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NEONATAL

STAPHYLOCOCCAL

INFECTION

Harold J. Simon, M.D., Ph.D., Juan Allwood-Paredes, M.D., M.P.H.,

and Alfonso Trejos, Ph.D.

I)epartmmaemmt of ltfedicimme, Stanford Unicersity School of Medicine, Palo Alto, California

I.

Ecology

and

Prevention

in

a

Maternity

Hospital

in

El

Salvador

(Sublnitted April 23; revision accepted for publication September 16, 1964.)

l)r. Simon is recipient of a Career Development Award from tile National Institute of Allergy and

Infectious l)is:ases, Umted States Public health Service; Dr. Allwood-Paredes is Chief, Department

of Preventive Medicine and PUl)lic Health, Facultad (le Medicina, Universidad de El Salvador; 1)r.

‘t’n.jos is Chief, Depaltlhlent of M icrOl)iOlOgy, Facultad de \tedicina, Universidad le El Salvador.

‘l’Iiis stud was financed through United States and Salvadorean sources. From the United States,

and mediated through Stanford University, the study was supported in part by the United States Public

health Service through a grant (AI-03371) from the National Institute of Allergy and Infectious

Dis-eases, and a training grant (TI-AI-185) from the National Institutes of Allergy and Infectious Diseases,

National Institutes of health. A grant was also obtained from Winthrop Laboratories, New York.

ADDRESS: (H.J.S.) Division of Infectious Diseases, Department of Medicine, Stanford University

School of Medicine, 300 Pasteur Drive, Palo Alto, California.

PEDIATRICS, February 1965

254

T

DESIIIPTION of an effective method

for the prevention of neonatal

staphy-lococcal colonizationl and confirmation of

tile results2 provoked the following

ques-tions:

1. Is the introduction and continued use

of this technique possible under adverse

technical, social, and economic conditions?

2. Does this program effectively prevent

staphylococcal colonization and consequent

(liSease among newborns in the first months

of life?

An invitation from the Faculty of

Medi-cine, University of El Salvador, to the

Stan-ford University School of Medicine to

un-(lertake a co-operative venture provided an

opportunity for a study designed to answer

these questions.

THE ENVIRONMENT

The 215-bed hospital de Maternidad in

San Salvador, El Salvador, was opened in

April, 1954, as the only public facility for

obstetrics in El Salvador. The patient load

averages more than

1,000

deliveries and 300

complicated obstetrical/gynecological

prob-lems each month. The usual hospital stay

for mother and infant is therefore limited to

24 hours following delivery.

The architectural design of the hospital

cannot be considered modern. Ventilation

is open to the ambient environmet at all

times. Illumination, working areas, scrub

sinks, equipment, and separation of the

pa-tient areas do not fit the standards

gen-erally demanded in the United States.3

At first, newborn infants were housed in

tvo large, rectangular rooms where

approx-imately thirty bassinets were spaced

im-mediately ad;acent to each Otiler along the

walls of each nursery. \Vhenever needed,

additional trays of six bassinets each were

placed wherever they could be

accommo-dated. On occasion, two infants would

oc-cupy the same bassinet.

Later on, one of the two nurseries was

converted into a suspect nursery. The other

was enlarged and extended around a corner

in the shape of a “L” without partition. This

became the study nursery alid always

housed at least 96 infants.

The bassinets consist of metal frames

covered by cloth drapes which are not

gen-erally changed between occupants. The

in-fants are clothed in diapers and shirts

which are washed in a steam laundry, but

are not autoclaved or otherwise treated.

(2)

between handling infants. The infants had

been bathed with soap and water after

de-livery.

The nursery is served by three shifts of

nurses and aides. The personnel to patient

ratio averages 1 to 10. The graduate nurses’

preparatory education approximates

high-school graduation in the United States, and

all receive their training in the School of

Nursing in San Salvador. The auxiliaries

are trained on the job. Their preparatory

education does not usually extend beyond

the sixth-grade level. The nursery is

super-vised by one pediatrician with an active

private practice.

PLAN OF THE STUDY

The rate, rapidity, and sequence of

staphylococcal colonization among

new-borns were determined prior to trials with

the new infant-care program. The program

was later established on a continuing basis

with a home follow-up routine. Any

individ-ual who developed disease was referred to

the clinic for diagnosis and bacteriological

examination.

One member of the team saw all patients admitted for delivery. If the prospective

mother resided within the predetermined

geographical limits of the study (6 km

radius), a record was opened and nasal and

perineal swab cultures were obtained for

immediate examination. The final decision

for or against inclusion in the study was

made the following morning by one of the

public health nurses on the basis of

proba-ble availability for follow-up. A coded

system of clinic, laboratory, and visit

rec-ords was used for all families.

Cultures of the mother’s nose and

peri-neum were obtained on admission, before

the prep, and once daily until delivery. Cul-tures of the infant’s nares and umbilicus

were obtained immediately after delivery,

daily for one week, weekly for the

re-mainder of the first month of life, and

monthly for a total of 3 months. Specimens

from the mothers were obtained on the

identical schedule. Anterior nares swab cul-tures were obtained from the family at the

first home visit (usually within hours of

the return of the mother and infant to tile

home), and 2 to 4 weeks later.

The study population was examined at

each visit, all detectable lesions were

cul-tured and problems referred to tile clinic.

Mothers were given stamped identification

chits and urged to report to the clinic at

the first symptom or sign of illness. Some

were provided with small sums of money

for bus fare and given a small quantity of

powdered milk at the time of the clinic visit.

THE STUDY POPULATION

All women accepted into tile study

pre-sented themselves voluntarily at the

Hos-pita! de Maternidad. Although of the lower

socioeconomic stratum, they represented a

sample of 70% of San Salvadorean women

\Vilo come to this hospital for delivery. The

remainder of the women in the city have

their babies at private hospitals or at home

with the assistance of family members,

mid-wives, or other non-medically trained

per-sonnel. All infants were breast fed.

The high mobility of the population had

been previously established. Of the 150

families selected, only 112 (58 from the

ex-perimental and 54 from the control group)

could be followed for the full 3 months.

Nineteen of the remaining 38 families were

lost to the study within 2 to 4 days because

they had provided false addresses. Four

stillbirths or perinatal deaths occurred

with-in the first 3 days of life; the remaining 15

moved out of the study area.

