ARTICLE
Auteur(s) : Sara WILLEMS*1,
Hilde LAPEERE*2, Nele
HAEDENS1, Inge PASTEELS1, Jean-Marie
NAEYAERT2, Jan De MAESENEER1
1Ghent University, Department of General Practice and
Primary Health Care, Campus UZ- 1K3, De Pintelaan 185, B-9000 Gent,
Belgium
2Ghent University, Department of Dermatology, Campus
UZ-1P6, De Pintelaan 185, 9000 Ghent, Belgium
accepté le 10 Juin 2005
Pediculosis, which is defined as an infestation with head, body or
crab lice, is a frequent occurring skin infection [1, 2].
Especially, head lice (Pediculus humanus capitis) infestations are
a common health problem mainly affecting schoolchildren aged
between 3 and 12 [1]. Head lice infestation prevalence rates of
5.8% to 35% have been reported [3-8]. In Belgium, the only
information concerning the prevalence of head lice in
schoolchildren comes from a recent but small survey in two primary
schools in the city of Ghent (an industrialised city in the
northern part of Belgium, 226,083 inhabitants), revealing
prevalence rates of 13.0% and 19.5% [9].The origin of a head lice
infestation is unclear. Most prevalence studies examine the
relationship between personal characteristics of the child (i.e.
sex, age, hair length, hair type) and infestation [3, 4, 7, 10],
but there are few studies that also consider the family’s
socio-economic status (SES) [6-8, 11]. All these studies have
conflicting results that can be partly explained by the use of
different diagnostic criteria, screening methods, the presence of
confounding factors, and limited statistical techniques. In some
studies, children are considered to be infested if either lice or
nits are present [6, 8]. However, an active infestation should only
be diagnosed when a living, moving louse is detected [12].
Furthermore, there are three methods of detecting head lice: visual
inspection, inspection with a detection comb and wet combing. It
has been demonstrated that the latter two are more accurate than
the first [10, 13]. Wet combing is probably more accurate then dry
combing because lice get stuck in the water and conditioner and are
therefore more easily found. Although wet combing is time-consuming
and laborious in comparison to other detection methods, it has been
illustrated elsewhere that it is feasible to screen large groups of
children with this method [9]. Apart from the differences in
diagnostic methodology, there is also a large variation in the
statistical methods applied. When analysing this kind of data,
statistical tests controlling associations between the different
factors should be used.Therefore, the complex mechanisms of
interaction between the multiple determinants of head lice are
still unexplained.The objective of this study is to determine the
prevalence of head lice in schoolchildren in Ghent, using the wet
combing technique, and to investigate the independent association
between individual characteristics of the child, socio-economic
status and head lice.
Materials and method
Population and sample
The three School Health Departments (SHD) screen all schoolchildren
yearly for head lice using dry inspection. In 2001, the SHD started
a pilot project in which children were screened using the wet
combing method. All kindergartens and primary schools in Ghent
(174) were invited to participate in this pilot project, of which
30 agreed. Between January and June 2001, all children from the
participating schools present on the day of the screening were
included in the project. A total of 6,169 children were screened,
representing 30% of the town’s total population of children aged
between 3 and 12.
Data collection
Several SHD staff screening teams were involved in the pilot
project, led by a staff member trained in the wet combing method by
experts on this subject. Where necessary, screening teams were
reinforced with parents and teachers, who were trained using an
educational package including a video of the wet combing method.
The team leader double-checked positive results found by the team
members. An ordinary shampoo, conditioner and a fine-toothed
plastic comb (as in a Bug Buster kit®) were used. First,
the hair of the child was washed with an ordinary shampoo and
plenty of conditioner was applied to the wet hair after
straightening with a grooming comb. Then the scalp was
systematically combed with a fine-toothed comb, first from back to
front and then vice versa. Combing was started at one side of the
head and ended at the other side. When conditioner is used, lice
get caught in the moisture and are unable to move. The fine-toothed
comb lifts out lice from the hair, even the smaller nymphal stages
that sometimes remain unnoticed by the naked eye.
