Association of positive and negative autologous serum skin test responses with clinical features of chronic spontaneous urticaria in Asian patients: A systematic review and meta‑analysis
- Authors:
- Published online on: February 13, 2019 https://doi.org/10.3892/etm.2019.7266
- Pages: 2603-2613
-
Copyright: © Niu et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
Abstract
Introduction
Chronic urticaria (CU), more commonly referred to as hives, is a frequently occurring condition that may persist for >6 weeks. CU is subdivided into chronic autoimmune urticaria (CAU), chronic spontaneous urticaria (CSU) and physical urticaria (PU), and CSU accounts for 35% of CU patients (1). The mechanisms of CSU are complex and may be triggered by drugs, physical stimuli, as part of inflammatory or inherited diseases, or may be idiopathic in nature. Over half of all CSU cases are thought to involve autoimmune mechanisms (2). The autologous serum skin test (ASST) provides an in vivo assay for diagnosing autoimmune urticaria. The ASST procedure consists of collecting an autologous serum sample from the CU patient, followed by injection of this sample into an area of normal skin. A positive response is indicated by the appearance of an erythematous papule within 30 min following injection (3).
The ASST serves as an effective clinical screening tool and has become the established method for the detection of functional circulating auto-antibodies in patients with CU. The negative predictive value (NPV) of the ASST has been reported to be 82.5±14% (4). This means that in CU patients with a negative response to the ASST, no functional circulating auto-antibodies were present in their serum. However, a positive ASST response may occur in patients with allergic diseases and even in healthy controls. Therefore, to confirm the presence of an autoimmune disorders, a quantitative analysis is required (5). It has been reported that in cases with positive ASST responses, a higher urticaria activity score (UAS), longer disease durations, lower scores on quality of life questionnaires and increased potentials for accompanying angioedema were present (6,7).
CU is a benign disease, has an autoimmune basis in 40% of cases (8) and is more prevalent in females. Immunoglobulin (IgE) has an indispensable role in the occurrence of CSU (9,10), with autoantibodies targeting high-affinity IgE receptors (FcεRI) or IgE in patients with CSU (11). Thyroid disease is the most commonly reported autoimmune condition in patients with CSU. CSU patients with coexisting thyroid autoimmunity tend to have a more severe and prolonged course of their urticaria than those without thyroid autoimmunity. A recent study has indicated that 9.8% of CU patients had hypothyroidism, compared with 0.6% in the control group (12). CU and thyroid disease may be interlinked, and the latter may promote the occurrence of CU (13). Previous studies have produced controversial results about the associations between positive ASST responses and the clinical features of CSU. Therefore, the current meta-analysis was undertaken to clarify the association between ASST and CSU.
Materials and methods
Literature search
The PubMed, Embase, Medline, Ovid, Cochrane Library, China National Knowledge Infrastructure, China Biology Medicine and Wangfang databases, as well as the VIP Database for Chinese Technical Periodicals were searched to identify relevant studies involving ASST and clinical features of CSU. This search included the period from inception of the database until March 2018. The search strategy combined the following terms: ‘Autologous serum skin test’ and ‘chronic spontaneous urticaria’. There was no restriction regarding language or the type of article. An additional manual search was performed by screening the references listed in key publications retrieved in this search.
Inclusion and exclusion criteria
An overall literature search was performed and relevant studies were screened independently by two reviewers. Eligible studies were selected based on the following criteria: i) Study design: Prospective observational study. ii) Patients with clinically defined CU. iii) Information on responses to the ASST. iv) Information on at least one of the following parameters: Average age, duration of disease, UAS, angioedema, anti-thyroid antibodies, total serum IgE, erythrocyte sedimentation rate and allergic rhinitis. The exclusion criteria were as follows: i) Experiments on animal models; ii) cases lacking a definitive diagnosis of CU; iii) intervention trials; iv) reports lacking relevant/sufficient data; v) duplicate publications.
Data extraction
Relevant data were extracted by two reviewers independently. Information included in the forms prepared by these reviewers comprised the following: First author's name, publication year, number of patients, mean age, duration of disease, results of ASST, UAS, angioedema, anti-thyroid antibodies, total serum IgE and allergic rhinitis.
