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Efficacy and safety of indigo naturalis extract in oil (Lindioil) in treating nail psoriasis: a randomized, observer-blind, vehicle-controlled trial.


Treating nail psoriasis is notoriously difficult and lacks standardized therapeutic regimens. Indigo naturalis has been demonstrated to be safe and effective in treating skin psoriasis. This trial was conducted to evaluate the efficacy and safety of refined indigo naturalis extract in oil (Lindioil) in treating nail psoriasis. Thirty-one outpatients with symmetrically comparable psoriatic nails were enrolled. Lindioil (experimental group) or olive oil (control group) was applied topically to the same subjects' two bilaterally symmetrical psoriatic nails twice daily for the first 12 weeks and then subjects applied Lindioil to both hands for 12 additional weeks. Outcomes were measured using Nail Psoriasis Severity Index (NAPSI) for five nails on one hand and for the single most severely affected nail from either hand. The results show a reduction of NAPSI scores for the 12-week treatment for the Lindioil group (49.8% for one hand and 59.3% for single nail) was superior to the reduction in the scores for the control group (22.9%, 16.3%, respectively). There were no adverse events during the 24 weeks of treatment. This trial demonstrates that Lindioil is a novel, safe and effective therapy for treating nail psoriasis.


Traditional Chinese medicine

Indigo naturalis



Nail psoriasis


Nail psoriasis is a notoriously difficult disease to treat and is common among patients with psoriasis, occurring in 50% of patients with the disease (Reich 2009). Psoriasis with nail involvement is a relevant manifestation of psoriasis and the estimated lifetime incidence is 80-90% (Reich 2009). The unsightly appearance of affected nails has a marked impact on the patient's quality of life (de Jong et al. 1996).

To date, there are no standardized therapies for the treatment of nail psoriasis. The most common therapies in treating nail psoriasis are topical steroid, vitamin A (Tazarotene) or vitamin D analog (Calcipotriol). These therapies may have a negative impact on patient's compliance because nail psoriasis requires prolonged treatment and continuity. Occasionally these therapies are associated with side effects, such as skin atrophy and irritation, and/or disappointing results. Therefore, it is necessary to establish safety profiles for treatments intended for long-term use.

Indigo naturalis has been used for centuries in traditional Chinese medicine because of its antipyretic, anti-inflammatory, antiviral, antimicrobial, and detoxifying effects. Indigo naturalis and its active component, indirubin, have been used for decades in China to treat systemic psoriasis and leukemia (Xiao et al. 2002; Koo and Arain 1998).

Previous studies have shown that topical application of indigo naturalis significantly improved skin psoriatic symptoms (Lin et al. 2007; Lin et al. 2008). However, compliance is affected because the ointment is difficult to wash off and causes esthetically unappealing dark blue stains on the applied area.

In 2008, we optimized the formulation for indigo naturalis and named it "Lindioil". Lindioil is a trademark product name created by the author using a proprietary extraction and formulation process which meets consistent commercial pharmaceutical Chemistry, Manufactory and Control (CMC) standards. The extract process for indigo naturalis was changed by the use of olive oil, which would be more acceptable to the patients because it could be easily washed off and would not leave visible stains on the skin or nails (Lin 2011).

To test the formulation change, a clinical trial was performed to compare Lindioil ointment to crude indigo naturalis ointment (Lin et al. 2012a). It was proven that Lindioil was equally effective in treating skin psoriasis. A concurrent non-controlled clinical trial also demonstrated that Lindioil was efficacious and safe in treating nail psoriasis; however, this pilot trial lacked a control arm (Lin et al. 2011). Consequently we conducted a randomized, observer-blind, vehicle-controlled, intra-subject trial to evaluate the efficacy and safety of Lindioil in treating nail psoriasis.

Materials and methods


Subjects with nail psoriasis were recruited from the Department of Traditional Chinese Medicine and Dermatology at the Chang Gung Memorial Hospital (CGMH), Taiwan, from September 2009 to May 2011. Subjects aged 20-65 years with symmetrically comparable psoriatic nails on each hand were eligible. Females of childbearing age were instructed to use birth control measures during the study period. Subjects were excluded if they had a known allergy to indigo naturalis, had any other obvious fingernail infection signs (such as redness, swelling, pus excretion), were pregnant or planning to become pregnant, were breast feeding or were currently using concomitant topical or systemic treatments that could affect nail psoriasis.

This study was approved by the Institutional Review Board of CGMH (approval number 98-2184C) and was registered in (Identifier: NCT00999687, http://register. Written informed consent was obtained from each subject.

