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ORIGINAL ARTICLE Risk factors for recurrence of scabies: A retrospective study of scabies patients in a long-term care hospital Kuniko MAKIGAMI, 1 Noriko OHTAKI, 2 Norihisa ISHII, 3 Tetsuko TAMASHIRO, 4 Sadao YOSHIDA, 5 Seiji YASUMURA 1 1 Department of Public Health, Fukushima Medical University, School of Medicine, Fukushima, 2 Department of Dermatology, Kudanzaka Hospital, Tokyo, 3 National Institute of Infectious Diseases, Leprosy Research Center, Departments of 4 Pharmacy and 5 Internal Medicine, Kitanakagusuku Wakamatsu Hospital, Kitanakagusuku Village, Japan ABSTRACT A considerable number of patients suffer recurrence of scabies. To elucidate risk factors for recurrence of scabies, we compared patients who experienced scabies recurrence and those who suffered scabies only once. We conducted a retrospective review of medical records of all scabies patients in a long-term care hospital for the elderly (300 beds; six wards) for a period of 42 months to determine frequency of scabies onsets, underlying diseases, history of treatment, and demographic data such as age and sex. One hundred and forty-eight patients and five hospital staff members suffered scabies during the 42-month study period. All staff members and 98 patients had no recurrence, while 50 patients experienced at least one recurrence of scabies. The cumulative number of scabies diagnoses was 228. The rates of scabies onset and recurrence were considerably different among wards. The dementia unit showed the highest rate of onset and recurrence. In addition to frequent exposure to infectious sources, problematic behavior, such as lying in other patients beds, might cause the high recur- rence rate in dementia units. Higher serum total lymphocyte count and topical use of c-benzene hexachloride were associated with lower risk of scabies recurrence. Recurrence of scabies is not uncommon among elderly patients in institutional settings. Impaired immunity may be a risk factor for recurrence of scabies. Groups with a high onset rate of scabies pose a high likelihood of recurrence. Problematic behavior of demented patients may increase the risk of recurrence. Use of effective topical treatment may effectively prevent recurrence. Key words: epidemiology, long-term care hospital, recurrence, re-infestation, scabies. INTRODUCTION Scabies is a pruritic dermal infection caused by the mite Sarcoptes scabiei var. hominis. The pres- ent scabies epidemic in Japan began around 1975 and continues mostly in institutional settings such as nursing homes, long-term care hospitals and psychiatric hospitals. 1–3 Various factors have con- tributed to the outbreak of scabies in institu- tions: delay of diagnosis, misuse of corticosteroid and iatrogenic crusted scabies, 4 increased number of immunocompromised hosts due to population aging, and frequent patient transfers among hospitals. 5 Through investigations on institutional scabies outbreaks, we have found that a considerable number of patients suffer from recurrence of sca- bies. This study was designed to reveal risk factors for scabies recurrence in order to better control the disease in institutions. We compared patients with single onsets to those with multiple onsets of scabies. Correspondence: Kuniko Makigami, M.D., Ph.D., M.S.G., Aozora Medical Clinic Shin-Matsudo, 3-15 Shin-Matsudo, Matsudo City, Chiba 270-0034, Japan. Email: [email protected] Received 10 August 2010; accepted 14 December 2010. doi: 10.1111/j.1346-8138.2011.01199.x Journal of Dermatology 2011; 38: 874–879 874 Ó 2011 Japanese Dermatological Association

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Page 1: JURNAL KULIT 2

ORIGINAL ARTICLE

Risk factors for recurrence of scabies: A retrospectivestudy of scabies patients in a long-term care hospital

Kuniko MAKIGAMI,1 Noriko OHTAKI,2 Norihisa ISHII,3 Tetsuko TAMASHIRO,4

Sadao YOSHIDA,5 Seiji YASUMURA1

1Department of Public Health, Fukushima Medical University, School of Medicine, Fukushima, 2Department of Dermatology,

Kudanzaka Hospital, Tokyo, 3National Institute of Infectious Diseases, Leprosy Research Center, Departments of 4Pharmacy and5Internal Medicine, Kitanakagusuku Wakamatsu Hospital, Kitanakagusuku Village, Japan

