THE JOURNAL OF INFECTIOUS DISEASES. VOL. 138, NO.1. JULY 1978 © 1978 by The University of Chicago. 0022-1899/78/3801-0003$00.75

Listeria monocytogenes Infection m Neonates: Investigation of an Epidemic From the Center for Disease Control, Atlanta, Georgia; the Department of Microbiology, Greenville Hospital System, Greenville; and the South Carolina Department of Health and Environmental Control, Columbia, South Carolina

Gregory A. Filice, H. Furman Cantrell, Alexander B. Smith, Peggy S. Hayes, James C. Feeley, and David W. Fraser

curs is unknown. In the few outbreaks of neonatal listeriosis that have been reported, most cases have been one of these two forms [5-7]. Parallels exist between neonatal disease due to group B Streptococcus and that due to L. monocytogenes which suggest that nosocomial infection may occur. Group B Streptococcus causes early and late forms of disease that are very similar to those caused by L. monocytogenes [8]. The early-onset form of listeriosis is often caused by serotype la or l b, and the late-onset form is often caused by serotype 4b [9]. The early- and lateonset forms of disease caused by group B Streptococcus also have different serotype patterns [10, 11]. Outbreaks of the late-onset form of disease caused by group B Streptococcus have been associated with person-to-person spread within the hospital [12, 13]. From March 10 through October 29, 1975, an outbreak of late-onset neonatal listeriosis occurred in patients in a hospital in Greenville, S.C. (hospital A). The findings of an epidemiologic investigation, which was designed to differentiate between nosocomial and community acquisition of L. monocytogenes, are presented in this report.

Two forms of neonatal listeriosis have been recognized [1-3]. In the early-onset form, sometimes referred to as granulomatosis infantisepticum, the infant is critically ill at birth or becomes so during the first day or two of life. Most infants have generalized disease and appear to have aspiration pneumonia. They are often premature, and their mothers commonly have a history of "flu-like" or other nonspecific illness during pregnancy. It is likely that infection is acquired in utero or at the time of birth. Listeria monocytogenes can frequently be isolated from the mother if vaginal cultures are processed appropriately. The late-onset form of neonatal listeriosis usually affects term infants who are considered healthy until the onset of meningitis or septicemia one to four weeks after birth [2-4]. Their mothers have usually had uneventful pregnancies, and L. monocytogenes is rarely isolated from cultures of specimens from the mother [2-4]. At what time the initial infection of the infant ocReceived for publication May 4, 1977, and in revised form December 5,1977. The authors thank Helen M. Camp, Wallis E. DeWitt, Carole Garrett, Joe L. Holliday, Catherine J. Phillips, G. Kenneth Reubish, Jr., Carolyn D. Steele, John W. Turner, Geraldine L. Wiggins, and the many nurses who contributed to this investigation. Please address requests for reprints to Center for Disease Control, Attn: Dr. Gregory A. Filice, Bacterial Diseases Division, Bureau of Epidemiology, Atlanta, Georgia 30333.

Background

Greenville had a population (standard metropolitan statistical area) in 1970 of 299,502, 84% white and 15% black. Eleven hospitals with a

17

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From March 10 through October 29, 1975, Listeria monocytogenes infection occurred in seven neonates born at a 401-bed general hospital in Greenville, S.C. In the preceding 19months, there had been only one case. Six of the seven isolates from the infected infants were of serotype 4b. Risk of listeriosis in neonates was associated with being born to mothers of low socioeconomic status and being born to mothers who had had vaginitis during pregnancy. Nosocomial transmission of L. monocytogenes appeared unlikely, but the source of the infection is unknown. Of the media used in this study for isolation of L. rnonocytogenes from mixed cultures, McBride's agar and McBride's agar with nalidixic acid were most useful.

Filice et al.