Plant material and drug preparation

The powdered form of indigo naturalis used in this study was prepared from the leaves of Baphicacanthus cusia (Nees) Bremek and purchased from Shufeng Shangrchia Indigo Farmer Cooperative, Xianyou county, Fujian province, China. The CMC report was created by Chuang Song Zong Pharmaceutical Co., Ltd. (CSZ), Taiwan. The material was identified and authenticated by Ms. Shu-Tuan Chiang, Research and Quality Control Department Manager of CSZ, with sample vouchers stored for reference under the code number M0813. The fingerprints and quantity analysis of standard samples, indirubin and indigo blue, were established. Pure indigo blue was purchased from Fluka (Buchs, Switzerland), indirubin was obtained from Alexis (Lausen, Switzerland). Indigo naturalis powder used in this trail contained 3.15% indigo blue and 0.15% indirubin as determined by the HPLC.

In this trial, olive oil was added to extract the powdered indigo naturalis from B. cusia (Nees) Bremek. Previous analyses of the leaves and the powdered form of this indigo naturalis plant detected indigo, indirubin, tryptanthrin and isatin (Chiang et al. 2013). According to the Guidance for Industry Botanical Drug Products, the CMC report isolated indirubin and indigo blue only.

Lindioil was prepared by the CSZ using powdered indigo naturalis mixed with olive oil (1:10), Kirkland Signature Pure Olive Oil (Italian, item 71008), then heated at 120[degrees]C for 1 h and filtered by 2-[micro]m filter (Millipore, France). The oil extract was tested using HPLC analysis and placed in 5-ml eye drop bottles for clinical use.

Analysis of indigo naturalis and Lindioil using HPLC

The HPLC analysis was performed on a Waters 2690 Separations Module/Waters 2996 Photodiode Array Detector and detected at [lambda] = 289 nm. The chromatographic separation was carried out on a Cosmosil C18 MS-II column (4.6 mm x 250 mm i.d.; 5 [micro]m particle size) eluted with the mixture of 0.2% phosphoric acid (A) and methanol (B). The linear gradient program was set from 50% of 0.2% phosphoric acid plus 50% of methanol to 30% of 0.2% phosphoric acid plus 70% of methanol for 40 min. The flow rate was 1.0 ml/min. The sample injecting volume for each program was 20 [micro]l.

A standard solution was prepared using indirubin from Sigma. The calibration curve was constructed with dilutions of 2.5, 5, 10, 20 and 40 [micro]g/ml in DMSO. A volume of 20 [micro]l was injected and the calibration curve was based on the peak areas of the HPLC chromatograms. The calibration curve showed an [R.sup.2] = 1.0.

Study design

This study was a randomized, observer-blind, vehicle-controlled, intra-subject trial. Lindioil was applied to the fingernails of one bilateral hand (Lindioil group) and olive oil was applied to the fingernails of the contra-lateral hand (control group) twice daily for 12 weeks. The randomization process was conducted by block randomization method with 1:1 ratio. Beginning with week 13, Lindioil was applied to all affected nails on both hands twice daily for another 12 weeks.

All subjects were instructed to apply one drop (0.05 ml) of Lindioil or olive oil onto the nail plate folds and hyponychium of affected nails twice daily (morning and before bed). Subjects were asked to avoid washing their hands during the first 30 min after application, to avoid activities that might injure the nails and to avoid cross-contamination between the two hands. Subjects were treated for a maximum of 24 weeks unless there was complete clearing of nail psoriasis or they developed obvious local or systemic adverse events (AEs) possibly related to treatment. Subjects who did not comply with the study protocol were terminated from the study. In addition, subjects were allowed to drop out of the study for any reason at any time.

Outcome measures

The primary efficacy measures used were single hand Nail Psoriasis Severity Index (shNAPSI) for all of the nails on one hand and modified target NAPSI (mtNAPSI) for the single most severely affected nail on both hands. Photos of the affected fingernails were taken at baseline and at 4-week intervals for 24 weeks. At each visit, all subjects were requested to clean their fingernails thoroughly so no staining was visible before photographs were taken. Two physicians, who were blinded to the treatment modality, rated the shNAPSI and mtNAPSI based on the photographs of the fingernails. Prior to the study, these two physicians underwent a special training course for the assessment of shNAPSI and mtNAPSI to minimize inter and intra-rater discrepancies.