ABSTRACT

A considerable number of patients suffer recurrence of scabies. To elucidate risk factors for recurrence of scabies,

we compared patients who experienced scabies recurrence and those who suffered scabies only once. We

conducted a retrospective review of medical records of all scabies patients in a long-term care hospital for the

elderly (300 beds; six wards) for a period of 42 months to determine frequency of scabies onsets, underlying

diseases, history of treatment, and demographic data such as age and sex. One hundred and forty-eight patients

and five hospital staff members suffered scabies during the 42-month study period. All staff members and 98

patients had no recurrence, while 50 patients experienced at least one recurrence of scabies. The cumulative

number of scabies diagnoses was 228. The rates of scabies onset and recurrence were considerably different

among wards. The dementia unit showed the highest rate of onset and recurrence. In addition to frequent exposure

to infectious sources, problematic behavior, such as lying in other patients beds, might cause the high recur-

rence rate in dementia units. Higher serum total lymphocyte count and topical use of c-benzene hexachloride were

associated with lower risk of scabies recurrence. Recurrence of scabies is not uncommon among elderly patients in

institutional settings. Impaired immunity may be a risk factor for recurrence of scabies. Groups with a high onset rate

of scabies pose a high likelihood of recurrence. Problematic behavior of demented patients may increase the risk of

recurrence. Use of effective topical treatment may effectively prevent recurrence.

Key words: epidemiology, long-term care hospital, recurrence, re-infestation, scabies.

INTRODUCTION

Scabies is a pruritic dermal infection caused by

the mite Sarcoptes scabiei var. hominis. The pres-

ent scabies epidemic in Japan began around 1975

and continues mostly in institutional settings such

as nursing homes, long-term care hospitals and

psychiatric hospitals.1–3 Various factors have con-

tributed to the outbreak of scabies in institu-

tions: delay of diagnosis, misuse of corticosteroid

and iatrogenic crusted scabies,4 increased number

of immunocompromised hosts due to population

aging, and frequent patient transfers among

hospitals.5

Through investigations on institutional scabies

outbreaks, we have found that a considerable

number of patients suffer from recurrence of sca-

bies. This study was designed to reveal risk factors

for scabies recurrence in order to better control

the disease in institutions. We compared patients

with single onsets to those with multiple onsets of

scabies.

Correspondence: Kuniko Makigami, M.D., Ph.D., M.S.G., Aozora Medical Clinic Shin-Matsudo, 3-15 Shin-Matsudo, Matsudo City, Chiba 270-0034,

Japan. Email: [email protected]

Received 10 August 2010; accepted 14 December 2010.

doi: 10.1111/j.1346-8138.2011.01199.x Journal of Dermatology 2011; 38: 874–879

874 � 2011 Japanese Dermatological Association

Page 2: JURNAL KULIT 2

METHODS

Outline of hospital studied

The hospital examined in this study was a long-term

care hospital for the elderly (300 beds; five wards) in

rural southwestern Japan. The authors (K. M., N. O.

and N. I.) have repeatedly visited this hospital, where

they have performed screening of scabies patients

and have held lectures to control the disease since

August 2005. Despite enthusiastic implementation of

control measures by the staff, however, sporadic epi-

sodes have been observed (Fig. 1). Surprisingly, inci-

dences of scabies did not decrease dramatically after

implementation of control measures. One of the most

notable issues in this hospital was that quite a few

patients were repeatedly diagnosed with scabies.

During the interval between symptoms, patients had

neither skin rash nor pruritus.

Review of clinical charts of scabies patients

In order to determine the nature and frequency of

scabies recurrence, we reviewed medical records of

all scabies cases reported to the Infection Control

Committee of the hospital between September 2003

and February 2007 (42 months). A database was

compiled of the following: patient profile and labora-

tory data, patient dynamics and behavior, and clinical

courses of scabies.

In the patient profile and laboratory data, we looked

for any correlations between susceptibility of scabies

and the following variables: age, sex, body mass

index, serum total protein (T-P), albumin, chorine

esterase, hemoglobin, white blood cell count, serum

total lymphocyte count (TLC), and coexisting illnesses

or conditions (dementia, diabetes mellitus, tube feed-

ing and use of corticosteroids). Only laboratory data

and bodyweights measured within 3 months before

or after the diagnosis of scabies were entered into the

database.

Of the information on patient behavior and inter-

or intra-institutional transfers, possible correlations

between exposure to infection sources and the fol-

lowing variables were examined: period of hospital

stay (date of admission, date of discharge, date of

death for deceased patients), ward of hospital stay,

previous institution (for transferred patients) and

problematic behaviors thought to increase the risk

of scabies (e.g. wandering, lying in other patients’

beds).

