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Skin Colonization by Malassezia Species in Neonates
A Prospective Study and Relationship With Neonatal Cephalic Pustulosis
Vincent Bernier, MD;
François X. Weill, MD;
Virginie Hirigoyen, MD;
Christophe Elleau, MD;
Anne Feyler, MD;
Christine Labrèze, MD;
Jean Sarlangue, MD;
Geneviève Chène, MD;
Bernard Couprie, MD;
Alain Taïeb, MD
Arch Dermatol. 2002;138:215-218.
ABSTRACT
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Objectives To assess skin colonization by Malassezia species
in full-term healthy newborns, to investigate factors associated with colonization,
and to look at acnelike cephalic pustulosis associated with this carriage.
Design Samples were obtained from neonates and their mothers 0 to 5 days after
birth and again 3 weeks later. Clinical patterns of common acnelike pustulosis
were reported as mild (<10 papulopustules), moderate ( 10 papulopustules),
or absent. Direct examination and culture of sample. Identification of yeasts
was based on microscopic and physiologic criteria.
Setting A maternity hospital and the pediatric dermatology unit of a university
hospital.
Participants Consecutive series of 102 neonates and their mothers.
Main Outcome Measures Incidence of skin colonization and type of Malassezia species found in neonates and correlation with neonatal cephalic pustulosis
(neonatal acne).
Results At the first visit, 11 neonates and 36 mothers had cultures positive
for Malassezia. Malassezia sympodialis and Malassezia globosa were preferentially
cultured. At 3 weeks, 29 (52%) of 56 neonates and 18 (32%) of 56 mothers had
cultures positive for only M sympodialis and M globosa. Breastfeeding was not associated with a higher
prevalence of Malassezia carriage in neonates. Malassezia colonization was higher when pustulosis was
more severe and M sympodialis was found in pustules.
Conclusions Malassezia colonization begins at birth and
increases in the first weeks of life. A high prevalence of M sympodialis in neonates is noted from birth. Its association with
neonatal acne is confirmed. Further investigation is needed to study the role
of sebum secretion rate and quality in the neonatal period.
INTRODUCTION
NEWBORN SKIN is essentially sterile at birth.1
Except for the transient flora originating mostly from the mother's genital
tract, which can be potentially life-threatening for the newborn,2 bacteria of the newborn's resident flora are not cultured
at birth but appear within the first hours of life. By age 6 weeks, the total
number of organisms is comparable to that found in adults. Staphylococcus epidermidis is the most common bacterium.1
In preterm infants, staphylococci colonize skin earlier than Propionibacterium and Malassezia species,
which have a slower growth rate and might require greater maturation of epidermal
structures.3 Yeast flora4
is represented by nonlipophilic yeasts (Candida species)
and lipophilic yeasts (Malassezia species). Candida albicans is not a regular member of the cutaneous
microflora.1, 4 Conversely, Malassezia organisms are saprophytic of normal human adult
and child skin.5-7
Although it can be implicated in some systemic neonatal infections,7-9 Malassezia species in healthy neonates are associated with the common acnelike
pustulosis of the cephalic area.10-15
Recent identification and differentiation of Malassezia species have opened new avenues for investigations.16-18
This study aimed to assess skin colonization by Malassezia species in full-term healthy newborns and to investigate the factors
associated with colonization. Another aim was to assess possible skin manifestations
associated with this carriage, especially neonatal acnelike cephalic pustulosis.
PARTICIPANTS AND METHODS
FIRST VISIT
Samples were first obtained from neonates and their mothers on the maternity
unit of the Pellegrin University Hospital 0 to 5 days after birth (December
1, 1997, to February 28, 1998). The mothers gave informed consent and agreed
to return for a follow-up outpatient visit at the pediatric dermatology unit
3 weeks later. A complete skin examination of the newborns was performed.