The large single nursery was divided into

two equal halves at the base of the “L” l)y

means of a knee-to-chest high partition

which allowed air to flow freely between the

nurseries but restricted the free flow of

per-sonnel. Upon delivery, tile infants were

as-signed to one or the other nursery sections

on the basis of their record numbers. The

experimental group (even numbers) was

treated with the new care program, the

control group with soap and water in the

standard manner.

The majority received only three

(3)

immedi-256 NEONATAL STAPHYLOCOCCAL INFECTION. I

a Kindly supplied by Winthrop Laboratories,

New York.

ately after delivery, immediately upon

ad-mission to the nursery, and on the

follow-ing day prior to discharge. Infants

remain-ing in the hospital received additional

ap-plications once a day. PHisohex#{176} washing

was not continued after discharge.

TREATMENT PROTOCOL

The antiseptic skin care technique

em-ployed was described previously.1

Immedi-ately after delivery, the skin and umbilical

cord were washed thoroughly with

pHiso-hex applied manually. Cotton balls and

applicator sticks were used only for the

umbilical region. The infant was wrapped

in a sterile double wrapper. The skin was

not dried.

The outer wrapper was retained by the

delivery room or operating room nurse as

she handed the infant to an attendant at

the entrance to the nursery. The infant was

washed again upon admission to the

nurs-ery, and received a thorough wash daily

thereafter. Particular attention was given

the umbilicus as the cord dried to cleanse

the trough created by the skin-cord margin.

A sterile, cotton-tipped applicator was used

for this purpose.

All personnel were to wash their hands

with pHisohex on entering the nursery and

between handling infants. Although

re-peatedly stressed, spot checks revealed that

this occurred irregularly.

MATERIALS AND METHODS

All cultures were obtained with sterile

saline-moistened swabs and transferred to

polymixin-blood-agar plates at once or

im-mediately upon their receipt in the

labora-tory.

The coagulase test was initially carried

out with citrated or oxalated blood. A

suc-cession of false positive results traceable to

group D hemolytic streptococci

(entero-cocci) necessitated the use of heparinized

blood in the laboratories at San Salvador

and Stanford.4

Appropriately standardized identification

of staphylococci and coagulase testing were

carried out in the laboratories of the

De-partment of Microbiology of the Faculty of

Medicine in San Salvador. Subcultures were

stored on agar slants in small vials and

shipped in batches to Stanford for

confir-mation of coagulase reactivity, phage

typ-ing, and antibiogram determinations. The

antibiogram consisted of tests against

peni-cillin (1.0 unit/mi), streptomycin (10

ig/ml), tetracycline (10 g/ml),

chioram-phenicoi (10 i.g/ml), and erytllromyciri

(10 p.g/ml) according to the method

previ-ously described. Phage typing was carried

out by means of a replicate plating

tech-nique.6 All consumable supplies were

shipped to El Salvador in order to

mini-mize dish washing and other variables.

The bacteriological results were

inter-preted by a visual estimate of the quantity

of growth; the fraction represented by

staphylococci was estimated. A body site

was considered to be colonized if even one

colony of coagulase-positive staphylococci

was identified. An individual was

con-sidered to be colonized if staphylococci

were recovered from any body site.

Prelim-inary results of these studies have been

summarized briefly in a previous

publica-tion.7

RESU LTS

Preliminary Studies on Colonization

Dynamics

CoLoNIzATIoN RATES: Initial colonization

rates were calculated on the basis of swab

cultures from the anterior nares and

umbili-cal sulci of all infants residing in the

nurs-eries at any one time regardless of their

respective ages. The population always

in-cluded a mixture of infants ranging in age

from a few minutes to several days. At

ran-dom, 88% of 100 infants in one of the

nurs-eries and 73% (61) of 84 infants in the other

were colonized on one or both sites.

RAPWrrY AND SEQUENCE OF

(4)

ARTICLES

STAPHYLOCOCCAL COLOPIZATION DURP4G HOSPITAL STAY

OCT 061 - APRL 063 (800 HFANTS)

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100

90

80

70

::

40

30

20

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/

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//

‘‘ S

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#{149} S

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I

TOTAL

-e NOSE

I

HOURS FROM BIRTH

-z

z

9

200

$00

Fic. 1.See text.

24 48 - >48

INFANTS- NEVER COLONIZED BY STAPHYLOCOCCI

(CUMULATIVE TOTALS)

TREATED CONTROL.

A NOSE

0 UMBUCUS

S TOTALS

1Y7( 2-6 7 4 21 28 2MOS 3 2-b 7 14 21 28 2MOS S

Fic. 2. See text.

obtained from 800 infants whose ages in

hours were recorded. Colonization occurred

rapidly,

was 95% at 24 hours, 98% at 48

hours, and 100% beyond 48 hours of age.

Nasal lagged far behind umbilical

coloniza-tion for the first 12 hours of life, but then

increased rapidly (Fig. 1).

The Effect of the Infant Care Program

COLONIZATION OF INFANTS: The

differ-ences in colonization between the treated

and control groups of infants are shown in

Figure 2. Nasal colonization on the first

I01 90 80 0 70

day of life was found in 44.4% of the

con-trol but only 1.6% of the treated group.

Umbilical colonization was found in 50%

of the control and 3.4% of the treated group.

Over-all, 64.8% of the control and 3.4% of

the treated group were colonized in the

hospital. Colonization rates of the treated

group were less than those of the control

group at every point in the study.

Figure 2 also shows that every infant in

the control group had become colonized at

some point between the second and sixth

(5)

$00 90 80 70 60 50 40

30 20 10

#{149}-- -CONTROLS

0- EXP GROUP

2-6 7 4 2$ 28 21,106 31.105

P1 STLOY

258 NEONATAL STAPHYLOCOCCAL INFECTiON. I

the treated group were never colonized.

The figure also demonstrates that nasal

colonization preceded umbilical

coloniza-tion in the treated group.

MATERNAL COLoNIzATIoN:

Approximate-ly one-third of all mothers were nasal

car-riers at admission to the hospital. Perineal

carriage alone added a small increment to

the total nunlber of carriers. The carrier

rates fluctuated slightly throughout the 3

montils of the study.#{176} No significant initial

differences were found in maternal carrier

rates between the experimental and the

control groups. Mothers from both also

be-came colonized at approximately equal

rates throughout the study. The cumulative

colonization experiences of the mothers are

shown in Figure 3. At the end of 3 months,

9 (17%) in the control group and 12 (21%) in

the experimental group remained

uncolo-nized.

