CUTANEOUS CANDIDIASIS IN EARLY INFANCY AND CHILDHOOD

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CUTANEOUS

CANDIDIASIS

IN

EARLY

INFANCY

AND

CHILDHOOD

By

Philip

J. Kozinn,

M.D., Claire L. Taschdjian, B.Sc., David Dragutsky, M.D.

and Arnold Minsky, M.D.

Department of Pediatrics, Maimonides Hospital, Brooklyn, New York

(Submitted April 9, accepted May 15, 1957.)

This work was supported by grants from the Jewish Philanthropic League of Brooklyn, New York, and the Squibb Institute for Medical Research, New Brunswick, New Jersey.

ADDRESS: (P.J.K.-Office) 141-05 Newport Avenue, Belle Harbor 94, New York. 827

I

N CONTRAST to the care devoted to the

detection and treatment of oral thrush

in the newborn infant little attention is

usu-ally paid to the problem of cutaneous

candi-diasis in these infants. It is not generally realized that such lesions occur frequently

in infants with oral hr2 These infants

invariably harbor Candida ahbicans in the

intestine,35 and the infected stools may

constitute a focus for cutaneous infection.68 Furthermore, it is not generally

appreci-ated that the mouth may be by-passed, and

the infection be confined exclusively to the

diaper area9 where it may be overlooked

or misinterpreted. Finally, many clinicians

are reluctant to accept Candida albicans as

the etiologic agent of skin lesions, in view

of the numerous statements in the literature

postulating saprophytism of the organism

on the skin.103

In an attempt to clarify these issues, the

following points were investigated in the

present study: 1) the distribution of clinical

findings in newborn infants harboring

Can-dida albicans in the intestine; 2) the

inci-dence and significance of Candida albicans

in the mouth, stools, and skin of newborn

and older infants suffering from various

diaper dermatoses.

METHOD

OF

STUDY

The incidence of candidiasis was established in the course of a routine laboratory study

in-volving 2,175 consecutive newborn infants. In

1,655 of these babies (Group I), oral smears

and cultures for Candida albicans were taken

routinely between the third and fifth day of life.

Examination of the stool was done only in those infants in whom the oral smear was positive.

In 520 unselected babies (Group II), exam-ination of material from the mouth and stool

was done simultaneously between the third and fifth day of life. This group included 15 infants with “red buttocks.”

In this manner, 48 carriers of C. albicans

were detected in Group I and 52 in Group II.

Of this total of 100 infants, 15 were lost from

observation before the presence or absence of clinical candidiasis could be established. Two additional infants immediately received prophy-lactic treatment with nystatin and did not de-velop lesions. These last 17 infants are there-fore omitted from the present study.

The manifestations of clinical candidiasis were analyzed in 83 newborn infants who harbored C. albicans in the intestine.

These 83 infants were inspected daily for

clinical evidence of oral and cutaneous lesions

until they were discharged from the hospital. Scrapings and cultures were taken from all cutaneous lesions in this group, as well as from the 15 infants with “red buttocks.”

In addition, diaper dermatoses clinically

sug-gestive of candidiasis were studied in 47 infants aged 5 weeks to 22 months. These were private patients who had been referred for mycologic

studies.

In the majority of these patients the condi-tion had been present for 1 to 2 weeks.

Scrap-ings and cultures from the cutaneous lesions were taken in all cases. Additional cultures from

the mouth and stools were done where feasible. Scrapings and cultures from the skin were repeated in areas which appeared cured and had previously been positive for C. albicans.

Oral and fecal specimens were incubated overnight on Sabouraud’s agar at 37#{176}C.Slides were read the following morning. Scrapings of the skin were cleared in 10% potassium hydrox-ide solution and read immediately.

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TABLE I

CLINICAL FINDINGS IN 83 NEWBORN INFANTS

IIARBOII-ING CANDIDA ALBICANS IN THE INTESTINE

16/35 45.7% 17/36 47.2% 23/34 67.6% 34/47 72.3% 36/36 45/47 100.0% 95.7% 828

the basis of formation of chiamydospores on

“cream of rice”-Tween 80 agar.’4 Yeast-like

iso-lates which failed to form chlamydospores on this medium were identified by their utilization and fermentation of dextrose, maltose, sucrose and Iactose, and by their color reaction on

Pagano-Levin medium.bo.17*

Newborn Infants

RESU LTS

CORRELATION BETWEEN LABORATORY AND

CLINICAL FINDINGS: Of 83 newborn infants,

75 were found to harbor C. albicans in both

mouth and intestine, while 8 harbored it in

the intestine only. The laboratory and chini-cal findings in these 83 cases are shown in

Table I.

