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ORIGINAL ARTICLE

Antibiotic-resistant Propionibacterium acnes among acne

patients in a regional skin centre in Hong Kong

N.-M.T. Luk,,**,* M. Hui, H.-C.S. Lee, L.H. Fu, Z.H. Liu, L.Y. Lam, M. Eastel, Y.-K.A. Chan,

L.-S.N. Tang, T.-S. Cheng,** F.-Y.C. Siu,** S.-C. Ng,** Y.-K.D. Lai,** K.-M. Ho**

Dermatology Research Centre, Department of Microbiology, Faculty of Medicine, the Chinese University of Hong Kong,

Hong KongPrivate Dermatologist, Dermatology Clinic, UMP Healthcare group, Hong KongDepartment of Chemical Pathology, Faculty of Medicine, the Chinese University of Hong Kong, Hong Kong

**Department of Health, Centre for Health Protection, Social Hygiene Service, Hong Kong

*Correspondence: N.-M.T. Luk. E-mail: [email protected]

AbstractBackground There has been no study on antibiotic-resistant Propionibacterium acnes in Hong Kong.

Objective We investigated the prevalence and pattern of antibiotic-resistant P. acnes and to identify any

associated factors for harbouring the resistant strains.Methods Culture and sensitivity testing of P. acnes to commonly used antibiotics were performed. Resistance to

tetracycline was defined at a minimal inhibitory concentration (MIC) of 2 lgmL or more; erythromycin at an MIC of

0.5 lgmL or more; clindamycin at an MIC of 0.25 lgmL or more according to EUCAST. For breakpoints of

doxycycline and minocycline, those with an MIC of 1 lgmL or more were defined as resistant strains.

Results Among the 111 specimens collected from 111 patients, 86 strains of P. acnes were recovered, one from

each specimen. Twenty-five specimens had no growth. Forty-seven (54.8%) strains were found to be resistant to

one or more antibiotics. Forty-six (53.5%), 18 (20.9%), 14 (16.3%), 14(16.3%) and 14 (16.3%) strains were resistant

to clindamycin (CL), erythromycin (EM), tetracycline (TET), doxycycline (DOX) and minocycline (MR) respectively. Ten

strains (11.6%) had cross resistance between the MLS antibiotics (erythromycin or clindamycin), one strain (1.2%)

had cross resistance among the cyclines and 14 strains (16.4%) had cross resistance between the MLS and cycline

antibiotics. Binary logistic regression showed an association between MLS antibiotic resistance with an increased

age whereas cycline resistance was associated with the duration of treatment.

Conclusions Antibiotic-resistant P. acnes is prevalent in Hong Kong. Dermatologists should be more vigilant in

prescribing antibiotics for acne patients.

Received: 8 June 2011; Accepted: 31 October 2011

Conflict of interest

None declared.

Funding sources

This work was not supported by any funding. The authors have no relationship with any pharmaceutical companies.

IntroductionProprionibacterium acnes (P. acnes) plays an important role in the

pathogenesis of acne vulgaris.1,2 The exact role of P. acnes in

comedogenesis and causing inflammation is still controversial. As

recently reviewed by Shaheen et al., P. acnes could just be a bystan-

der and not an active participant in the development of inflamed

and non-inflamed acne lesions.3 Antibiotics are frequently used to

treat acne patients either as a bactericidal or anti-inflammatory

agent.4 However, with the increased use of antibiotics, resistant

strains of P. acnes began to emerge in the late 1970s. Since then,

antibiotic-resistant P. acnes has been reported in various parts ofthe world.59 Antibiotic-resistant P. acnes may spread from patients

to close contacts.10 It has also been shown to associate with a poor

treatment outcome.11 Besides, antibiotic-resistant genes passed

from P. acnes to other skin pathogens, e.g. Staphylococcus aureus

and Streptococcus pyogenes, may have public health implications.12

In Hong Kong, treatment of acne patients with topical and sys-

temic antibiotics is a common practice. There has never been a

study on the prevalence and types of antibiotic resistance among

the P. acnes strains found locally. The aim of this study was to

2011 The AuthorsJEADV2013, 27, 3136 Journal of the European Academy of Dermatology and Venereology 2011 European Academy of Dermatology and Venereology

DOI: 10.1111/j.1468-3083.2011.04351.x JEADV

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determine the prevalence and antibiotic-resistant pattern of

P. acnes among acne patients attending a regional skin clinic. We

further attempted to identify any associated factors for the anti-

biotic resistance.