MOTItRS $EVER COLOMZED BY STAPHYWCOCCA

Fic. 3. See text.

C0L0N1zATI0N OF FAMILY MEMBERS: Of

the 112 families, 107 yielded data from

family members. Tile number of additional

members beyond mother and infant ranged

from 1 to 11, a total of 344 individuals (3.2

per family). Colonization was found on the

first home visit in 125 family members (36%),

a rate almost identical with that of mothers

on admission to the hospital. Sixty-six (38%)

of 175 individuals from experimental and

59 (34%) of 169 individuals from control

families were colonized at the first home

visit.

o Data available on request from the senior

author.

An analysis of family colonization data

revealed no age-related differences and

were very similar to the over-all maternal

and family colonization rates. There were

98 children and 77 adults in the

experi-mental group and 96 children and 83 adults

in the control group. Thirty-three (34%) of

tile children in the experimental group and

35 (36%) in the control group were

cob-nized.

Incidence and Nature of Disease Occurring

During the Study

STAPHYLOCOCCAL DISEASE - INFANTS:

Three instances of staphylococcal disease

occurred in 3 (5%) of the 59 treated infants,

and 17 instances affected 12 (22%) of the 54

infants in the control group.

There were 11 males (92%) in the 12 infants

of the control group who experienced

dis-ease episodes, and one male among the 3 in

the experimental group. The male to female

ratio of disease occurrence was 4.3 to 1.

The control group contained 29 males (54%)

and the experimental group 31(53%), a

pro-portion of 1 to 1. Racial differences were

not studied. The nature, timing, and

epi-demiology of these and all other cases are

defined in a companion paper.8

STAPHYLOCOCCAL DISEASE - MOTHERS:

There were three episodes of staphylococcal

disease in 3 mothers of treated infants,

and five episodes in 4 mothers of the

con-trol group.

STAPHYLOCOCCAL DISEASE-FAMILY: Two

minor staphylococcal abscesses occurred in

one family member of a treated infant but

were due to different strains of

staphy-lococci.

Seven instances of staphylococcal

dis-ease affected family members of infants in

the control group. Five cases of

furuncu-bosis occurred in the same family 2 months

postpartum in 5 individuals, one of whom

appeared to have infected all the others.8

NON-STAPHYLOCOCCAL DISEASE:

Statisti-cal analysis failed to indicate any

signifi-cant differences between the treated and

control groups of infants, mothers, and other

(6)

C,ASTRO(NTERTIS U- H -$ ALL OT#{128}RS 1OTAL

a’

NON -STAP$4YLOCOCCAL DISEAS(

FIG. 4. See text.

Control

2 3.Ii 2 3.7

1 1.7 0 0

17 29.3 6 11.1

2 3.14 5 9.3

22/58 37.9 13/514 213.1

2 1.2

TOTAL 108/292 36,9 90/277 32.5

or incidence of non-staphylococcal disease

were concerned (Fig. 4 and Table I).

COMMENT

Studies on an antiseptic skin-care

pro-gram for newborn infants previously

re-ported from this laboratoryl suffered

be-cause a suitable control population was not

available. Consequently, controlled studies

were designed to evaluate neonatal

staphy-lococcal colonization and resultant disease

in a nursery where conditions were

modi-fied only by the skin-care technique.

The earlier study was further limited by

the uncontrolled use of pHisohex after

dis-charge from the hospital which was not true

of the present study. This could have

in-fluenced the results and interfered with a

quantitative interpretation of the

impor-tance of prevention of staphylococcal

colo-nization in the hospital.

The investigations conducted at

Stan-ford took place ill a new, modern,

well-equipped and well-staffed university

hos-pital. The studies at Yale2 and elsewhere9’#{176}

took place in older, major centers located

TABLE I

NON-STAPHYLOCOCCAL DISEASE DATA

IANTS

Gastro-enteritis

IT-R-I

cjnctivitis

Maculo-pepular rash Pustular rash

MOTHERS

Infected Episiot Gastro-enteritis

U-R-I

Mastitis

OTHER FAMILY HEMWRS Gastro-enteritis

U-R-I

Macu1o-pu1ar rash conjwcuvitis

Experlaental

!2.e. Percent

18 30.5

32 514.2

9 15.3

3 5.1

2 3.13

61i/59 108.14.

0 0

12 6.9

is 2.3

6 3.5

22/175 12.6

!!a.

Percent

21 38.9

214 1314.14

8 lJs.8

2 3.7

3 5.5

58/514 107.13

8

14

S

19/169

13.8

2.14

3.0

(7)

260 NEONATAL STAPHYLOCOCCAL INFECTION. I

in advanced sections of technologically

highly developed countries. It remained to

be seen whether this technique was

appli-cable to less-advanced areas, whether its

introduction could be studied on a

con-trolled basis in such an environment, and

what the impact of the technique would be

under conditions of very high

staphylococ-cal prevalence.

Staphybococcal colonization of untreated

infants was heavy and occurred early. An

apparent discrepancy (between the data

in-dicating essentially 100% colonization at 48

hours of age and that indicating only 73 to

88% at any one time) results from an

ad-mixture of newborn, 1-, 2-, and even

3-day-old infants in the nursery.

The sequence and rapidity of

coloniza-tion found among untreated infants confirm

and extend previous w12 indicating

tllat colonization occurs rapidly in a heavily

contaminated environment, and that other

body sites are infected before the anterior

nares. In the treated group, colonization

oc-curred much less rapidly and involved the

nares before the umbilicus. Once the

urn-bilicus was colonized, other body sites and

the nares became infected rapidly and

per-sistently. The treatment program

mini-mized umbilical colonization in the first

days of life and reduced secondary

coloni-zation. The moist cord stump probably

favored bacterial multiplication more than

did the dry stump or normal umbilicus.

A study of the impact of the antiseptic

skin care program indicated that a few

treatment applications in the first 1 or 2

days of life exerted a definite effect on

colonization and disease incidence which

extended over the entire 3 months of the

study, although some staphylococcal

coloni-zation did eventually occur. Other workhll5

also indicates that staphylococcal infection

is common in the newborn period. Some

disease is probably unavoidable as a

con-sequence of extra-hospital acquired

staphy-lococcal infection.45 In one

representa-tive study, disease occurred in 15% of

in-fants born at home.15 In the present study,

staphylococcal colonization acquired early

in life afl(l in tile hospital caused 17

epi-sodes in 12 control infants (22%).

