Yonago Acta medica 1999;42:193–200

Epidemiological Surveys of Methicillin-Resistant Staphylococcus aureus
in Tottori Prefecture, Japan
Yoshinori Tanaka, Akiko Adachi and Miyoko Tanaka
Department of Bacteriology, Faculty of Medicine, Tottori University, Yonago 683-0826, JapanTo study the isolation frequency of methicillin-resistant Staphylococcus aureus (MRSA)
and susceptibility of MRSA to antibiotics, a questionnaire survey was performed every
half year from 1993 until 1997. The questionnaire was sent to medical doctors, and it
asked retroactively about the isolation of S. aureus from clinical specimens. The isolation
rate of MRSA from patients over 65 years of age was higher, and that from patients
under 16 years of age was lower, than the rates in other age groups (P < 0.01). Ratios ofisolation of MRSA among S. aureus strains were from 12 to 38% in the clinics, from 39
to 71% in the small-scale hospitals and from 47 to 62% in large-sized hospitals. These
isolation rates increased gradually from 1993 to 1997 (P < 0.001). The isolation rate of
MRSA from the sputum was higher, and those from pus, pharyngeal secretion andurine were lower, than those from feces and other specimens and from total specimens.
The isolation rate of antibiotic-resistant strains of MRSA was highest for penicillins
and cepharosporins. MRSA was highly susceptible to arbekacin (isolation rate ofresistant strains: 3.0%) and vancomycin (3.0%), and was slightly susceptible to minocycline (21%), doxycycline (24%), amikacin (39%) and dibekacin (37%). These results
indicate that more careful surveillance of MRSA and more stringent precautions against
nosocomial infection with antibiotic-resistant MRSA are needed in hospitals even in
relatively isolated parts of Japan.
Key words: epidemiology; methicillin-resistance; nosocomial infection; Staphylococcus aureus

There are many bacteria which evoke nosocomial infections, including Escherichia coli,
Pseudomonas aeruginosa, Klebsiella, Staphylococcus aureus, etc. Antibiotic susceptibilityof these bacteria varies with genus, species andstrain. The serious problem of nosocomial infections with multiply antibiotic-resistant bacteria
has increased since the early 1980’s (Locksley
et al., 1982; Thomson et al., 1982). An outbreak of nosocomial infection with multidrugresistant S. aureus was first reported by Locksley
et al. (1982). During a 15-month period, multiply
antibiotic-resistant S. aureus was transferredfrom a burn patient to 34 patients in the hospital. Seventeen of the 34 patients died. Typing
and plasmid analysis showed the spread of multiply resistant S. aureus from the burn unit to thesurgical intensive care unit.
In the late 1980’s, several patients died from

nosocomial infection with methicillin-resistant
S. aureus (MRSA) in Japan, resulting in somelegal proceedings against unwarranted nosocomial infections. We investigated contamination by MRSA in Tottori Prefecture, a relatively isolated prefecture of Japan. The questionnaires were sent to members of medical
institutions in Tottori Prefecture, and the trendsof infections with MRSA in the clinics and hospitals were analyzed.

Subjects and Methods

Questionnaire surveys
At first, questionnaires were sent to clinicaldoctors asking whether or not specimens weresent to a clinical laboratory for bacterial exami-

193

Y. Tanaka et al.

A

B Others (7.7)< 16 (15.9)

Pharyngeal secretion(15.8)

16–30
(4.2)
65 <
(65.7)

Pus(24.6)

31–50
(5.5)

Sputum(34.3)

51–65(8.7)
Feces (1.8)
Urine(10.9)
Rhinorrhea(4.8)

Fig. 1. The frequency of S. aureus isolation in various age groups and from different types of specimens.
Distribution of S. aureus strains isolated in the age groups (A) and from various specimens (B). Total numberof strains isolated was 2,527 during a 5-year period. The isolation frequency (percentage) from each type of
specimen is shown in parentheses.

nation. If we got the answer “yes”, then we sent
the following questionnaires every half year
from 1993 to 1997. The contents of the questionnaires asked the age and sex of the patient,origins of the specimens, species of Staphylococcus, antibiotic susceptibility testing and existence of any abnormal physical background.
Identification of Staphylococcus spp. anddrug susceptibility testing were usually performed by standard methods. Staphylococcus
spp. was identified using commercially available identification kits after selection by mannitepositiveness and coagulase activity. Antibiotic
susceptibility testing was performed by disk
methods (Barry and Thornberry, 1991) andmethicillin-resistant or oxacillin-resistantstrains of S. aureus were defined as methicillinresistant S. aureus (MRSA). However, thesemethods of testing might have varied in different clinical laboratories.

