Eur J Clin Microbiol Infect Dis (2013) 32:373380
DOI 10.1007/s10096-012-1752-1
ARTICLE
Investigation of a scabies outbreak in a kindergarten
in Constance, Germany
L. Ariza & B. Walter & C. Worth & S. Brockmann &
M.-L. Weber & H. Feldmeier
Received: 1 June 2012 / Accepted: 10 September 2012 / Published online: 28 September 2012
# Springer-Verlag 2012
Abstract In industrialized countries, scabies occurs sporad-
ically or in the form of protracted epidemics, typically in
nursing homes for elderly people. Outbreaks of scabies in a
kindergarten are very rare. The main goal of our study was
to investigate an outbreak of scabies in a kindergarten and to
identify risk factors for the infestation with the ectoparasi-
tosis. We investigated an outbreak of scabies in a kindergar-
ten in the City of Constance, southern Germany, with a
particular pedagogical concept. Risk factors indicating a
transmission of Sarcoptes mites through body contact or
via fomites were assessed using questionnaires and by fol-
lowing the daily routine in the kindergarten. A total of 16
cases were identified. The attack rate was significantly
higher in nursery teachers (risk ratio 42.1) compared to
children (risk ratio 10.5). In all cases, scabies had developed
rather recently, with minimal clinical manifestations. In
L. Ariza
Department of Community Health, School of Medicine,
Federal University of Cear,
Fortaleza, Brazil
B. Walter : C. Worth : H. Feldmeier (*)
Institute of Microbiology and Hygiene, Campus Benjamin
Franklin, Charit University Medicine Berlin,
Hindenburgdamm 27,
12203 Berlin, Germany
e-mail: hermann.feldmeier@charite.de
S. Brockmann
Landesgesundheitsamt Baden-Wrttemberg,
Stuttgart, Germany
M.-L. Weber
Local Health Department,
District of Constance, Germany
S. Brockmann
Local Health Department,
District of Reutlingen, Germany
nursery teachers, the probability of scabies was 4.4 times
higher in those teachers who hugged children regularly.
Children who preferably played with their own soft toys
had a lower probability of developing scabies [risk ratio
0.14, 95 % confidence interval (CI) 0.050.42; p00.04]. It
seems conceivable that the particular pedagogical concept of
the kindergarten favored the spread of Sarcoptes mites. We
were unable to show whether transmission had preferably
occurred through body contact or via fomites.
Introduction
Scabies is a parasitic skin disease caused by Sarcoptes
scabiei var. hominis. The infestation is characterized by an
intense local pruritus and a pattern of unspecific skin alter-
ations, such as papules, vesicles, and nodules [1]. The itch
induces scratching of the lesion(s), which, in turn, causes
excoriation and denudation of the skin, eventually leading to
bacterial superinfection [2]. After primo-infestation, lesions
develop with a delay of 3 to 4 weeks, indicating a delayed-
type hypersensitivity response [3]. Due to the unspecific
nature of symptoms and signs, scabies is frequently mistak-
en for other inflammatory skin diseases and the correct
diagnosis is often made with a considerable delay [3]. The
easy transmissibility of Sarcoptes mites and the delayed
diagnosis explain the occurrence of epidemics in outpatient,
hospital, or institutional settings. Such epidemics continued
for months and affected up to 195 individuals [418].
Epidemics in institutions taking care of children are rare
and, hitherto, only occurred under particular circumstances,
such as in a resource-poor orphanage in rural Thailand or in
a camp for homeless children in Sierra Leone during civil
war [10, 19]. In Europe, outbreaks occurred in a further
education college for persons with learning disabilities, in
a school for children with learning disabilities, as well as in
a workshop for handicapped children [5, 8, 16]. Sargent and
374
Martin described a scabies outbreak in a day care center,
with 36 individuals affected [4].
Here, we describe an outbreak of scabies in a kindergarten
in the city of Constance, south-west Germany. We investigat-
ed factors which might explain the unusual dimension of the
epidemic and which could indicate whether transmission had
preferably occurred through body contact or via fomites.
Materials and methods
Setting
On February 22, 2010, two cases of scabies were notified by
the Local Health Department of Constance, a city with
84,000 inhabitants in the south-west of Germany bordering
Switzerland. One patient was a nursery teacher of a public
kindergarten and the other was her 16-year-old son. Within
the next 4 weeks, 57 suspected cases of scabies were
reported to the Local Health Department by local physicians
and dermatologists. Cases were staff members and children
of the kindergarten, or siblings from other educational insti-
tutions in the city, as well as family members of staff and
children.
Sixteen cases occurred in the public kindergarten, a fa-
cility based on the pedagogical concept of an open kinder-
garten. The concept implies that there are no fixed
playgroups and that children can choose their field of activ-
ity as they please at the beginning of the day. Every morn-
ing, each nursery teacher proposes a defined activity, such as
life role-playing, cooking, painting, story-telling, etc., and
enrols children for the corresponding activity. This results
in a mixing of all age groups and multiple body contact
among children and between children and nursery teachers.
Most children take an afternoon nap either in beds or on
mattresses on the floor in a separate room. Sometimes,
several children sleep together on the same mattress. In case
a child has difficulties in falling asleep, a nursery teacher
huddled them to assist in sleeping.
A very popular place in the kindergarten is the so-called
adventure cave, a tube-like structure with blankets and pil-
lows. Here, several children crawl or lay down together,
while a nursery teacher reads a story.
When the outbreak began, 19 adults (17 nursery teachers
and two auxiliary workers) were working in the kindergar-
ten. They took care of 76 children aged 27 years. Based on
the dynamics of the epidemic and taking into consideration
that an unknown number of individuals presumably were in