A child was found positive if a living louse was found. The
presence of nits was also recorded, but no distinction was made
between viable or dead eggs or empty eggshells. The positive
children were given a letter for their parents with treatment
advice and were screened again two weeks later. For every child,
the SHD staff collected data about demographic characteristics
(sex, date of birth, class and school), properties of the hair
(length, colour and type) and characteristics of the family (number
of children in the family and socio-economical status). Hair length
was defined as very short (< 2 cm), short (≥ 2 cm but
less than shoulder length), medium (= shoulder length) or long
(> shoulder length). Hair colour was divided into 4 categories
(black, brown, red or fair) (( figure 1 )) and hair type
into 3 categories (straight, curly or frizzy).
The socio-economic status of the family was based on the person
with the highest occupational status in the household and retrieved
from the children’s school file. Occupation was classified
according to the Standard Occupational Classification, published by
the Office of Population Censuses and Surveys, using 4 categories:
unemployed, manual worker, non-manual worker and professional
[14].
The nationality of the child was also recorded but not included
in the analysis since there were too many different nationalities
and recording this information into a dichotomous variable (Belgian
versus other) led to an important loss of data. All parents of
positive children were given treatment advice and the treatment
chosen was recorded for 25% of the positive children. No
information was obtained on whether the treatment was applied
correctly. Positive children were screened again 14 days after
baseline screening. Results from the second screening are available
for 87% of the children found to have lice at the baseline.
Statistical analysis
The data was analysed using SAS® release 8.02. First,
two-dimensional crosstabs with χ2-test statistics and
correlation matrices were built in order to study the bivariate
relationships between the prevalence of head lice and the
independent variables. Secondly, to determine the relative
importance of the different variables in explaining or predicting
the presence of head lice, the Glimmix macro written by Russ
Wolfinger from SAS was used to construct a logistical model with
random effects [15]. Since the sample design was typically
hierarchical, this type of multilevel model was most appropriate
for a dichotomous outcome variable because it incorporated the fact
that observations from same subpopulations were more equivalent
than observations from other ones. P < 0.05 was set as the level
of statistical significance.
Results
The prevalence of head lice infestations in children from
kindergartens and primary schools in Ghent was 8.9%. Another 4.6%
had nits without lice, a sign of a past infestation.
Bivariate analysis demonstrated a significant association
between head lice and the child’s sex, educational level, hair
length and colour, number of children in the family and SES (table
1)( Table 1 ).
Multilevel analysis showed that the variance at school level is
1.93 (P = 0.011). The same parameter at class level within schools
is 2.58 (P < 0.001) and the residual level (level of the
different children within classes) is 0.59 (P < 0.001).
This shows that a child’s school and in particular his or her
class have a greater impact on the risk of head lice than
individual characteristics. The impact at child level can be
attributed to SES (P = 0.017), the number of children in the family
(P < 0.001), the length of the child’s hair (P = 0.028) and the
hair colour (P = 0.021) (table 2)( Table
2 ).
Being from a family with a lower SES, more children and having
longer hair tend to result in a higher risk of getting head lice
(respectively OR: 0.80,95% CI: 0.68-0.96; OR: 1.2,95% CI:
1.10-1.32; OR: 1.2, 95% CI: 1.02-1.43). For example, for every
child that a family has, the probability ratio of getting head lice
increases by 1.2 times. Having black hair entails a lower risk than
having brown hair (OR: 0.6,95% CI: 0.43-0.89).
Head lice were still found in 41.4% of the children screened
fourteen days after baseline screening.
According to the multilevel analysis, only the hair colour (P =
0.011) and SES (P = 0.031) were statistically significant. The
lower the SES, the higher the chance of still being positive on the
second screening (OR: 0.6, CI: 0.37-0.95). Children with black hair
have a higher chance of being lice-free at the screening than
children with brown hair (OR: 0.3, CI: 0.11-0.74).
