977 revealed group C streptococci. in only eight patients. Acute bacterial endocarditis, meningitis, pneumonia, cellulitis and bacteremia due to group C streptococci are described in a host who had undergone immunosuppression (immunosuppressed host), and the relatively few cases previously reported are reviewed. Although severe, these infections may respond favorably to penicillin therapy. Endocarditis caused by group D streptococci is acute and destructive, and associated with early cardiac decompensation. The manifestations of cellulitis and pneumonia are similar to those when group A streptococci are causative organisms. Meningitis due to group C streptococci is acute and severe, and responds slowly to antimicrobial therapy. Colonization also occurs. Streptococci of Lancefield’s group C are a common cause of infections in animals, including mastitis in cows, lymphadenitis in guinea pigs [1,2], jaw abscesses in swine [l] and equine strangles. It is not widely appreciated that group C streptococci can be the cause of serious infections in man. From 1968 to 1977, approximately 150,000 blood cultures were obtained at the Mayo Clinic, and eight patients were identified whose blood cultures yielded group C streptococci. Clinical and microbiologic features of these patients are provided. METHODS AND MATERIALS Case 1 (Bacterial Endocarditisj

From the Mavo Clinic and Mavo Foundation, Rochester, Minnesota. Requesis for reprints should be addressed to Dr. D. N. Mohr. c/o Section of Publications, Mayo Clinic, 200 First Street SW, Rochester, Minnesota 55901. Manuscript accepted September 27,1978,

450

A 70 year old farmer was evaluated in 1976 for bacterial endocarditis. Murmurs of aortic stenosis and insufficiency had been present since 1958. Two weeks before admission, the patient punctured a finger with a thorn. At the wound site, a small abscess subsequently drained. Three days before admission, he had nausea an,d shaking chills with a temperature of 39.4 OC. He was hospitalized: his leukocyte count was 27.600 cells/mm3. Two blood cultures were obtained, and ampicillin was given orally. with resolution of the fever within 24 hours. The patient was then referred to our clinic. He had a labial herpetic vesicle and one small conjunctival hemorrhage. The blood pressure was 138/90 mm Hg. the pulse rate 9O/min and the respiwere .ratory . rate 20/min. Murmurs of aortic stenosis and insufficiency heard. The hemoglobin was 13.7 g/d1 and the leukocyte count li’,ooO cells/mms with 84.5 per cent neutrophils, 9.5 per cent lymphocytes and 6 per cent monocytes. Results of 12 chemical tests were normal except for a slightly elevated glutamiboxaloacetic transaminase value (SGOT) of 28 U/liter.