In all 15 infants with “red buttocks” the

stools, mouth and skin were negative for

C. albicans.

It will be noted that a higher percentage of lesions of the skin was seen in Group II than in Group I, both in combination with oral thrush and in terms of over-all

mci-dence.

The main reason for this difference lies in the method used to detect CandiJa albicans.

In Group I, where examination of the stool

was done only in those infants who had

I)Ositive oral smears, no eruptions on the skin were noted prior to the onset of oral thrush, and no special effort was made to detect lesions on the skin in infants whose oral smears were negative.

In Group II it was attempted to detect

both oral and cutaneous lesions by simul-taneous examinations of oral and fecal ma-terial. Here 26% of the cutaneous lesions were detected before the onset of oral thrush, while in 11 of the 34 cases in this group oral thrush did not develop at all. Cutaneous lesions are therefore easily over-looked if the only method of detection em-ployed is the examination of the oral smear and culture, especially since the mouth may be negative for C. albicans, as was the case in 8 out of the 47 infants in Group II.

0 Candida krusei, Candida parakrusei, and

Can-dida tropicalis were isolated in one instance each from newborn infants but were not associated with

clinical findings.

Clinical and .ifycologic Findings Group I 36 Positive Infants Out of 1655 Oral Tests Preceding Stool Examina-tion Group II 47 Posilire Infants Out of 520 Siinal-tar eous Oral and Fecal Examina-tions

Cutaneous lesions only Oral smear or culture positive Oral smear or culture negative

Cutaneous and oral lesions

Oral lesions only

No lesions at discharge

Oral smear or culture positive

Oral smear or culture negative

1 0 16 19 0 0 5 6 23 11 0 2

Incidence of cutaneous lesions in oral thrush

Number

Per cent

Over-sill illcidence of cutane-ous lesions

Number Per cent

Total incidence of eandidiasis Number

Per ce;it

The time of detection of the cutaneous

lesions in the two groups is shown in Table

II. It will be noted that in the majority of

cases the lesions developed during the first week of life.

It was noted in the course of this study

that in some patients, Candida albicans could be detected in the stools as early as

the second day of life while it appeared

in the mouth later or not at all. However, the majority of the infants was not studied prior to the third or fourth day of life.

It follows that combined examinations of

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TABLE IL

I 17

II 34

10 60 7

28 82 (;

74.5

4() 18

23.3

13

ARTICLES 829

ONSET OF CUTANEOUS CANDIDIASIS DURING TIlE FIRsT Two WEEKS OF LIFE IX 51 INFANTS

First H’eek Second Ii eel

TotalNuinber Group

of Infants .‘s umber of .‘su’nherof

Per (‘ent Per ( en!

i ases (uses

Total 51 38

of Candida albicans than will oral tests alone. Both methods permt prediction of

oral thrush with a high degree of certainty.5

However, results obtained here show that

fecal examinations furnish more reliable

indications of existing or potential

cutane-ous candidiasis, especially since the

or-ganism may “skip” the mouth enthrehy.

It is significant that only 2 out of 83

new-borns who harbored C. albicans in the

in-testine failed to develop clinical candidiasis

before discharge from the hospital. In

con-trast to conditions in older individuals, it

appears that the presence of the organism

in newborns is hIghly indicative of clinical

candidiasis in the form of oral thrush,

cu-taneous lesions, or both. A high percentage

of these dermal lesions may appear before

the seventh day of life, while the infant is

still in the newborn nursery.

SYMPTOMATOLOGY AND RESPONSE TO TREATMENT OF NEONATAL CUTANEOUS CAN-DIDIASIS: In most cases the first clinical

manifestations noted consisted of

macera-tion of the anal mucosa and the perianal

skin. This picture distinguishes neonatal

cutaneous candidiasis from “red buttocks”

in which the perianah region is usually not affected (see Fig. 1).

From th:s focus the condition spread

rap-idly to adjacent areas. In female infants

raw red areas appeared between the labia

majora which were partly denuded and

partly covered with a pseudomembrane.