18

Description of the Outbreak

Records of all cultures of blood and cerebrospinal fluid obtained at hospital A between August 1973 and August 1975 were searched for recorded isolations of L. monocytogenes and diphtheroids. No other bacteriology laboratory in the city had isolated Listeria species from clinical material during this period. Isolates had been obtained from seven patients between March 10 and October 29, 1975 (figure 1). An additional isolate had been obtained in September 1974; however, this case was not considered a part of the present outbreak because it was separated in time from the 1975 cluster, and the hospital bacteriologist reported that there had been a case every year or two in previous years. The pediatrics department of hospital A had not changed its culturing practices in the diagnosis of illness in neonates during the period August 1973 to August 1975, nor had the methods of processing blood or spinal fluid in the laboratory changed. The number of blood and cerebrospinal fluid cultures submitted to the lab-

4 '"

E

3

SEROTYPE 4b

0

SEROTYPE I b

~

SEROTYPE UNKNOWNI1I

...........-..............+-+-,,....,.....,......,.-+-I'-4-4-I'''4-1-l-4-,.~

oh-...,.....,,....,.....,......,.~

JASONDJFMAMJJASONDJFMAMJJASOND

1973

1914

1975 ONSET

Figure 1. Incidence of neonatal infection due to Listeria monocytogenes in Greenville, S. C., by month from July 1973 through December 1975.

oratory during this period did not change. The number of blood cultures from which diphtheroids were isolated did not drop as the outbreak of listeriosis appeared, a finding which suggested that the appearance of the outbreak was not an artifact of improved identification of Listeria species. The isolates obtained in 1975 were from seven infants. Six had meningitis with or without documented septicemia, and one had septicemia without meningitis. All infants appeared healthy at birth and when they were discharged a few days later. The pre· and postnatal courses of the mothers were considered to have been healthy, except for suspected endometritis in one mother after delivery. L. monocytogenes was not isolated from a culture of her endometrial discharge. Infants appeared well until their onsets of listeriosiseight to 16days after birth. Common signs at the time of readmission were fever, irritability, and diarrhea (table 1); only three infants had a bulging fontanel, and only two had meningismus. Five infants had leukocytosis; the differential counts were similar to those seen with most neonatal infections. Cerebrospinal fluid from all seven infants was examined and cultured. Treatment with antibiotics was started on the day of admission in six ill infants and two days after admission in the seventh. Defervescence occurred 24-48 hr after treatment was started. All infants responded quickly with return of ap· petite and the appearance of well-being, Treatment was continued for 10-14 days. Case-Control Analysis

The seven cases (case infant) were compared with 14 temporal controls (temporal-control infant) and 14 matched controls (matched-control infant). Two temporal-control infants were randomly chosen from the 32 infants closest to each case in the birth log. In addition, the two matched-control infants chosen for each case infant were the two infants closest in the birth log who were similar in sex, race, service (private or nonprivate), birth weight (within 2 lb), and nursery (well-infant or intensive care). Chart review and interviews. The hospital and prenatal charts of case and control infants and their mothers were reviewed. Attempts were

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total of 1,356 beds serve the Greenville area. The hospital that was involved, a 401·bed general hospital, serves the central city and the majority of the indigent population. The hospital has private and nonprivate patients who occupy the same wards. Fourteen percent of the 21,000 pa· tients discharged per year are nonprivate, and 20% are black. The hospital has a well-baby nursery and an intensive care nursery. In the well-baby nursery, newborns are initially observed in one room. Then, private patients are usually placed in one of two rooms, and nonprivate patients are usually placed in a third. The assignment of rooms to mothers is not dependent on private or nonprivate status of the patients.

L. monocytogenes in Neonates

19

Table 1. Clinical and laboratory information on seven cases of neonatal listeriosis at a general hospital in Greenville, S. C., 1975. Clinical or laboratory information

Result *

Mothers of

12.1 7/7 5/7 4/7 3/7 3/7 2/7 1/7 13,600 36.4 4.3 54.7 3.1

0.4

o 3,874 88 12 174 38 3/6 6/7 4/7

5 1 1

36

*Results are number with indicated sign/number tested, unless noted otherwise. tIn patients with L. rnonocy togenes isolated from cerebrospinal fluid.

made to interview the mothers about their prenatal health, health of the infant during the first three weeks of life, the environment in which the mother and her household lived during pregnancy, exposure to animals, and consumption of undercooked or raw meat and unpasteurized milk. All mothers of case infants (case mothers), five mothers of temporal-control infants (temporalcontrol mothers), and 10 mothers of matchedcontrol infants (matched-control mothers) were interviewed in person. Six temporal-control mothers and two matched-control mothers could not be interviewed in person but were inter-

Characteristic White Private patients Mean Hollingshead index Persons per room in household

Case infants

Ternporalcontrol infants

2/7 1/7 67

10/14 8/14 53*

Matched Matched 67

1.24

0.87

1.16

Match edcontrol infants

NOTE. Data are number with characteristic/number tested, unless noted otherwise. *p =0.05, Wilcoxon signed rank test.