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Antibiotic therapy was discontinued for 36 hours, three blood cultures were obtained, and the finger abscess was cultured. The fever recurred, and treatment was begun with 20 million IJ of aqueous penicillin intravenously per 24 hours. The blood cultures obtained at the local hospital and our three grew group C streptococci. Minimal inhibitory concentrations were penicillin 0.1pg/ml. cephalothin 1 pg/ml, ampicillin 1 Mg/ml, chloramphenicol 5 pg/ml and clindamycin 1 gg/ml. The finger abscess culture grew Staphylococcus aureus. The patient defervesced by the fourth hospital day. On the fifth day, he suffered seizures associated with a third-degree atrioventricular block, which came under control with a permanent epicardial pacemaker. The intravenous use of penicillin was continued. Oxacillin was added as prophylaxis, 1 g every 4 hours intravenously for four days, before and after insertion of the pacemaker. On the 12th day, progressively severe heart failure developed. On the 24th day, the aortic valve was replaced by a Hancock valve prosthesis. Fibrous thickening of the aortic valve, fenestration of the noncoronary cusp and excavation into the membranous septum were noted. Cultures of material from the valve were negative. Penicillin G was given for six days after the procedure. Endocarditis did not recur during a follow-up period of one year. Case 2 (Cellulitis in Lymphedematous Arm). A 68 year old white woman was hospitalized in 1969 because of celhtlitis gradually involving the entire left arm and upper chest wall. In 1966, a left radical mastectomy had been performed for scirrhous adenocarcinoma. In 1968, a locally recurrent carcinoma was treated with radiation. Medications at the time of admission were hydrocortisone, 30 mg, and warfarin, 2.5 mg a day. The patient was moderately obese with a temperature of 39.2 “C. There was lymphedema of the left arm with swelling and erythema of the wrist, forearm, shoulder and anterior portion of the chest. Two blood cultures obtained on admission grew group C streptococci. Minimal inhibitory concentrations were penicillin 1.0 pg/ml, erythromycin 0.5 pg/ml, cephalothin 1 pg/ml. chloramphenicol 5 rg/ml and lincomycin 0.1 kg/ml. The hemoglobin level was 13.7 g/dl. The leukocyte count was 18,200 cells/mm3 with 92.5 per cent polymorphonuclear leukocytes, 6.5 per cent lymphocytes and 1 per cent monocytes. The patient was treated for seven days with 1 g of ampicillin intramuscularly every 6 hours rather than penicillin G because of a simultaneous asymptomatic gram-negative bacillary urinary tract infection. She defervesced on the third day, at which time blood cultures were pegative. The inflammation was diminished at dismissal. Cellulitis did not recur during a follow-up period of three months. Case 3 (Pneumonia). A 39 year old white man was hospitalized in 1977. He had had shaking chills, fever and malaise for 10 days, right-sided pleuritic pain and brown, occasionally blood-streaked, sputum for three days, and increasing dyspnea. He has been a smoker for 20 years and had had bronchitis. The patient was dehydrated, with a pulse rate of 12O/min, a respiration rate of 40/min and a temperature of 39.3 OC. Decreased breath sounds at the bases of both lungs with coarse rales at the base of the right lung were heard. A roentgenogram of the chest showed bilateral pulmonary infiltrates. The leukocyte count was 25,800 cells/mm3 with 83 per cent polymorphonuclear leukocytes, 10.5 per cent lym-

C STREPTOCOCCI

INFECTIONS

IN MAN-- ILIOHR ET AL

phocytes and 6.5 per cent monocytes. The plasma ghlcose was 148 mg/dl, serum creatinine 1.4 mg/dl, SGOT 24 U/liter and alkaline phosphatase 252 U/liter. Three blood cultures on admission grew group C streptococci. Agram stain of sputum showed gram-positive cocci. A sputum cultme grew nongroup A beta hemolytic streptococci. Treatment consisted of 20 million U of aqueous penicillin intravenously during the first 24 hours and, for the next four days, 600,000 U of procaine penicillin intramuscularly every 6 hours. This was changed to 500 mg of erythromycin orally every 6 hours because of a skin rash. The fever continued and a right pleural effusion developed. On the eighth hospitalday, erythromycin was replaced by cephalothin, 1.5 g intravenously every 6 hours, increased after six days to 2 g every 4 hours, and continued for 12 days. The patient became afebrile and less dyspneic. The pleural effusion and the infiltrate in the right lung began to resolve, revealing cavitation. Ccphalexin, 500 mg four times a day, was given for 10 days after dismissal on the 27th day. An increase in the alkaline phosphatase to 403 U/liter with normal SCOT remains unexplained. One week after dismissal and six weeks later, chest roentgenograms showed continued slow resolution. Case 4 (Bacteremia in Acute Myelomonocytic Leukemia). A 59 year old man was hospitalized in 1971 for treatment of acute myelomonocytic leukemia discovered 11 months earlier but for which chemotherapy was not required until his hospitalization. Examination revealed only pallor and slight enlargement of the tonsils. Temperature was normal. He was treated with lomustine (CeeNU@) for one day and cytosine arabinosidc for five days. A brief febrile episode attributed to tonsillitis was treated successfully with oral penicillin for three days. One week later, the chemotherapy schedule was repeated. The patient’s condition deteriorated, and fever developed on the 19th day of hospitalization. On that day, a leukocyte count was 600 cells/mm3, and blood cultures were obtained. Two of these grew Escherichia coli and one grew a mixture of Esch. coli and group C streptococci. At the onset of the fever, the administration of gentamicin, 70 mg intravenously every 8 hours, and cephalothin, 1 g intravenously every 6 hours, was begun. The temperature never abated, and the patient died on the 23rd hospital day. No definite source of the infection was found. Case 5 (Bacteremia in Acute Myelomonocytic Leukemia). A 16 year old boy with acute myelomonocytic leukemia in remission presented in 1976 with a one week history of fever. Protocol chemotherapy with 5-azacytodine had been completed two weeks before admission. On admission, he was pale, lethargic and depressed. Temperature was 40%. There were numerous small abscesses on the left side of his face, and vesicles on the tongue and lips, a few enlarged servical nodes, and moist rales at the base of the left lung. A roentgenogram demonstrated bilateral, ill-defined pulmonary nodular densities, which disappeared eight days later. The hemoglobin level was 7.1 g/d1 and the leukocyte count l,000/mm3 with 5 per cent neutrophils, 92 per cent lymphocytes and 3 per cent monocytes. The patient was treated with oxacillin, 2 g intravenously every 6 hours, and gentamicin, 40 mg intravenously every 8 hours. A throat culture grew nongroup A beta hemolytic streptococci. Two blood cultures and a nasal culture obtained at admission grew group C strepto-