Regarding clinical courses of scabies, the following

variables were examined: date of scabies diagnosis,

basis of diagnosis (parasitological examination or

symptom and history of scabies mite exposure),

number of times diagnosed with scabies, and treat-

ment protocol (choice of scabicide, number of appli-

cations, response to treatment).

Case definition and diagnosis

Scabies diagnoses were confirmed by physicians at

the study hospital by microscopic detection of mites

in skin specimens and ⁄or epidemiological informa-

tion, such as chance of close contact with scabies

patients.6 The accuracy of skin check and diagnostic

procedures were confirmed by a trained dermatolo-

gist (N. I.).

Statistical analysis

Statistical analysis was performed using SPSS

ver. 15.0J. Univariate analysis was first performed

with frequency of scabies diagnosis as the depen-

dant variable. Stepwise multivariate logistic regres-

sion was then performed using variables from the

univariate analysis results with P < 0.10 set for the

independent variables.

Ethical approval

The study design was reviewed and approved by the

Ethical Committee of Fukushima Medical University

and the study hospital. Prior to conducting the study,

0

10

20

30

40

50 OthersDementia unit

2004 2005 2006 2007

Figure 1. Incidences of scabies in the hospital studied.

� 2011 Japanese Dermatological Association 875

Risk factors for recurrence of scabies

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patients or proxies for consent were given explana-

tions on the study and agreed to the study.

RESULTS

Prevalence of scabies in the study hospital

During the 42-month study period, 153 people

(148 patients, five hospital staff members) suffered

from scabies at least once (Table 1). Among them,

50 patients were diagnosed with scabies multiple

times (i.e. recurrence of scabies), while 98 patients

were diagnosed with scabies only once. Thirty-one

patients were diagnosed with scabies twice, 12 were

diagnosed three times, four were diagnosed four

times and two were diagnosed five times. An

84-year-old woman in the dementia unit was diag-

nosed the most frequently at six times in 13 months.

The total number of scabies diagnoses was 228.

None of the staff members had multiple onsets. The

average interval between onsets was 141.1 days

(n = 80, range 17–588 days, median 89 days).

Risk factors for recurrence

The relationship between patient variables and num-

ber of onsets was examined using univariate analysis,

with whether or not a patient experienced scabies

recurrence set as the dependent variable (Table 2).

Variables from Table 2 with P < 0.10 which did not

conceptually overlap with other variables were used

as independent variables in the multivariate analysis

(Table 3). Patients with higher TLC and patients trea-

ted with c-benzene hexachloride (c-BHC) experi-

enced significantly fewer scabies recurrences. No

significant relation was found between scabies recur-

rence and age, sex, BMI, serum T-P, tube-feeding,

problematic behavior, diabetes and use of cortico-

steroids.

Difference of prevalence and recurrence rate

among wards

As shown in Table 2, the rates of scabies onsets were

considerably different among wards. For example,

105 onsets occurred in the dementia unit (48 beds)

while 11 onsets occurred in long-term care unit A

(54 beds). The high prevalence among patients in

dementia units is also evident in Figure 1. Frequency

of recurrence also differed among wards. The

dementia unit had the highest rate of recurrence

(67.6%), whereas the lowest recurrence rate was

observed in the rehabilitation unit (20.0%).

DISCUSSION

Recurrence rate of scabies

It is widely known among practitioners that recur-

rence of scabies is not uncommon, especially among

elderly patients.7 In the hospital examined in the

present study, the recurrence rate was quite high at

31.1%; approximately one-third of scabies patients

experienced multiple onsets of the disease. However,

epidemiological information on relapse of scabies is

scarce and we could not identify any standards with

which to compare recurrence rates in this population

relative to others.