Materials and methods

Subjects

Patients with acne vulgaris attending FLITC (a secondary referral

skin clinic) were invited to participate in the study. Written con-

sent was obtained from the patients after detailed explanation.

Basic clinical information, including age, gender, age of onset and

types of treatment, was obtained at the time of patients entry into

the study or subsequently retrieved from the consultation records.

The study was approved by the ethics committee of The Chinese

University of Hong Kong.

Specimen collection and processingFor each patient, material was sampled from an inflammatory pap-

ule or pustule with a comedo extractor. The material was then col-

lected by cotton-tipped swab and transported immediately in a

pouch containing Amies Medium. For financial reason, only one

specimen was taken from each patient. The specimens were cultured

and subsequent susceptibility tested (detailed below) on the same

day in the microbiology laboratory of the Prince of Wales Hospital.

Culture and antibiotic susceptibility testing

The sample swabs were smeared onto the anaerobic agar (Oxoid)

plates supplemented with vitamin K1 (Sigma-Aldrich, St. Louis,

MO, USA) and incubated anaerobically at 35

C for 7 days beforebeing discarded. Proprionibacterium acnes bacteria were identified

by Gram staining, by their appearance in the culture medium and

by their biochemical characteristics. They appeared as Gram-posi-

tive non-spore-forming anaerobic rods, capable of catalase and

indole production as well as nitrate reduction (rapid ID 32A, bio-

Merieux SA, Marcy IEtoile, France), but unable to hydrolyse escu-

lin. Volatile acetic acid and propionic acid were detected after

anaerobic incubation in peptone-yeast extract-glucose broth for

48 h (Hewlett-Packard 5890 Series II Gas chromatograph, Gen-

Tech Scientific, Arcade, NY, USA). Susceptibility was detected by

the CLSI (Clinical and Laboratory Standards Institute) agar dilu-

tion method to MLS (macrolideslincosamidesstreptogramins)

and cycline antibiotics, namely, clindamycin (CL), erythromycin(EM), tetracycline (TET), doxycycline (DOX) and minocycline

(MR). All antibiotic-containing plates were freshly prepared and

utilized immediately. Resistance to tetracycline was defined at a

minimal inhibitory concentration (MIC) of 2 lgmL or more,

erythromycin at an MIC of 0.5 lgmL or more, clindamycin at an

MIC of 0.25 lgmL or more according to the European Commit-

tee on antimicrobial Susceptibility Testing (EUCAST).13 For doxy-

cycline and minocycline, those with an MIC of 1 lgmL or more

were defined as resistant strains.14

Patients demographics and Antibiotic history

Patients demographics that included age, gender, age of onset,

duration of disease and antibiotic treatment was retrieved for anal-

ysis. For the antibiotic treatment, the kinds and quantities of topi-

cal and oral antibiotics taken over the treatment period (from

initial consultation to the day of enrolment, i.e. previous and cur-

rent treatments) was calculated for further analysis.

Calculation of treatment duration

Patients who had been treated with oral erythromycin and topical

clindamycin simultaneously, the longer duration between the two

was used for analysis e.g. if a patient had been treated with topical

clindamycin for 26 weeks and at the same time oral erythromycin

for 16 weeks, the treatment duration was taken as 26 weeks. For

patients who had taken different cyclines at various stages of treat-

ment, the total treatment period was used for analysis e.g. if a

patients had taken tetracycline for 26 weeks and subsequently

minocycline for 16 weeks, the treatment duration would be 42(26 plus 16) weeks.

Statistical analysis

Chi-squared test was used to determine the association between

antibiotic resistance and individual clinical parameter, namely age,

gender, disease duration, age of onset and duration of antibiotic

treatment. Binary logistic regression model (forward conditional)

was used to identify independent associated factors. A P < 0.05

was considered significant. SPSS version 15, (SPSS Inc., Chicago IL,

USA) was used for all analyses.

