Comparison Between Brazilian Propolis and Chinese Propolis: Results From the North American Contact Dermatitis Group 2019

Abstract

Abstract: Background: Prevalence of positive patch test (ppt) reactions to propolis in Europe has varied with different allergen source origins. Compared with previous cycles, the North American Contact Dermatitis Group (NACDG) noted a marked increase in propolis positivity in 2019–2020.

Objective: To compare propolis positivity in North American centers between 3 periods (2019, 2020, and 2021/2022), based on geographic origin and supplier.

Methods: Retrospective analysis of NACDG patch test data (2019–2022) utilizing 3 different sources of propolis: Chinese propolis (Allergeaze—CPA), Chinese propolis (Chemotechnique—CPC), and Brazilian propolis (Allergeaze—BPA).

Results: Proportions of ppt reactions to propolis were: 3.7% (84/2260) to CPA in 2019, 14.7% (271/1838) to BPA in 2020, and 2.2% (66/3052) to CPC in 2021/2022. There was a statistically significant difference in prevalence of reactions for BPA compared with both CPA and CPC (P < 0.00001).

Conclusions: When unexpected changes are noted in patch test positivity, especially with naturally derived allergens, the reasons behind those changes should be investigated. The substitution of Brazilian for Chinese propolis resulted in a significant increase in ppt reactions.

Capsule Summary

A marked increase in propolis patch test positivity was noted by the NACDG in 2019-2020.

It was determined that the substitution by the manufacturer in 2020 of Brazilian propolis for Chinese propolis resulted in a significantly higher propolis positivity.

INTRODUCTION

Propolis is a natural resinous substance produced by bees to build and modify their hives. As bees utilize material extracted from trees and other plants to make propolis, specific components vary according to climate and geography.¹ Propolis was used as a medicinal preparation for centuries and more recently has been incorporated into dietary supplements, topical therapy for various dermatologic conditions and cosmetic preparations. Over time, it was recognized as a possible contact allergen¹ and is included in screening patch test series in North America and Europe.^2-4 Prior to 2021, most studies found positive patch test prevalence for propolis of ≤3.9% (Table 1).^{4B5 -7}

Table 1.

European Studies Reporting Patch Test Results to Propolis (10% Petrolatum) in Consecutive Patients

First Author, Location	Years Tested	Propolis Source/Supplier	No. +/ No. Tested %	Percent Positive
Chinese propolis
Schubert⁵: Germany, Austria, Switzerland	2013–2019	CPA	2598/66,104	3.9%Range: 3.5–4.7%
Nyman⁶: Lithuania, Spain, Sweden	2017–2019	CPCCPACPC	13/5485/47426/722	2.4%1.1%3.6%
Uter⁴: 13 European countries	2019–2020	CPA^a	416/11,952	3.5%
Antelmi¹⁴: Sweden	2023	CPC	3/329	0.9%
Brazilian propolis
Piontek⁹: Switzerland	2021–2022	BPA	303/1290	23.5%
Both
Kocabas⁷: Netherlands	20192020202120222023	NR^aCPACPALikely CPA/BPABPA	Total: 299/3134No. tested/year: NR	9.5%3.4%2.8%6.1%16.1%16.4%

Propolis supplier not reported, personal communication Anton de Groot.

NR, not reported; CPA, Chinese propolis (Allergeaze); CPC, Chinese propolis (Chemotechnique); BPA, Brazilian propolis (Allergeaze).

The North American Contact Dermatitis Group (NACDG) publishes patch test data and analysis from its screening series every 2 years. Propolis (10.0% petrolatum) is routinely tested in the screening series. In the 2019/2020 period, propolis had a significant increase in positivity and moved up to the 7^th most frequent positive allergen, with a prevalence of 8.6%. There was a statistically significant increase both for 2019/2020 versus 2017/2018 (4.7% propolis positivity P < 0.001) and versus 2009–2018 (1.7–4.7%, P < 0.001) NACDG testing periods.³

The patch test preparation was provided by the same allergen supplier throughout the 2-year period of 2019/2020. However, due to supply chain shortages, the manufacturer informed NACDG members in November 2019 of the need to switch the source for propolis for 2020. Analysis of NACDG data from 2021/2022, using propolis from a different manufacturer, noted that propolis positivity had declined in a statistically significant manner back to a more expected prevalence of 2.2%.⁸ Two previous studies had found significant changes in propolis positivity by source (Brazilian rather than Chinese propolis); the percentage of reactions to Brazilian propolis ranged from 16.1% to 23.5% (Table 1).^7,9

The objective of this study was to compare the prevalence of positive reactions with propolis during 3 timeframes: 2019, 2020, and 2021/2022, when the propolis tested differed by supplier and/or geographic source.