If we assume that the recurrence rate at this hos-

pital was unusually high, several factors may be

Table 1. Number of patients and frequency of scabies diagnosis

Number of scabies onsets

TotalSingle onset

Multiple onsets

Two Three Four Five Six

Number of patients 98 31 12 4 2 1 148

50

% 66.2 20.9 8.1 2.7 1.4 0.7 100.0

Number of onsets 98 62 36 16 10 6 228

130

% 43.0 27.2 15.8 7.0 4.4 2.6 100.0

Age (average) 81.4 83.2 86.8 71.5 84.5 84.0 82.0

83.3

876 � 2011 Japanese Dermatological Association

K. Makigami et al.

Page 4: JURNAL KULIT 2

considered. First, infection control measures could

have inadvertently caused continuous scabies

outbreaks. However, this is unlikely because the

authors themselves, two of whom are trained

dermatologists (N. O., N. I.) and one of whom is an

epidemiologist (K. M.), confirmed the accuracy of

scabies diagnosis and the adequacy of the infection

control protocol used at the hospital. Second, this

study population may have had a particularly high

susceptibility to recurrence, because most of its

members were frail elderly patients. High rate of

re-infection is another possible reason for the high

recurrence rate. Scabies outbreaks were quite com-

mon in health-care institutions in the surrounding

community. Transferred patients were frequently

infested with scabies, which could serve as a source

of infection. Drug-resistant parasites, although

unlikely, may have also contributed to the high

recurrence. Currie et al.8 reported ivermectin- and

c-BHC-resistant scabies in Aboriginal communities

in northern Australia. Van den Hoek et al.9 reported

a prolonged outbreak with several recurring cases

and suggested the resistance of scabies to ivermec-

tin and c-BHC. However, c-BHC treatment signifi-

cantly lowered the relapse rate in this study, and

c-BHC and ivermectin are generally effective in

Table 2. Univariate analysis of risk factors for multiple onsets of scabies

No. of scabies onsetsNo. of

missing

data P-value

Single

onset (%)

Multiple

onsets (%) Total (%)

Total 98 (100.0%) 130 (100.0%) 228 (100.0%)

Patient characteristics

Mean age (years) 81.45 83.26 82.50 0 0.206†‡

Sex

F 54 (55.1%) 82 (63.1%) 136 (59.6%) 0 0.192†§

M 44 (44.9%) 48 (36.9%) 92 (40.4%)Body mass index (mean) 19.68 19.88 19.80 40 0.836–

Serum data (mean)

Total protein (g ⁄ dL) 6.69 6.63 6.57 80 0.965–

Albumin (g ⁄ dL) 3.52 3.46 3.48 73 0.600–

Total lymph count (cells ⁄ mm3) 1862 1468 1665 122 0.011†–

Hemoglobin (g ⁄ dL) 11.65 12.05 11.86 68 0.184–

Coexisting illness or condition

Diabetes mellitus 7 (7.1%) 14 (10.8%) 21 (9.2%) – 0.489§

Tube feeding 32 (32.7%) 28 (21.5%) 60 (26.3%) – 0.067†§

Use of corticosteroids 9 (9.2%) 15 (11.5%) 24 (10.5%) – 0.667§

Dementia 59 (60.2%) 96 (73.8%) 155 (68.0%) – 0.062†§

Problematic behaviors 23 (23.5%) 34 (26.2%) 57 (25.0%) – 0.758§

Drugs for treatment (multiple answers)

c-BHC 79 (80.6%) 83 (63.8%) 162 (71.1%) – 0.003§

Ivermectin 18 (18.4%) 31 (23.8%) 49 (21.5%) – 0.416§

Crotamiton 21 (21.4%) 39 (30.0%) 60 (26.3%) – 0.175§

Sulfur 21 (21.4%) 40 (30.8%) 61 (26.8%) – 0.173§

Permethrin 3 (3.1%) 14 (10.8%) 17 (7.5%) – 0.040†§

Ward at the point of diagnosisDementia unit (48 beds) 34 (32.4%) 71 (67.6%) 105 (100.0%) 0.005†§

Acute care unit (25 beds) 17 (58.6%) 12 (41.4%) 29 (100.0%) 0.072†§

Long-term care unit A (54 beds) 7 (63.6%) 4 (36.4%) 11 (100.0%) 0.147§

Long-term care unit B (60 beds) 23 (44.2%) 29 (55.8%) 52 (100.0%) 0.873§

Rehabilitation unit (36 beds) 8 (80.0%) 2 (20.0%) 10 (100.0%) 0.020†§

Convalescent care unit (100 beds) 9 (42.9%) 12 (57.1%) 21 (100.0%) 0.818§

c-BHC, gamma benzene hexachloride. †Variables put into the logistic model. ‡Student’s t-test. §Fisher’s exact test. –Mann–Whitney U-test.

Table 3. Final multivariate logistic regression of multiplescabies onsets

P Odds ratio 95% CI

Total lymph count* 0.005 0.565 0.378–0.843

Treatment with c-BHC 0.001 0.205 0.077–0.543

*Ordinal data: quartile. CI, confidence interval; c-BHC, c-benzenehexachloride.