The infectious inocuba received by the

control group were probably greater than

those received by the treated group

accord-ing to the appearance of the culture plates

and the results of the coagulase tests. The

problem of the numbers of infectious units

required to initiate an infectious process

has been approached in highly artificial

animal modelsl6 and in adult human beings

by means of intradermal infection.17 There

is essentially no information concerning the

conversion of superficial staphylococcal

colonization into a progressive infection,

especially among newborn infants.

Most of the staphylococcal disease

epi-sodes in the control group occurred in the

first 2 weeks of life, could be attributed to

hospital colonization according to

Raven-holt and Ogden,18 and were, in fact, caused

by hospital-derived strains.8 These strains

often caused the disease episodes even

when the infants had also been colonized

later by other strains. This might argue for

greater virulence of hospital-derived strains

if the effects of timing and inoculum size

could be distinguished clearly from each

other and from virulence. The initial

cob-nizing strains did not always protect the

infants from later colonization, nor were

the initial colonizers necessarily the

etio-logical agents of later disease episodes.8

Controlled studies of similar skin care

programs have now been reported by

Plueckhahn and Banks from Australian and

by Gezon et al. from Pittsburgh.b0 The

re-sults from Australia were strikingly similar

to those presented here with respect to

re-duction of both neonatal colonization and

consequent staphylococcal disease.

Gezon et al.b0 carefully studied the effects

of hexachlorophene washing on neonatal

staphylococcal infection and disease with

results comparable to those in San Salvador.

Their studies differed in that

hexachboro-phene washing was continued for 3 weeks

after discharge from the hospital and the

infants were followed for only 6 weeks. At

(8)

ARTICLES

and 19% of 177 untreated infants had

ex-perienced staphylococcal disease, compared

to the 5% and 22% incidence in the

respec-tive groups followed for 3 months in San

Salvador. Elimination of all cases of

dis-ease occurring beyond 6 weeks from the

San Salvador calculations results in disease

mcidences among the experimental and

control groups of 3% and 17%, respectively.

The San Salvador studies offer additional

confirmation of other work reported from

Pittsburgh.b0 19 The ratio of males to

fe-males experiencing disease in San Salvador

was 4.3 to 1 in a population characterized

i)y an even male to female ratio, and was

SOme\vilat less than 3 to 1 in the Pittsburgh

study.

Initial staphylococcal colonization among

mothers and other family members was

es-sentially the same for both control and

ex-perimental groups, as was the

non-staphy-bococcal disease experience. Therefore, the

differences in colonization rates and

staphy-lococcal disease among the infants in the

two groups were probably due to the skin

care program.

Tile techniques employed to prevent

staphybococab colonization and subsequent

disease do not prevent diarrheas of infancy

and other, non-Gram positive coccal

infec-tions. The prevention of staphybococcal

dis-ease is of great interest to the

technologi-cally advanced regions of the world where

they are of relatively great numerical and

epidemiobogical importance. They are much

less important in the underdeveloped

re-gions where infantile diarrheas, neonatal

tetanus, respiratory infections, and the

other great killers of newborn infants are

widely prevalent. Anything that can reduce

morbidity under these conditions is

cer-tainly most welcome, but where funds and

personnel are in critically short supply,

large investments in either must first be

de-voted toward solution of the major

prob-lems.2#{176}

SUMMARY

The dynamics, consequences, and

pre-vention of neonatal staphybococcal

coloni-zation were studied in San Salvador, El

Salvador. The results indicate that:

All untreated infants who resided in the

hospital for more than 48 hours became

colonized. Umbilical preceded nasal

cob-nization in this group.

An antiseptic skin care program

effec-tively prevented colonization among treated

infants in the hospital. Colonization in this

group did occur in the first 3 months of

life, but never to the extent found among

the controls. Nasal

preceded

umbilical

cob-nization in the treated group.

Staphylococcal disease occurred four

times as frequently in the control group as

in the treated group and four times as often

in males as in females.

Initial staphylococcal colonization in

mothers and family members of the two

study

groups and the non-staphylococcal

disease experiences of both populations

were essentially identical. Therefore, the

differences in colonization rates and

staphy-bococcal disease among the infants were

probably due to the infant care program.

REFERENCES

1. Simon, H. J., Cluck, L., and Yaffe, S. J.:

Effective control of staphylococci in a

nursery. New EngI. J. Med., 265:1171, 1961.

2. Gluck, L., and Wood, H. F.: Effect of an

antiseptic skin care regimen in reducing

staphlococcal colonization in newborn

in-fants. New EngI. J. Med., 265:1177, 1961.

3. Standards and Recommendations for Hospital

Care of Newborn Infants. American

Acad-emy of Pediatrics, 1801 Hinman Avenue,

Evanston, Ill., 1960.

4. Elek, S. D.: Staphylococcus Pyogenes and Its

Relation to Disease. Edinburgh and

Lon-don: E. and S. Livingston, Ltd., 1959, pp.

178-218.

5. Rantz, L. A., and Rantz, H. H.: Sensitivity of

various clinically important bacteria to four

antibiotics: Results obtained with a plate

screening method. Stanford Med. Bull.,

11:183, 1953.

6. Simon, H. J., and Undseth, S.: Simple method

for phage-typing of staphylococci. J. Bact.,

85:1147, 1963.

7. Allwood-Paredes, J., Simon, H. J., and

Tre-jos, A.: Infeccion Estafilococcica en el

Hos-pital de Maternidad. Arch. Col. Med. El

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262 NEONATAL STAPHYLOCOCCAL iNFECTION. II

8. Simon, 11. J., Allwood-Paredes, J., and Trejos,

A. : Studies on neonatal staphylococcal

in-f’ction. II. Epidemiology of staphylococcal

infection and diseaSe. PEDIATRICS 35:262.

1965

9. Plueckhahn, \ D., and Banks, J.: Antisepsis

and staphlococcal disease in the newborn

child. Nte(l. J. Aust., 2:519, 1963.

10. Gezon, 11. M., Thompson, D. J., Rogers, K. D.,

Hatch, T. F., and Taylor, P. M. :

Hexa-chlorophene bathing in early infancy: Effect

on staphvlococcal disease and infection.

New EngI. J. Med., 270:379, 1964.

11. hurst, V.: Transmission of hospital

staphy-lococci among newborn infants. I.

Observa-tions on the contamination of a new

nurs-cry. PEDIATRICS, 25:11, 1960.