Assessment of study quality
Quality assessment of included studies was independently performed and crosschecked by two reviewers using the Newcastle-Ottawa scale (NOS), which assesses bias on a scale of up to nine stars; >6 stars on the NOS were regarded as indicative of a high quality.
Statistical analysis
The meta-analysis was performed using Review Manager 5.2 (the Cochrane Institute, London, UK). The inverse-variance test was applied for continuous variables and the Mantel-Haenszel test for examination of dichotomous variables. The weighted mean difference (WMD) was used for continuous variables across studies that were measured on the same scale. Dichotomous variables were assessed by calculating the odds ratio (OR). All data were expressed as the WMD or OR along with their associated 95% confidence intervals (CI). Heterogeneity between studies was tested by using I2 tests. P<0.1 or I2>50% was considered to indicate a high degree of heterogeneity between studies. If a significant heterogeneity was present (P<0.1), the random effects model was selected for heterogeneous outcomes (P<0.05 or I2≥50%), otherwise, the fixed effects model was performed for homogeneous outcomes (P≥0.05 and I2<50%). P<0.05 was considered to represent statistically significant differences.
A sensitivity analysis was performed by removing studies one at a time to confirm the robustness of the results. Finally, publication bias in the analysis was determined using a funnel plot and Egger's regression test.
Results
Study characteristics
A total of 1,629 relevant studies were retrieved. After removal of duplicates by title, 851 articles were further screened. Following a careful review of these studies, the full text of 39 studies were assessed. Finally, 16 articles met the inclusion criteria and were included in the systematic review (6,7,14–27). The selection process for these studies is summarized in Fig. 1. A total of 2,554 patients, including 1,284 with positive and 1,270 with negative ASST results were assessed. The characteristics of these patients are presented in Table I. The publication year ranged from 2005 to 2017. Of note, the search of all databases for eligible articles revealed that the region of all studies retrieved was Asia, including China, Thailand, Korea, India, Taiwan and Japan.
Quality assessment of included studies
Detailed results regarding the quality assessment are summarized in Table I. All included studies were prospective observational studies. The present meta-analysis was restricted to studies with a low risk of bias (NOS ≥7), and the entire analysis was replicated following removal of the most influential study on the basis of its weight.
Comparison of the influence of ASST responses on CSU cases and heathy controls
Of all studies reviewed, 6 provided data on ASST responses in heathy controls (15,19,21,23,25). Statistical analysis revealed a high degree of homogeneity across studies (P=0.18, I2=34%). Meta-analysis using the fixed-effects model indicated that CSU cases were more frequently associated with positive ASST responses than the healthy controls (P<0.01, OR=17.16, 95% CI, 9.31–31.63; Fig. 2).
Comparison of age, duration of disease and UAS in positive and negative ASST cases
Of all 16 studies, 14 (6,7,14,18,20,24,26,27) and 10 (6,14,16,17,19,22,24,26,27) provided data on age and duration of disease, respectively, in the two groups. A significant heterogeneity was present across the studies (age: P<0.001, I2=95%; duration: P<0.001, I2=83%), necessitating use of the random-effects model. The meta-analysis indicated that the two groups displayed no statistically significant differences in age (P=0.96, WMD=0.11, 95% CI, −4.31 to 4.52; Fig. 3) and duration (P=0.08, WMD=5.48, 95% CI, −0.71 to 11.68; Fig. 4). A subgroup analysis regarding patient age was then performed, in which patients were stratified by region. Results from China and India indicated that the two groups exhibited no difference in age (China: P=0.15, WMD=3.95, 95% CI, −1.49 to 9.39; India: P=0.18, WMD=−1.88, 95% CI, −4.63 to 0.87). Of note, the results from Korea, Thailand and Taiwan indicated that a positive ASST response was associated with younger age (Korea: P=0.04, WMD=−3.68, 95% CI, −7.21 to −0.16; Taiwan: P=0.01, WMD=−9.6, 95% CI, −16.9 to −2.30; Thailand: P=0.002, WMD=−5.50, 95% CI, −9.04 to −1.96), while the opposite result was obtained in Japan (P=0.02, WMD=6.06, 95% CI, 0.85–11.27; Fig. 3). Another subgroup analysis was performed with stratification by duration of disease (≤30 vs. >30 months). It was revealed that in patients with a duration of disease of ≤30 months, the disease duration was not significantly associated with the result of the ASST (P=0.59, WMD=−1.52, 95% CI, −7.03 to 3.99), while in those with a duration of disease of >30 months, a positive ASST response was associated with a significantly increased duration of disease as compared with that in patients with a negative ASST response (P=0.002, WMD=15.93, 95% CI, 56.64–26.22; Fig. 4).