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451

Norm

19 (1970)

F, 64

F, 74

None

14 (1966) Uncertain (systolic murmu)

Mitral

F. 28

V&s Nfsctsd

18 (1963)

SOX

Mftral

4

CXW

Rt

PstkokOlc

to lreairnsni frmWathg FsctOre

Died

not indicated) Fungating mitral Fever responded Unknown to 1V ampicillin vegatation with and IM strepto dastructicn of anterior cusp; mycin, but patient muitipie gross died 56 hours and microscopic after admission; infarcts in my-rpostmortem valdlum. kidneys, vuiar meningsai spleen and brain; cuttures positive earty focal areas for group c streptococci of meningitis: bronchcpnaunwnia

6 wk (dosage

Septic abortion Larga friable Sutfanilamkfes, with no complicated by vegetation on mitral valve; response of group C utceration and fever streptococcal bacteremia destruction of leaflets; rupture of chordae; rnyocardiai abscesses; renal and splenic infarction Nme Fever subsided Doubtfully FkCOVWed during 1st wk; significant penicillin 24 X septic abortton 1O6 U/24 hours 10 mo before IV for 3 wk: and symptoms streptomycin 1 developed gevery 12hour.s IM for 1 wk. foilowed by procaine penicillin 3X WUevery 4hoursiM for3wk Biiaterai purulent “Stormy course” Unknown “stormy and endophthaimitis while receiving ccnlpiicated penicillin and 6wk course,” causing blindness; (7) streptomycin, recovered subdural abscess approximately

Died, largs occluding saddle embolus at bifurcation of aorta

outcans

T

Patients With Group C Straptococcal Endocardttls Reported in the Literature

F, 28

I

10 (1940)

Rsfsrsscs

TABLE

Fsvm

Fever for 1 wk (6 wk of mild, iiidefinad symptoms)

Fever for 4 days

Fever and chills for 1 mo

Endocarditls detected in 3rd wk d hospitalization

04

rhmtbm

ApprorLnr(a

Conjunctival hemorrhages; Roth spots

i-ferpetic lip lesions: pneumcnitis associated at onset; CSF pieocytosis

streptococci

h9lllCiytiC

&ttive th&t cufture for &

Migratory arthritis fcrlrno.