12. Hurst, V.: Transmission of hospital

staphy-lococci among newborn infants. II.

Coloniza-tion of the skin and mucus membranes of

the infants. PEDIATRICS, 25:204, 1960.

13. hurst, V.: Staphylococcus aureus in the

in-fant upper respiratory tract. I. Observations

on newborn babies. J. Hvg. (Cantab), 55:

299, 1957.

14. Hurst, V.: Staphylococcus aureus in the infant

upper respiratory tract. II. Observations on

domiciliary delivered babies. J. ilyg.

(Can-tab.), 55:313, 1957.

15. \Villiams, R. E. 0.: Carriage of staphylococci

in the newborn. Lancet, 2:173, 1961.

16. Simon, II. j.: Effect of tetracycline on a

stand-ardized instracutaneous staphylococcal

in-fection of guinea pigs. Proc. Soc. Exp. Biol.

Med., 113:518, 1963.

17. Foster, \V. D., and Hutt, M. S. R.:

Experi-mental staphylococcal infection in man. Lancet, 2:1371, 1960.

18. Ravenholt, R. T., and Ogden, M. :

Epidemi-ology of staphylococcal disease of mothers

and infants. Amer. J. Dis. Child., 106:73,

1963.

19. Thompson, D. J., Cezon, H. M., hatch, T.

F., Rycheck, R. R., and Rogers, K. D. : Sex

distribution of staphylococcus aureus

cob-nization and disease in newborn infants.

New EngI. J. Med., 269:337, 1963.

20. McDermott, W. : The role of biomedical

re-search in international development. J. Med.

Educ., 39:655, 1964.

Acknowledgments

Individuals and organizations from El Salvador

who aided these studies were: Srs. Armando

Frenkel, Andres Molins, Jainie Pascual, Jaime

Pascual Portet, Carlos Cuirola, Alvaro Velasquez,

Roberto Daglio, Juan T. Wright; The Max Freund

Foundation; Bonibla, Wilson y Co.; Handal y

So-brinos; Casa Goldtree; Liebes y Co.

The assistance of the following is gratefully

acknowledged: Birgitta Akerblom, Amada Cuirola,

Juan Menendez, Mauricio Ramirez, Shirley

Robin-son, and Solveig Undseth, technicians; Albertina

de Mayoral, Barbara Ryder, and Maria Elena

Val-des, nurses; Jorge Chicas, Enrico Hcnriquez, Carol

Cullum, Stephen Gregg, and Richard Stifler,

medi-cal students from the Facultad de Medicina,

Uni-versidad de El Salvador, Stanford University School

of Medicine, respectively.

Dr. Antonio Lazo-Cuerra and the personnel of

the Hospital de Maternidad de San Salvador

rendered invaluable assistance.

II.

Epidemiology

of

Infection

and

Disease

T

IlE OCCURRENCE of staphylococcal

infec-tion and disease among newborn

in-fants in San Salvador, El Salvador,

pro-vided an opportunity to study these

prob-lems in a country undergoing technological

development. The companion paper1 dealt

with the dynamics of neonatal colonization

in the Hospital de Maternidad of San

Sal-vador, the incidence of colonization among

mothers and family members of the study

population, and the prevention of

staphylo-coccal colonization and consequent disease

in the infants.

The present paper is concerned with

studies of the staphylococci encountered in

the hospital and community, and with the

epidemiology of staphylococcal

coloniza-tion and disease.

General

MATERIALS AND METHODS

The environment, over-all plan, source

and composition of the study population,

and the techniques employed have been

described.’ Epidemiobogical and analytical

methods are considered below under the

appropriate subheadings.

Identification of Strain Relationships

To be considered identical, two

staphy-lococcal isolates should not differ in more

(10)

SIS?ANCE

PA1TEI #{149} TOTAL

PER CENT

HOSPITAL

ACQUIRED PER CENT

CONIUNIT! PREVALENT

PER CENT

pstce 178 26.02 2 1.12 176 98.88

Pate. 211i 31.3 16 7.138 198 92.52

PStce 88 12.87 60 68.2 28 31.8

PsTce 18 2.6 15 83.33 3 16.67

PSTce 173 25.3 iSis 914.8 9 5.2

PSTCe 6 0.9 5 83.3) 1 16.67

PSTCE 7 1.02 0 0.0 7 100.0

TOTAL 68l 100.0 262 (38.3) 1422 (61.7)

PIIACE

GRcXJP TOTAL

PER

CENT

HOSPITAL

AOQUIRED

PER

CENT

CW1I1TY

PREVALENT

PER

CENT

I 201 29.14 liii 56.7 87 143.3

Misc.se 80 11.7 76 95.0 la 5.0

7 Selected Stra.ina 227 33.2188 82.8 39 17.2

II 86 12.6 18 20.9 68 79.1

III 182 26.6 148 26.1, 1314 73.6

IV 1 0.11. 0 0.0 1 100.0

NT..’ 131a 19.6 6 14.5 128 95.5

TOTAL 681k 100.0 262 38.3 1422 61.7

. pj: 80/81, 52A/80, 80, 29/52A/80, 52A/80/81

187, 81

I aild i\I, in more tilan two strong reactions

in group III, or in more than two weak

reactions in Group II. Tile antibiograms of

tile two strains should match or differ only

in resistance to streptomycin. The

combina-tion of phage-typing patterns with

antibio-grams greatly simplifies identification.

Other workers have used similar criteria

vith comparable results (reviewed in 2).

RESULTS

I. Phage-Typing and Antibiograms

A summary of tile results of phage-typing

and antimicrobial sensitivity testing is

shown in Table I. The 684 separate

in-stances of colonization were defined as

fob-lows:

A family member was considered

cob-nized once if staphylococci were present at

either of the 2 culturing episodes. Two

colonizations were recorded when the

strain(s) recovered at the second session

differed from the first isolate(s).

A mother was considered colonized once

if cultures from either site were positive on

admission or became so thereafter. An

ad-ditional episode was recorded whenever the

strain(s) at either site differed from the

original isolate(s), or when multiple

cob-nizations at the same site occurred.