The NAPSI is a reproducible, objective, and simple tool for clinical assessment of nail psoriasis and is the only clinical scale that has been validated. The nail is divided by imaginary horizontal and longitudinal lines into quadrants. Each nail is given a score for nail bed psoriasis (0-4) and nail matrix psoriasis (0-4) depending on the presence of any of the features of nail psoriasis in that quadrant. The NAPSI evaluates presence of signs in the nail bed (onycholysis, splinter hemorrhages, nail bed discoloration, and subungual hyperkeratosis) and on the nail matrix (pitting, leukonychia, red spots in the lunula and nail plate crumbling) in all 10 fingernails, providing a maximum score of 80 (Rich and Scher 2003). Since this study is an intra-subject hand-to-hand comparison and all 5 fingers on each hand for each treatment method were rated, the range of shNAPSI was between 0 and 40.

Although NAPSI reflects the overall severity of nail psoriasis, it cannot reflect the severity of each nail (Augustin and Ogilvie 2010). Consequently, the mtNAPSI was used to measure the severity of psoriasis in the nail matrix and nail bed for the most severely affected nail. Each nail quadrant was scored from 0 (no sign) to 3 (severe involvement), providing a maximum score of 96 (Parrish et al. 2005).

The subject global assessment (SGA) and physician global assessment (PGA) were performed at week 12 to measure the improvement of nail psoriasis. Each hand was scored separately, taking into consideration the quality and extent of nail disorders relative to the baseline photos. These assessments were based on a 6-point scale: 0 = worse; l=poor (0-24% clearing with little or no change); 2 = fair (25-49% clearing with slight improvement); 3 = good (50-74% clearing with moderate improvement); 4 = excellent (75-99% clearing with striking improvement); 5 = clear (100% clearing). A positive response was defined as attaining a score above 3 (Farhi et al. 2008). Additionally, at week 12 the subjects were questioned as to which treatment method they preferred.

At each visit we assessed the occurrence of AEs such as pain, erythema, irritation or itching that might have been caused by the medication.

Statistical analysis and sample size

Continuous variables such as subject age and duration of psoriasis are expressed as mean [+ or -] SD or as a percentage. Categorical variables, such as gender, are expressed as frequency or as a percentage. "As-treated" analysis was performed using a mixed effect model with two within-factors (group and time) to compare shNAPSI or mtNAPSI. One advantage of the mixed effect model is that there is no deleted missing data because the linear combination of the random-effect parameters is always estimable. shNAPSI or mtNAPSI was compared between the two groups within the same time frame. They were compared with computed generalized least-squares means and the standard errors for the random effects in the mixed effect model, including the Bonferroni adjustment (Brown and Prescott 2006). SGA or PGA was compared using the Wilcoxon signed rank test. SAS 9.3 was used to do the statistical analysis.

The sample size of 30 was calculated based on the following:

(1) mixed effect model with two within-factors (group and time), (2) a 3 unit difference in shNAPSI or mtNAPSI scores between two groups, (3) intra-class correlation of 0.9, (4) significance level of 0.05, and (5) the power of 0.9 (Brown and Prescott 2006).


HPLC-fingerprint analysis of Lindioil

HPLC analysis was performed to identify and confirm the major components of Lindioil. The HPLC-fingerprint of Lindioil revealed that one of the two major components of indigo naturalis, indirubin, could be clearly identified by comparisons with synthetic standard of indirubin for a retention time of 26.68 min. Based on our HPLC quantification, the original concentration of indirubin in the Lindioil extract was determined to be 276.63 [micro]g/g (Fig. 1). Another major component of indigo naturalis, indigo blue, cannot be detected at its expected retention time (19.37 min); therefore, it cannot be quantified by the current HPLC method.

The final concentration of indirubin in the oil extract has been adjusted because each batch of botanical drugs may be slightly different and is not standardized. In this study, the final concentration of indirubin in Lindioil was adjusted to 200 [micro]g/g for use in clinical trials.


A total of 31 subjects out of 35 (88.6%) were eligible for this study. Of the 31 subjects (24 men, 7 women), the mean age was 40.7 [+ or -] 12.6 years. The mean duration of skin and nail psoriasis was 9.4 [+ or -] 6.6 and 5.2 [+ or -] 5.5 years, respectively. The mean Psoriasis Area Severity Index (PAS1) was 9.0 [+ or -]8.6 and the mean NAPSI for two hands was 41.2[+ or -]15.8 (Table 1). Of the 31 subjects, 30 subjects (96.8%) remained in the study at week 12 and 27 subjects (87.1%) remained at week 24 (Fig. 2).