Splenomagaly, conjunctival petechiae noted at autopsy

Ausciafsd

n v! r z 2

2 ‘t

n

Bicuspid aortic

None

AortiC M, 76 stenosis and aortic insuf% ciency

21 (1974)

21 (1974)

Present (Case 1)

Recovered

Died suddenly after initial improvement

Right cerebral hemisphere embofus or cerebritis

freeedge commissure between right and ~nc~o~~ cusp

Seizures; 2 mm vegetatii on ventricular surface of leaflets; 4 mm perforati~ at

Aortic

Mitral

0.5 g every 6 hours orally

day; changed to cephalexin

Trimethopeim 100 mg and sulfadiazine 500 ml IV every 6 hours for 36 hours, followed by oral cotrimoxazole; skin rash on 9th

septum

Heart failure; heart Good response to block: cardiac penicillin G, 20 valve fenestration X 10s U/24 with abscess in hours IV for 4wk membranous

Heart failure; vegetations on mitral valve, rupture of one of chordae; right parietal lobe abscess

cer&ospinal fluid.

Prosthetic valve implanted, recovered

Died, cardiac failure

Fever for 1 wk

Uncertain

Skin infection

Fever and chills for 3 days

Kicked by cow 17 Uncertain mo before, resulting in septic skin lesion; dental abscess 4 mo before onset of symptoms; pedal edema present for 1 yr before admission Profuse diarrhea “Short history of fever” and fever

Cephalothin with Scrotal infection kanamycin; with chronic penicillin (26 draining lesion days) combined fordyrasa with streptomycin result of and erythromycin; perforating then tetracycline, trauma gentamictn. nafcillin, dosages not indicated; temperature response on 20th day Penicillin 20 X lo6 Brief episode of U124 hours IV gastroenterltis for 8 wk; fever 2 wk before persisted 5 wk. onset of fever

Aortic? Well 12 mo Heart failure and Penicillin 20 X lo6 (infection renal failure at U/24 hours IV after excision with good initial of valve of fistula from su&MY; aneurysm of not sinus of response; anterior sinus described Valsalva and peritoneal of Valsalva, with analysis at surgery) closure of fistula to right opening ventricle

Mitral

Aortic

NOTE: lV = intravenously: IM = intramuscularly; CSF =

F, 65

M, 40

M, 43

Cardiac murmur for many years

21(1974)

M, 66

None

20 (l-.72)

Conjunctival hemorrhage: herpetic lip lesions

...

Extensive ecchymosis, left hemiplegia and homonymous hemianopia, microscopic hematuria Hepatosplenomega ly, ascites, edema; renal failure; low serum complement; proteinuria, cylindruria, and hematuria; hemorrhage of optic fundus

Splinter hemorrhage petechiae on soft palate

GROUP C STREPTOCOCCI INFECTIONS IN MAN-MOHR

cocci. Minimal

inhibitory

concentrations

were penicillin

ET AL.

0.1

fig/ml, erythromycin 0.1 @g/ml, cephalothin 1 #/ml, ampicillin I &ml. chloramphenicol5 pg/ml and clindamycin 1 pg/ml. Multiple units of blood and granulocytes were infused. After identification of the streptococci on the fourth hospital day, treatment was continued with penicillin intravenously, 2 million U every 6 hours, for 12 days. The fever resolved on the 12th day, and the patient was dismissed on the next day. There was no recurrence of infection during the ensuing year. Case 6 (Meningitis). A 59 year old man (previously described [a]) had severe meningitis due to group C streptococci without a known primary site of infection or underlying disease. He remained febrile and comatose for seven days before responding to treatment with 30 million U of penicillin given intravenously every 24 hours. Unilateral loss of hearing and vestibular function were the only neurologic sequelae to his infection. Case 7 (Contaminated Blood Culture). A 44year old man was hospitalized in 1971 for treatment of severe atopic dermatitis. He was afebrile and had a grade 2/6 apical systolic murmur. Two blood cultures were obtained on admission. One was negative, and the second grew Staph. aureus and group C streptococci. Because the patient had no clinical evidence of infection, the blood culture was considered to have been contaminated, and no antibiotic therapy was given. He remained afebrile during five weeks of hospitalization. ‘Case 6 (Contaminated Blood Culture). A 75year old man was

hospitalized for a traumatic closed fracture of the right tibia. Gradually progressing mental deterioration, hypoxia, petechiae, and a low grade fever were attributed to fat emboli. Antibiotics were not given. A blood culture obtained on the fifth day, when the patient had become afebrile, grew viridans streptococciand group C streptococci.These were considered to be contaminants. No antibiotic therapy was given. The patient remained afebrile during the remaining 26 days of hospitalization.