Rever-TABLE I

CorII’AmsoN OF hOSPITAL-ACQUIRED WITH CorIrxuNrry-PnEvALENr

STRAINS OF STAPHYLOCOCCI-SAN SALVADOR Combined Data

‘lower case letters - sensitive Upper case letters - resistant **Miscellaneous

‘sNon-Typabl. at RTD and at 100 x RYD

P(p) - penicillin-C 1.0 unit/al

S(s) - streptoeycin 5aagJal

T(t) - tetracycline 10 a’g/sl C(c) - chiorsaphenicol 10 8g/al

(11)

264 NEONATAL STAPHYLOCOCCAL INFECTION. II

sion to the original strain at an initially

colonized site was not counted as a

sepa-rate episode.

Data obtained from infants were

ana-lyzed in the manner described for mothers.

The decision as to whether any

particu-bar colonization represented acquisition of

a strain from the hospital environment or

from the community was based chiefly on

timing.

Strains found on infants during their stay

in the hospital or at the first home visit

(

generally within hours of discharge) were

considered hospital derived unless the

mother had been colonized on admission

with the strain later recovered from the

in-fant, or acquired a strain during her

hos-pitab stay later isolated from the infant.

Strains isolated from the mothers on

ad-mission to the hospital were considered

community derived, as were all strains

ac-quired beyond the first day after discharge.

Those isolated in the hospital or on the first

day after discharge were considered

hos-pitab derived, as were later isolates if the

respective infants had become colonized

with hospital-derived strains later found on

the mother.

Colonizations of family members were

considered community derived if found at

the first home visit, or if their strains

dif-fered from those of mother or infant.

Fam-ily members’ strains were considered

hos-pital derived if colonization ocurred with

hospital-derived strains first found on

mother or infant or later occurred in

ac-cord with these criteria.

The phage-types and antibiograms of

hospital-prevalent strains differed sharply

from those in the community.#{176} This

infor-mation was not generally used for decisions

concerning hospital versus community

derivation, but chiefly to detect

intra-familial spread of staphylococci and to

trace the bacteriological causes of disease

episodes. On this basis, 262 (38.3%) of the

#{149}A tabular analysis of the phage-types and

antimicrobial sensitivity patterns of the strains is

available on request from the senior author.

684 cobonizations were considered hospital

acquired and 422 (61.7%) were considered

community derived (Table I).

The data show that 5 selected strains of

phage group I and the 2 strains of phage

group M occurred much more commonly

in the hospital than in the community

(Table I). Phage groups II, III, and the

non-typable strains predominated in the

community. Most of the hospital-derived

strains were resistant to 2 or 3

antimicro-bials, whereas the overwhelming majority

in the community was either sensitive to all

5 antimicrobials or resistant to penicillin

alone. All but two (1%) of the 178 completely

sensitive strains were community derived.

The 7 strains (phage type 75) resistant to all

five antimicrobials were found only in tile

community in 4 families without apparent

contact. This strain was encountered 19

times, but only once in the hospital-derived

specimens. No quintuply resistant strains of

any type were hospital derived.

II. Staphylococcal Disease Episodes

The incidence of staphylococcal disease

among mothers and family members did

not differ significantly between the control

and experimental groups, but that among

infants in the control group differed

sharp-by (17 episodes involving 12 infants (22%))

from the experimental group (3 episodes

among 3 infants [5%])’ (Table II). Analysis

of tile timing of these episodes and the

etio-logical agents revealed further significant

divergences.

MOTHERS-EXPERIMENTAL GRoup: Three

episodes occurred in 3 mothers (5%). The

case of mastitis-breast abscess caused by

strain 80/81 RSRSSf 10 weeks following

delivery was traced to a strain first isolated

from her infant at 4 weeks of age. It had

not been previously isolated from other

family members or the patient until 2

f The letters R and S are used to designate the

resistance (R) or susceptibility (S) of a strain to an

antimicrobial. The patterns are always listed in the

same order: Penicillin, streptomycin, tetracycline,

erythromycin, chloramphenicol, RSRSS means

(12)

TABLE II

STAPHYLOCOCCAL DISEASE EPISODES

0

3

0

0

0

8

STAPHYLOCOCCAL DISEASE - IMBIVIDIJALS AFFECTED Mastitts-Brea.gt Abscess

Furuncies

Dacryocystitis - Conjunctivitis

Infected Episiotom.y

Total

I!OANTS:

Pyoderaa

Conjunctivitis

Ma.stitis

Furuncles Total FAMILY MEMBERS:

Abscesses

Paronychia

Total

TOTAL EPISODES

Mothers Infants Family Members

Total

1 0

5

10

2

1

I’

17

6 1

7

29

DISEASE CATEGORY M0?HE:

months after delivery. This infection was

therefore presumed to be extra-hospital

de-rived and spread from infant to mother

(Table III).

The source of the episiotomy infection

with strain NT RSSSS on day 11 after

de-livery was not defined since neither the

patient, the infant, nor other family

mem-bers were colonized prior to the episode.

Therefore, the strain was presumed to have

been community derived (Table III).

In the third instance, the mother became

colonized with strain 187 RRSSS on the

second hospital day despite colonization

with strain 3B/3C/55/71 SSSSS at both

test sites on admission. The infant became

colonized on the third day of life with

strain 187. The mother experienced a vulval

EXPERIMENTAL GROUP

CONTROL

GRJP

No./Total. Percent Nq,JTotal.

3/58 5.2

3/59 5.1 12/514

1/175 0.6 7/169

7/292 2.1 22/277

Percent

7.14

22.2

Li

7.8

furuncle 3 months after delivery, and strain

187 RRSSS was recovered from this lesion.

This episode was probably hospital

de-rived (Table III).

MOTHERS-CONTROL GROUP: Five

epi-sodes occurred in 4 of these mothers (7%).

Strain 80 RRRSS caused 2 cases of

mastitis-breast abscess in the same patient 5 days

and 2 weeks postpartum. This strain was

acquired by mother and infant on the

mother’s second hospital day, the infant’s

day of birth (Table IV).

The third case of mastitis-breast abscess,

strain

7

RSSSS, occurred on the fourth

postpartum day. The infant was colonized

on his second day of life; the mother’s

colonization was not detected until after

(13)

Status of

Inf ant & Fsmi

Infant first colonized

at 14weeks with this

strain

wr

55555

187

55555

11 days Infant never colonized

89878 Infected

Episiotomy

1456914 Boil on

Vulva

FAMILY MEMBERS

69168. Boil on 52A/?9

ear 55555

69168. Stye 3C

55555

Hospital

Self

Self

Hospital to

mother to

infant

Grandparent to infant

I?ANTS

67530 Pyoderma 187

RRRSS

89878 Conjuncti- 71

vitis SSSSS

2147514 Conjuncti- 7

Titis RSSSS

3months Infant colonized with

this strain at tmo

months. First

coloni-zation. Mother

colonized earlier.