viewed by telephone. The remaining three temporal-control mothers and two matched-control mothers could not be contacted. Case mothers appeared to be of lower socioeconomic status than temporal-control mothers, but were similar in socioeconomic status to matched-control mothers (table 2). Case mothers were from more crowded households and had significantly higher Hollingshead indexes (indieating lower socioeconomic status) [14]. Higher proportions of case mothers were nonprivate patients and black. Case mothers were more likely to have had vaginitis during pregnancy than temporal- and matched-control mothers (table 3). Vaginitis was defined in two ways: (1) vaginitis or an inflamed vagina or cervix recorded on the prenatal or hospital chart or (2) a history, obtained from the mother, of a vaginal discharge that was distinctly unusual for her during her pregnancy. A chart record of vaginitis was significantly more common for case mothers than for temporal- and matched-control mothers, and the presence of vaginitis by either definition was more common in case mothers than temporal-control mothers. The case mothers were not more likely to have had other symptoms or illnesses during pregnancy, such as fever or diarrhea, which could possibly have been associated with listeriosis. Case and control mothers were of similar ages (mean, 20 years). Similar proportions of case and control mothers were primigravidas, had had pri-

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Mean age (days) at onset Signs Fever Irritability Diarrhea Poor feeding Bulging fontanel Meningismus Lethargy Laboratory data (mean) White blood cell countjmm'' Neutrophils (%) Bands (%) Lymphocytes (%) Monocytes (%) Eosinophils (%) Basophils (%) Cerebrospinal fluid (mean value)t White blood cell countjmrrr' Neutrophils (%) Mononuclear cells (%) Protein (mg/dl) Glucose (mgjdl) Organism seen on gram stain Listeria monocytogenes isolated from Cerebrospinal fluid Blood Number treated with Ampicillin and kanamycin Ampicillin and gentamicin Ampicillin, kanamycin, penicillin Mean interval (hr) between institution of treatment and sustained normal temperatures

Table 2. Socioeconomic indicators of mothers of case and control infants studied in an investigation of neonatal listeriosis in Greenville, S. C., 1975.

Filice et al.

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Table 3. Vaginitis and other symptoms or illnesses, which could have been caused by Listeria monocytogenes, during pregnancy of mothers of case and control infants in Greenville, S. C., 1975. Mothers of

Symptom or illness

Matchedcontrol infants

5/7

0/14 *

3/14 t

5/7

1/11

4/12

6/7 2/7

1/11 :j: 4/11

5/12 5/12

NOTE. Data are number with symptom or illness/number tested. *p = 0.004, matched-control exact test [15]. tp = 0.05, matched-control exact test [15]. :j:p = 0.05, matched-control test based on x 2 statistic [16].

or spontaneous abortions or stillbirths, and gave birth on nonsterile fields. The mean duration of labor and the mean interval between rupture of membranes and delivery were not longer in case mothers than control mothers. Similar proportions of case and control mothers were exposed to animals during pregnancy (individual species and all species combined), and the same was true for infants during the first three weeks of life and for the mothers' household members during the mothers' pregnancies. Similar proportions of case and control mothers consumed raw or undercooked meat and unpasteurized milk. Higher proportions of families of cases had urban residences (seven of seven) than families of matched controls (six of 12), but the difference was not significant. Case residences were not clustered within the city. Characteristics of case and control infants were similar in almost all respects (table 4). Four case infants had minor neonatal complications: one had a congenital phimosis, one had an anomalous foreskin, one was considered "possibly postmature," and one passed a small amount of meconium during delivery. All had otherwise uneventful postnatal courses and were considered well at discharge. Hospital experiences of infants and mothers. Experiences of all mothers and infants in the hospital were similar. No treatments, procedures, medications, or infant formulas were associated with illness. Only two case infants and

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Chart record of vaginitis History of vaginitis obtained from the mother Chart record or history of vaginitis Other