A total of 11 studies provided data on UAS (6,7,15,17,21,23,27). Statistically significant heterogeneity was present across these studies (P=0.01, I2=59%), again resulting in the use of the random-effects model. The meta-analysis revealed that the positive ASST response group had a higher UAS than that of the negative ASST response group (P<0.001, WMD=0.42, 95% CI, 0.35–0.50; Fig. 5). Therefore, a subgroup analysis was performed based on the range of UAS as estimated by employing different guidelines, including European (28) and Korean guidelines (29). The results of this subgroup analysis also indicated that the positive ASST response group had a higher UAS than the negative ASST response group [UAS (0–6): P<0.001, WMD=0.41, 95% CI, 0.33–0.49; UAS (0–9): P<0.001, WMD=0.77, 95% CI, 0.36–1.18; UAS (0–18): P=0.00, WMD=1.18, 95% CI, 0.57–1.80]. However, the results of UAS of 0–12 was at the verge of statistical significance, however it was not statistically significant (P=0.05, WMD=0.60, 95% CI, 0.00–1.20, and an inverse result was observed for UAS of 0–15 (P=0.04, WMD=−0.73, 95% CI, −1.41 to −0.05). In addition, two studies provided the median and range of UAS but no standard deviation (SD) (25,27). The SD was then calculated using an established formula (30).
Comparison of total serum IgE, angioedema and anti-thyroid autoantibodies in positive and negative ASST groups
Of all studies included in the present review, 4 (16–18,26) provided data on total serum IgE and 8 (16,18–22,26,27) on the presence of thyroid autoantibodies in the two groups. Statistical analysis indicated that a significant homogeneity was present across these studies (serum total IgE: P=0.78, I2=0%; anti-thyroid autoantibodies: P=0.38, I2=7%). Meta-analysis using the fixed-effects model indicated that a positive ASST result was associated with higher levels of total serum IgE (P<0.001, WMD=41.99, 95% CI, 20.40 to 63.58; Fig. 6) and thyroid autoantibodies (P<0.01, OR=1.87, 95% CI, 1.19–2.94; Fig. 7) than a negative ASST result.
Data from 7 studies provided information on angioedema in the two groups. As the results on angioedema displayed a statistically significant heterogeneity across studies (P=0.03, I2=57%), it was necessary to use the random-effects model. Meta-analysis revealed that a positive ASST result was associated with a higher risk of angioedema than that of a negative ASST result (P=0.03, OR=1.92, 95% CI, 1.08–3.40; Fig. 8). Angioedema is a subjective index of urticaria and manifests in a relatively short-lived edema in the skin. The occurrence of angioedema is affected by inherited and environmental factors; furthermore, physical stimulators, including shock and pressure, may also induce angioedema (31). As a result, a substantial heterogeneity in angioedema data may be present.
Sex differences among subjects with positive ASST responses
An included study demonstrated that females are more likely to have a positive ASST response as rates of ASST were 78% and 22% in females and males, respectively (15). Of all studies included in the present review, 12 (7,14,18,20,22,24,27), which accounted for 1462 cases, contained 756 cases with positive responses to ASST. Of these 756 cases, 210 were males and 546 were females. Statistical analysis of positive ASST responses in CSU cases indicated that a statistically significant homogeneity was present across studies (P=0.97, I2=0%), and the fixed-effects model was therefore used. The meta-analysis revealed that females had a higher prevalence of positive ASST responses (P<0.001, OR=0.63, 95% CI, 0.50–0.79; Fig. 9). The detailed results of the meta-analysis for the above indexes are presented in Table I.