17 days Infant never colonized.

Grandparent colonized

with this strath on

first home visit.

26 days This strain was not found on any famtly member. Infant colonized with

other strain.

266

NEONATAL

STAPHYLOCOCCAL

INFECTION.

II

MOThERS

TABLE III

STAPHYLOCOCCAL DISEASE DATA EXPERiMENTAL GROUP

Reg, No. Lesion

38014 Mastitis

Phage Type!

Antibiograa Onset

80/81 10weeks

RSRSS

3 months Infant not colonized

Mother colonized on 3rd

day with this strath. (Colonized on admission nnd later with three

other strains.)

2 month., No one else in family

colonized with this strain.

2 month, No one else in family

colonized with this

strath.

* Neither mother nor infant th tily 69168 were colonized.

Probable Source Infant to

mother

spread were hospital to infant to mother.

The source of infection for the case of

dacryocystitis occurring on day 13 could

not be determined, but was probably

com-munity derived on the basis of timing and

antibiogram. It was caused by a mixed

in-fection with completely sensitive strains

29 and 7/77. Neither tile patient, her

in-fant, nor other family members ilarbored

these strains prior to the disease episode.

Tile patient was the probable source of

the case of furunculosis (strain 3C RSSSS)

wllich occurred at 3 months. She carried

this strain on admission and harbored it

throughout the study. The infant was

colo-nized in the hospital with another strain,

but acquired his mother’s strain at 4 weeks

of age (Table IV).

In summary, hospital-derived infection

was found in only one of the three disease

episodes occurring in mothers of the

ex-perimental group of infants, but was

di-rectly or indirectly implicated in 3 of the 5

episodes in the control group.

FAMILY MEMBERS-EXPERIMENTAL GROUP

AND CONTROL GROUP: The sources of

staphylococcal disease episodes in family

members of the 2 study groups were

usually autogenous (Table III and IV).

Only one case of hospital-derived infection

occurred in the control group. The

inci-dence of disease among control group

fam-ily members probably was raised

fortui-tously by a family epidemic (Table IV).

INFANTS-EXPERIMENTAL Gnoup:

(14)

STAPHYLOCOCCAL C3SEASE - INFANTS

U CONTROL GROLP

2 3 4 5 6 7 8 9 0 2 WEEKS WEEKS 4WTER DELIVERY

STAPHYLOCOCCAL DISEASE - MOTHERS

267

that one of the 3 cases was due to

hospital-derived colonization of the mother with

secondary spread to the infant, and the

second to a strain derived from a

grand-parent. The source of the third case was

never determined since neither hospital

derivation nor secondary spread within the

family could be documented (Table III).

INFANTS-CONTROL GROUP: Eight of the

10 cases of pyoderma in this group

occur-red between the third and tenth days of

life. The timing of these episodes, the

na-ture of the infecting strains, the

coboniza-tion sequences, and the probable sources

of infection are shown in Table IV.

The significant excess morbidity in the

control group was clearly due to

hospital-ac(1uired strains; 15 of the 17 episodes

among 11 of the 12 controls fell into this

category. The timing also suggests hospital

derived infection in the great majority3

(Figure 1).

The first strain to colonize an infant was

often but not always the cause of the

dis-ease episodes. Furthermore, prior

coloniza-tion did not necessarily protect an infant

from eventually acquiring a diseasepro

(lucing strain (Table IV).

In.

Sources of Infant Colonization

FIRST COLONIZATION AT NOSE AND/OR

UMBILICUS: Data from timing,

phage-typ-ing, and antibiograms were pooled for

determinations of the precise routes of

primary colonization of infants’ nares and

umbilici. Two hundred six strains were

re-covered from 162 cobonizations, 60 (79

strains among 59 infants) in the

experimen-tal group and 102 (127 strains among 54

in-fants) in the control group (Tables V and

VI). The routes of colonization differed in

several particulars.

Direct primary hospital-derived

coloni-zation of the infants occurred 2.3 times

(38%) in the experimental group and 89

times (87%) in the control group (Table V).

Thirteen (22%) of the 59 infants in the

ex-perimental group were never colonized

whereas all of the control group were

colonized.1 Half (50.1%) of the colonizations

-j-I 3 4 5 6 7 8 9 0 ii 2WEEKS

WEEKS AFTER DELIVERY

STA5,qfL000CCAL DSEASE - FAM,LY P.#{128}MBERS

2 123456789,01112

WEEKS AFTER DELIVERY

Fic. 1. See text.

ill the experimental group, I)ut only 10.5%

in the control group, were traced to spread

from mothers and other family members

(Table V). These first episodes represented

only 54.9% of the total colonizations among

the infants (see Sections I and V).

The 162 first colonizations involved 206

separate strains; their distribution by site

and phage group is shown in Table VI. The

60 episodes among the experimental group

involved 19, and the 102 episodes among

the controls involved 2 colonizations with

2 strains at eitiler test site (double

coloni-zations).

The chief differences in the strains which

colonized the two groups of infants

per-tamed to phage groups M and NT. In the

control group, 25.2% were due to group M

as against 7.6% in the experimental group.

Non-typable strains accounted for 24.1% of

the colonizations among the experimental

group as compared with 8.7% among the

controls.

IV. Sources and Routes of Maternal

Colonization

The criteria employed to trace maternal

colonizations were identical to those used

for infants (Section III) (Table VII).

Fifty-five colonizations were recorded among

mothers of the control group and 44 in the

experimental group. Nine (17%) in the

(15)

through-268 NEONATAL STAPHYLOCOCCAL INFECTION. II

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(17)

TABLE VI

ANALYSIs OF FIRST COLONIZATI0NS#{176} Arioxc,

INFANTS BY SITE AND PHAGE Cnour

Percent

32.3

Experimental Group

flares Umbilicus Total Percent

16 7 23 29.1

N 16 16 32 2.2 2

h

6 7.6 38 18.b

II 3 9 12 9.h h 6 10 12.7 22 10.7

III 16 l 31 2h.h 13 8 21 26.6 2 2.2

NT

S

6 II 8.7 13 6 19 2b.l 30 lh.6

TOTAlS 66 61 127 38.S b8 31 79 61.S 206 100.0

Catagry

TABLE VII

Rotrrr.s OF COLONIZATION OF MOTHERS

First

Psr-2L ! !