Type of feeding, breast or formula, was recorded. Children were defined as
formula fed when they had never received any breastfeeding. Antimicrobial
drug use (topical antiseptic or antibiotic agents and oral antibiotics) was
recorded. The ethnic origins of the mother and father were noted. Social class
was defined arbitrarily by the mother's occupation at the time of the child's
birth according to the 1950 British classification of the Registrar.19
SECOND VISIT
Neonates and their mothers attended the outpatient visit for a second
sampling at a mean ± SD age of 21 ± 5 days. Information about
skin care was noted, and a complete skin examination was performed. Clinical
patterns of common acnelike pustulosis were reported as mild (<10 papulopustules),
moderate (10 papulopustules), or absent. Pustular material was obtained
when technically possible.
PROCEDURES AND LABORATORY INVESTIGATIONS
Each sample from newborns was obtained by the same operator (V.B.) using
a skin swab applied on a 1-cm2 area of the cheek. Sampling of the
mothers was performed on the neck using identical techniques.
Whenever feasible, newborns' smears were obtained from pustules using
a microlance after disinfection with 0.1% alcoholic hexamidine di-isetionate
solution. Technical limitations to sampling were the size of the lesion and
the anxiety of the mothers. Pustular material was directly applied to a glass
slide for direct examination after May-Grünwald-Giemsa staining. Skin
swabs and pustule smears were then seeded in modified Dixon agar culture medium
(3.6% malt extract, 0.6% peptone, 2.0% desiccated ox-bile [Sigma, St Louis,
Mo], 1.0% Tween 40, 0.2% glycerol, 0.2% oleic acid, 0.05% chloramphenicol,
0.05% cycloheximide, and 1.5% agar [pH 6]). Colonies were counted after 15
days of incubation at 32°C. Identification of yeasts was based on microscopic
(after May-Grünwald-Giemsa staining) and physiologic criteria, namely,
Tweens and cremophor EL assimilation test, with splitting of esculin according
to Guillot et al16 and Mayser et al.17
STATISTICAL ANALYSIS
Comparison of proportions was performed using the Fisher exact test.
A test for trend in proportions was used to compare Malassezia-positive participants according to clinical patterns.
RESULTS
The overall results are given in Table 1.
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Table 1. Overall Clinical and Mycological Data
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FIRST VISIT
While on the maternity unit, samples were obtained from 102 neonates
and their mothers 0 to 5 days after birth. All the newborns were born at term
and were in good health. Routine skin care of the face was done with isotonic
sodium chloride solution. No newborn had received antimicrobial local treatment
or oral antibiotics, except eyedrops to prevent gonococcal ophthalmia.
The initial mycological data in neonates and mothers are reported in Table 2. Eleven percent of neonates and
36% of mothers had cultures positive for Malassezia
organisms. Malassezia sympodialis and Malassezia globosa were preferentially cultured. One mother's culture
was positive for Malassezia slooffiae.
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Table 2. Initial Mycological Data in 11 Neonates and 36 Mothers With
Positive Culture Findings
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Of 10 M sympodialis–positive neonates,
6 had M sympodialis–positive mothers, 1 had
a M globosa–positive mother, and 3 had Malassezia species–negative mothers. The mother of
the neonate positive for M sympodialis and M globosa was also Malassezia
negative. Sixty-seven percent of Malassezia-negative
newborns had Malassezia-negative mothers.
FOLLOW-UP VISIT
A total of 56 mothers and their newborns attended the outpatient visit
at a mean ± SD of 21 ± 5 days (Table 3). There was no significant difference in the mothers' mycological
status at birth between the group that completed the study and the group that
did not (data not shown). Twenty-nine neonates (52%) and 18 mothers (32%)
had positive cultures that grew only M sympodialis
and M globosa. Of 25 M sympodialis–positive neonates, 7 (28%) had the same species as their mother;
4 (16%) had mothers positive for M sympodialis and M globosa. The 3 M globosa–positive
neonates and the neonate positive for M sympodialis
and M globosa showed no association with their mother's
status (2 newborns) or a partial association (2 newborns). Sixty-three percent
of Malassezia-negative neonates had Malassezia species–negative mothers.