METHODS

NACDG Database

NACDG members regularly contribute patch test data from patch test centres in the United States and Canada for pooled analysis. Institutional Review Board approval for data collection is obtained by each member, specific to their organization.

Consecutive patients who were referred with possible allergic contact dermatoses were patch tested with the NACDG screening series of 80 allergens, including propolis. The study population included all patients tested to propolis (10.0% pet) between 2019 and 2022. Previous NACDG reports described data collection methods in detail.^8,10,11 Patch testing was performed with a standardized technique using Finn chambers® (SmartPractice Phoenix, USA) on Scanpor® tape (Norgesplaster Alpharma AS Vennesla, Norway). For patients <18 years of age, IQ chambers (Chemotechnique® Vellinge, Sweden/Dormer Laboratories Inc., Toronto, Canada) could be used at the tester’s discretion.

All patients had patch test readings at 48 hours and at 72–168 hours (most commonly 96 or 168 hours) after patch placement. Reaction strength was graded (+++, ++, +, +/−, irritant, negative). A final interpretation was coded as “allergic” or “not allergic” based on clinical factors and reactions to other allergens. For each reaction with a final interpretation of “allergic,” clinical relevance, and the most likely source of exposure were recorded. Clinical relevance was coded as “definite,” “probable,” “possible,” “past,” or “unknown.”

Deidentified patient characteristics recorded included age, sex, race/ethnicity, and the presence or absence of personal atopy (hay fever/allergic rhinitis, asthma, atopic eczema). Based on the history, physical examination, and patch testing results, the investigator recorded up to 3 final diagnoses.

Allergen Supplier/Geographic Origin

AllergEAZE® SmartPractice® Calgary, Canada supplied Chinese propolis in 2019 and Brazilian propolis in 2020. For the period 2021/2022, Chinese propolis was supplied by Chemotechnique® Vellinge, Sweden/Dormer Laboratories Inc., Toronto, Canada.

Data Analysis

All data were manually entered at a centralized location. Demographic data were organized according to MOAHLFA guidelines (male, occupational, atopic, hand, leg, face, and age >40 years).^12,13 Reaction strength, clinical relevance, and exposure sources were presented using descriptive analyses.

Patients were separated into 3 study groups based on the source of propolis: (Chinese Allergeaze 2019—CPA, Brazilian Allergeaze 2020—BPA, Chinese Chemotechnique 2021/2022—CPC) and final interpretation: propolis allergic and not allergic. Demographics were compared between the 3 study groups. For every propolis positive patient in each study group, co-reactions to 7 fragrance-related test preparations on the NACDG screening series [fragrance mixes I and II, Myroxylon pereirae resin (M. pereirae), hydroperoxides of linalool, hydroperoxides of limonene, ylang-ylang oil, colophony] were examined. Counts were calculated with Excel (2025; Microsoft Corporation, Redmond, WA). Categorical data were analyzed with Pearson χ-squared test. A P value of <0.05 was considered statistically significant. The Bonferroni correction was used for multiple comparisons of secondary analyses (fragrance co-reactivity).

RESULTS

Patient Characteristics

In the 3 study cohorts (CPA N = 2260, BPA N = 1838, and CPC N = 3052), the majority of patients were white (73.7–80.8%) as well as female (73.5–74.1%). The mean age ranged from 44.5 to 46.8 years. Approximately one third (29.5–34.8%) had a history of atopic dermatitis (AD). There were no statistically significant differences in patient characteristics (sex, history of AD, or primary site of dermatitis) between the 3 groups. With respect to propolis allergic patients, there were no statistically significant differences in patient characteristics (sex, race/ethnicity, AD) between the 3 groups (data not shown).

Allergen Frequencies/Proportions

Positive patch test reactions to propolis by supplier and geographic origin were:

CPA 3.7% (84/2260); BPA 14.7% (271/1838); and CPC 2.2% (66/3052) (Table 2). There was a statistically significant difference in prevalence of positive patch test reactions between CPA and BPA as well as between BPA and CPC (P < 0.00001 for both comparisons).

Table 2.