Results

Demographics and treatment history

A total of 111 acne patients were recruited for the study between

June and December 2009. There were 40 female patients and 71

male patients. The patients age ranged from 13 to 52 years with a

mean of 21 years. The disease duration varied from 1 to 24 years,

with a mean duration of 6.25 years. The mean age of disease onset

was 14.9 years (1044 years). The number of patients treated with

various antibiotics was: topical clindamycin (n = 57, 66.3%), oral

erythromycin (n = 10, 11.6%), oral doxycycline (n = 33, 38.4%),

oral minocycline (n = 7, 8.1%) or oral tetracycline (n = 5, 5.8%).

Eight patients had not received any antibiotic treatment. The aver-

age cumulative duration of treatment with clindamycin, erythro-mycin, doxycycline, minocycline and tetracycline were 94, 20, 37,

49 and 21 weeks respectively.

Propionibacterium acnes minimal inhibitory

concentration (MIC) and resistance pattern

Among the 111 specimens collected from 111 patients, 86 strains

of P. acnes were recovered, one from each specimen. Twenty-five

specimens had no growth. The MICs of the 86 strains of P. acnes

are shown in Table 1. By applying the EUCAST breakpoints for


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resistance, 47 of the 86 (54.7%) strains were found to be resistant

to at least one antibiotic. Forty-six (53.5%), 18 (20.9%), 14

(16.3%), 14(16.3%) and 14 (16.3%) strains were resistant to clin-

damycin, erythromycin, tetracycline, doxycycline and minocycline

respectively. Twenty-five (29.2%) strains were resistant to more

than one antibiotic. Ten (11.6%) strains had cross resistance

among MLS antibiotics, 14 (16.4%) strains had cross-resistance

among cycline antibiotics and 14 (16.4%) strains had cross resis-

tance between the MLS and cycline antibiotics (Table 2). Of the

eight patients who never had any antibiotic treatment, seven

strains of P. acnes were recovered (one strain from each patient).

Their resistant patterns were: one strain, sensitivity to all MLS and

cycline antibiotics; five strains, resistant to clindamycin only; onestrain, resistant to clindamycin, erythromycin and tetracycline.

Clinical factors associated with P. acnes resistance

With chi-squared test, an increased age was found to be signifi-

cantly associated with MLS resistance (P = 0.001) (Table 3). A

significant association was also found between cycline resistance

and increased age (P = 0.013), a longer duration of disease

(P = 0.008) and a longer duration of antibiotic treatment

(P < 0.001) (Table 3). Binary logistic regression analysis of these

same variables showed that MLS resistance was associated with an

increased age (OR: 1.745, 95% CI: 1.0902.796, P = 0.021),

whereas cycline resistance was only associated with a longer dura-

tion of antibiotic treatment (OR: 3.746, 95% CI: 1.7787.891,

P = 0.001).

Discussion

Resistance of P. acnes to antibiotics was first reported in the Uni-

ted States in 1979.15 Since then, antibiotic-resistant P. acnes has

been reported in other parts of the world,9,10,1618 and a trend

towards increasing antibiotic-resistant was observed in UK.19

Among the reported studies, resistance to erythromycin and

clindamycin were the most common, followed by resistance to

tetracycline antibiotics.

The mechanism underlying erythromycin and clindamycin

resistance was elucidated by Ross et al.,20 who identified four phe-

notypes with cross sensitivity to macrolide, lincosamide and strep-

togramin B (MLS) antibiotics. Genetic mutations occur mainly in

23S rRNA, and strains that possess the erm (X) resistance gene are

highly resistant to MLS antibiotics. On the other hand, tetracycline

resistance is associated with a single G-C transition in the 16 S

rRNA of the small ribosomal subunit.21 There is also an associa-

tion between resistance to tetracycline, doxycycline and minocy-

cline.20

The prevalence of antibiotic-resistant P. acnes varies in different

parts of the world. The prevalent rates are high among European

countries, with erythromycinclindamycin resistance ranges from

45% to 91% and tetracycline resistance from 5% to 26.4% (except

Italy and Hungary which has 0%).22 In Asia, there is a great differ-

ence in the prevalence of antibiotic-resistant P. acnes between

various Asian countries. For example in Japan, the erythromy-cinclindamycin resistant rate is only 4% and tetracyclinedoxycy-