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Table 3. Mycological Data at 21 ± 5 Days in 29 Neonates and
18 Mothers With Positive Culture Findings
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Breastfeeding (49 newborns) was not associated with a higher prevalence
of Malassezia carriage in neonates (n = 23) (Fisher
exact test, P = .11). However, the formula-only group
was small (n = 7). No difference in Malassezia colonization
was found according to social class (data not shown). White individuals were
overrepresented (n = 48, 86%), and we could not check whether ethnic origin
of the mother contributed to the type of colonization. The use of cosmetic
products for routine skin care of the face did not interfere with Malassezia colonization (data not shown).
CEPHALIC PUSTULOSIS
In affected patients, the pustulosis developed between day 5 and 3 weeks.
When noted, lesions consisted of red papules of pinpoint size (first stage),
papulopustules (second stage), or overt pustules (third stage), mostly located
on the cheeks, chin, and forehead. Extension could occasionally be found on
other seborrheic areas, such as the scalp or upper neck. No comedos were observed.
Mycological data at 3 weeks were compared with clinical patterns of neonatal
cephalic pustulosis (Table 4).
Thirty-seven (66%) of 56 newborns had lesions classified as mild or moderate.
Eleven pustules were sampled successfully, and 4 were positive on direct examination
and culture: 3 cultures grew M sympodialis and 1
grew M globosa. Two of these 11 pustules had positive
findings on direct examination and negative culture results, and 2 of 11 had
positive culture findings and negative findings on direct examination. Of
11 children with pustules sampled, 3 had negative skin culture findings. Of
the 4 patients with positive pustules (by direct examination and culture),
all had positive skin culture results, and 3 were highly colonized (50-500
colonies). There was a correlation between positive culture findings using
skin swabs on cheeks and clinical severity of presentation. Three of 11 children
with successfully sampled pustules at 3 weeks already had colonization at
day 5. Of these, 2 had positive pustules at 3 weeks (by direct examination
and culture).
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Table 4. Mycological Data at 3 Weeks and Correlation With Severity
of Neonatal Cephalic Pustulosis in 56 Neonates*
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COMMENT
Yeasts of the genus Malassezia are components
of the microflora of human skin and of many warm-blooded animals.4, 20 However, researchers do not agree
on the age at which skin is colonized after birth.3, 6-7,21
Recently, the taxonomic revision of the lipophilic yeast genus using morphologic,
ultrastructural, physiologic, and molecular biological methods has included
7 species comprising 3 former taxa (Malassezia furfur, Malassezia
pachydermatis, and M sympodialis) and 4 new
taxa (M globosa, Malassezia obtusa, Malassezia restrict, and M slooffiae).18
In this study, based on samples obtained from mothers, M sympodialis and M globosa were the exclusive
residents of female skin, except for 1 isolate of M slooffiae. In children, M sympodialis was the most
prevalent Malassezia species in the first 3 weeks
of life. On the maternity unit, Malassezia species–positive
mothers had a more balanced distribution of the 2 species (M sympodialis and M globosa). Differences
in sebum secretion rate and sebum composition could probably explain some
differential growth patterns of each yeast; particularly, the endocrine environment
of pregnancy could be more suitable for the growth of M
globosa since, as at 3 weeks, the relative percentage of Malassezia species was nearly the same as in children.
Malassezia is found in more than 90% of adults21; in children, this yeast has been found in 50% of
healthy newborns at birth and in 80% after 7 days of life6
or, in a mostly premature population, from 13% in the first days of life to
77% between 1 and 3 month of age.7 The following
differences in methods should be kept in mind if comparisons with our data
are envisaged. Previous studies were performed before the taxonomic revision
that has introduced identification and differentiation of the new Malassezia species, based in our study on culture conditions and morphologic
and physiologic criteria. Sampling the cheeks on a 1-cm2 area permitted
standardization of the method, and this site correlated better with the usual
location of neonatal cephalic pustulosis. The scalp and chest were preferentially
sampled in another study.7 Finally, participant
recruitment on the maternity unit could assess skin colonization of the full-term
healthy newborn.
Progressive colonization by Malassezia species
from birth was recently proposed by Eastick et al3
and Niamba et al,15 but infants in these studies
were recruited in a neonatal care unit.