Strength of Propolis Reactions and Clinical Relevance by Type of Propolis/Year

Year/Cycle	Total N Tested	Propolis Positive/Allergic	Percent Positive	Final Reading n (%)	Clinical Relevance n (%)
3+	2+	1+	+/−	Definite	Probable	Possible	Past	Unknown
Chinese Propolis (Allergeaze) 2019	2260	84	3.7%	4 (4.8%)	15 (17.9%)	46 (54.8%)	19^a (22.6%) [37]^b	3 (3.6%)	19 (22.6%)	36 (42.9%)	3 (3.6%)	24 (28.6%)
Brazilian Propolis (Allergeaze) 2020	1839	271	14.7%	24 (8.9%)	51 (18.8%)	168 (62.0%)	28^a (10.3%) [65]^b	3 (1.1%)	42 (15.5%)	120 (44.3%)	24 (8.9%)	82 (30.3%)
Chinese Propolis (chemo-technique) 2021/2022	3050	66	2.2%	3 (4.5%)	11 (16.7%)	45 (68.2%)	7^a (10.6%) [23]^b	4 (6.1%)	8 (12.1%)	32 (48.5%)	5 (7.6%)	19 (28.8%)

doubtful reactions that were determined to have an allergic/positive interpretation.

total doubtful reactions.

Reaction Strength and Clinical Relevance

BPA elicited strong/extreme reactions (++ or +++) in 27.7% of propolis positive patients, whereas CPA and CPC elicited these reactions in 22.7% and 21.2%, respectively. Reaction strength did not show a statistically significant difference.

Positive reactions were deemed to be currently relevant (definite, probable, and possible) in 69.0% (58/84) of patients tested to CPA, 66.7% (44/66) to CPC and 60.9% (165/271) to BPA (Table 2). Unknown and possible clinical relevance made up the great majority of cases. When more stringent clinical relevance criteria were applied (definite and probable), relevance was found in 26.2% of CPA, 18.2% of CPC and 16.6% of BPA (Table 2). In all years, 1+ (weak) reactions were associated with most of the unknown and possible clinical relevance (data not shown).

All 3 study cohorts had the same top 2 primary sources for current relevance: cosmetic/beauty preps and lipsticks/lip balms.

Co-Reactions to Fragrance Allergens/Markers in Propolis-Positive Patients

The co-reactivity patterns of BPA, CPA, and CPC were examined. For BPA, there was a statistically significant association between propolis-positive patients versus propolis-negative patients to fragrance mix 1 (FM I), fragrance mix II (FM II), M. pereirae, hydroperoxides of limonene, ylang-ylang and colophony. The association was even stronger between CPA and fragrance mixes I and II, M. pereirae, hydroperoxides of limonene, hydroperoxides of linalool, ylang-ylang oil, and colophony (P < 0.0001 for all) (Table 3). CPC showed similar statistical significance for co-reactions with FM I, FM II, M. pereirae, hydroperoxides of limonene, hydroperoxides of linalool, ylang-ylang oil and colophony. As an example, 12.9% of BPA positives had co-reactions to M. pereirae as compared with 6.0% in the BPA negative group, whereas CPA and CPC had much higher co-reactivity with M. pereirae (CPA 32.1% vs 6.9%; CPC 33.3% vs 6.4%).

Table 3.

Co-Reactivity of CPA, BPA, and CPC With Fragrance Allergens/Markers

	2019 (Tested: CPA)	2020 (Tested: BPA)	2021–2022 (Tested: CPC)
	Propolis-AllergicN = 84n (%)	Propolis Non-allergicN = 2176n (%)	P Value	Propolis-AllergicN = 271n (%)	Propolis Non-allergicN = 1568n (%)	P Value	Propolis-AllergicN=66n (%)	Propolis Non-allergicN = 2984n (%)	P Value
M. pereirae resin 25% pet	27 (32.1%)	148 (6.8%)	^*	35 (12.9%)	94 (6.0%)	^*	22 (33.3%)	192 (6.4%)	^*
Fragrance Mix I 8% pet	39 (46.4%)	274 (12.6%)	^*	45 (16.6%)	166 (10.6%)	0.004	19 (28.8%)	223 (7.5%)	^*
Fragrance Mix II 14% pet	13 (15.5%)	114 (5.2%)	^*	20 (7.4%)	60 (3.8%)	0.008	6 (9.1%)	85 (2.8%)	0.003
Hydroperoxides of Limonene 0.3% pet	12 (14.3%)	58 (2.7%)	^*	23 (8.5%)	48 (3.1%)	^*	14 (21.2%)	158 (5.3%)	^*
Hydroperoxides of Linalool 1% pet	25 (29.8%)	224 (10.3%)	^*	32 (11.8%)	167 (10.7%)	0.571	19 (28.8%)	288 (9.7%)	^*
Ylang-ylang oil 2% pet	11 (13.1%)	37 (1.7%)	^*	7 (2.6%)	15 (1.0%)	0.023	3 (4.5%)	44 (1.5%)	0.045
Colophonium 20% pet	17 (20.2%)	55 (2.5%)	^*	14 (5.2%)	39 (2.5%)	0.015	13 (19.7%)	64 (2.1%)	^*

P < 0.0001.