Statistical analysis
Statistical analysis was performed as follows.
Significant differences between the two groups
were determined by Student’s or Welch’s t-test.
Comparisons of several groups controlled by

two factors were made by the two factor analysis of variance or Friedman’s test.

Results

Total cases and hospitals
The number of clinics and hospitals was about
460 in May, 1993. A preliminary investigation
was performed by sending the doctors in these
institutions a questionnaire about whether
microbial examinations were done or not. The
answer was returned from 370 institutions(80.4%).
Out of 300 medical doctors who answeredthat microbial examinations were done if necessary, or that the patients were sent to a big hospital, an average of 57 answered the subsequent
questionnaires which we sent them twice a year.
Accordingly, the average rate of replies was
about 20%. Most of the medical doctors in theclinics did not have patients with bacterial
infection who needed microbial examination,
because the patients were getting better by haphazard treatment with some antibiotics.

Abbreviations: MRSA, methicillin-resistant Staphylococcus aureus; MSSA, methicillin-sensitive Staphylococcus aureus

194Epidemiology of MRSA in Tottori Prefecture(%)

Isolation of S. aureus in the age groups
and from various types of specimens

Isolation rate of MRSA
The rates of isolation of S. aureus strains fromclinical specimens in the period from 1993 until
1997, are shown in Fig. 2. In the clinics, 25 to
75 cases of S. aureus were identified during
every half-year term and the isolation rate of
MRSA varied from 12 to 38%. These isolation
rates were significantly lower than those insmall- and large-sized hospitals (P < 0.001).
The isolation rate of MRSA in relatively small-

Rate of isolation of MRSA

The specimens of 1,391 men and 1,136 women
were examined from 1993 until 1997 (Fig. 1A).
The ratio of men to women was approximately
5 to 4; the difference between the number ofmen and women was not significantly different.
Comparison of the number of specimens in thevarious age groups showed that greater numbers of specimens were isolated from the group
under 16 years of age (16%) and the group over
65 years of age (66%) than from other age
groups. Isolation rates of S. aureus in the agegroups from 16 to 30 years of age, from 31 to 50
years of age and from 51 to 65 years of age were4.2%, 5.5% and 8.7%, respectively. These agegroups showed similar ratios of men to women.
A larger proportion of specimens from women
were isolated from the group over 65 years ofage (70%) as compared with the proportion
from the men isolated from the group over 65
years of age (62%).
In testing the kinds of specimens from which
S. aureus was isolated (Fig. 1B), sputum (34%)
and pus (25%) were the most frequent, and pharyngeal secretion (16%) and urine (11%) were
the next most frequent. There was a low rate ofisolation from sputum, and relatively higher
rates from pus and urine in 1993 (data notshown). The rate of isolation from sputum
increased after 1994 and that from pus varied
from year to year. Rates of isolation from nasal
mucus (rhinorrhea) and urine did not vary fromyear to year. There were few isolations fromblood specimens, and they were included in thegroup of “Others”.

80

60

40

**

20

0
1

2
'93

1 2
'94

1 2
'95

1 2
'96

1 2
'97

Fig. 2. Isolation rates of MRSA in different kinds ofinstitutions. The isolation rates of MRSA in clinics( ), small- ( ) and large- ( ) sized hospitals andtotal isolation rate ( ) were investigated every halfyear. The “1” in the Figure shows the first half of theyear and the “2” shows the latter half of the year.
The isolation rate of MRSA in clinics was significantly lower (**P < 0.001) than that in the otherthree groups, which were not significantly different
from each other. During the period from 1993 until
1997, all four MRSA isolation rates significantly increased (P < 0.001).

sized hospitals and large-sized hospitals gradually increased from 39% and 47% in the firsthalf of 1993 to over 71% and 62% in the second
half of 1997, respectively. Isolation rates of
MRSA in clinics and in small- and large-sized
hospitals increased significantly as the time
elapsed during the period from 1993 until 1997
(P < 0.001).
The total numbers of S. aureus and MRSA
isolated between 1993 and 1997 were about
3,000 and 2,000, respectively. The isolation
rate of MRSA increased gradually and significantly from 47% in the first half of 1993 to
63% in the second half of 1997 (P < 0.001).

