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ARTICLE IN PRESS
doi:
10.4103/ijdvl.IJDVL_148_19
pmid:
31650979
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A short, 8-week course of imiquimod 5% cream versus podophyllotoxin in the treatment of anogenital warts: A retrospective comparative cohort study

1st Department of Dermatology and Venereology, Sexually Transmitted Diseases Unit, School of Medicine, “Andreas Sygros” Hospital for Skin and Venereal Diseases, National and Kapodistrian University of Athens, Athens, Greece
Department of Biostatistics, Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, Germany
Department of Statistics, CBS Laboratory, Athens University of Economics and Business, Athens
School of Medicine, National and Kapodistrian University of Athens, Athens, Greece
Corresponding author: Prof. Electra Nicolaidou, 1st Department of Dermatology, “A. Sygros” Hospital, 5, Dragoumi Street, 115 28 Athens, Greece. electra.nicol@gmail.com
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This is an open-access article distributed under the terms of the Creative Commons Attribution-Non Commercial-Share Alike 4.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under the identical terms.
How to cite this article: Nicolaidou E, Kanelleas A, Nikolakopoulos S, Bezrodnii G, Nearchou E, Gerodimou M, et al. A short, 8-week course of imiquimod 5% cream versus podophyllotoxin in the treatment of anogenital warts: A retrospective comparative cohort study. Indian J Dermatol Venereol Leprol 2020;1-5.

Abstract

Background:

Studies comparing head-to-head treatment modalities for anogenital warts are lacking.

Aim:

We sought to compare a short, 8-week course of imiquimod 5% cream to versus the standard 4 week course of podophyllotoxin in the treatment of anogenital warts and to assess factors that may affect response to treatment.

Methods:

This was a retrospective cohort study. We reviewed medical files of otherwise healthy patients with a first episode of anogenital warts who were treated with either a short, 8-week course of imiquimod or the standard 4-week course of podophyllotoxin. Inverse probability of treatment weighted (IPTW). Logistic regression was employed to evaluate factors that may affect response to therapy.

Results:

The study included 347 patients. In patients with lesions on dry, keratinized anatomical sites, the complete clearance rates were 7.6% for imiquimod and 27.9% for podophyllotoxin (P < 0.001). In patients with lesions on moist, partially keratinized sites, no difference between the treatments was revealed. Significant predictors of > 50% reduction in wart area were location of lesions [odds ratio (OR) (95% confidence interval (CI)): 3.6 (1.84–7.08), P = 0.0002] for “partially keratinized” versus “keratinized” sites and treatment used [OR (95% CI): 1.79 (1.08–2.97), P = 0.024] for podophyllotoxin versus imiquimod.

Limitations:

The retrospective design of the study was a limitation that we mitigated against with the use of IPTW logistic regression.

Conclusion:

A standard 4 week course of Podophyllotoxin was more effective than an 8-week course of imiquimod only for lesions on keratinized sites. Treatment with podophyllotoxin and location of lesions on partially keratinized sites were independent predictors of >50% reduction in wart area.

Keywords

Anogenital warts
comparison
human papillomavirus
imiquimod
podophyllotoxin

Introduction

Anogenital warts rank among the most frequent sexually transmitted infections.1Treatment modalities for the management of anogenital warts are divided into provider-administered (such as cryotherapy) and patient-applied (imiquimod, podophyllotoxin, and sinecatechins).2,3

Imiquimod and podophyllotoxin are the most commonly used patient-applied treatments for anogenital warts. To our knowledge, there are only two studies comparing imiquimod and podophyllotoxin in the treatment of anogenital warts which concluded that both treatments were equally effective.4,5 Reports on the cost-effectiveness of anogenital wart treatments favor podophyllotoxin over imiquimod, because imiquimod is more expensive and the duration of treatment with imiquimod is longer.6,7 On the other hand, because imiquimod enhances the immune responses against human papillomavirus, recurrence rates following treatment with imiquimod are lower, compared with podophyllotoxin.7 Thus, the choice between the two agents is not clear cut.

Imiquimod can be used for up to 16 weeks.2,3 Shorter courses (4-week, 8-week, and 12-week) have been evaluated and produced results comparable to the 16-week course.8,9

In this study, we compared response rates between a short, 8-week course of imiquimod 5% cream and podophyllotoxin in patients with anogenital warts. Apart from general response rates, we also assessed factors that may affect response to treatment. We decided to evaluate an 8-week course of imiquimod instead of the licensed 16-week course, because we need more data on this more practical and less expensive imiquimod regime.