COMMENTS Colonization in man by group C streptococci is of interest. This includes positive umbilical cultures in newborns without signs of infection [4], nasopharyngeal cultures in normal persons [5], occasional genital tract cultures [6] and routine puerperal vaginal cultures [71. Before considering our case reports, it should be mentioned that other infections by group C streptococci in other sites have been observed. These include puerperal infections [~-IO], although anaerobic bacteriologic studies were not always performed, tonsillitis [7,11,12], cervical adenitis [13], urinary tract infections [14], bacteremia without known source [15,16] and an infected abdominal aortic aneurysm [17]. Bacterial Endocarditis. The features of eight previously described patients who had group C streptococcal endocarditis and of our own patient [Case 1) are summarized in Table I. The infection involved previously normal heart valves in six of the nine patients [20]. The

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mitral valve was infected in five patients, the aortic valve in two and the sinus of Valsalva in one; in one, the site was not determined. All were severely ill. Of the four patients who died, two had received inadequate therapy and one died early during the course of treatment: in one, the dosage of antibiotics was not reported. The antimicrobial management of the five surviving patients suggests that 20 million u of penicillin G every 24 hours, administered intravenously for four weeks, is adequate therapy. Replacement of the infected valve by a prosthetic valve in one patient and excision of a fistula from the sinus of Valsalva in another patient were necessary. Destruction of a valve, perforation of a valve or rupture of chordae was documented in four of the eight patients. In our patient, fenestration of the,noncoronary cusp and infection in the membranous septum caused an atrioventricular conduction block. The embolic complications of this infection are also severe and include brain abscess, ophthalmitis [14], meningitis [19], and cerebral [19,21], renal [19], myocardial [19] and splenic [19] emboli. Hemorrhages and petechiae have been reported [10,19,20].The probable initiating events were gastroenteritis in two patients [21], soft-tissue infection in three (including ours) [20,21], septic abortion in one [lo] and unknown in three [14,19]. One patient had clinical features that included migratory arthritis [22]. The duration of the symptoms of endocarditis before medical attention was sought was one week or less in five patients, probably one to two weeks in two and not determined in two. Thus, group C streptococcal endocarditis usually follows an acute destructive course requiring strict monitoring for signs and symptoms of early cardiac decompensation. Pneumonia. In addition to our patient (Case 3), only one patient with primary pneumonia due to group C streptococci has been described [7]. Thjs patient had bronchitis for 10 days, and then pneumonia developed with a pleural effusion and positive blood cultures, all responding to penicillin, as did our patient. Two others possibly had pneumonia associated with endocarditis [14,19]. Interestingly, a pleural effusion or empyema developed in both patients with pneumonia, as often happens in group A streptococcal pneumonia. The pulmonary abscess and the possible empyema of our patient could explain the long duration of fever despite adequate antibiotic therapy. Cdlulitis. Cellulitis, wound infection and cutaneous ulcers due to group C streptococci occur [7,16,23,24]. In an outbreak of cellulitis involving 27 patients, the pectoral-axillary region was frequently affected [25]. Red, hot, tender lesions of approximately three days’ duration, preceded by pain, spread locally, with a distinct nonraised edge without associated lymphangitis. Group C streptococci were cultured from aspirates of the skin lesions. Group C streptococci were cultured from lesions of nine patients who had impetigo, infected dermatitides and infected wounds with ascending lymphangitis [14].