Isolation of MSSA and MRSA from specimens in various age groups and isolationfrom various types of specimens
Out of all S. aureus-positive specimens, 66%
were from patients more than 65 years of age,and 16% were from patients under 16 years of195

Y. Tanaka et al.

Number of strains

A
0

< 16

200

400

600

Number of strains

B

800

1000

0

200

400

600

Sputum

**

16–30

Pus
Pharyngeal
secretion
Urine

MSSA
MRSA

31–50

**
**
**
**

Rhinorrhea

51–65

MSSA

Feces
65<

**

MRSA

OthersFig. 3. Isolation of MSSA and MRSA in various age groups and their isolation from various types of specimens. MSSA ( ) and MRSA ( ) were isolated from various specimens. (A) isolation of MSSA and MRSA
in age groups. (B) isolation of MSSA and MRSA from various specimens. The asterisks indicate a significant difference between the ratios of MSSA to MRSA in the groups with asterisks and the groups without
asterisks (**P < 0.001).

age (Fig. 1A). The variance of the number of
specimens from which methicillin-sensitive S.
aureus (MSSA) was isolated was not the sameas that of MRSA (Fig. 3A). The isolation rateof MRSA in the age group under 16 years of age
was significantly lower (P < 0.001) and that in
the age group over 65 years of age was significantly higher than those in the groups from 16 to
30 years of age, from 31 to 50 years of age andfrom 51 to 65 years of age, and higher than theisolation rate of MRSA in the total specimens.
The isolation rates of MRSA from the patientsin the age groups from 16 to 30 years of age,from 31 to 50 years of age and from 51 to 65
years of age and the isolation rate of MRSA
from the total specimens, were 54%, 44%, 52%

and 61%, respectively, and were not significantly different.
The numbers of MSSA and MRSA strains
isolated from specimens between 1993 and 1997
are shown in Fig. 3B. There were large variances in the numbers of MSSA and MRSA. The
isolation rate of MRSA from sputum was higher,
and those from pus, pharyngeal secretion andurine were lower than that of MSSA from eachspecimen (P < 0.001). The isolation rates of
MRSA from rhinorrhea, feces, others and total
specimens were similar to those of MSSA. Many
specimens of sputum were tested from patientsover 65 years of age (87% of total specimens of
sputum), whereas pharyngeal secretion specimens were largely from patients under 15 yearsof age (51% of total specimens of pharyngeal
secretion).

Number of strains
0

100

200

300

400

Background diseases
Immunosuppressive
treatments

**

MSSA
MRSA

Local injuries
Senescence and/or
bed-ridden persons

196

Fig. 4. Isolation of MSSA and MRSA frompatients with compromised conditions.
MSSA ( ) and MRSA ( ) were isolated
from patients with background diseases, immunosuppresive treatments or local injuries,
or from aged and/or bedridden persons. The
isolation ratio of MRSA to MSSA from thepatients with immunosuppresive treatments
is significantly higher than the ratios from thepatients of other groups (**P < 0.001).

Epidemiology of MRSA in Tottori Prefecture

Background of S. aureus infection
We investigated whether or not patients with S.
aureus infection were compromised hosts. As
shown in Fig. 4, the isolation rate of MRSA
from patients with immunosuppressive treatments was clearly higher than that of MSSA
(P < 0.001). However, there were no significant differences in the isolation rates of MRSA
among the groups with background diseases,
local injuries and senescence and/or bedridden
persons.
Patients with background diseases and senescent or bedridden persons were not always
predisposed to MRSA. Although only a few
specimens were analyzed, it appears that only
the immunosuppressive treatments might predispose patients to MRSA, and other factors
might include longer terms of treatment or hospitalization.

Table 1. Isolation rate of antibiotic-resistantstrains of MSSA, MRSA and total strains of
Staphylococcus spp.
Antibiotic
nameAntibiotic resistance
The isolation rates of antibiotic-resistant strainsof staphylococci were investigated (Table 1).
Most (over 95%) MRSA were resistant toampicillin (ABPC), amoxicillin (AMPC) andpiperacillin (PIPC), and the isolation rates ofstrains resistant to these PCs increased between
1993 and 1997 among total strains of staphylococci. The isolation rates of resistant strains of
MSSA varied from 25% (PIPC and SBTPC) to
60% (AMPC).
Cephalosporin antibiotics, such as cefaclor(CCL), cefazolin (CEZ), cefatrizine (CFT), cefmetazole (CMZ), cefotiam (CTM) and ceftazidime (CAZ), were effective against MSSA,
but more than 90% of MRSA strains were resistant to these cephalosporins, except for CMZ.
Strains resistant to various cephalosporins increased gradually among all staphylococci(data not shown).
MSSA was susceptible to flomoxef (FMOX),
imipenem/cilastatin (IPM/CS), latamoxef(LMOX), but MRSA was less susceptible tothese antibiotics.
Arbekacin (ABK), minocycline (MINO) anddoxycycline (DOXY) were effective against
MRSA. However, macrolides were not effective