Subsequently small papules were seen on

the glabrous skin. These developed into

vesicles which ruptured, leaving

char-acteristic erythematous, “white-collared”

patches. Intertrigo in the supra-anal cleft

and in the groin was present in some cases.

One infant, 5 days of age, had paronychiae

of two fingers in addition to oral thrush and lesions in the diaper area.

In all instances, scrapings of the skin

showed spores and mycehia of C. albicans

in direct examination.

Therapy was begun within 24 to 48 hours after the appearance of the eruptions. Cures were obtained with nystatin ointment*

within 5 days, and with amphotericin B

ointment0 within 7 to 8 days, with

ui-formly good results.’5 However, in some

cases the condition became aggravated after circumcision, and longer treatment was

re-quired thereafter.18

Older Infants (Ages 5 Weeks to 22 Months)

LABORATORY AND CLINICAL FINDINGS: Of

the 47 young infants in this group, 30

pre-sented the erythematous plaques bordered

by “white-collared” satellite lesions which

are characteristic of cutaneous candidiasis.

Six of these infants had oral thrush.

Seventeen patients had erythematous he-sions in the diaper area which had been provisionally diagnosed as seborrheic, con-tact, or ammoniacah dermatitis, but in which candidiasis had to be ruled out. In these 17 cases C. albicans was not isolated from the

skin, mouth or stools.f

In all 30 cases cLnically suggesting

can-0 Both ointments were used in 2% concentration

in “plastibase” (95% liquid petrolatum, 5%

poly-ethylene) and applied three times daily.

f Candida parapsilosis was isolated from the

skin and stools of one of these patients. No

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Fic. 1. Cutaneous candidiasis in an infant, 6 (lays of age. Note maceration of anal

niucosa and spreading of the condition from the anal region.

(lidiasiS, C. albicans was demonstrated in

the skin by direct examination and culture.

Cultures were obtained from the mouth and

stools of 25 of these patients.

Table III shows that 88% of these infants

harbored C. albicans in the stools, while

56% harbored it in the mouth.

RESPONSE TO TIUnIAPY: In the patients

in this group the lesions had been present

for 1 to 2 weeks before treatment could be

begun (see Fig. 2). They were significantly

slower to respond to therapy than those

in newborn infants, requiring 17 to 18 days

with nystatin and 12 to 13 days with

amphotericin B ointment. Eighteen per

cent were cured only after supplementary

nonspecific therapy with

fluorohydrocorti-sone and other medications was given.*

DISCUSSION

It has been shown conclusively that C.

albicans may occur on the mucous

mem-branes of healthy children and adults

with-out causing clinical manifestations.192’

In such cases the organism apparently

* Clinical trials with a preparation containing

nystatin, fluorohydrocortisone, gramicidin and neo-mycin are now in progress and show promising

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ARTICLES 831

Fic. 2. Cutaneous candidiasis of 10 days’ duration in an infant 8 months of age. Note confluent

plaques and “satellite” lesions.

does not form mycelia and does not invade

the tissues, and is seen in the form of spores

(Y-phase) only.5 Evidently C. albicans can

subsist as a saprophyte on the mucous

mem-branes. A similar saprophytic existence of

the organism on normal skin has often been

postulated. 10-13 Experimental evidence,

how-TABLE III

INCIDENCE OF CANDIDA ALBICANS IN TIlE MOITlI AND

STOOLS OF 25 OLDER INFANTS WITh CUTANEOUS CANDIDIA5I5

Mycologic

Findings

Number of

(‘ases

Total

Stools

Positive

Total

Mouth

Positive

Stools positive

Mouth positive 13 13 13 (6 cases

of oral thrush)

Mouth negative 8 8 0

Mouth not done 1 1

Stools negative

Mouth positive 1 0 1

Mouth negative 2 0 0

Total 25 22

88%

14 56%

ever, supports those who hold that, “Can-dida albicans is not one of the yeast-like

fungi found commonly on the normal skin

(although it is frequently present in the mouth and stools), nor is it commonly found

in skin disorders of other etiohogy.”2225

Ta-ble IV sums up the findings of several in-vestigators on a total of 3,518 healthy adults

and children. Candida albicans was isolated

from only 11 specimens of apparently healthy skin, mainly from the interdigital spaces of the hands and feet. In these sites the organism might conceivably subsist in

superficial debris without attacking the skin

itself.