Our data prove that colonization by Malassezia
species begins in the first days of life (11% at day 5) and increases during
the first weeks (52% at day 21). Maternal Malassezia
colonization was stable at the 2 visits in contrast to Malassezia specificity. The rate of carriage at 3 weeks was higher
in newborns than in mothers (52% vs 32%), but the sampling site was different.
The elevated flow of sebum in neonates owing to sebaceous gland hyperactivity
could also partially explain this finding.
The mother seems to be the first reservoir for the child's colonization.
At birth, 60% of M sympodialis–positive neonates
shared the same yeast species with their mother, as well as 44% at 3 weeks.
A two-thirds correlation was also obtained in the Malassezia species–negative pairs at birth and at 3 weeks. A comparative
molecular approach using restriction fragment length polymorphisms of yeast
isolates from mothers and children could be interesting to validate this finding.
To explain an absence of complete correlation, it remains possible that Malassezia species are not equally distributed on the skin
of the mother and that M sympodialis is more adapted
to the skin of newborns than is M globosa. Alternatively,
other sources such as nursery personnel or other family members may be important
to consider in future studies.
If maternal factors are implicated in Malassezia
colonization at birth, close contact with the mother during breastfeeding
and social class origin do not seem to affect the composition of the newborn's
skin flora. Furthermore, variations in routine skin care did not significantly
affect skin colonization. The child's intrinsic characteristics should probably
be considered more closely, especially concerning sebum production.
In adults, tinea versicolor, seborrheic dermatitis, and folliculitis
are well-known dermatoses in which Malassezia organism
is implicated as an etiologic agent.12 In neonates,
the possible role of Malassezia species in the cause
of facial acnelike pustulosis was first suggested by Aractingi et al10 and subsequently by other authors.11-15
More specifically, M sympodialis has been proposed
to be a triggering agent for this transient rash.15
Our data suggest that Malassezia colonization is
higher when the pustulosis is more severe (Table 3). Moreover, M sympodialis grew
in 3 cultures from 4 pustular samplings. These results confirm, in nonselected
neonates, that M sympodialis plays a role in common
neonatal cephalic pustulosis. However, cephalic pustulosis with negative mycological
data suggests multifactorial causes for this common disorder.
In conclusion, Malassezia colonization of the
skin begins at birth and increases within the first weeks of life. A high
prevalence of M sympodialis in neonates is noted
from birth. Its association with neonatal acne is confirmed. Environmental
factors and maternal contact probably affect this colonization, but neonatal
skin characteristics are probably important. Further investigation is needed
to study the role of sebum secretion rate and quality in the neonatal period.
Other studies should also address the role of culture medium specificity for
the cultivation of each species.
AUTHOR INFORMATION
Accepted for publication May 14, 2001.
The pediatric dermatology fellowship (Dr Bernier) was supported by a
grant from the Cliniques St Joseph, Liège, Belgium.
We thank the midwives who were involved in recruitment of the mothers
for the study.
Corresponding author and reprints: Alain Taïeb, MD, Service
de Dermatologie, Hôpital Saint André, 1 rue Jean Burguet, 33075
Bordeaux, France (e-mail: alain.taieb{at}chu-bordeaux.fr).
From the Pediatric Dermatology Unit (Drs Bernier, Labrèze, and
Taïeb), the Laboratory of Mycology (Drs Weill, Hirigoyen, Chène,
and Couprie), and the Departments of Neonatal Medicine (Drs Elleau and Sarlangue)
and Medical Information (Drs Feyler and Chène), Centre Hospitalier
et Universitaire de Bordeaux, Bordeaux, France.
REFERENCES
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1. Leyden JJ. Bacteriology of newborn skin. In: Maibach H, Boisits EK, eds. Neonatal Skin:
Structure and Function. New York, NY: Marcel Dekker Inc; 1982:167-181.
2. Tessin I, Trollfors B, Thiringer K. Incidence and etiology of neonatal septicaemia and meningitis in Western
Sweden 1975-1986. Acta Paediatr Scand. 1990;79:1023-1030.