the incubation phase, the Local Health Department recom-
mended a prophylactic mass treatment to all employees,
children, and close family contacts between March 19 and
21 (Friday to Sunday), either by permethrin 5 % ointment or
benzyl benzoate 25 % ointment (10 % in case of children).
Eur J Clin Microbiol Infect Dis (2013) 32:373380
The kindergarten was closed down during this weekend and
all kinds of textiles (including toys, furniture, and other
objects with a textile part) were temporarily removed from
the rooms and stored outside of the building or in plastic
bags for 3 days.
The outbreak investigation was carried out 8 days after the
mass treatment had been performed. At this point in time, still
new cases of scabies emerged in other educational facilities or
households. Therefore, the Local Health Department asked
the Public Health Authority of Baden-Wrttemberg for help
regarding the containment of the epidemic.
Study design
The outbreak investigation was carried out in the public
kindergarten, which was considered to be the source of the
epidemic by the Local Health Department. During one day,
the investigators followed the daily activities of the children
to identify activities which could facilitate the transmission
of Sarcoptes mites by close body contact or through fomites,
such as textiles consecutively used by several children.
Focus group discussions were carried out with staff mem-
bers to understand risk behavior such as hugging children.
All nursery teachers and all children enrolled in the
kindergarten were included in the study. One questionnaire
was developed for nursery teachers and one for the parents
of the children. The questions tried to identify clinical char-
acteristics of scabies (duration of disease, type and develop-
ment of lesions), risk factors related to exposure (such as
time present in the kindergarten), preferred activities of
children (changing clothes with other children, using the
adventure cave), and risk behaviors of nursery teachers
(hugging children, cuddling, etc.). Two of the investigators
(B.W. and C.W.) helped the nursery teachers and parents to
fill out the questionnaire. Questionnaires were collected on the
same day they were distributed. The degree of itching was
assessed using a visual ordinal scale ranging from 0 to 5 [2].
Nursery teachers and children were classified as cases
when a diagnosis of scabies had been established by dermo-
scopy or based on characteristic clinical findings by a local
dermatologist.
Data analysis
Data were entered using Epi Info software (version 3.5.1;
Centers for Disease Control and Prevention, Atlanta, GA,
USA) and were checked for entry-related errors. Data anal-
ysis was conducted using STATA (version 11; Stata
Corporation, College Station, TX, USA).
The median and interquartile ranges (IQRs) were used to
indicate the central tendency and the dispersion of the data,
respectively. Fishers exact test was applied to determine the
significance of differences of relative frequencies. The
Eur J Clin Microbiol Infect Dis (2013) 32:373380
MannWhitney test was used to identify significant differ-
ences between quantitative measurements. Risk ratios were
calculated, together with their respective 95 % confidence
intervals (CIs).
Ethical considerations
Nursery teachers and parents of children were informed that
answering the questionnaire was voluntary and that data
privacy was ensured by anonymizing the results. Sessions
were organized with the nursery teachers to provide infor-
mation on scabies and to better understand the concerns and
fears of the kindergarten staff. Since the outbreak investiga-
tion was authorized by the National Protection Against
Infection Act (Infektionsschutzgesetz; IfSG) and the status
of disease in staff members and children was already pub-
licly known, ethical clearance was not necessary.
Results
Characteristics of the epidemic
From February 22 to March 19, 2010, the City Health
Department notified 16 cases of scabies among staff and
children of the public kindergarten. Eight cases occurred in
nursery teachers and eight in children. The risk ratio was
42.1 in nursery teachers (95 % CI 20.366.5) and 10.5
(95 % CI 4.719.7) in children (p00.003). All nursery
teacher cases were females (median age 29.5 years, range
2051 years). 62.5 % of the children cases were male
(median age 5.5 years, range 37 years).
Fig. 1 Epidemic curve of 16
cases of scabies in the
kindergarten, based on onset
of symptom
375
Figure 1 depicts the epidemic curve. The pattern of the
epidemic curve indicates a propagated type of epidemic. The
index case was a nursery teacher. Her symptoms started in
December 2009, but scabies was not diagnosed until February
22, 2010. The index case did not consult a dermatologist until
her son also developed symptoms in February 2010. Eighty-
seven days after the symptoms had been noted by the index
case, scabies started to develop in other nursery teachers and
children. Since the consecutive cases developed symptoms
during a rather short period of time, it may be assumed that
all consecutive cases were secondary cases. However, it can-
not be excluded that cases with symptoms appearing at the
end of March (only children) were tertiary cases.
Whereas the index case was diagnosed with a consider-
able delay (81 days after the onset of symptoms), subse-
quent cases were diagnosed rather shortly after the Local
Health Department became aware of the outbreak (Fig. 2).
The second nursery teacher case was diagnosed a few days
(3 days) after the index case. However, she could not re-
member when the symptoms had appeared.
Clinical findings
Table 1 summarizes the demographic and clinical character-
istics of the cases. The number of topographic areas affected
was low (median 2; IQR 12; maximum 6). However, the
number of body parts affected was significantly higher in
nursery teachers than in children (median 2 versus 1; p0
0.04). In 7/8 (87.5 %) of the nursery teachers, at least two
topographic areas were affected. The intensity of itching
was low: the median itching score in children was 2 (IQR
12) and in nursery teachers, it was 1 (IQR 13; p00.90).
376 Eur J Clin Microbiol Infect Dis (2013) 32:373380