BPA, Brazilian Propolis (Allergeaze); CPA, Chinese Propolis (Allergeaze); CPC, Chinese Propolis (Chemotechnique).

DISCUSSION

Our multicentre retrospective analysis of Chinese versus Brazilian propolis represents the first study to address this subject in a North American setting, comprising the largest comparative patch test cohorts to date (>1500 patients per year). The substantially higher propolis positivity in the BPA cohort as compared with the CPA and CPC cohorts accounts for the unexpectedly high total propolis positivity of 8.6% that was reported in the NACDG 2019 to –2020 patch test results.³

NACDG reports patch test results every 2 years. A granular breakdown of our data by individual test year showed that in 2019, when CPA was tested, 3.7% of patients were positive to propolis, whereas in 2020, when BPA was used, 14.7% were positive. For comparison, the CPC that was tested in 2021 and 2022, yielded 2.2% positivity, a statistically significant decrease from 2019–20 overall. The backstory of the switch from Chinese to Brazilian propolis due to supply chain issues between 2019 and 2020 explains the underlying reason for this result.

For each type of propolis, currently relevant reactions were ascribed to the same top 2 primary sources: cosmetics/beauty preps and lipsticks/lip balms sources.

Prevalence of Positive Reactions to Propolis by Source

Here we found positive prevalence of 3.7% in 2019 (when CPA was tested), 14.7% in 2020 (when BPA was tested), and 2.2% in 2021/2022 (when CPC was tested). These figures are consistent with other studies of <3.9%^{4B5 -7} for CPA, 16.1–23.5%^7,9 for BPA, and 0.9% for CPC¹⁴ (Table 1). Several studies have shown higher positivity to Brazilian propolis than Chinese propolis. Including our study, Chinese propolis (CPA and CPP) has yielded positive reactions in 0.4–3.9%.^4-6,14 In contrast, BPA has shown a much higher proportion of positive reactions ranging from 5.1% to 23.5% in Europe and 14.8% in North America (this study).^7,9,14,15

Studies of Concomitant Testing of Brazilian and Chinese Propolis

A literature search found 3 European studies of small patient cohorts simultaneously tested with both Brazilian and Chinese propolis (Table 4),^9,14,15 These studies showed major differences in positivity between patients patch tested with Brazilian propolis versus Chinese propolis.^9,14,15 Positivity to BPA was 5.1% (13/257),¹⁴ 6.3% (9/143),⁹ and 23.8% (57/239)¹⁵ whereas results to Chinese propolis were much lower with 2.5% (6/239 CPC),¹⁵ 1.3% (3/239 CPA),¹⁵ 0.4% (1/257 CPC),¹⁴ and 0% (0/143 CPC).⁹

Table 4.

Studies of Concomitant Patch Testing to Chinese and Brazilian Propolis (10% Petrolatum)

First Author, Location	No. Tested	% BPA + (n)	% CPA + (n)	% CPC + (n)
Piontek⁹, Austria, 2023	143	6.3% (9)	NT	0 % (0)
van Oers¹⁵, Netherlands, 2023	239	23.8% (57)	1.3% (3)	2.5% (6)
Antelmi¹⁴, Italy, 2023	257	5.1% (13)	NT	0.4% (1)

BPA, Brazilian Propolis (Allergeaze); CPA, Chinese Propolis (Allergeaze); CPC, Chinese Propolis (Chemotechnique); NT, not tested.

Van Oers and colleagues performed patch testing with a dilution series of Brazilian propolis of 10%, 3.3%, and 1% in petrolatum. Of 200 patients tested, 28% had one or more positive reactions. 32.1% of propolis-positive individuals reacted only to the 10% concentration, 37.5% reacted to all 3 concentrations, 23.2% to 2 concentrations, and 7.1% only to a lower concentration.¹⁶ The authors concluded that a large portion of positive reactions could be allergic in nature.