Methods

In this retrospective cohort study, we reviewed the database of all patients with anogenital warts who presented to the sexually transmitted infections unit of “Andreas Sygros” hospital for skin and venereal diseases, between January 2012 and December 2016. The study was approved by the institutional review board.

The inclusion criteria were the following: (a) otherwise healthy males and females age 18 years and older with a clinically diagnosed first episode of anogenital warts lasting no more than 3 months and (b) monotherapy with either an 8-week course of imiquimod 5% cream or a 4-week course of podophyllotoxin. Exclusion criteria included (a) receiving any treatment for anogenital warts before presentation to our department, (b) presence of either intra-anal/intravaginal warts or warts of the urethral meatus, (c) presence of giant condylomata (Buschke–Lowenstein tumors), (d) presence of only one wart or wart area larger than 6 cm2, and (e) pregnancy.

Anatomical sites of anogenital warts were divided into two groups. The first group included sites covered by dry, keratinized skin, such as pubic area, penile shaft, scrotum, groin, and the outer surface of labia majora of the vulva (“keratinized” sites). The second group included sites covered by moist, partially keratinized skin, such as perianal area, perineum, preputial cavity, inner surface of labia majora, and labia minora of the vulva (“partially keratinized” sites). Disease extent was defined as small, if the number of lesions was between 2 and 4 or affected area was <1 cm2; medium, if lesions were between 5 and 10 or area between 1 and 4 cm2, and large, if lesions were more than 10 or area affected was 4–6 cm2.

Imiquimod was applied three times weekly. Podophyllotoxin was applied each week twice daily for 3 consecutive days, followed by 4 days of rest. Podophyllotoxin 0.5% solution was prescribed for lesions on “keratinized” sites and podophyllotoxin 0.15% cream was prescribed for lesions on “partially keratinized” sites, in agreement with the recent European guidelines.2

For the comparison of the response rates between the different treatment groups, Chi-square test was used. We also performed a stratified analysis using Chi-square test for the comparison of response rates among the categories of location (“keratinized” sites vs. “partially keratinized” sites). For the comparison of medians between independent groups of patients, we used Mann–Whitney U-test.

Estimated odds ratios (OR) and 95% confidence intervals (CIs) were determined using a logistic regression model. To account for the observational nature of the study and possible confounding, inverse probability of treatment weighted logistic regression was also applied, with weights stabilized by the marginal probabilities of receiving each treatment. Analyses were conducted in R, version 3.5.1, and IPT weights were estimated using package “ipw.”

Results

In total, 347 patients were included in the study. Demographic and baseline characteristics of the treatment groups are shown in Table 1.

Table 1:: Overview of demographic and baseline characteristics of the two groups
Treatment Imiquimod (n=202), n (%) Podophyllotoxin (n=145), n (%) P
Gender
Men 148 (73.3) 129 (89.0) <0.001*
Women 54 (26.7) 16 (11.0)
Age (median) 34 33 0.509
Location of AGW
“Keratinized” sites 92 (45.5) 104 (71.7) <0.0001*
“Partially keratinized” sites 76 (37.6) 23 (15.9)
Both 34 (16.8) 18 (12.4)
Extent of AGW
Small 62 (30.7) 56 (38.6) 0.282
Medium 70 (34.7) 47 (32.4)
Large 70 (34.7) 42 (29.0)

AGW: anogenital wart. “Keratinized” sites: pubic area, penile shaft, scrotum, groin, and outer surface of labia majora of the vulva. “Partially keratinized” sites: perianal area, perineum, preputial cavity, inner surface of labia majora, and labia minora of the vulva. *Statistically significant

Complete clearance rates and more than 50% reduction in wart area for the groups as a whole and separately for lesions on “keratinized” and “partially keratinized” sites are shown in Tables 2 and 3. For lesions on “keratinized” sites, the difference between imiquimod and podophyllotoxin both in clearance rates (7.6% and 27.9%, respectively) and in >50% reduction in wart area (54.3% and 76.0%, respectively) was statistically significant.

Table 2:: Complete clearance rates of anogenital wart for both groups
Patients Imiquimod, n/ntreated (%) Podophyllotoxin, n/ntreated (%) P
All 51/202 (25.2) 46/145 (31.7) 0.185
With lesions on “keratinized” sites 7/92 (7.6) 29/104 (27.9) <0.001*
With lesions on “partially keratinized” sites 38/76 (50.0) 12/23 (52.2) 0.855
Both 6/34 (17.6) 5/18 (27.8) 0.621

AGW: anogenital wart. Keratinized” sites: pubic area, penile shaft, scrotum, groin, outer surface of labia majora of the vulva. “Partially keratinized” sites: perianal area, perineum, preputial cavity, inner surface of labia majora, labia minora of the vulva. *Statistically significant