Case infants

Temporalcontrol infants

their mothers were in the hospital at the same time. Patients' room numbers, except for postpartum rooms of the mothers, had not been recorded. Since six of the seven case infants were nonprivate, they were probably cared for in the same room of the newborn nursery. This room contained bassinets and night-stands, which were frequently rotated, and a frequently cleaned sink. Environmental cultures were taken from this room, but L. monocytogenes was not isolated. Illness in infants was not strongly associated with contact between any staff member and ill infants or their mothers. One nurse (nurse A) had contact with four case mothers, two temporal-control mothers, and one matched-control mother, and the difference between proportions of case mothers and matched-control mothers with recorded contact with the nurse is associated with a P value of 0.04 (matched-control analysis) [6]. Recorded contact with other staff members was more evenly distributed among cases and controls. Antibody to and carriage of L. monocytogenes. Specimens from the pharynx, vagina, and rectum for the isolation of L. monocytogenes and serum for the measurement of antibody to L. monocytogenes were obtained from each mother interviewed in person. Similar specimens were requested from staff members who were associated with three or more cases and/or case mothers. Agglutinating antibody was measured in serum by the method of Larsen et al. [17]. Specimens for the isolation of L. monocytogenes were obtained with calcium alginate or cotton swabs, placed in Stuart's medium, and incubated at room temperature (about 24 C) for one week [18]. Material on the calcium alginate swabs was dissolved in calgon Ringer's solution, and material on the cotton swabs was suspended in phosphate-buffered saline with a vortex mixer. Subcultures were made, and the remaining solutions were added to 4.S-ml aliquots of trypticase soy broth (TSB) and kept at 4 C. Subcultures were again made after one and five months of cold enrichment. For all subcultures, inocula from each specimen were streaked on McBride's agar and MeBride's agar that contained 40 ftg of nalidixic acid/rnl. In addition, three other media were used for various subcultures: McBride's agar that

21

L. monocytogenes in Neonates

Table 4.

Characteristics of ill infants and controls studied in an investigation of listeriosis in Greenville, S. C.,

1975.

Characteristic

Case infants

Temporalcontrol infants

Male Birth weight (mean) Estimated gestational age (weeks, mean) Apgar test result (mean) * Neonatal complications Hospital stay (days, mean) Exposure to ill persons in first two weeks of life or before illness Out-of-doors during first two weeks of life or before illness

4/7 61b150z

4/14 61b 8 oz

40.2 8.6/9 4/7

39.1 7.4/7.7 7/14

3.4

4.6

2/7

3/12 11/12

7/7

Matchedcontrol infants Matched 71b 1 oz (matched)

39.9 8.3/8.9 8/14 4.8 2/9 8/9

contained 3 JLg of polymixin/rnl, trypticase soy agar (TSA) that contained 40 JLg of nalidixic acidjrnl, and TSA that contained 40 JLg of nalidixic acid rml and 25 JLg of acriflavine neutral (NOKA 565, MA/LHI-35584; Cassella Farbwerke, Frankfurt/Main, West Germanyjj ml [19]. Positive controls consisting of L. monocytogenes alone and mixed fecal flora seeded with L. monocytogenes were included as positive controls. Isolates with the typical blue-gray appearance under oblique light were identified by standard techniques [20] and serotyped [9]. L. monocytogenes was not isolated from case or control mothers. L. monocytogenes serotype lb was isolated from one of 18 staff members from whom specimens were obtained; serotype 4b was not found. L. monocytogenes was not isolated from nurse A. Titers of agglutinating antibody were not significantly different between case and control mothers. The geometric mean titers (95% confidence interval) of antibody to L. monocytogenes serotype 4b in mothers of case, temporal-control, and matched-control infants were 28.1 (13.4-58.7), 21.0 (6.6-67.1), and 20.3 (11.9-34.8), respectively. These data do not include those from the mother whose child had illness caused by L. monocytogenes l b and the corresponding controls. Prospective Culture Survey

From September 29 through October 27, 1975, a culture survey was done to explore further the possibility of nosocomial transmission of L. monocytogenes. Specimens were obtained from the pharynx, vagina, and rectum of mothers in labor

during this period at the hospital involved. Specimens were taken from the ear, pharynx, umbilicus, and meconium of their infants at the time of birth arid from the pharynx, umbilicus, and stool at the time of discharge from the hospital. Specimens were handled in the same manner as those from mothers of case and control infants. Cultures were obtained from 213 (80%) of 265 mothers who delivered during the prospective study period, from 219 (82%) of their 268 infants at birth, and from 242 (90%) of their infants at discharge. L. monocytogenes serotype 4b was isolated from rectal swabs taken from two mothers (0.9%), and L. monocytogenes serotype lb was isolated from the external ear canal and umbilicus specimens taken from one infant (0.5%) at the time of birth. The organism was not recovered from this infant at discharge or from any other infant. The two mothers with serotype 4b organisms were not in the hospital at the same time. Cold Enrichment and the Media Used for Isolation

Of the four specimens from which L. monocytogenes was isolated, one was positive in the initial subculture, this and one other were positive in the one-month subculture, and all four were positive in the five-month subculture. Since L. monocytogenes was isolated from few persons, statistical analysis of differences between the effectiveness of the various media was not possible, but a few observations were of note. Calcium alginate dissolved in Calgon Ringer's solution became viscous at 4 C, and this viscosity made it difficult to

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NOTE. Data are number with characteristic/number tested, unless noted otherwise. *Result at 1 min/result at 5 min.