ISI
| PUBMED
3. Eastick K, Leeming JP, Bennett D, Millar MR. Reservoirs of coagulase negative staphylococci in preterm infants. Arch Dis Child Fetal Neonatal Ed. 1996;74:F99-F104.
4. Noble WC. Microbiology of Human Skin. 2nd ed. London, England: Lloyd Luke Medical Books; 1981.
5. Powell DA, Hayes J, Durell DE, Miller M, Marcon MJ. Malassezia furfur skin colonization of infants
hospitalized in intensive care units. J Pediatr. 1987;111:217-220.
FULL TEXT
|
ISI
| PUBMED
6. Koseki S, Takahashi S. Serial observation on the colonization of Pityrosporum
orbiculare (ovale) on the facial skin surface of newborn infants. Jpn J Med Mycol. 1988;29:209-215.
7. Borderon JC, Langier J, Vaillant MC. Colonisation du nouveau-né par Malassezia
furfur. Bull Soc Fr Mycol Med. 1989;1:129-132.
8. Long JG, Keyserling HL. Catheter-related infection in infants due to an unusual lipophilic
yeast Malassezia furfur. Pediatrics. 1985;76:896-900.
FREE FULL TEXT
9. Chang HJ, Miller HL, Watkins N, et al. An epidemic of Malassezia pachydermatis in
an intensive care nursery associated with colonization of health care workers'
pet dogs. N Engl J Med. 1998;338:706-711.
FREE FULL TEXT
10. Aractingi S, Cadranel S, Reygagne P, Wallach D. Pustulose néonatale induite par Malassezia
furfur. Ann Dermatol Venereol. 1991;118:856-858.
ISI
| PUBMED
11. Plantin P, Cartier H, Geffroy F, Broussine L. Une pustulose néonatale à reconnaître: la pustulose
induite par Malassezia furfur [letter]. Arch Pediatr. 1995;2:1016.
12. Rapelanoro R, Mortureux P, Couprie B, Maleville J, Taïeb A. Neonatal Malassezia furfur pustulosis. Arch Dermatol. 1996;132:190-193.
ABSTRACT
13. Patrizi A, Bardazzi F, Neri I, Varotti E. La pustolosi neonatale da Malassezia furfur. Giorn Int Derm Ped. 1996;8:3.
14. Amoric JC. Quand Malassezia furfur (ou Pityrosporum) envahit la peau: dermatoses connues et nouvelles. Pédiatrie Pratique. 1997;85:1-3.
15. Niamba P, Weill FX, Sarlangue J, Labrèze C, Couprie B, Taïeb A. Is common neonatal cephalic pustulosis (neonatal acne) triggered by Malassezia sympodialis? Arch Dermatol. 1998;134:995-998.
FREE FULL TEXT
16. Guillot J, Guého E, Lesourd M, Midgley G, Chévrier G, Dupont B. Identification of Malassezia species: a practical
approach. J Mycol Med. 1996;6:103-110.
17. Mayser P, Haze P, Papavassilis C, Pickel M, Gruender K, Guého E. Differentiation of Malassezia species: selectivity
of cremophor EL, castor oil, and ricinoleic acid for M furfur. Br J Dermatol. 1997;137:208-213.
FULL TEXT
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ISI
| PUBMED
18. Guého E, Midgley G, Guillot J. The genus Malassezia with description of four
new species. Antonie Van Leeuwenhoek. 1996;69:337-355.
FULL TEXT
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ISI
| PUBMED
19. Power C, Matthews S. Origins of health inequalities in a national population sample. Lancet. 1997;350:1584-1589.
FULL TEXT
|
ISI
| PUBMED
20. Ingham E, Cunningham AC. Malassezia furfur. J Med Vet Mycol. 1993;31:265-288.
21. Faergemann J, Fredriksson T. Age incidence of Pityrosporum orbiculare on
human skin. Acta Derm Venereol. 1980;60:531-533.
ISI
| PUBMED
THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES
Neonatal Acne and Cephalic Pustulosis: Is Malassezia the Whole Story?
Bergman and Eichenfield
Arch Dermatol 2002;138:255-257.
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