14

(, 61.8

20 29J

LI 6 10.9

3 5’)

9.1

0) 10 18.2

(9)

36 19 55* 100.0

0

S

Per-______

Total cent

ii)..)

143.2 53 53.5 5)

0 0 6 6.1

9)

22.7 15 15.2

1)

15 314.1 25 25.3

(12)

33 11 14144’*lOO.O 99 100.0

270 NEONATAL STAPIIYLOCOCCAL INFECTION. II

tontrol Grop

2!2

!!!!

Umbilicus Total

I 26

]S

hi

Control Group -

b

Infants

Experimental Group - 9 Infants

Totals Percent

6h 31.1

* All colonisations ire counted, whether they’ occurred once

only or not. First colonisations re also counted whenever

they occurred - from the day of birth through three months of age.

H -> N

H -> B --> N ? -> B --> N

F --> P1

F -a B -> N

7 -> N Never colonised

TOTALS

Control Group

Second

1

9

0

5

Experimental Group First Second

10 1K

3 2

0 0

11 5

1 0

15 0

Total

Per-No. cent

C Includes one double and one triple colonization *5 Inclucs three double colonizations

H- Hospital

B - Infant

F - Family Member

N - Mother

7 - Undetermined (neither hospital, nor infant, nor family yielded the

(18)

corded as “never colonized” (13 (22%) of

the experimental group of infants and none

of the control group) (Table VIII).

Single colonizations at either site

pre-ceded and followed by negative cultures

were recorded as “once only” (only in the

experimental group).

“Persistent colonization” referred to 2 or

more sequential identical isolates from ally

one site (25 infants (42.4%) of the

experi-mental group and 39 (72.2%) of the

con-trots) (Table VIII).

A “change in colonization” indicated that

any one site first yielded one or more

strains and later another (or others) with

or without persistence of the first. No

change was recorded when the first culture

yielded 2 strains and later cultures

mdi-cated persistence of only one (Table VIII).

Most (93%) of the changes in colonization

TABLE VIII

SECONDARY STAPHYLOCOCCAL CoLONIzATIoN AMNC INFANTS

SAN SALVADOR

Category

No.

Infants Sites Chs

0 0 0

No.

Infants SE Chans

13 26 0

0 0 0 11K

8

39* 25.

17 22

25 II

U) 1l)

39 12

15 U

21 1

3 0

21 5

12 3

11 2

3 0

Nr of First Colonization. 102 60

Total Number of Colonization. 215 s---.s 295 s-.---. 80

out the study as compared to 12 (21%) in

the experimental group.

Hospital-to-infant-to-mother accounted

for 53%, and all hospital-derived

coloniza-tions for 62%. Direct colonization of the

mother from hospital sources accounted

for 14 (32%) in the experimental group.

Directly or indirectly, the hospital was

found to he the source of 19 (44%) of the

44 colonizations. The largest fraction (34%)

of maternal colonizations in the

experi-mental group, but only 10 (18%) of those

in the control group, could not be traced

(Table VII).

V. Analysis of Changes in Colonizations

Among Infants

The criteria for the conclusions and

re-sults were: No colonization at either site

for the entire period of the study was

re-Never colonized Colonized o,a:e onl.y

Wares

Uabilic.s Persistent colonizations

Wares

t’sbilicus

Changes in colonization

Wares

On. Change Two Changes Three Changes Usbilicag

0.e Change Two Changes Three Changes

Poer chang.s

$er of 0’’a,!

Control Grasp Ezp.ria.ntal Grasp (51. InfantiJ (59 Inf ante)

1 0

113 20

e Wanbers in this colean indicate ner of infants counted in the series.

(19)

272 NEONATAL STAPHYLOCOCCAL INFECTION. II

Number of separate colonizations 52 55.9 hi LL:!.

\ere inter-phage-group changes, a

consid-crable advantage in data analysis. The data

and an interpretation will be published

separately.

VI. Changes in Maternal Colonizations

Twenty-one mothers (39%) in the control

group and 14 (24%) in the experimental

group changed strains at least once (Table

IX). Fifty-two (56%) separate colonizations

occurred among the control group and 41

(44%) in the experimental group. These 93

episodes involved 99 separate

staphylococ-cat strains. Sixty-two interchanges were

recorded among individuals whereas 31

involved only changes in site. Ninety-three

percent were inter-phage group changes.

VII. The Relationships between Maternal

and Infant Colonization

MATERNAL COLONIZATION WHEN

IN-FANTS REMAINED UNCOLONIZED: Only 13

infants in the experimental group fulfilled

the necessary criterion. Seven of the 13

mothers remained uncolonized although 2

family members of one mother-infant pair

were carriers and 2 family members of

another pair cxperienced staphylococcal

disease.

Four of the remaining 6 mothers were

staphylococcal carriers on admission or

be-came colonized during hospitalization.

Three returned to families in which carriers

were present. There were no other family

members in the home of the fourth. One

mother became colonized on the sixth day

after delivery and remained so for 2 weeks,

although none of the 7 others in her family

was ever colonized. The thirteenth mother

was colonized only at the 3-month visit.

Three of her family members had been

colonized throughout the follow-up period.

COLONIZATION OF INFANTS WHOSE

MOTH-ERS REMAINED UNCOLONIZED: Twelve

moth-ers in the experimental group and 9 in the

control group fulfilled the necessary

enter-ion. Six of the 12 infants in the

expenimen-tat group remained uncolonized. The

re-maining 6 experienced 10 colonizations, 6

were colonized 6 times in their first week

of life. Three of these infants were

defi-nitely colonized with hospital-derived

strains, and the other 3 by family members.

The fourth was colonized after 2 weeks,

and the fifth after 2 months, both with

family-derived strains. The sixth infant

acquired 2 additional strains at 2 months

of age after an initial colonization on day

TABLE IX

STAPHYLOCOCCAL COLONIZATION OF MOTHERS

SAN SALVADOR

Category

Never colonized

Not colonized on admission

Colonized persistently thereafter

Changed Strains Once

Colonized on adRis3ion

Persistently colonized

Changed strains once

Changed strains twice

Changed strains one or more times

Control Group

(sb)

L2.:.

Percent

9 16.7

28 Sl.9

15

13

17 31.5

9

S

3

21 38.9

rimenta]. Group

Percent

12 207

26

20

6

20 31.S

13

2

References

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