The mixed-effect model revealed that there were significant interactions between groups and time after 12 weeks of treatment in shNAPSI and mtNAPSI (Fig. 3). At baseline there were no significant differences in shNAPSI and mtNAPSI between the Lindioil and the control groups (p = .5909, p = 1.000, respectively). At week 12 the Lindioil group had a significantly lower shNAPSI (10.7 [+ or -]6.2) than the control group (15.5[+ or -]6.2) (pc.0001). Furthermore, the Lindioil group had significantly lower mtNAPSI (5.5 [+ or -] 3.4) than the control group (10.3 [+ or -] 5.0) (p < .0001). Beginning with week 13, the Lindioil treatment was applied to both hands. There were no significant differences in shNAPSI or mtNAPSI at week 20 and 24 between the two groups. Comparative photographs of the clinical effects of Lindioil and olive oil treatment can be seen in Fig. 4.

At week 12, the Lindioil group had better SGA scores than the olive oil group (2.4 [+ or -] 1.1 vs. 1.2 [+ or -] 1.2, p < .001) and had better PGA scores (2.8[+ or -]1.2 vs. 1.2[+ or -] 1.1, p<.001). Positive-response rate was significantly higher in the Lindioil group than in the control group (18 vs. 4 or 60% vs. 13.3%). Of the treatment methods, 22 out of 30 subjects (73.3%) preferred Lindioil, 1 out of 30 (3.3%) preferred olive oil, and 7 out of 30 (23.3%) reported no preference.


There were no AEs or severe AEs noted such as pain, itching, or erythema around the nail folds during the 24 weeks of treatment.


In this study, we found that Lindioil is markedly more effective than olive oil at reducing the severity of nail psoriasis. The improvement in shNAPSI and mtNAPSI for the 12-week treatment in the Lindioil group (49.8%, 59.3%, respectively) was better than that of the control group (22.9%, 16.3%, respectively). The 12-week improvement in the Lindioil group is similar to that obtained in our previous pilot study (Lin et al. 2011). Furthermore, both the SGA and PGA revealed that Lindioil was superior to the olive oil treatment.

As stated previously, the most common topical therapies for nail psoriasis are steroids and vitamin D3 analogs. Rigopoulos et al. reported that a two-compound ointment comprising of calcipotriol and betamethasone dipropionate applied once daily for 12 weeks resulted in a 72% improvement in NAPSI scores (Rigopoulos et al. 2009). Other treatments for nail psoriasis include acitretin and infliximab. Recent studies have shown that low-dose oral acitretin therapy for 24 weeks resulted in a 41% reduction in NAPSI scores and a 50% reduction in mtNAPSI scores. In addition, infliximab injections for 24 weeks led to a mean reduction in NAPSI of 57% (Tosti et al. 2009; Rigopoulos et al. 2008).

In this study we found that a 24-week course of Lindioil resulted in a 61.0% reduction in shNAPSI scores and a 76.6% reduction in mtNAPSI scores (Fig. 3). Based on these results, the efficacy of Lindioil is comparable to that of steroids, vitamin D3 analogs, and other treatments without the associated side effects. More rigorous clinical trials are needed to make further comparisons.

The mechanism of the anti-psoriatic nail effects of indigo naturalis may be due to three factors: (1) regulation of keratinocyte proliferation and differentiation, or (2) restoration of epidermal barrier function, or (3) anti-inflammatory properties. Our previous studies have demonstrated that indigo naturalis can inhibit proliferation and promote differentiation in epidermal keratinocytes (Lin et al. 2009a). Indigo naturalis also up-regulated claudin-1 expression and restored tight junction proteins in keratinocytes, helping to restore the impaired epidermal barrier (Lin et al. 2013). The findings from these two studies indicate that indigo naturalis functions to help repair the nail bed and folds. Furthermore, indigo naturalis has been demonstrated to have anti-inflammatory properties that can inhibit human neutrophil pro-inflammatory responses (Lin et al. 2009b), suppress tumor necrosis factor-a-induced vascular cell adhesion molecule-1 expression in endothelial cells (Chang et al. 2010) and reduce oxidative stress in epidermal keratinocytes (Lin et al. 2012b). These anti-inflammatory effects may help improve the nail matrix signs and symptoms.

In this trial, we added olive oil to extract the powdered indigo naturalis and used olive oil as a control treatment because it can improve nail psoriasis. In addition, olive oil is edible, safe, and has anti-inflammatory and antioxidant effects (Budiyanto et al. 2000). Olive oil is known to be beneficial in the treatment of psoriasis by increasing hydration of the stratum corneum and through the keratolytic effect (Ruiz et al. 2010). Olive oil is currently used in topical applications for the treatment of several skin conditions, including dry skin, itching, and inflammation as well as disorders such as psoriasis and atopic dermatitis. (Al-Waili 2003)

In this study, a slight improvement in the severity of nail psoriasis in the control hands treated with olive oil alone was noted. This observation supports the suggestions in popular media that olive oil is an effective home remedy for some nail disorders.