Sensitivity analysis
Studies that failed to satisfy the criterion of high quality were excluded from the present review. In addition, a sensitivity analysis was applied for each index involving ASST comparisons. The sensitivity analysis demonstrated that the results obtained using the random- and fixed-effects models were in accordance with each study included in the review. These results suggested that no individual studies significantly affected the pooled results. This indicated that the meta-analysis performed provided reliable results.
Detection of publication bias
An analysis of publication bias was performed by using Egger's regression test. The results indicated that no publication bias was present regarding the UAS and sex differences among patients with positive ASST responses (UAS: Z=−2.18, P=0.06; sex differences among patients with positive ASST response: Z=−0.73, P=0.48). However, publication bias was present with regard to age and duration of CSU (age: Z=−3.93, P=0.002; duration of CSU: Z=4.23, P=0.003). Although the above results revealed that studies included in the present review displayed an inconformity in publication bias, the funnel plots had typical shapes, and the funnel plot of anti-thyroid autoantibodies is presented in Fig. 10.
Discussion
To the best of our knowledge, the present study is the first systematic review comparing ASST responses in patients with CSU. The results obtained by the meta-analysis suggest that cases with positive ASST responses had higher UAS and higher levels of serum total IgE than those of cases with negative ASST responses. In addition, cases with positive responses to ASST were more likely to have accompanying angioedema and were positive for thyroid autoantibodies. CSU was more prevalent in females, who were also more likely to exhibit a positive response to ASST. It was also confirmed that a greater incidence of ASST was present in CSU patients as compared with that in heathy controls. No statistically significant differences were present between cases with positive vs. negative responses to ASST with regard to patient age and duration of disease.
Angioedema, which is the clinical manifestation of urticaria, develops when urticaria is located within the subcutis. It is a syndrome characterized by a sudden and limited subcutaneous and/or submucous swelling. Angioedema in CU is caused by a non-specific histamine release from activated mast cells (32). The occurrence of angioedema in CU, while not an indication for disease severity, is associated with a longer duration of urticarial disease. Non-steroidal anti-inflammatory drugs and/or systemic corticotherapy are classic triggers of angioedema in CU (33). Mast cells may be activated primarily by IgE-dependent (allergen, anti-IgE) as well as by IgE-independent mechanisms (34). Increased levels of IgE are thought to provoke urticaria. Auto-antibodies for IgE and the α-chain of FcεRI contribute to the occurrence of CU (35). It has been reported that one third of patients with CU have significantly elevated levels of total IgE and levels of serum total IgE are associated with disease severity and duration (36). The severity of CSU was also identified to be associated with a positive response in the ASST (37), which is in accordance with the results of the present meta-analysis.
CSU is linked with thyroid diseases, which are the most commonly reported autoimmune condition in patients with CSU. Patients with thyroid dysfunction and CSU have a more severe and prolonged course of urticaria than those without thyroid dysfunction. A significantly greater number of anti-thyroid antibodies are present in CSU patients. Even in clinically euthyroid CSU patients, anti-thyroid antibodies remain present and are considered to be associated with CSU. Thyroid disease may worsen urticaria through activation of the complement system (2).
CU is characterized by mast/basophil cell activation, which initiates an inflammatory response. Sex hormones modulate immune and inflammatory cell functions, including mast cell secretion. Of note, urticaria may be associated with certain diseases and conditions associated with hormonal changes, including endocrinopathy, the menstrual cycle, pregnancy, menopause and hormonal contraceptives or hormone replacement therapy. Dehydroepiandrosterone (DHEA) is a modulator of endocrine and immune functions and depletion of DHEA may lead to adverse events (38). Serum concentrations of DHEA sulfate in CSU patients are significantly lower than those in healthy subjects and are associated with positive responses to ASST (39). This is in accordance with the results of the present meta-analysis, which indicate a female predominance for CSU and a positive response in the ASST (6–8,15).
Although the average NPV of the ASST was 92.8%, a negative ASST was identified as a significant determinant of urticaria remission and a negative ASST serves as a good predictor for achieving urticaria remission within 2 years (8,14,40). A positive ASST response is a significant predictor of CSU in controls (14).