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Discussion

This investigation was designed to differentiate between two hypotheses: (1) that infants acquired L. monocytogenes within the hospital after birth and (2) that L. monocytogenes was acquired by mothers before or during pregnancy and spread to infants at or before birth. The results are not conclusive, but inferences can be made. Only two case infants were in the hospital at the same time; this fact makes direct spread unlikely, but does not exclude a common source of L. monocytogenes. Contact of nurse A with case mothers appeared to be significantly more common than her contact with matched-control mothers, but contact of 74 staff members with patients and with matched and temporal controls was examined. One or more associations with this degree of probability (P = 0.04) would be expected to occur by chance alone in this number of comparisons. The weakness of the association and the negative cultures taken from nurse A make it unlikely that she was the source of the outbreak. L. monocytogenes was not isolated from several sites within the room in the nursery in which six of the seven case infants probably stayed and has not been isolated from similar environments before. The prospective culture survey gave no evidence of nosocomial transmission. The carriage rate was low, and because the study was begun six days after the last case infant was born, it is possible that an unknown nosocomial source had been removed. The high incidence of vaginitis in case mothers during pregnancy suggests that L. monocyto-

genes might have been acquired by them before or during pregnancy. The incidence of vaginitis in matched-control mothers seemed closer to the incidence in case mothers than did the incidence in temporal-control mothers. One possible explanation for this is that vaginitis and other minor problems were more common among mothers of lower socioeconomic status served by the hospital, represented by case mothers and matched-control mothers, than among mothers in all of the different levels of socioeconomic status served by the hospital during that period, represented by the temporal-control mothers. However, the incidence of vaginitis appeared to be higher in case mothers than in temporal- or matched-control mothers, while the incidence of other nonspecific symptoms and illnesses was similar in all three groups. The association between vaginitis during pregnancy in mothers and subsequent illness in their infants suggests that case mothers had a different experience before hospitalization and that the community may have been the source of the outbreak. That case mothers were not found to carry L. monocytogenes at the time of the investigation does not make prior carriage or infection unlikely. Most attempts to isolate the organism from mothers of infants with the late-onset disease have been unsuccessful just a few weeks after delivery. Most mothers in this study were cultured months after delivery. Of media used in this study, McBride's agar and McBride's agar with nalidixic acid were the most effective for isolation of L. monocytogenes from mixed cultures. TSA containing nalidixic acid and acriflavine tended to inhibit the growth of L. monocytogenes as well as other organisms, whereas TSA containing only nalidixic acid supported the growth of many organisms, often causing L. monocytogenes to be missed. Agglutinating antibody to serotype 4b was not of significantly higher titer in case mothers than in control mothers. Small numbers of serum samples were available, and some were collected long after the mothers had delivered. The relationship between agglutinating antibody and listeriosis is not well understood; L. monocytogenes in the genital tract may not provoke rises in antibodv titer. No sources of L. monocytogenes within the community for these patients could be epidemi-

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obtain adequate samples for subsequent subcultures. Cotton swabs were easier to handle. L. monocytogenes were consistently found on McBride's agar and McBride's agar with nalidixic acid, when they were found on any medium. They often were not found on TSA containing nalidixic acid even when they were found in other media simultaneously inoculated with known positive specimens. Organisms were also not found consistently on TSA with nalidixic acid and acriflavine, and on this medium colonies of L. monocytogenes were not easily differentiated from colonies of other organisms.

Filice et al,

23

L. monocytogenes in Neonates

ologically incriminated. Listeriosis is recognized in many species of animals [21], but case and control mothers, infants, and household members had similar degrees of contact with animals. L. monocytogenes has been isolated from raw poultry [22] and from unpasteurized milk [21], but case mothers and case infants were not more likely to have consumed poorly cooked or raw meat or unpasteurized milk. It may have been that L. monocytogenes was common in the environment during this period and that the mothers became infected from several sources.