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Groups A, C and G streptococci were similar in their predilection for this type of infection, in contrast to groups B and D streptococci, which were found in ischemic wounds, in the perineal region or in operative wounds [l4]. In our patient (Case z), the cellulitis and lymphangitis occurred in a lymphedematous arm secondary to radical mastectomy and radiation therapy for carcinoma. Bacteremia of Unknown Source. Bacteremia due to group C streptococci without a known source of infection occurred possibly in our Case 4 and was well documented in our Case 5. In both cases the patients received therapy for leukemia, resulting in leukopenia. The significance of group C streptococci recovered from one single blood culture in our Case 4 is not certain in the presence of a definite Esch. coli bacteremia. One additional patient with aplastic anemia, a skin infection and group C streptococcal bacteremia has been described [26]. Thus, group C streptococci should be considered as potential pathogens in the immunosuppressed host. Meningitis. Three patients with meningitis due to group C streptococci, including our Case 6, have been described [3]. One of these had meningitis due to cerebral emboli secondary to endocarditis [19]. Both in our patient and in a 14 day old infant [27], seizures occurred as a complication of severe acute meningitis, responding only slowly to appropriate antimicrobial therapy. The absence of demonstrable underlying disease or portal of entry in either case is contrary to the usual experience in streptococcal meningitis [3]. Contaminants. Group C streptococci were identified in single blood cultures from two of our patients (Cases 7 and 8) in association with other microorganisms, but a true bacteremia could not be substantiated clinically. One of our patients had an extensive dermatitis. Group C streptococci have not been reported previously as a skin contaminant, and this possibility should be considered when evaluating the significance of positive blood cultures. General Considerations. Several features common to group C streptococcal infections were noted in our cases. Total leukocyte counts ranged from 16,700 to 27,600/ mm3 with neutrophilia at the peak of the infection except for two patients who had preexisting leukopenia. Abnormally high SGOT and alkaline phosphatase levels were noted in three of our patients-one each with endocarditis, pneumonia and meningitis. Whether this results from the infection or is a side effect of therapy cannot be determined. The organisms were invariably susceptible to 0.1 pg/ml of penicillin. The low minimal inhibitory concentrations for cephalothin, ampicillin, chloramphenicol and clindamycin suggest that these drugs are acceptable alternatives for treatment. However, large doses of penicillin G are recommended as the treatment of choice for endocarditis due to group C streptococci.

C STREPTOCOCCI

TABLE II .---

.-

INFECTIONS

IN MAN-MOHR

ET AL.

Patients With Streptococci in Blood Cultures, by OrganismGroup, 1968-1977 Group

A B C D F Other specified Lancefield groups Other fl-hemolytic (ungrouped) Viridans 01- or y-hemolytic (unspecified) Total

No. of Palfents 107 58 8 302 7 21 28 547 29 1.107

Rheumatic fever occurring after group C streptococcal infections has not been reported. However, in one patient with group C streptococci in a wound, acute glomerulonephritis developed [28]. Also, in one third of 87 patients with group C streptococcal pharyngitis (Streptococcus zooepidemicus), acute glomerulonephritis developed in a milk-borne epidemic reported from Romania [12,29]. In 15 patients, the presence of group C streptococcal infection was documented by cultures of material from the throat or cervical lymph nodes. The antistreptolysin 0 (ASO) titers of these patients were low. In the United States, both elevated [11,26] and low or normal [9,18]AS0 titers have been reported in group C streptococcal infections. The exact incidence of group C streptococcal infections is difficult to determine. According to Rantz [23], 0.25 per cent of all streptococcal isolates from blood, urine, ulcers, abscesses and cerebrospinal fluid belong to Lancefield’s group C. Duma et al. [2] classified 0.6 per cent of all streptococcal isolates from blood cultures as group C. Of all streptococci isolated from blood, throat, wound, skin and abscess by Hutchinson [7] in England, approximately 10 per cent were of group C. Hill and Butler [8] in Australia found that, of postpartum and postabortum vaginal cultures, 9 per cent of all streptococcal isolates were of group C. In the identification of group C streptococci in clinical specimens, it should be emphasized that gamma hemolysis may predominate on horse-blood agar [l4] and that beta hemolysis is more frequent on sheep blood agar [24]. Because susceptibility to bacitracin is common [14], group C organisms may be misclassified as group A streptococci. Our data allow an estimate of the frequency with which group C streptococci are isolated from blood. From 1968 to 1977,2,660 blood cultures from 1,107 patients yielded streptococci. The frequency of various groups of streptococci is listed in Table II. Our experience and data from the literature indicate that, although infections caused by group C streptococci are relatively rare, the infections caused by these microorganisms may be extremely severe.