While the studies included in the present meta-analyses were selected based on strict inclusion and exclusion criteria, certain unavoidable limitations and bias remain. As compared with a randomized controlled trial, the quality of observational studies is low, which represents a limitation of the present meta-analysis. However, all subjects enrolled in the present meta-analysis were patients with CU who voluntarily underwent an ASST. The major observational endpoints were UAS, serum total IgE and anti-thyroid autoantibodies, all of which are objective parameters. Furthermore, all of the studies included were on Asian populations, which is a cause of publication bias. Although ASST has a high specificity to test for functional autoantibodies, their absence has a high specificity for CU. According to the European expert consensus from 2009 (8), the value and meaning of the ASST remains to be fully established. Furthermore, skin testing requires the collection of venous blood and separation of serum prior to hypodermic injection. It is essential that failsafe precautions are taken to ensure that the patient's own serum is used for skin testing and aseptic procedures are required. Commercial ELISA is now sufficiently mature for testing for functional autoantibodies, including IgE. The dermatologists of developed countries may be more likely to identify anti-IgE antibodies using ELISA compared with certain Asian dermatologists. An additional source of potential bias may be differences within health care providers and hospitals regarding the techniques applied for detecting ASST and the conditions of the patients. Although all studies included in the present review involved comparisons of/within case groups with positive and negative ASST responses, inherent differences in researchers' approaches to, and interpretations of, CSU may exist. Finally, the limited sample size and resultant data available for the present meta-analyses may have affected the final results obtained. The conclusions require verification by subsequent studies and the resolution of remaining issues.
In conclusion, the results of the present analyses of pooled data indicate that CSU patients with a positive ASST response have more severe clinical features and are more likely to have an accompanying autoimmunity condition as compared with those with a negative response to the ASST.
Acknowledgements
Not applicable.
Funding
The current study was supported by National Natural Science Foundation of China (grant nos. 81673070 and 81872538).
Availability of data and materials
All data generated or analyzed during this study are included in this published article.
Authors' contributions
XLN analyzed autologous serum skin test data of all involved studies and drafted the manuscript. LLZ searched the literature and collected the data associated with chronic urticaria. MHS and YJZ performed the statistical analysis. XHG and RQQ critically revised the manuscript for important intellectual content. All authors have read and approved the final version of the manuscript prior to submission.
Ethics approval and consent to participate
Not applicable.
Patient consent for publication
Not applicable.
Competing interests
The authors have no competing interests to declare.
References
|
Irinyi B, Széles G, Gyimesi E, Tumpek J, Herédi E, Dimitrios G, Adány R, Hunyadi J and Szegedi A: Clinical and laboratory examinations in the subgroups of chronic urticaria. Int Arch Allergy Immunol. 144:217–225. 2007. View Article : Google Scholar : PubMed/NCBI | |
|
Fraser K and Robertson L: Chronic urticaria and autoimmunity. Skin Therapy Lett. 18:5–9. 2013.PubMed/NCBI | |
|
Al-Hamamy HR, Hameed AF and Abdulhadi AS: Autologous serum skin test as a diagnostic aid in chronic idiopathic urticaria. ISRN Dermatol. 2013:2915242013. View Article : Google Scholar : PubMed/NCBI | |
|
Sabroe RA, Grattan CE, Francis DM, Barr RM, Kobza Black A and Greaves MW: The autologous serum skin test: A screening test for autoantibodies in chronic idiopathic urticaria. Br J Dermatol. 140:446–452. 1999. View Article : Google Scholar : PubMed/NCBI | |