cline resistant rate is 2%.22 In Korea, a recent study only found

one out of 33 strains (3.2%) isolated was resistant to clindamycin

and the authors opined that antibiotic-resistant P. acnes has not

yet developed appreciably in Korea.23 Whereas in Singapore, anti-

biotic-resistant P. acnes is common with erythromycinclindamy-

cin resistant rate of more than 50% and tetracyclinedoxycycline

resistant rate over 11.5%.14 Hong Kong has a high prevalence of

antibiotic-resistant as described above. This could be due to the

Table 1 Minimum inhibitory concentrations (MICs) of various antibiotics for 86 strains of Propionibacterium acnes recovered from

culture

Antibiotic Number of strains inhibited at various MICs (lgmL)

128 MIC50 MIC90

Tetracycline 65 7 3 5 4 2 0.5 4

Doxycycline 1 61 10 4 3 3 2 2 0.25 2

Minocycline 44 18 10 8 1 3 2 0.25 1

Erythromycin 11 56 1 18 0.06 128

Clindamycin 26 14 6 18 3 1 1 1 1 3 12 0.25 128

Table 2 Antibiotic resistance patterns of 47 strains of Propioni-

bacterium acnes

Antibiotic Number Percentage (%)

No resistant 39 45.3

CL 18 20.9

EM 4 4.7EM, CL 10 11.6

MR, CL 1 1.2

TET, DOX, MR 1 1.2

TET, DOX, CL 1 1.2

TET, DOX, MR, CL 4 4.7

TET, DOX, MR, EM, CL 8 9.3

Total 86 100.0

Resistant breakpoints: clindamycin 0.25 lgmL; erythromycin 0.5 lgmL;

tetracycline 2 lgmL; doxycycline and minocycline 1 lgmL.

CL, clindamycin; EM, erythromycin; TET, tetracycline; DOX, doxycycline;

MR, minocycline.


Antibiotic-resistant P. acne in Hong Kong 33

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overuse of antibiotics as first-line treatment in the past 20 yearsfor acne patients. The reason for the difference in prevalence

among various countries is not clear and probably contributed by

the different prescribing habits of the caretakers and different eth-

nicity of the patients. The similar high rates of antibiotic resistance

among predominant Chinese populations in Hong Kong and Sin-

gapore is particularly of note.

The pattern of antibiotic-resistant P. acnes seems to be similar

in various countries with predominant MLS antibiotic resistance

(clindamycin and erythromycin).10,14,18,22,24,25 Hong Kong is of no

exception with a high prevalence (20.953.3%) of MLS antibiotic

resistant whereas a relatively low prevalence of cycline resistance

(16.3%).

There are two possible ways by which patients with acne vulga-ris acquire the resistant strains. Firstly, with the continual use of

antibiotic, resistant strains develop over time; secondly, through

contact with people who harbour the resistant strains.26,27 These

influences are not mutually exclusive although the effect of one

may overshadow the other. Our correlation study suggests that a

prolonged course of cycline antibiotics could be responsible for

the development of cycline resistance P. acnes. Of those who had

taken cycline for more than 104 weeks, seven of 11 (63.6%)

patients harboured the resistant strains. This association, however,

is not observed in patients who harboured MLS antibiotic-resistant P. acnes. Instead, an increased age was found to be an

independent associated factor for this observation. Fifteen of 16

patients (93.8%) aged 25 harboured the resistant strains. We

hypothesize that most of the patients harbouring MLS antibiotic-

resistant P. acnes could have contracted the resistant strains from

their close contacts. The high prevalence of MLS antibiotic resis-

tant strains in our study could support our suspicion as the chance

of contracting the resistant strains in a widespread environment

would readily increase with time i.e. the older you are, the higher

the chance you may contract the resistant strains from your

friends or relatives. Also in agreement with our supposition is the

large proportion (814) of patients younger than 15 years of

age that harboured the resistant strains. Among those eightpatients who harboured the resistant strains, four had no topical

clindamycin or oral erythromycin and there could be no way for

resistance to develop due to drug exposure as in the case of cycline

resistance.