Table 3:: >50% reduction in wart area for both groups
>50% reduction in wart area
Patients Imiquimod, n/ntreated (%) Podophyllotoxin, n/ntreated (%) P
All 142/202 (70.3) 111/145 (76.6) 0.196
With lesions on “keratinized” sites 50/92 (54.3) 79/104 (76.0) 0.001*
With lesions on “partially keratinized” sites 66/76 (86.8) 20/23 (87.0) 0.989
Both 26/34 (76.5) 12/18 (66.7) 0.667

“Keratinized” sites: pubic area, penile shaft, scrotum, groin, outer surface of labia majora of the vulva. “Partially keratinized” sites: perianal area, perineum, preputial cavity, inner surface of labia majora, labia minora of the vulva. *Statistically significant

The results of the univariate logistic regression for patients with >50% reduction in wart area versus <50% reduction in wart area are presented in Table 4.

Table 4:: Univariate logistic regression model for >50% reduction in wart area
OR (95% CI) P
Treatment
Podophyllotoxin vs. Imiquimod 1.38 (0.85-2.25) 0.197
Gender
Women vs. men 2.03 (1.04-3.98) 0.0389*
Location of AGW
“Partially keratinized” vs. “keratinized” sites 3.44 (1.79-6.61) 0.0002*
“Both” vs. “keratinized” sites 1.41 (0.71-2.78) 0.32
Extent of AGW
Medium vs. small 0.95 (0.53-1.69) 0.851
Large vs. small 0.82 (0.46-1.46) 0.493
Age 0.98 (0.95-1.006) 0.12

OR: odds ratio, CI: confidence interval, AGW: anogenital wart. “Keratinized” sites: pubic area, penile shaft, scrotum, groin, outer surface of labia majora of the vulva. “Partially keratinized” sites: perianal area, perineum, preputial cavity, inner surface of labia majora, labia minora of the vulva. *Statistically significant

Multivariate analysis revealed that only type of treatment and location of lesions were independent predictors of response to treatment [Table 5]. More specifically, treatment with podophyllotoxin [OR (95% CI): 1.9 (1.11–3.23), P = 0.018] and location on “partially keratinized” sites [OR (95% CI): 3.75 (1.88–7.49), P = 0.0001] were statistically significantly associated with > 50% reduction in wart area.

Table 5:: Multivariate logistic regression model for >50% reduction in wart area, with and without inverse probability of treatment weighted
OR (95% CI) P OR (95% CI) IPTW P (IPTW)
Treatment
Podophyllotoxin vs. imiquimod 1.9 (1.11-3.23) 0.018* 1.79 (1.08-2.97) 0.024*
Gender
Women vs. men 1.74 (0.83-3.66) 0.14 1.87 (0.89-3.92) 0.10
Location of AGW
“Partially keratinized” vs. “keratinized” sites 3.75 (1.88-7.49) 0.0001* 3.6 (1.84-7.08 0.0002*
“Both” vs. “keratinized” sites 1.26 (0.6-2.63) 0.54 1.15 (0.55-2.39) 0.72
Extent of AGW
Medium vs. small 1.03 (0.56-1.89) 0.93 0.98 (0.54-1.78) 0.95
Large vs. small 0.95 (0.51-1.76) 0.87 0.93 (0.51-1.69) 0.80
Age 0.98 (0.96-1.01) 0.15 0.99 (0.97-1.01) 0.39

OR: odds ratio, CI: confidence interval, AGW: anogenital wart, IPT: inverse probability of treatment, IPTW: inverse probability of treatment weighted. IPT weights were calculated using marginal treatment probability as stabilizing factors and age, gender, extent of AGW, and location of AGW as probability of treatmentfactors. “Keratinized” sites: pubic area, penile shaft, scrotum, groin, outer surface of labia majora of the vulva. “Partially keratinized” sites: perianal area, perineum, preputial cavity, inner surface of labia majora, labia minora of the vulva. *Statistically significant

Due to the observational nature of the study and nonrandom assignment of treatments, an inverse probability of treatment weighted logistic regression model was estimated. Stabilized inverse probability of treatment weights were calculated with marginal treatment probabilities as stabilizing factors and age, gender, extent of lesions, and location of lesions as probability of treatment factors. inverse probability of treatment weighted diagnostics demonstrated that weighting resulted in a balanced sample between treatment groups in important predictors for treatment and response [Table 6]. The inverse probability of treatment weighted model estimated a slightly smaller treatment effect of podophyllotoxin [OR (95% CI): 1.79 (1.08–2.97), P = 0.024], while the rest of the variables were found to have similar effects compared with the unweighted analysis [Table 5].