10.

II.

12.

References I. Gray, M. L., Killinger, A. H. Listeria monocytogenes and listeric infections. Bacteriol. Rev. 30:309-382, 1966. 2. Sepp, A. H., Roy, T. E. Listeria monocytogenes infections in metropolitan Toronto. Can. Med. Assoc. J. 88:549-561,1963. 3. Ray, C. G., Wedgewood, R. l Neonatal listeriosis. Six case reports and a review of the literature. Pediatrics 34:378-392, 1964. 4. Nichols, W., Jr., Wooley, P. V., Jr. Listeria monocytogenes meningitis. Observations based on 13 case reports and a consideration of recent literature. J. Pediatr. 61:337-350, 1962. 5. Levy, E., Nassau, E. Experience with listeriosis in the newborn. An account of a small epidemic in a nursery ward. Ann. Pediatr. 194:321-330, 1960. 6. Olding, L., Philipson, L. Two cases of listeriosis in the newborn, associated with placental infection. Acta Pathol. Microbiol. Scand. 48:24-30, 1960. 7. Becroft, D. M. 0., Farmer, K., Seddon, R. J., Sowden, R., Stewart, J. H., Vines, A., Wattie, D. A. Epidemic listeriosis in the newborn. Br. Med. J. 3:747-751, 1971. 8. Baker, C. J., Barrett, F. F., Gordon, R. C., Yow, M. D. Suppurative meningitis due to streptococci of Lancelield group B: A study of 33 infants. J. Pediatr. 82: 724-729, 1973. 9. Albritton, W. L., Wiggins, G. L., Feeley, J. C. Neonatal

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listeriosis: distribution of serotypes in relation to age at onset of disease. l Pediatr. 88:481-483, 1976. Baker, C. J., Barrett, F. F. Group B streptococcal infections in infants. The importance of the various serotypes. lA.M.A. 230:1158-1160, 1974. Wilkinson, H. W., Facklam, R. R., Wortham, E. C. Distribution by serological type of group B streptococci isolated from a variety of clinical material over a live-year period (with special reference to neonatal sepsis and meningitis). Infec. Immun. 8:228-235, 1973. Steere, A. C., Aber, R. C., Warford, L. R., Murphy, K. E., Feeley, l C., Hayes, P. S., Wilkinson, H. W., Facklam, R. R. Possible nosocomial transmission of group B streptococci in a newborn nursery. l Pediatr. 87:784-787,1975. Aber, R. C., Allen, N., Howell, J. T., Wilkenson, H. W., Facklam, R. R. Nosocomial transmission of group B streptococci. Pediatrics 58:346-353,1976. Hollingshead, A. B., Redlich, F. C. Social class and mental illness: a community study. John Wiley and Sons, New York, 1958, p. 398-407. Miettinen, O. S. Individual matching with multiple controls in the case of all-or-none responses. Biometrics 25:339-355, 1969. Pike, M. C., Morrow, R. H. Statistical analysis of patient-control studies in epidemiology. Br. l Prevo Soc. Med.24:42-44, 1970. Larsen, S. A., Wiggins, G. L., Albritton, W. L. Immune response to listeria. In N. R. Rose and H. Friedman [ed.], Manual of clinical immunology. American Society for Microbiology, Washington, D.C., 1976, p. 318-323. Kampelmacher, E. H., Van Noorle Jansen, L. M. Stuart's medium voor transport van material verdacht van aanwezigheid van L. monocytogenes. Tijdschr, Diergeneeskd. 93:1297-1299,1968. Ralovich, B., Forray, A., Mero, E., Malovics, H., Szazados, I. New selective medium for isolation of L. monocytogenes. Zentralbl. Bakteriol. [Orig. A] 206:88-91,1971. Weaver, R. E., Tatum, H. W., Hollis, D. G. Identification of unusual pathogenic gram-negative bacteria. Center for Disease Control, Atlanta, Ga., 1972. 12 p. Gray, M. L. Epidemiological aspects of listeriosis. Am. J. Public Health 53:554-563, 1963. Kwantes, W., Isaac, N. Listeriosis. Br. Med. l 4:296297,1971.

Listeria monocytogenes infection in neonates: Investigation of an epidemic.

THE JOURNAL OF INFECTIOUS DISEASES. VOL. 138, NO.1. JULY 1978 © 1978 by The University of Chicago. 0022-1899/78/3801-0003$00.75 Listeria monocytogene...
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