Clinical Relevance

In our study, definite/probable current clinical relevance was low, ranging from 16.6% with BPA to 18.2% with CPC and 26.2% with CPA. Lack of clinical relevance has been noted by others. A Swiss study utilizing BPA found that only 16% of positive reactions were determined to have current or past clinical relevance.⁹ In Amsterdam, 3.5% of BPA-positive reactions were considered currently relevant; 33% of CPA and CPC-positive reactions were denoted as clinically relevant. However, the numbers of positives were small.¹⁵

Co-Reactions with Fragrance and Fragrance Markers

Positive patch test reactions to propolis from various sources have been associated with co-reactions to the fragrance mixes, M. pereirae, and colophony.^6,7,14,17,18

Brazilian Propolis

In this study, there was a statistically significant association between Brazilian propolis and fragrance mix (FM) 1, FM II, M. pereirae, hydroperoxides of limonene, ylang-ylang oil, and colophony in propolis-positive versus propolis-negative individuals.

This association with fragrance allergens was also found in other studies. In Amsterdam, of 239 tested, 34 (59.6%) of the 57 patients reacting to BPA co-reacted to one or more fragrance allergens.¹⁵ Positivity to FM I, II, and limonene hydroperoxides was significantly higher in the BPA-positive group compared with the negative group. A follow-up propolis dilution study also showed significant associations of BPA positivity with both fragrance mixes and hydroperoxides of limonene along with M. pereirae and colophonium.¹⁶ In the Italian study, concomitant reactions were common, with 26.7% of BPA-positive patients reacting to FM I and 20% to FM II. Positive patch test reactions to FM I and II, M. pereirae, and colophony were observed in almost half of BPA positives but in only 13% of BPA-negative patients.¹⁴ The number of positive reactions to the 2 Chinese propolis test preparations was too small to allow for statistical comparisons. In contrast to other studies of BPA positivity, Swiss patients who were BPA positive less often had positive patch test reactions to FM I, FM II, and M. pereirae.

Chinese Propolis

In our current study, an even stronger, statistically significant association was found between CPA and FM I, II, M. pereirae resin, hydroperoxides of limonene, hydroperoxides of linalool, ylang-ylang oil, and colophony. Previous studies reported an association between positive reactions to Chinese propolis and M. pereirae, FM I, FM II, colophony,^6,9 and ylang-ylang oil.⁹ In 1470 consecutive patients patch tested to Chinese propolis in centers in Denmark, Lithuania, and Spain, frequent concomitant positive test reactions to propolis were found, mainly to FM I and M. pereirae. Positive patch test reactions to fragrances were significantly more frequent among propolis-positive versus propolis-negative patients.⁶

Our study showed a significantly higher propolis positivity in the BPA cohort from 2020 as compared with the CPA cohort tested in 2019 and the CPC cohort tested in 2021 and 2022. This accounts for the unexpectedly high proportion of propolis-positive reactions reported in our NACDG 2019–20 patch test results.³ Why Brazilian propolis causes many more positive patch reactions than Chinese propolis is not known. Strong differences in composition between the 2 varieties, recently shown by chemical analyses, may play a role.^19,20 Products made with Brazilian propolis could conceivably be more allergenic than those sourced with Chinese propolis, with implications for future labeling requirements. However, the nature of the culprit allergen(s) in Brazilian propolis is completely unknown. Patch testing with its main ingredients in patients with positive patch tests to Brazilian propolis may shed light on this issue.

LIMITATIONS

The limitations of this study include its retrospective design and selection of patients investigated in a tertiary referral center who do not necessarily reflect the general population or the general dermatology patient population. Determinations of patch test positivity and clinical relevance are subject to the inherent variability of clinical judgment and are usually made without the benefit of clinical follow-up and confirmatory use tests.

CONCLUSIONS

When unexpected changes are noted in patch test positivity, especially with naturally derived allergens, the reasons behind those changes should be investigated. The substitution of Brazilian for Chinese propolis resulted in a significant increase in positive patch tests.

References

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Comparison Between Brazilian Propolis and Chinese Propolis: Results From the North American Contact Dermatitis Group 2019–2022

Abstract

Capsule Summary

INTRODUCTION

METHODS

NACDG Database

Allergen Supplier/Geographic Origin

Data Analysis

RESULTS

Patient Characteristics

Allergen Frequencies/Proportions

Reaction Strength and Clinical Relevance

Co-Reactions to Fragrance Allergens/Markers in Propolis-Positive Patients

DISCUSSION

Prevalence of Positive Reactions to Propolis by Source

Studies of Concomitant Testing of Brazilian and Chinese Propolis

Clinical Relevance

Co-Reactions with Fragrance and Fragrance Markers

Brazilian Propolis

Chinese Propolis

LIMITATIONS

CONCLUSIONS

References