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ET AL.

REFERENCES 1. Olson LD, Schueler RL. Riley GM, et al.: Experimental induction of cervical lymphadenitis in guinea-pigs with group C streptococci. Lab Anim 110:2231976. 2. Duma RJ, Weinberg AN, Medrek TF, et al.: Streptococcal infections: a bacteriologic and clinical study of streptococcal bacteremia. Medicine (Baltimore) 48:87,1969_ 3. Mohr DN. Feist DJ, Washington JA II, et al.: Meningitis due to group C streptococci in an adult patient. Mayo Clin Proc 53: 529.1978. 4. Drusin LM, Ribble JC, Topf B: Group C streptococcal colonization in a newborn nursers._ Am .1 Dis Child 125: 820,

14. 15. 16. 17.

18.

1973.

5. 6.

7. 8.

9. 10.

11. 12. 13.

456

Hare R: The classification of haemolvtic streptococci from the nose and throat of normal human beings by means of precipitin and biochemical tests. J Path01 41: 499,1935. Christensen KK, Christensen P, Flamholc L, et al.: Fre uencies of streptococci of groups A. B, C, D and G in uretB ra and cervix swab specimens from patients with susoected nonococcal infection. Acta Path01 Microbiol Stand [B] 82: 470,1974. Hutchinson RI: Pathogenic@ of group C (Lancefield) haemolytic streptococcus. Br Med J 2: 575,1946. Hill AM, Butler HM: Haemolytic streptococcal infections following childbirth or abortion. II. Clinical features, with special reference to infections due to streptococci of groups other than A. Med J Aust 1: 293,194O. Ramsay AM, Gillespie M: Puerperal infection associated with haemolytic streptococci other than Lancefield’s group A. J Obstet Gynecol Br Emp 48: 568,194l. Rosenthal AH, Stone FM Puerperal infection with vegetative endocarditis: report of sulfanilamide therapy in two fatal cases due to streptococcus haemolyticus groups B and C. JAMA 114:840.1940. Benjamin JT, Perriello VA Jr: Pharyngitis due to group C hemolytic streptococci in children. J Pediatr 89: 254, 1976. Duca E, Teodorovici G, Radu C, et al.: A new nephritogenic streptococcus. J Hy (Camb] 67: 691.1969. Kijhler W, Cederberg w : Streptococcus zooepidemicus [group C streotococcil as a cause of human infection. Stand I Infeet Djs 8: 217,‘1976.

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19. 20. 21. 22. 23.

24. 25. 26.

27. 28. 29.

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Feingold DS. Stagg NL, Kunz LJ: Extrarespiratory streptococcal infections. N Engl J Med 275:356.1966. Hazenberg BP: Sepsis door streptococcus zooepidemicus. Ned TiJdschr Geneeskd 107: 1361.1963. Evans AC: Studies on hemolytic streptococci. VIII. Streptococcus equisimilis. J Bacterial 48: 267,1944. Perkins DE Ir. McRae RP: An arteriosclerotic aneurvsm of the abdominal aorta secondarily infected with group C, beta-hemolytic streptococci: report of a case. Am J Clin Path01 62:646,1974. Sanders V: Bacterial endocarditis due to a sroun C beta hemolytic streptococcus. Ann Intern Med