|
Feng L, Song ZQ and Hao F: Application of autologous serum skin test in chronic urticaria: Current advances. J Clin Dermatol. 08:508–510. 2011. | |
|
Song Z, Zhai Z, Zhong H, Zhou Z, Chen W and Hao F: Evaluation of autologous serum skin test and skin prick test reactivity to house dust mite in patients with chronic spontaneous urticaria. PLoS One. 8:e641422013. View Article : Google Scholar : PubMed/NCBI | |
|
Zhong H, Song Z, Chen W, Li H, He L, Gao T, Fang H, Guo Z, Xu J, Yu B, et al: Chronic urticaria in Chinese population: A hospital-based multicenter epidemiological study. Allergy. 69:359–364. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Konstantinou GN, Asero R, Maurer M, Sabroe RA, Schmid-Grendelmeier P and Grattan CE: EAACI/GA(2)LEN task force consensus report: The autologous serum skin test in urticaria. Allergy. 64:1256–1268. 2009. View Article : Google Scholar : PubMed/NCBI | |
|
Auyeung P, Mittag D, Hodgkin PD and Harrison LC: Autoreactive T cells in chronic spontaneous urticaria target the IgE Fc receptor Iα subunit. J Allergy Clin Immunol. 138:761–768.e4. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Kulthanan K, Nuchkull P, Ungaksornpairote C, Chularojanamontri L and Tuchinda P: Prevalence and clinical correlation of serum immunoglobulin E in patients with chronic spontaneous urticaria. Ann Allergy Asthma Immunol. 116:258–259. e2. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Navines-Ferrer A, Serrano-Candelas E, Molina-Molina GJ and Martin M: IgE-related chronic diseases and Anti-IgE-based treatments. J Immunol Res. 2016:81638032016. View Article : Google Scholar : PubMed/NCBI | |
|
Confino-Cohen R, Chodick G, Shalev V, Leshno M, Kimhi O and Goldberg A: Chronic urticaria and autoimmunity: Associations found in a large population study. J Allergy Clin Immunol. 129:1307–1313. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Sugiyama A, Nishie H, Takeuchi S, Yoshinari M and Furue M: Hashimoto's disease is a frequent comorbidity and an exacerbating factor of chronic spontaneous urticaria. Allergol Immunopathol (Madr). 43:249–253. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Boonpiyathad T and Sangasapaviliya A: Autologous serum and plasma skin test to predict 2-year outcome in chronic spontaneous urticaria. Asia Pac Allergy. 6:226–235. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Aktar S, Akdeniz N, Ozkol HU, Calka O and Karadag AS: The relation of autologous serum and plasma skin test results with urticarial activity score, sex and age in patients with chronic urticaria. Postepy Dermatol Alergol. 32:173–178. 2015. View Article : Google Scholar : PubMed/NCBI | |
|
Ye YM, Park JW, Kim SH, Ban GY, Kim JH, Shin YS, Lee HY and Park HS;: PRANA Group: Prognostic factors for chronic spontaneous urticaria: A 6-month prospective observational study. Allergy Asthma Immunol Res. 8:115–123. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Kim JH, Lee HY, Ban GY, Shin YS, Park HS and Ye YM: Serum clusterin as a prognostic marker of chronic spontaneous urticaria. Medicine (Baltimore). 95:e36882016. View Article : Google Scholar : PubMed/NCBI | |
|
Lee MF, Lin TM, Liu SW and Chen YH: A rapid method of detecting autoantibody against FcεRIα for chronic spontaneous urticaria. PLoS One. 9:e1095652014. View Article : Google Scholar : PubMed/NCBI | |
|
Alpay A, Solak Tekin N, Tekin IÖ, Altinyazar HC, Koca R and Cinar S: Autologous serum skin test versus autologous plasma skin test in patients with chronic spontaneous urticaria. Dermatol Res Pract. 2013:2672782013. View Article : Google Scholar : PubMed/NCBI | |
|
Kumar YH, Bhaskar S and Shankar K: Comparative study of positive versus negative autologous serum skin test in chronic spontaneous urticaria and its treatment outcome. N Am J Med Sci. 8:25–30. 2016. View Article : Google Scholar : PubMed/NCBI | |
|
Yadav S, Kanwar A, Parsad D and Minz R: Chronic idiopathic urticaria and thyroid autoimmunity: Perplexing association. Indian J Dermatol. 58:3252013. View Article : Google Scholar : PubMed/NCBI | |