Table 1 Sex, age, educational level, hair
characteristics, number of children in the family and
socio-economic status (SES) of the family: bivariate results at
baseline and two weeks after baseline screening
|
Baseline screening
|
2 weeks after baseline screening
|
|
n (%)
|
Head lice
|
n (%)
|
Head lice
|
|
|
%
|
P
|
|
%
|
P
|
|
Sex
|
6104
|
|
< 0.001
|
469
|
|
0.110
|
|
Boys
|
2938 (48.1)
|
6.8
|
|
174 (37.1)
|
36.2
|
|
|
Girls
|
3166 (51.9)
|
10.7
|
|
295 (62.9)
|
43.7
|
|
|
Age (years)
|
5519
|
|
0.194
|
420
|
|
0.333
|
|
≤ 5
|
1297 (23.5)
|
9.1
|
|
95 (22.6)
|
33.7
|
|
|
6-7
|
1252 (22.7)
|
9.2
|
|
106 (25.2)
|
39.6
|
|
|
8-9
|
1413 (25.6)
|
9.5
|
|
124 (29.5)
|
41.9
|
|
|
10-11
|
1136 (20.6)
|
7.0
|
|
66 (15.7)
|
47.0
|
|
|
≥ 12
|
421 (7.6)
|
8.6
|
|
29 (6.9)
|
51.7
|
|
|
Educational level
|
|
|
< 0.001
|
459
|
|
0.731
|
|
Kindergarten
|
1619 (26.8)
|
10.2
|
|
139 (30.3)
|
40.3
|
|
|
1st and 2nd year of primary school
|
1778 (29.4)
|
9.7
|
|
153 (33.3)
|
41.2
|
|
|
3rd and 4th year of primary school
|
1553 (25.7)
|
8.0
|
|
114 (24.8)
|
42.1
|
|
|
5th and 6th year of primary school
|
1090 (18.0)
|
6.1
|
|
53 (11.5)
|
49.1
|
|
|
Hair length
|
6124
|
|
< 0.001
|
470
|
|
0.078
|
|
Very short
|
1329 (21 .7)
|
5.1
|
|
60 (12.8)
|
26.7
|
|
|
Short
|
2218 (36 .2)
|
8.5
|
|
163 (34.7)
|
45.4
|
|
|
Medium
|
1336 (21 .8)
|
11.5
|
|
136 (28.9)
|
44.1
|
|
|
Long
|
1241 (20 .3)
|
10.6
|
|
111 (23.6)
|
42.3
|
|
|
Hair type
|
6076
|
|
|
464
|
|
0.459
|
|
Straight
|
5192 (85.5)
|
8.6
|
0.211
|
386 (83.2)
|
42.0
|
|
|
Curly
|
785 (12.9)
|
10.6
|
|
72 (15.5)
|
41.7
|
|
|
Frizzy
|
99 (1.6)
|
8.1
|
|
6 (1.3)
|
16.7
|
|
|
Hair colour
|
6128
|
|
|
472
|
|
0.418
|
|
Fair
|
2137 (34.9)
|
7.7
|
0.035
|
148 (31.4)
|
39.9
|
|
|
Red
|
121 (2.0)
|
9.1
|
|
10 (2.1)
|
30.0
|
|
|
Brown
|
2808 (45.8)
|
10
|
|
246 (52.1)
|
44.7
|
|
|
Black
|
1062 (17.3)
|
8.2
|
|
68 (14.4)
|
35.3
|
|
|
Number of children in family
|
5943
|
|
< 0.001
|
458
|
|
0.004
|
|
1
|
948 (15.9)
|
7.8
|
|
65 (14.2)
|
38.5
|
|
|
2
|
2580 (43.3)
|
7.6
|
|
174 (38.0)
|
32.8
|
|
|
3
|
1499 (25.2)
|
8.6
|
|
112 (24.5)
|
45.5
|
|
|
≥ 4
|
916 (15.6)
|
13.9
|
|
107 (23.4)
|
54.2
|
|
|
SES
|
3742
|
|
< 0.001
|
303
|
|
0.66
|
|
Unemployed
|
296 (7.9)
|
17.6
|
|
38 (12.5)
|
50.0
|
|
|
Manual worker
|
1570 (42.0)
|
12.4
|
|
173 (57.1)
|
48.0
|
|
|
Non-manual worker
|
1490 (39.8)
|
5.8
|
|
75 (24.8)
|
34.7
|
|
|
Professional
|
386 (10.3)
|
5.2
|
|
17 (5.6)
|
23.5
|
|
Table 2 Multilevel analysis at baseline screening and
two weeks after baseline screening
|
Base line screening
|
14 days after baseline screening
|
|
Estimate
|
P-value
|
Estimate
|
P-value
|
|
School-level
|
1.933
|
0.011
|
1.745
|
0.044
|
|
Class-level
|
2.581
|
< 0.001
|
1.316
|
0.014
|
|
Child-level
|
0.594
|
< 0.001
|
0.713
|
< 0.001
|
|
Odds ratio (95%CI)
|
P-value
|
Odds ratio (95%CI)
|
P-value
|
|
Sex
|
1.3 (0.89-1.82)
|
0.187
|
0.9 (0.37-2.33)
|
0.885
|
|
Age (years)
|
0.9 (0.91-1.07)
|
0.839
|
1.0 (0.89-1.20)
|
0.679
|
|
Hair length
|
1.2 (1.02-1.43)
|
0.028
|
1.3 (0.80-2.00)
|
0.308
|
|
Hair type
|
|
Straight
|
1.5 (0.51-4.30)
|
0.465
|
1.4 (0.12-16.26)
|
0.778
|
|
Curly
|
1.6 (0.55-4.84)
|
0.376
|
1.3 (0.10-15.96)
|
0.840
|
|
Frizzy
|
1.0
|
|
1.0
|
|
|
Hair colour
|
|
Fair
|
0.9 (0.75-1.27)
|
0.861
|
0.8 (0.43-1.62)
|
0.580
|
|
Red
|
0.4 (0.14-1.37)
|
0.155
|
1.9 (0.16-23.14)
|
0.593
|
|
Brown
|
1.0
|
|
1.0
|
|
|
Black
|
0.6 (0.44-0.89)
|
0.008
|
0.3 (0.11-0.74)
|
0.011
|
|
Number of children in family
|
1.2 (1.10-1.32)
|
< 0.001
|
1.1 (0.92-1.40)
|
0.240
|
|
SES
|
0.8 (0.68-0.96)
|
0.017
|
0.6 (0.37-0.95)
|
0.031
|
|
Intercept
|
0.01(0.01-0.16)
|
0.003
|
0.4 (0.01-10.2)
|
0.556
|
Discussion
The prevalence of head lice infestation in a large sample of
schoolchildren in Ghent was 8.9%, lower than the previously
reported 13.0% and 19.5% from a previous small study in the town.