The prevalence of antibiotic-resistant P. acnes strains might not

affect only the clinical outcome of antibiotic treatment; it might

also have implications for other potential systemic infections.

Coagulase-negative staphylococci (CNS), a commensal skin bacte-

rium, have been shown to develop resistance to antibiotics used to

Table 3 Clinical characteristics of patients with and without antibiotic resistance

MLS antibiotics Cycline antibiotics

Resistance No resist ance P-value Resistance No resistance P-value*

Age range (years)

15 8 6 0.001* 0 14 0.013*

1620 14 22 6 30

2125 9 11 2 18

>25 15 1 7 9

Gender

Male 26 24 0.744 11 39 0.189

Female 20 16 4 32

Age at onset (years)

15 22 22 0.507 5 39 0.128

>15 24 18 10 32

Duration of disease (years)

15 23 26 0.127 5 44 0.008*

610 12 11 7 16

1115 6 3 0 9

>15 5 0 3 2

Duration of treatment (weeks)

152 30 28 0.101 8 68 156 10 2 1 0

*Chi-squared test, P < 0.05 is considered as significant.

Erythromycin, clindamycin.

Tetracycline, doxycycline, minocycline.


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treat acne patients. Furthermore, multi-drug resistance, regardless

of the antibiotic used, has also been noted.28 Although CNS is

non-pathogenic in immuno-competent hosts, it is an opportunis-

tic pathogen in those who are immuno-compromised, for exam-

ple, patients undergoing haemodialysis. More pathogenic

organisms such as S. aureus, a major causative agent for skin and

soft tissue infections, may also acquire the resistance via plasmids

and transposons from CNS.29

In the present era of increasing antibiotic-resistance, it is essen-

tial that dermatologists and family physicians treating acne

patients be vigilant in prescribing antibiotics. The Global Alliance

to Improve Outcome in Acne Group recommended the following

strategies to limit the development of resistance in P. acnes which

included: (1) combine a topical retinoid plus an antimicrobial; (2)

limit the use of antibiotics to short periods and discontinue when

there is no further improvement or the improvement is only

slight; (3) co-prescribe a benzoyl peroxide-containing product or

use as washout; (4) oral and topical antibiotics should not be usedas monotherapy; (5) concurrent use of oral and topical antibiotics

should be avoided, particularly if chemically different; (6) do not

switch antibiotics without adequate justification; (7) use topical

retinoids for maintenance therapy, with benzoyl peroxide added

for an antimicrobial effect if needed; and (8) avoid use of antibiot-

ics for maintenance therapy.30 These recommendations should be

closely observed by physicians prescribing antibiotics to acne

patients.

In conclusion, our study showed that antibiotic-resistant

P. acnes is prevalent in Hong Kong and is associated either with

an increased age (MLS antibiotic resistance) or the duration of

antibiotic treatment (cycline resistance). Dermatologists should bemore cautious in prescribing antibiotics to patients with acne.

Acknowledgement

We thank all the nursing staff of FLITC for helping us in this

study.

Author contributions

Nai-Ming T. Luk and Yee-Ki A. Chan were responsible for

writing the study proposal, making the application to the local

ethics committee, drafting the study questionnaire, analysing

the results and writing the manuscript. Mamie Hui, L.H. Fu,

Z.H. Liu, L.Y. Lam, M. Eastel, C.Y. Chan were responsible for

performing the culture and sensitivity tests. Hau-Chi S. Lee

was responsible for inputting data. Leung-Sang N. Tang

advised on the statistical analysis used in the study. Tin-Sik

Cheng, Fung-Yee C. Siu, Shun-Chin Ng, Yik-Kiu D. Lai and

King-Man Ho were responsible for recruiting patients.

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