|
Krupashankar DS, Shashikala K and Madala R: Clinical and investigative assessment of patients with positive versus negative autologous serum skin test: A study of 80 South Indian patients. Indian J Dermatol. 57:434–438. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Zhou PM, Lu YH, Chen T, Huang J, Fang J, Liu P and Liu H: Analysis of autologous serum skin test results in 154 cases of patients with chronic spontaneous urticaria. Chin J Dermatov Integr Tradit and West Med. 02:135–137. 2017. | |
|
Yang SL, Xie SX, Yin SC, Ou FX, Zhang YQ and Lai W: Analysis of the clinical value of autologous serum skin test in chronic urticaria. Chin J Health Lab Technol. 21:3158–3160. 2016. | |
|
Chen MC, Li D, Guo Q and Zhai FQ: Investigation into the correlation of clinical features and autologous serum skin test of chronic urticaria. China Tropical Med. 05:736–738. 2008. | |
|
Li MM, Guo ZP, Li JY, Xie XQ, Song Q, Ye YY and Chen SY: Autologous serum skin test and some laboratory test analysis in 136 patients with chronic urticaria. Chin J Leprosy and Skin Dis. 10:595–597. 2016. | |
|
Sun WL and Bi ZG: Clinical features of chronic urticaria in patients with positive and negative autologous serum skin test. Chin J Dermatol. 06:342–344. 2005. | |
|
Zuberbier T, Bindslev-Jensen C, Canonica W, Grattan CE, Greaves MW, Henz BM, Kapp A, Kozel MM, Maurer M, Merk HF, et al: EAACI/GA2LEN/EDF guideline: Definition, classification and diagnosis of urticaria. Allergy. 61:316–320. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Ye YM, Park JW, Kim SH, Choi JH, Hur GY, Lee HY, Lee EH and Park HS: Clinical evaluation of the computerized chronic urticaria-specific quality of life questionnaire in Korean patients with chronic urticaria. Clin Exp Dermatol. 37:722–728. 2012. View Article : Google Scholar : PubMed/NCBI | |
|
Hou XW, Shi JP and Chen X: How to estimate the mean and standard deviation based on the median, range and sample size when conducting meta-analysis. Chin J Evid-based Med. 15:484–487. 2015. | |
|
Bork K: Angioedema. Immunol Allergy Clin North Am. 34:23–31. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Boccon-Gibod I and Bouillet L: Angioedema and urticaria. Ann Dermatol Venereol. 141 (Suppl 3):S586–S595. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Hacard F, Nosbaum A, Bensaid B, Nicolas JF, Augey F, Goujon C and Bérard F: Histaminergic angioedema and chronic urticaria. Presse Med. 44:37–42. 2015.(In French). View Article : Google Scholar : PubMed/NCBI | |
|
Petra AI, Panagiotidou S, Stewart JM, Conti P and Theoharides TC: Spectrum of mast cell activation disorders. Expert Rev Clin Immunol. 10:729–739. 2014. View Article : Google Scholar : PubMed/NCBI | |
|
Chang KL, Yang YH, Yu HH, Lee JH, Wang LC and Chiang BL: Analysis of serum total IgE, specific IgE and eosinophils in children with acute and chronic urticaria. J Microbiol Immunol Infect. 46:53–58. 2013. View Article : Google Scholar : PubMed/NCBI | |
|
Kessel A, Helou W, Bamberger E, Sabo E, Nusem D, Panassof J and Toubi E: Elevated serum total IgE-a potential marker for severe chronic urticaria. Int Arch Allergy Immunol. 153:288–293. 2010. View Article : Google Scholar : PubMed/NCBI | |
|
Toubi E, Kessel A, Avshovich N, Bamberger E, Sabo E, Nusem D and Panasoff J: Clinical and laboratory parameters in predicting chronic urticaria duration: A prospective study of 139 patients. Allergy. 59:869–873. 2004. View Article : Google Scholar : PubMed/NCBI | |
|
Kasperska-Zajac A, Brzoza Z and Rogala B: Sex hormones and urticaria. J Dermatol Sci. 52:79–86. 2008. View Article : Google Scholar : PubMed/NCBI | |
|
Kasperska-Zajac A, Brzoza Z and Rogala B: Lower serum concentration of dehydroepiandrosterone sulphate in patients suffering from chronic idiopathic urticaria. Allergy. 61:1489–1490. 2006. View Article : Google Scholar : PubMed/NCBI | |
|
Hizal M, Tüzün B, Wolf R and Tüzün Y: The relationship between Helicobacter pylori IgG antibody and autologous serum test in chronic urticaria. Int J Dermatol. 39:443–445. 2000. View Article : Google Scholar : PubMed/NCBI |