Fig. 2 Date of diagnosis of 16

cases of scabies

Factors associated with the presence of scabies
Demographic and health status characteristics associated
with the presence of scabies are depicted in Table 2.
Factors associated with the presence of scabies were a
pre-existing clinical condition (neurodermatitis, allergy,
or type 1 diabetes [only children]: risk ratio 5.24; 95 %
CI 1.3120.96 [p00.03]) and presence of at least one
other household member presenting skin lesions suspi-
cious for scabies (only nursery teachers: risk ratio 3.75;
95 % CI 1.628.68 [p00.02]). The risk ratio for the
presence of scabies was significantly higher in nursery

Table 1 Demographic and clin-

ical characteristics of the 16 Variables Children, n08 Nursery teachers, n08 Total, n016
cases in the kindergarten
Demographic
Sex
Male 5 (62.5 %) 0 5 (31.3 %)
Female 3 (37.5 %) 8 (100.0 %) 11 (68.7 %)
Age (years)
Median (minmax) 5.5 (37) 29.5 (2051) 13.5 (351)
Diagnosis established
Clinical criteria 4 (50.0 %) 4 (50.0 %) 8 (50.0 %)
Dermoscopy 4 (50.0 %) 4 (50.0 %) 8 (50.0 %)
Number of topographical areas affected
Median (minmax) 1 (14) 2 (16) 2 (16)
At least two sites affected 3 (37.5 %) 7 (87.5 %) 10 (62.5 %)
Type of lesionsa
Papules 3 (60.0 %) 5 (83.3 %) 8 (72.7 %)
Nodules 1 (20.0 %) 0 1 (9.1 %)
a Signs of bacterial superinfection 1 (20.0 %) 1 (16.7 %) 2 (18.2 %)
Intensity of itching graded from
0 to 5 (see Materials and Intensity of itchinga
methods) Median (IQR) 2 (12) 1 (13) 1 (12)
b
Data not available in all cases; Therapyb
10 % in children, 25 % in Permethrin cream 5 % 6 (75.0 %) 5 (62.5 %) 11 (68.8 %)
adults
c
Benzyl benzoate cream 10 %/25 %c 1 (12.5 %) 3 (37.5 %) 4 (25.0 %)
Benzyl benzoate
Eur J Clin Microbiol Infect Dis (2013) 32:373380 377