Number Rate of resistant strains of:of
MSSA MRSA Total
strains tested (%)
(%)
(%)

ABPC
AMPC
PIPC
SBTPC

903
348
1,062
408

57.3
67.4
24.6
24.5

94.0
96.7
96.8
64.2

72.2
74.7
79.6
43.8

CCL
CEZ
CMZ
CTM
CAZ
SBT/CPZ

804
1,136
1,195
1,194
694
515

16.2
4.9
3.0
3.2
12.3
18.0

96.3
96.0
71.4
93.9
94.9
90.7

52.1
51.4
39.8
54.6
62.2
53.8

FMOX
IPM/CS
LMOX

1,195
1,340
344

5.8
9.2
5.4

64.8
77.7
94.8

30.5
47.5
82.6

ABK
AMK
DKB

381
1,063
381

2.3
10.5
36.1

3.0
38.7
36.9

2.7
26.2
34.9

EM
CLDM
MINO
DOXY

75
428
2,022
386

36.3
30.5
3.2
0.9

92.2
86.2
21.1
24.2

60.9
55.4
11.6
15.3

NFLX
OFLX
LVFX

593
591
805

26.2
19.3
9.3

80.6
56.5
41.4

55.6
33.0
27.2

FOM
1,054
12.3
72.1
45.3
VCM
841
1.2
3.0
2.3
MRSA, methicillin-resistant Staphylococcus
aureus; MSSA, methicillin-sensitive Staphylococcus
aureus.
ABPC, ampicillin; AMPC, amoxicillin; PIPC,
piperacillin; SBTPC, sultamicillin; CCL, cefaclor;
CEZ, cefazolin; CMZ, cefmetazole; CTM, cefotiam;
CAZ, ceftazidime; SBT/CPZ, sulbactam/cefoperazone; FMOX, flomoxef; IPM/CS, imipenem/cilastatin; LMOX, latamoxef; ABK, arbekacin; AMK,
amikacin; DKB, dibekacin; EM, erythromycin;
MINO, minocycline; DOXY, doxycycline; CLDM,
clindamycin; NFLX, norfloxacin; OFLX, ofloxacin;
LVFX, levofloxacin; FOM, fosfomycin; VCM,
vancomycin.

against MRSA, and, for example the isolation
rate of MRSA resistant to erythromycin (EM) is
shown in Table 1. New quinolone antibiotics hadvarious effects on MRSA, and the average rates ofantibiotic resistance to these agents were 40 to
80% throughout this 5 year period.

197

Y. Tanaka et al.

Although MRSA was resistant to fosfomycin (FOM) at a rate of 60% during this 5-year
period, very few strains of vancomycin (VCM)resistant MRSA were observed.

Discussion
Tottori Prefecture is located on Japan’s western
coast along the Sea of Japan, 200 km northwestof Osaka. It is one of the smallest prefectures inJapan, having a population of about 630,000 in
an area of about 3,500 km2. The chief industries are farming and fishery. Tottori Prefectureis thus a relatively isolated and rural district ofJapan. However, this area is widely contaminated with MRSA, or multiply antibiotic-resistant
S. aureus.
Nosocomial infections with MRSA havebeen observed in all parts of the world, especially in the advanced countries. Careful surveillance of MRSA has been performed in large
cities and districts (Aparicio, 1992; Marples andReith, 1992; Mylotte et al., 1992; Heffernan et al.,
1993; Ida et al., 1994; Voss et al., 1994; Zaman
and Dibb, 1994; Riley and Rouse, 1995; Maguire
et al., 1996; Johnson et al., 1997; Schmitz et al.,1997). Schmitz et al. (1997) observed the incidence of MRSA isolates over a period of 3 years
and reported that from a total of 7,814 S. aureus
isolates, 6.3% were methicillin resistant. Furthermore, the highest incidence, 7.8%, wasfound in a 1,500-bed hospital, and the lowest
incidence, 0.5%, was in a smaller 200-bed
hospital. In a general hospital in Jaddah in
Saudi Arabia, the isolation frequency of MRSA
was 7.5% (Zaman and Dibb, 1994). In US hospitals, 66,132 S. aureus isolates were tested andit was found that the percentage of MRSA rosefrom 2.4% in 1975 to 29% in 1991, and that
hospitals with many beds (500 or more beds)
were higher in percent MRSA than hospitals
with few beds (< 200 beds) (Panlilio et al.,1992).
The isolation frequency of MRSA in Japan
increased up to 60% by 1993 (Hashimoto, 1993),
which is a much higher incidence of MRSA
than those in the above-mentioned reports. In
our surveys in Tottori Prefecture, the total isola-tion rate of MRSA increased from 47% in 1993
to 63% in 1997, and was higher in general hospitals than in clinics (Fig. 2). The reasons why
the isolation rates of MRSA in hospitals werehigher than those in clinics were not clear. Generally speaking, when a high dose of antibiotics
was used in hospitals, antibiotic-resistantstrains of microorganisms easily appeared in
the same circumstances. The doctors in many
clinics used the antibiotics for several days only
on the patients, who were suspected of infection
before isolation of microorganisms. The patients attending the clinics may only come incontact with antibiotics for relatively shorttime.
The ratios of MRSA to MSSA in the agegroup under 16 years of age and in the group over
65 years of age were significantly different fromthose in the other age groups (both: P < 0.01).
The isolation frequency of MRSA in the group
under 16 years of age was lower and that in thegroup over 65 years of age was higher thanthose in the other groups (Fig. 3A). These differences are due to the fact that most of the patients over 65 years of age were bedridden patients with compromised conditions who were
hospitalized due to some diseases, whereas manyof the children under 16 years of age were outpatients who visited clinics, and only a few
were admitted to the hospital.
Investigating the clinical specimens for isolation of MRSA, 46% out of 1,449 MRSA strains
were isolated from sputum, and 19% were frompus, although S. aureus strains were observed at
the rate of 34% in sputum and at the rate of 25%
in pus. Ida et al. (1994) also reported that theisolation frequency of MRSA was high in sputum (42.9%) and pus (33.1%). As shown in Fig.
3B, the isolation frequency of MRSA strainsfrom sputum was significantly higher, and thatfrom pus was lower, than that of total S. aureus
strains. Sputum is collected for isolation ofbacterium from aged persons who are often infected by opportunistic pathogens, and sufferfrom chronic pulmonary diseases or general diseases. Pus was examined not only from decubitus, but also from various lesions such as wound
infections, catheter insertions, post-operationand local infections, and MRSA was often iso-198