As Khigman has explained,30 a pathogenic

fungus has to invade and actively grow

within the skin in order to maintain itself.

Otherwise it would soon be sloughed off

in the continual shedding process of the

horny layer of the epidermis. The invasion

provides a stimulus to which the skin

sponds with the more or less inflammatory

reactions symptomatic of superficial fungus

infections.

Each papular “satellite” lesion in the

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can-TABLE IV

INCIDENCE OF CANDIDA ALBI(’ANS ON NORMAL SKIN ACCORI)ING TO \ARIOVS AUThORS

Number of . (‘. albicans

Authors , . Site

Subjects Iound

Kuroelikin 1111(1 (‘hen2’

Benham and hopkins1’

r%Iarsvin27

Marples and l)i Menna21’2’

Walker29

150

100

309

(1333 specimens)

949

1010

skill, nails, toewebs

interdigital, axillary, (rural, inframam-mary, umbilical areas

skin, nails

skin, feet

0

11

0

(acute candidiasis pe(lis)

didiasis is actually an intracutaneous colony

of C. albicans. Growing radially, adjacent

colonies coalesce, to form the erythematous

plaques which characterize the disease.

The chronically moist and macerated

skin, and the warm and humid atmosphere

of the diaper area of the young infant

pro-vide ideal conditions for invasion by and

proliferation of C. albicans. The invariable

presence of mycehia in scrapings from the

lesions proves tissue invasion and coloniza-tion by the organism.

Presumably candidiasis may become

superimposed on pre-existing diaper

derma-toses and vice versa. This is implied by the

frequent necessity of supplementing specific

antimycotic medication with nonspecific

therapy. On the other hand, the writers

were unable to demonstrate C. albicans in

the mouth, skin, or stools of patients with

“red buttocks,” ammoniacal dermatitis,

con-tact dermatitis, or seborrheic dermatitis.

Similar negative findings were reported by

Bound.#{176} It may be concluded that

candidi-asis can become superimposed on such a

condition only if the organism is a priori

present in the mouth or intestine of the

patient.

It is noteworthy that C. albicans occurs

in the mouth and intestine of newborn

in-fants with only about one-tenth to one-third

of the frequency reported for healthy older

individuals.192’ Moreover, its presence was

indicative of clinical candidiasis in 81 of

the 83 newborns studied here, although the

organism did occur in the intestine in

asso-ciation with oral thrush without causing

dermal lesions, and in the mouth in

associa-tion with dermal lesions without causing

oral thrush. This latter observation is

im-portant, since it shows that the mouth may

be bypassed and the lesions be confined

exclusively to the diaper area, as seen in 12

of the 83 newborns in the present series.

It also appears highly significant that

the majority of the older infants with

cu-taneous candidiasis harbored C. albicans in

the intestine (88%). These findings suggest

that infected stools constitute a primary

focus of candidiasis in the diaper area. This

was particularly evident in the early

neo-natal period where the infection clearly

originated in the anal and perianal region.

In this connection it is interesting to note

that an intestinal focus has also been

as-sumed for vaginal candidiasis in adults.31

It follows that special attention should be

paid by the nursery staff to the eruption

of diaper rashes in infants with oral thrush,

and to all such rashes which fail to respond

to routine care. Cultures of the skin and

stools should be taken in all such cases, so

that specific treatment may be given. Oral

therapy designed to eliminate C. albicans

from the digestive tract should accompany

local medication in order to prevent

recur-rences of the dermatitis. Both nystatin and

amphotericin B have been shown to

effec-tively decrease C. albicans in the intes-tine.32’ 33

SUMMARY

AND

CONCLUSIONS

The presence of Candida albicans in the

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rou-ARTICLES 833

tine laboratory tests, was overwhelmingly indicative of subsequent oral and/or Cu-taneous candidiasis.

Cutaneous candidiasis in newborn

in-fants may occur independently of oral

he-sions, and in such cases C. albicans may

be present in the stools only.

Cutaneous candidiasis may appear during the first week of life. It should be suspected in all infants suffering from oral thrush or from unmanageable diaper dermatoses. The diagnosis should be confirmed by labo-ratory examination of scrapings from the he-sions and stool specimens.

One hundred per cent of the newborn

infants and 88% of the older children who suffered from candidal diaper rashes

har-bored C. albicans in the intestine.