Table 2 Demographic and health status characteristics associated with scabies

Exposure Children Nursery teachers Total

variable
Positive, n (%) Risk ratio p-value Positive, n (%) Risk ratio p-value Positive, n (%) Risk ratio p-value
(95 % CI) (95 % CI) (95 % CI)

Demographic
Sex
Male 5/40 (12.5) Reference 0/3 (0.0) Reference 5/43 (11.6) Reference
Female 3/36 (8.3) 0.66 (0.172.59) 0.72 8/16 (50.0) N.A.a 0.23 11/52 (21.2) 1.82 (0.684.83) 0.28
Age (years), Median (IQR)
Controls 5 (46)b 0.50 39 (2147) 1.00 5 (47) 0.006
Cases 5.5 (4.56.5)b 29.5 (2546) 13.5 (5.529.5)
Presence of allergy, neurodermatitis, or type 1 diabetes
No 3/59 (5.1) Reference 3/6 (50.0) Reference 6/65 (9.2) Reference
Yes 4/15 (26.7) 5.24 (1.3120.96) 0.03 5/12 (41.7) 0.83 (0.292.37) 1.00 9/27 (33.3) 3.61 (1.429.16) 0.01
Family member with scabies-suspicious symptoms
No 6/71 (8.4) Reference 4/15 (26.7) Reference 10/86 (11.6) Reference
Yes 2/5 (40.0) 4.73 (1.2717.69) 0.08 4/4 (100.0) 3.75 (1.628.68) 0.02 6/9 (66.7) 5.73 (2.7312.05) 0.001

a
Not applicable; no case occurred among male nursery teachers
b
Median (interquartile range)

teachers compared to children (4.00; 95 % CI 1.739.28; When the nursery teachers were analyzed separately, the
p00.003). probability of scabies was 4.4 times higher in nursery

Table 3 Factors associated with

the occurrence of scabies in Exposure variable Positive, n (%) Risk ratio (95 % CI) p-value
nursery teachers
Occupation-related
Full time work in the kindergarten
No 3/6 (50.0) Reference 1.00
Yes 5/13 (38.5) 0.77 (0.272.21)
Type/area of work
No contact with children (office, kitchen) 0/2 (0.0) Reference 0.49
Contact with children 8/17 (47.1) N.A.a
Regularly hugs the children
No 1/7 (14.2) Reference 0.07
Yes 7/11 (63.6) 4.45 (0.6828.87)
Lies down with the children on a mattress
No 7/16 (43.8) Reference 1.0
Yes 1/3 (33.3) 0.76 (0.144.15)
Changes diapers of the children
No 3/9 (33.3) Reference 0.64
Yes 5/9 (55.6) 1.67 (0.564.97)
Family and social characteristics
Private relationship with other colleague teachers
No 5/14 (35.7) Reference 0.60
Yes 3/5 (60.0) 1.68 (0.624.58)
Has own children
a
Not applicable; no case oc- No 4/10 (40.0) Reference 1.00
curred among nursery teachers Yes 4/9 (44.4) 1.11 (0.383.18)
working in the office or kitchen Own children enrolled in kindergartenb
b
In the kindergarten in which the No 5/13 (38.5) Reference 1.00
epidemic took place or other Yes 3/6 (50.0) 1.30 (0.453.73)
kindergarten
378 Eur J Clin Microbiol Infect Dis (2013) 32:373380