The schools in the latter study were selected because of their high
motivation, which was probably related to the fact that they have
encountered head lice before. The multilevel analysis shows that
clustering of children in groups (in classes and schools) is the
most important factor determining the risk of head lice. Head lice
are transmitted by head-to-head contact and probably also by
fomites [16]. Children from the same class have intense contact
with each other, providing frequent opportunities to transmit head
lice. However individual characteristics do have some impact: hair
length, hair colour, the number of children in the family and
socio-economic status of the family are statistically significant
associated with the prevalence of head lice.
The strength of this study is its methodology. No similar survey
applying the same diagnostic criteria and screening method and
including a comprehensive set of confounding factors has ever been
performed on such a large sample. Furthermore, the use of
multilevel analysis allowed the unique impact of each independent
variable to be determined. A source of concern in the present study
could be the lack of a randomised sample. However, a good
representative sample of the population was achieved with only a
slight overrepresentation of larger kindergartens and primary
schools. Furthermore, the prevalence might be influenced by
seasonal trends in head lice infestations as this study was carried
out between January and June. Some authors found a difference in
prevalence according to the month when a screening was performed
[17, 18]. Finally, information on SES was not always recorded in
detail in the child’s school record, resulting in a loss of
data.
This study confirms the results of other studies in the field,
yet on some points it nuances, refutes or explains earlier
findings. The clustering of head lice within classes was observed
in a prevalence study on 735 pupils from one school [4]. Our study,
performed on a larger sample of children from different schools,
confirms the observation of the latter study. Concerning hair
characteristics, as reported earlier by Mumcuoglu et al. [3], we
found higher prevalence rates in children with brown hair. One can
assume that brown-coloured lice contrast more in fair, red and
black hair and are therefore detected earlier. Earlier treatment of
these children may lead to lower prevalence at formal
cross-sectional screening sessions. Hair length can probably be
considered as an important transmitting factor, as head lice need
specific conditions to move from one head to another [16], which
occur more frequently in longer hair. It also seems that the
infestation rate rises with the number of children in the family,
possibly because children in large families have a higher risk of
being infested by their siblings (or parents). The influence of the
family’s socio-economic status on the presence of head lice has
been investigated before, using indicators such as educational
level or profession of the parents, family income, recourse to
social security and socio-economic class of the school. A positive
correlation has been found [1, 6, 11, 19] in some reports but not
in others [7, 8]. However, in most surveys, only bivariate analysis
has been used. This study shows that when adjusting for a range of
confounding factors, SES (defined as the highest occupational class
in the household) is significantly related to the prevalence of
head lice. In several studies, a difference was found in prevalence
rates between girls and boys [1, 4, 6, 7, 20]. It is believed that
gender-related behaviour differences affect transmission rates,
e.g. difference in personal grooming, close contact, hairstyle
changes and the use of hair accessories [21]. Counahan et al.