Since infected stools are obviously a focus for such cutaneous lesions, local therapy should be supplemented with medi-cation designed to eliminate C. albicans from the digestive tract.

Candida albicans was not isolated from

the mouth, skin, or stools of 15 newborn infants with “red buttocks” and of 17

pa-tients with ammoniacal, contact or

sebor-rheic dermatitis.

Scrapings and cultures from healthy skin, and from the site of cured candidal lesions were negative for C. albicans.

On the basis of these findings and reports

in the literature, it is concluded that C. albicans occurs on the skin only in patho-logic conditions attributable to the organ-ism.

ACKNOWLEDGMENTS

The authors wish to acknowledge the

valuable help of Dr. Benjamin Kramer, Dr.

Max Michael, Jr., Mrs. Charlotte Older,

RN., and Miss Angela Chiusano, RN.

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P. : Thrush napkin rashes. Brit.

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L., and Martin, D. S.: Manual of Clinical Mycology, 2nd Ed. Philadelphia, Saunders, 1954, p. 169. 11. Robinson, H. M. : Monihiasis complicating

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and Winkler, A. : Beitrag um

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: Die

He-fesammhung des “Centraalbureau voor Schimmelcultures,” Part II, Die

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F., and Levin,

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Taschdjian, C. L., Dragutskv,

D., and Minsky, A. : Treatment of cutaneous candidiasis in infancy and childhood with nystatin and amphoteri-cm B. Antibiotics Annual 1956/57. New York, Medical Encyclopedia, Inc., 1957, p. 128.

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incidence of Candida albicans in Dun-edin, New Zealand.

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SUMMARIO IN INTERLINGUA

Candidiasis

Cutanee

in

le

Prime

Infantia

Inter 2175 apparentemente normal neonatos

de 2 a 5 dies de etate, 101 se provava hospites

de Candida albicans. Le presentia del or-ganismo esseva constatate in he bucca e in he

intestinos o in le intestinos sol. Le majoritate

de iste C.-positive infantes disveloppava

can-didiasis ante he septime die de br vita, in he

forma de hesiones oral o cutanee o ambes. In certe casos, he hesiones cutanee in le area coperite per pannos precedeva he lesiones oral, sed plus frequentemente illos se disveloppava

al mesme tempore como he aphthas oral o

brevemente plus tarde.

Feces inficite constitute apparentemente un

foco primari pro candidiasis cutanee, proque

100 pro cento del neonatos e 88 pro cento de

30 plus avantiate infantes con candidal

erythema gluteal se provava hospites de C.

albicans intestinal. Maceration e necrosis

superficial del mucosa anal esseva usualmente

he prime visibile symptomas de candidiasis

cutanee in he area gluteal.

Casos tractate intra 24 a 48 horas post le

eruption respondeva sin exception ben e

rapidemente al medication con unguentos a

2 pro cento de nystatina o amphotericina B

in “plastibase” e esseva curate intra un sep.

timana. Conditiones de un duration de plus

que 8 dies requireva therapias de 2 a 3

septimanas. In certes de iste casos, he specific

therapia antimycotic debeva esser

supple-mentate con medication non-specific pro

alheviar irritationes secundari.

Viste iste differentia del prognose e del

responsa al tractamento, ii es importante recognoscer e tractar eandidiasis cutanee he plus promptemente possibile. Le condition debe esser expectate in omne casos de aphthas oral. Le diagnose clinic debe esser confirmate per le identification de C. albicans in le

lesiones e in specimens fecal.

Le therapia local debe esser supplementate

per he administration oral de nvstatina pro eliminar C. albicans ab le intestinos e pro

prevenir he recurrentia del lesiones cutanee.

C. albicans non esseva identificate in le bticca, he feces, e le pehie de 15 neonatos con :ghuteos rubie” e de 17 infantes plus avantiate

con dermatitis contactic, ammoniacal, o

seborrheic in he area gluteal.

Le observationes del autores supporta he

conception que C. albicans occurre solmente

como pathogeno al superficie del pelle. In plus,

he autores trova que C. albicans occurre

rarmente in neonatos como innocente sapro-phyto oral o intestinal. Per contrasto con he

conditiones in plus avantiate individuos, he

presentia del organismo in neonatos es

usual-mente un indication de potential o actual

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1957;20;827

Pediatrics

Philip J. Kozinn, Claire L. Taschdjian, David Dragutsky and Arnold Minsky