teachers who regularly hugged the kindergarten children Discussion

than in those who hugged children rarely (risk ratio 4.45;
95 % CI 0.6828.87; p00.07). However, none of the expo- The epidemiology of scabies is understood only rudimentar-
sure variables were significantly associated with scabies ily. Whereas in resource-poor communities in the developing
(Table 3). world scabies is endemic and may be present in astounding
None of the children who only stayed part time in the prevalence in children, in industrialized countries, only spo-
kindergarten developed scabies, in contrast to 17.8 % of radic cases occur. But epidemics may develop in special
those staying full time (p00.02; Table 4). Children who settings, such as hospitals or nursing institutions. In these
preferably played with their own soft toys had a lower settings, both staff and patients are affected [14, 15, 17].
probability of developing scabies (risk ratio 0.14, 95 % CI Several features of scabies make it difficult to investigate
0.050.42; p00.04) (Table 4). its epidemiology. First, after primo-infestation, symptoms
appear with a delay of 34 weeks [3]. Second, scabies can
Table 4 Factors associated with the presence of scabies in children mimic many skin diseases of infectious and non-infectious
Variables Positive, n (%) Risk ratio (95 % CI) p-value origin, making a clinical diagnosis difficult [3]. Third, the
various diagnostic techniques currently used considerably
Kindergarten-related differ in their diagnostic accuracy, are difficult to standard-
Full time in the kindergarten ize, and depend on patient-related factors, such as duration
No 0/31 (0.0) Reference of disease [2022]. Finally, it is still a matter of debate as to
Yes 8/45 (17.8) N.A.a 0.02 whether transmission predominantly occurs via intimate
Afternoon nap in the kindergarten body-to-body contact, such as sexual intercourse, breast
No 6/62 (9.7) Reference feeding, sleeping in the same bed, or through fomites [23].
Yes 2/14 (14.3) 1.48 (0.336.56) 0.64 An important role of fomites is suggested by a series of
Shares towel with other children experiences performed by Arlian et al. [24, 25]. The authors
No 4/23 (17.4) Reference examined dust samples collected in households of scabies
Yes 4/40 (10.0) 0.58 (0.162.08) 0.45 patients and found mites in 44 % of the samples. Two-thirds
Child has her/his own stuffed animal of the samples contained viable parasites. In another study,
No 6/66 (9.1) Reference Arlian et al. [24] showed that mites extracted from bed linen
Yes 1/9 (11.1) 0.82 (0.116.04) 1.00 used by scabies patients remained infectious for 96 h when
Wears clothes belonging to the kindergartenb stored at room temperature. Transmission through textiles is
No 1/3 (33.3) Reference also suggested by the analysis of an epidemic in a teaching
Yes 7/72 (9.7) 0.29 (0.051.68) 0.29 hospital in So Paulo, Brazil, where 45 of 200 (23 %)
Plays only with own textile toys employees of the laundry section developed scabies after
No 2/3 (66.7) Reference contact with the laundry of a patient with crusted scabies, a
Yes 6/65 (9.2) 0.14 (0.050.42) 0.04 disease manifestation with extended skin lesions and a myr-
Carries diapers iad of Sarcoptes mites shed from the skin [26].
No 7/58 (12.1) Reference However, a more recent investigation suggests that the risk
Yes 1/18 (5.6) 0.46 (0.063.50) 0.67 of transmission of Sarcoptes mites through textiles is rather
Crawls into the adventure cavec low. Tsutsumi et al. [27] analyzed risk factors during a scabies
No 1/4 (25.0) Reference
outbreak in dementia patients in a geriatric hospital and
Yes 6/63 (9.5) 0.38 (0.062.44) 0.36
showed that patients who were able to move without assis-
Family and social behavior
tance had a significantly higher risk of infection compared to
bedridden patients. Gender, types of room, and sleeping
Shares bed with siblings
arrangements, on the other hand, were not associated with
No 4/43 (9.3) Reference
the presence of scabies. In summary, the role of transmission
Yes 3/31 (9.7) 1.04 (0.254.32) 1.00
through fomites during scabies epidemics remains unsolved.
Frequently welcomes other children to play at home
We hypothesized that investigating an outbreak in a
No 1/13 (7.7) Reference
kindergarten would allow finding definitive answers as to
Yes 7/63 (11.1) 1.44 (0.1910.76) 1.00
how transmission occurs. However, this was not the case.
a
Not applicable; no cases occurred among children who were not full The finding that nursery teachers who hugged children
time in the kindergarten regularly had a greater risk of developing scabies (risk ratio
b
Also used by other children; for example, during life role-playing 4.5) compared to staff members who rarely embraced chil-
c