supported the gender difference based on a large study that used
multilevel statistical techniques and included type of residence,
class, gender and hair length as confounding factors [20]. However,
when building a model that adjusts to a more detailed set of
determinants including other hair characteristics, no difference
was found. We found that the commonly assumed risk factor of age
was not associated with active infestation [6, 10]. Probably, this
could be explained by the high association with school class which
was introduced as a level in the model. This study did not confirm
earlier findings of lower infestation rates in children with curly
hair [3]. Nymphal stages are easily missed in curly or long hair
when using the dry inspection method, possibly leading to an
underestimation of head lice infestation in children with curly or
long hair [22]. When applying wet combing, even the small lice are
found in straight as well as in curly hair [23].
A striking result from the screening after treatment advice is
that 41.4% of the children found to be positive in the baseline
screening were still positive, meaning they were not adequately
treated. This is rather high, considering that every parent
received treatment advice. Vander Stichele et al. also found a low
treatment effectiveness of 51% [9]. Several factors could be
responsible for the high rate of treatment failure. It cannot be
excluded that some parents, regardless of the advice given, did not
treat their children. It is more likely, however, that there was
resistance to the chosen pediculicide or that a lot of children
were not treated correctly. Pediculicides are often expensive and
should be applied correct in order to have optimum results. The wet
combing method was also discussed as a treatment option. This
method is relatively cheap but requires stringent implementation
and is time-consuming. Wet combing should be repeated meticulously
once every 3 to 4 days over a period of 14 days to break the life
cycle of the head louse [9] and is not effective if the
instructions are not followed correctly.
Attention should be paid when interpreting the results of this
study. A significant association was found between head lice and
several factors at child level, yet this does not imply a causal
relationship. Presumably, these factors lead indirectly to higher
prevalence rates because they hamper the detection (e.g. hair
colour) or treatment (e.g. SES) of lice.
This survey illustrated that the clustering of children in
classes and schools is a more important determinant of the
prevalence of head lice than personal characteristics. Head lice
infection is therefore difficult to avoid, making its early
detection and effective treatment all the more important. Although
earlier studies indicated it was feasible to screen larger groups
of children for head lice using the wet-combing technique, the
feasibility of organising large screening campaigns in schools
several times per year is questionable. Probably, it is more
advisable to introduce screening in the daily routine of the
family, e.g. as part of the weekly bathing ritual. Schools and
school health departments could play an important supporting role
for the parents by organising information campaigns and “practice
sessions” on the screening and treatment of children.
The current study showed that children from families with a
lower SES are particularly at risk of getting head lice. Previous
studies showed that the lives of people from the lowest
socio-economic classes are often characterised by a short-term
“survival” perspective. “Compliance” is, from a socio-culturally
point considered, a middle-class concept because in lower social
classes, the need for an adequate follow-up of the treatment
instructions could be overruled by acute social problems related to
income, housing conditions… [24]. Therefore special emphasis should
be put on the need to establish specific support systems (e.g. by
school nurses and primary care nurses) for children from low SES
families with lice infestations. As Whitehead has indicated,
efforts to decrease social inequalities in health must adopt a
multi-level approach and focus on empowering families,
strengthening communities (by educational efforts towards
caregivers) and encouraging macro-economic and cultural change
[25].
Further research is needed to confirm the findings of this study
using a randomised sample and more detailed measurement scales,
e.g. for SES. A cost-effectiveness study should be performed in
which the benefits and costs of wet combing versus
detection-combing of dry hair are assessed.
Acknowledgements
We would like to thank all staff members of the School Health
Departments who collected the data, and the parents and children
for their participation in this study. We also would like to thank
the workgroup “Luis ze erin” for their enthusiasm and substantial
contribution. Finally, we thank Dr. R.H. Vander Stichele for his
very useful comments on the manuscript.
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