Epidemiology of MRSA in Tottori Prefecture

lated from the decubitus that occurred in theaged and bedridden persons. However, wounds
were observed in persons of various ages (datanot shown), and this might be one reason why
the isolation rate of MRSA from pus was not ashigh as that from sputum.
S. aureus has been one of the most dangerousorganisms causing nosocomial infections during
past 20 years. Many guidelines have been considered and adopted to protect against nosocomial infections (Crowcroft et al., 1996; Wenzel
et al., 1998). Strategies for the surveillance andcontrol of MRSA include quantitative antibiogram (Marple and Reith, 1992; Panlilio etal., 1992; Voss et al., 1994; Blanc et al., 1995;
Schito et al., 1996), phage-typing and DNArestriction map by pulsed-field gel electrophoresis (Aparicio et al., 1992; Mlynarczyk etal., 1996).
According to the study reported by Ida et al.
(1996), more than 80% of MRSA strains werehighly resistant to methicillin, and were also resistant to macrolide antibiotics and toburamycin. MRSA was also resistant to gentamicin(60%), minocycline (50%) and ofloxacin (70%).
Only a small percentage of strains were resistant to arbekacin, and most of the MRSA tested
were susceptible to vancomycin. Schito et al.
(1996) reported that doxycycline, chloramphenicol, co-trimoxazole, ofloxacin and ciprofloxacin (ratios of resistant strains: < 1%) wereeffective against MRSA. Other authors reported that MRSA was susceptible to vancomycin,
amikacin, bacitracin, chloramphenicol, framycetin, fusidic acid and novobiocin (Riley andRouse, 1995). Our study showed that only
vancomycin and arbekacin were effective
against MRSA, and that minocycline and doxycycline were partially effective against MRSA
(Table 1).
In the course of comparing these data withother reports, especially with reports from foreign countries (Aparicio et al., 1992; Marples
and Reith, 1992; Mylotte et al., 1992; Heffernan
et al., 1993; Voss et al., 1994; Zaman and Dibb,
1994; Riley and Rouse, 1995; Maguire et al.,
1996; Johnson et al., 1997; Schmitz et al., 1997), it
became clear that the isolation rates of MRSA
from patients in hospitals are exceptionallyhigh. Even in a relatively isolated area like
Tottori Prefecture, the increased incidence of
MRSA has occurred. There will be increasing
numbers of victims of MRSA infection, if weleave MRSA as it is. We must grapple with thisdifficult problem.

Acknowledgment: The authors are also grateful to
all the medical doctors in Tottori Prefecture for replying to the questionnaires.
This work was supported by a grant from the
Tottori Prefecture Health Promoting Council.

199

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(Received August 13, Accepted September 6, 1999)

200