Built from textiles with cushions, pillows, and carpet floor dren, may point to the transmission of mites by intimate
Eur J Clin Microbiol Infect Dis (2013) 32:373380
body contact. In contrast, the observation that the use of
own textile toys by children was a protective factor (risk
ratio 0.14) indicates that transmission through fomites may
have played a role. Both methods of transmission may
explain the finding that the risk ratio to develop scabies
significantly increased with the time that the children stayed
in the kindergarten during the day: none of the children
arriving during the afternoon developed scabies, whereas
17.8 % of children staying full time (and who usually slept
together with other children at noon) became infested (p0
0.02). We suppose that the particular pedagogical concept of
the kindergarten exposed children and staff in an indiscrim-
inative manner to Sarcoptes mites via body contact or
through textiles. By consequence, a preferred route of trans-
mission could not be singled out.
To our knowledge, only two epidemics in educational
facilities for children have been published. One concerned a
workshop at a residential home for disabled persons [8], the
other a boarding school for children with learning difficul-
ties [16]. Both institutions were peculiar in the way that they
cared for children with a mental handicap, that the children
lived in the institution, and that the epidemic continued for
several months.
Hitherto, a single scabies outbreak in a normal kindergarten
has been reported [4]. It is, therefore, reasonable to assume
that scabies outbreaks in a kindergarten are very rare.
In Constance, the delayed diagnosis of the index case and
the difficulty to diagnose scabies when skin lesions are
minimal do explain why the outbreak only became obvious
when already a dozen nursery teachers and children had
been infested (Figs. 1 and 2). In fact, the pedagogical con-
cept of the kindergarten, the daily routine, and the behavior
of the nursery teachers made it very likely that the transmis-
sion of Sarcoptes mites could have occurred through both
intimate body contact and fomites.
Scabies was significantly more frequent in children with
a pre-existing skin disease, e.g., neurodermatitis. We are
unable to provide a conclusive answer for this finding. A
hypothetical explanation is that a pre-existing itching skin
disease provokes scratching and a subsequent denudation of
the stratum corneum, which, in turn, may facilitate the
infestation with Sarcoptes mites.
There are several hints indicating that the epidemic was
initiated by the kindergartens staff. First, the index case was a
nursery teacher. Second, the attack rate was significantly
higher in nursery teachers as compared to children. Finally,
the fact that more topographic areas were affected in nursery
teachers compared to children indicates that the duration of the
infestation had progressed for longer in the former group [21].
Our study has several limitations. First, the number of cases
was small. This may have precluded the identification of
relevant risk factors and explains the rather large confidence
379
intervals of risk ratios. Second, since the investigations were
performed 8 days after mass treatment, it was impossible to
verify the diagnosis. In addition, it was not known whether
dermatologists differed in their experience in diagnosing sca-
bies. Since the accuracy of the diagnosis of scabies depends
on the experience a dermatologist has [22], we cannot exclude
that some of the patients were falsely classified as positive.
Third, for logistic constraints, it was not possible to investigate
the cases of scabies which had occurred in other kindergartens
of the city. We are, therefore, unable to confirm that the
pedagogical concept of the kindergarten was actually respon-
sible for the dimension of the outbreak.
In conclusion, we describe an outbreak of scabies in a
kindergarten with a particular pedagogical concept. Since
exposure patterns were rather similar in all children of the
kindergarten, it was impossible to disentangle whether
transmission predominantly occurred through intimate body
contact, via fomites, or through both forms.
Acknowledgments We express our gratitude to the city heath de-
partment and the employees of the public kindergarten in Constance,
Germany. The data of this study are part of the medical thesis by B.W.
L.A. received a postdoctoral scholarship from the GermanBrazilian
PROBRAL program jointly supported by the German Academic Ex-
change Service (DAAD, Germany) and Coordenao de Aperfeioa-
mento de Pessoal de Nvel Superior (CAPES, Brazil).
Conflict of interest The authors declare that they have no conflict of
interest.
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