There are a number of limitations in this study. First, blinding to the subjects is impossible because Lindioil has a slight purple-red color, making it visibly distinct from olive oil for the subjects. Hence, the SGA or preference to Lindioil may have been over-estimated. In contrast, the rating of shNAPSI and mtNAPSI by physicians was not affected because observers were blinded and the photos were rated with no staining left on the nails. Second, the subjects' work style and habits of hand washing could affect the efficacy of the treatment: however, such problems should cancel out since this is an intra-subject trial. Third, compliance (administering the oil every day) could not be guaranteed, but subjects that neglected treatment for more than two days per week were withdrawn from the study. Fourth, the duration of the study was short (24 weeks) relative to the 6-to 12-month growth cycle of nails. Finally, the sample size in this study was relatively small.

As far as we know, indigo naturalis is among one of the first botanical drugs that were used to treat psoriatic nails. According to drug regulatory and standardization methods, the marker used for the 12-month stability testing is indirubin, because it is the major active component of indigo naturalis for the treatment of psoriasis (Lin et al. 2009b, 2013). In previous in vitro and in vivo studies, we also found that indigo blue had no effect in treating psoriasis at all; its darkened blue color only stained patients' skin, nails and clothing (Lin et al. 2009b, 2012a, 2013).

In conclusion, we found that Lindioil was an effective and safe treatment for nail psoriasis and was acceptable to the subjects, indicating that it has great potential to become a safe and effective alternative therapy for treating nail psoriasis.

Abbreviations: AE, adverse event; Cl, confidence interval; NAPSI, Nail Psoriasis Severity Index; mtNAPSl, modified target Nail Psoriasis Severity Index; PASI, psoriasis area and severity index; PGA, physician global assessment; SD, standard deviation; SGA, subject global assessment; shNAPSI, single hand Nail Psoriasis Severity Index.


Article history:

Received 16 October 2013

Received in revised form 20 January 2014

Accepted 24 February 2014


This study was supported by Grant CMRPG280191-2 from Chang Gung Medical Foundation, Chang Gung Memorial Hospital in Keelung, Taiwan. We are indebted to Ms. Shu-Tuan in Chiang Chuang Song Zong Pharmaceutical Co., Ltd., Taiwan for preparing the study medication.


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Yin-Ku Lin (a,b), *, (1), Lai-Chu See (c,1), Yu-Huei Huang (d,e), Ya-Ching Chang (d,e), Teng-Cheng Tsou (a), Tung-Yi Lin (a), Na-Ling Lin (c)

(a) Department of Traditional Chinese Medicine, Chang Gung Memorial Hospital at Keelung, Taiwan

(b) School of Traditional Chinese Medicine, Chang Gung University, Taoyuan, Taiwan

(c) Biostatistics Consultation Center, Department of Public Health, and Biostatistics Core Laboratory, Molecular Medicine Research Center, Chang Gung University, Taoyuan, Taiwan

(d) Department of Dermatology, Chang Gung Memorial Hospital at Taipei, Taiwan

(e) College of Medicine, Chang Gung University, Taoyuan, Taiwan

* Corresponding author. Tel.: +886 2 24313131x2777; fax: +886 2 25462083.

E-mail addresses:, (Y.-K. Lin).

(1) Yin-Ku Lin and Lai-Chu See are co-first authors.

Table 1
Demographic characteristics of 31 patients with nail psoriasis.

Characteristic                   Data                 Range

Gender, male/female              24/7
Age, mean (SD), years            40.7 [+ or -] 12.6   (21-66)
Duration of skin psoriasis,      9.4 [+ or -] 6.6     (1-22)
  mean (SD), years
Duration of nails involvement,   5.2 [+ or -] 5.5     (1-21)
  mean (SD), years
Family history, n (%)            7 (22.6%)
PASI score (0-72), mean (SD)     9.0 [+ or -] 8.6     (0-42.6)
Number of fingernails involved   291
Mean of fingernails involved     9.4 [+ or -] 1.1     (5-10)
  (0-10), mean (SD)
NAPS1 score (0-80), mean (SD)    41.2 [+ or -] 15.8   (13-80)

PASI, Psoriasis Area Severity Index;
NAPSI, Nail Psoriasis Severity Index.
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Author:Lin, Yin-Ku; See, Lai-Chu; Huang, Yu-Huei; Chang, Ya-Ching; Tsou, Teng-Cheng; Lin, Tung-Yi; Lin, Na-
Publication:Phytomedicine: International Journal of Phytotherapy & Phytopharmacology
Article Type:Report
Date:Jun 15, 2014
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