Table 6:: Chi-square statistics for the association between treatment received and patients’ gender as well as location of anogenital wart in the unweighted sample and after weighting by inverse probability of treatment weighted
Variable Chi-square statistic (df) unweighted sample Chi-square statistic (df) IPT weighted sample P(unweighted sample) P(IPT weighted sample)
Gender 12.5 (2) 0.08 (2) 0.0001* 0.78
Location of AGW 25.3 (2) 0.1 (2) <0.0001* 0.95

AGW: anogenital wart, IPT: inverse probability of treatment. Marginal probabilities of treatment were used as stabilizing factors and gender, location of AGW, extent of AGW, and age as IPT factors. Results are presented for gender and location of AGW, which were unbalanced in the unweighted sample. *Statistically significant

Discussion

In everyday clinical practice, imiquimod and podophyllotoxin are often considered first-line treatments for anogenital warts. Imiquimod is shown to have a clearance rate ranging widely between 35% and 75% for treatment periods up to 16 weeks.5,8-14 In our study, the imiquimod clearance rate after 8 weeks of treatment was 25.2%. However, the clearance rate was 50%, for lesions on “partially keratinized” sites, and 7.6%, for lesions on “keratinized” sites. So, if imiquimod is prescribed for patients with warts on “partially keratinized” sites, our study showed that even an 8-week course can lead to a clearance rate comparable to the clearance rates mentioned in the literature for treatment up to 16 weeks.

Podophyllotoxin 0.5% solution has been shown to have a clearance rate between 54% and 85% after use for 4 weeks.5,15-18 For podophyllotoxin 0.15% cream, clearance rates of 63%19 and 75%18 have been reported. In this study, the clearance rate was 27.9% for podophyllotoxin solution (for lesions on “keratinized” sites) and 52.2% for podophyllotoxin cream (for lesions on “partially keratinized” sites). The low clearance rate that we observed for podophyllotoxin 0.5% solution can be attributed to the fact that we used it only for lesions on “keratinized” sites, which, according to the results of our study, are more resistant to treatment.

Previous studies comparingimiquimodand podophyllotoxin in the treatment of anogenital wartsinclude a meta-analysis4 (that evaluated three placebo-controlled trials of imiquimod and nine placebo-controlled trials of podophyllotoxin) and a head-to-head comparison in a randomized, open-label trial that included 45 patients.5 Both studies concluded that imiquimod and podophyllotoxin were equally effective. In this study, we compared podophyllotoxin with a shorter, 8-week imiquimod course. For lesions on “keratinized” skin, the difference between imiquimod and podophyllotoxin both in clearance rates and in >50% reduction in wart area was statistically significant. For lesions on “partially keratinized” skin, no difference was detected between the two treatments.

In univariate analysis, lesions on “partially keratinized” sites and female patients were statistically significantly associated with a >50% reduction in wart area. In the multivariate analysis, however, gender of patients was no longer associated with response to treatment and only location of lesions on “partially keratinized” sites and treatment with podophyllotoxin were independent predicting factors of >50% reduction in wart area. These findings reflect the fact that patients with lesions on “keratinized” sites, that is, with “difficult-to-treat” lesions, were mostly men and had been treated more frequently with podophyllotoxin, compared with imiquimod. Men more often have lesions on “keratinized” sites, such as the penile shaft and the pubic area, while women usually have lesions on “partially keratinized” sites, such as the perineum, inner surface of labia majora, and labia minora of the vulva. In the multivariate model that took into account the location of lesions, gender was no longer a predictor of response to treatment and, on the contrary, type of treatment was. So, our study showed that location of lesions and not patients’ gender predicts response to treatment.

The main limitation of our study is its retrospective design. We mitigated this shortcoming by basing the main results of our study on an inverse probability of treatment weighted analysis, creating a sample in which treatment assignment was independent of (measured) baseline covariates.

Conclusion

Our study showed that lesions’ location plays a central role on response to patient-applied treatments for anogenital warts. For lesions on “partially keratinized” sites, an 8-week course of imiquimod was equally effective to the standard 4-week course of podophyllotoxin. For lesions on “keratinized” sites, the 8-week course of imiquimod was less effective, compared with podophyllotoxin, so either podophyllotoxin or the standard “up to 16 weeks” imiquimod regime should be preferred. Lesions on “partially keratinized” sites responded more favorably to both treatments.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patients have given their consent for their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

EN has received honoraria from Meda Pharmaceuticals and Glaxosmithkline. AK and GB have received honoraria from Meda Pharmaceuticals.

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