� 2011 Japanese Dermatological Association 877

Risk factors for recurrence of scabies

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treating scabies in Japan. Thus, the contribution of

drug-resistant parasites is unlikely. Also, many

patients in this particular hospital are elderly and

afflicted with dementia, and often walk barefoot,

more so than their counterparts in northern Japan.

Due to the warm climate of the community, patients

were not accustomed to wearing socks or shoes.

We found scabies mites from the feet of elderly

inpatients in the hospital and other hospitals in the

same community. Further investigations are required

to determine whether each of these potential factors

increases the risk of scabies.

Treatment failure or re-infestation?

Recurrences of scabies include both recrudescence

of scabies with surviving mites through incom-

plete eradication (treatment failure) and re-infestation

from contacts. However, it is difficult to distinguish

between the two pathways. Walton et al.10 used

molecular analysis to distinguish between these two

types of recurrences. However, their method is not

yet widely available in clinical settings, and we were

unable to determine the cause of recurrence in this

study.

Host susceptibility and recurrence

Higher TLC was associated with a lower scabies

recurrence. Many researchers have proposed TLC as

an indicator of patient immunity against infectious

diseases. Taniguchi et al.11 reported that lower TLC

was associated with higher mortality rate of patients

with opportunistic infections. All other factors thought

to increase susceptibility to infectious diseases, such

as advanced age and use of corticosteroids, were

not significantly related to scabies recurrence, though

the small sample size may have undermined the

effects of these factors. Lack of recurrence among

hospital staff also suggests the importance of host

susceptibility in recurrence. Further studies examin-

ing host susceptibility are needed to determine the

risk factors for scabies recurrence.

Exposure risk and re-infestation

Prevalence and recurrence rate of scabies were con-

siderably different among the various wards in the

hospital. Differences in certain patient characteristics

among wards, such as immune function and fre-

quency of problematic behaviors, may have contrib-

uted to this difference. For instance, the dementia

unit, where many patients have problematic behav-

iors, has a higher recurrence rate of scabies. More-

over, in wards with a large number of scabies

patients, such as the dementia unit, risk of exposure

to infectious sources and therefore re-infestation

are high, further increasing the number of scabies

patients and possibly creating a vicious cycle. Differ-

ences in patient characteristics and risk of exposure to

infectious sources among wards suggest that these

differences may be factors for scabies recurrence.

Effective topical treatment may prevent

recurrence

In Japan, ivermectin was the only approved scabicide

under the National Health Insurance Plan. In the study

population, only one-fifth of patients were treated

with ivermectin while over 70% of them were treated

with c-BHC because of the timing of the approval of

ivermectin in August 2006. The study showed that

patients treated with c-BHC were less likely to experi-

ence recurrence of scabies.

There are limited studies regarding comparison of

effectiveness and safety of scabicides; generally

speaking, crotamiton and sulfur are less effective

than ivermectin, permethrin, c-BHC and benzyl ben-

zoate.12 There are no treatment guidelines for recur-

rent scabies. Due to increasing concerns on its

toxicity and environmental impact, c-BHC is no

longer the drug of choice in developed countries.

Many reports have been published on treatment fail-

ure of crusted scabies with ivermectin.9,13 The thick

hyperkeratosis of crusted scabies hampers drug

delivery. Currie et al.14 reviewed scabicides, mainly

permethrin and ivermectin, and stated that patients

with crusted scabies should be treated by combined

use of topical and oral scabicides. Regarding all these

circumstances of scabicides, we interpret the results

on c-BHC as follows: effective topical treatments

may suppress recurrence of scabies.

Limitations to this study

The subjects of this study were mainly elderly

inpatients, thus we should be cautious about genera-

lizing the results to other populations. However, to

the best of our knowledge, this study is the first to

examine risk factors for scabies recurrence. Further

investigations in the other types of settings are

878 � 2011 Japanese Dermatological Association

K. Makigami et al.

Page 6: JURNAL KULIT 2

needed to better understand general risk factors for

scabies recurrence.

ACKNOWLEDGMENTS

The authors thank all the staff at the hospital for

their support and participation. Funding for this

study was provided by a Grant-in-Aid for scientific

research from the Japan Society for the Promo-

tion of Science in 2004–2006 (#16590506).

REFERENCES

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2 Ohtaki N. [Epidemiology of scabies in institutions for theelderly in Japan (in Japanese)]. Hifubyo Shinryo 1997;19: 468–472.

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