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Concentration of cytokines in plasma of dogs with atopic dermatitis and healthy dogs. Symbol * represents the level of significance: P ≤ 0.05
Source publication
Background
Canine atopic dermatitis (cAD) is a common chronic and pruritic skin disease in dogs. The development of cAD involves complex interactions between environmental antigens, genetic predisposition and a number of disparate cell types. The aim of the present study was to perform comprehensive analyses of peripheral blood of AD dogs in relati...
Context in source publication
Context 1
... level of cytokines in plasma of AD and healthy dogs was determined based on ELISA tests, and the results obtained are presented in Fig. 1. In four out of seven analyzed cytokines significant differences were observed between the two groups of dogs. The level of IL-13 and TNF-α was significantly higher in AD dogs than in controls (P = 0.02); whereas L-10 was significantly lower in AD patients (P = 0.03). No differences were noted in the case of IL-4. In most patients ...
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Citations
... In the chronic phase, trefoil factors (TFF-1, 2 and 3) are peptides that play a role in the protection and repair of epithelial surfaces, including the gastrointestinal tract (Aamann et al., 2017). Also, as a result of the organism's type 1 hypersensitivity response to environmental allergens in atopic dermatitis, a significant increase in IL-4 and IL-13 concentrations in addition to intense IgE production has been reported (Chaudhary et al., 2019;Maden et al., 2013;Majewska et al., 2016) In recent years, it has been established in human medicine that chronic intestinal diseases (such as irritable colon syndrome, Crohn's disease and celiac disease) predispose to dysbiosis as a result of disruption of the intestinal microbiota or leaky gut by causing damage to the intestinal wall and that this condition may form the basis of the development of atopic dermatitis. However, no studies have been conducted to determine whether there is an association between atopic dermatitis and intestinal damage in dogs. ...
... It has been reported that the specific diagnostic cytokines of atopic dermatitis are IL-4 and IL-13 (Chan, 2018). In dogs with atopic dermatitis, serum IL-13 increased more than IL-4, suggesting that IL-13 may play an important role in the development of the atopic response, compared to IL-4 (Majewska et al., 2016). Similarly, Majewska et al. (2016) reported that IL-13 concentrations were significantly increased in dogs with atopic dermatitis, while IL-4 did not change. ...
... In dogs with atopic dermatitis, serum IL-13 increased more than IL-4, suggesting that IL-13 may play an important role in the development of the atopic response, compared to IL-4 (Majewska et al., 2016). Similarly, Majewska et al. (2016) reported that IL-13 concentrations were significantly increased in dogs with atopic dermatitis, while IL-4 did not change. It has been reported that IL-17, IL-31 and IgE concentrations are significantly increased in dogs with atopic dermatitis (Chaudhary et al., 2019). ...
Background
A significant association between atopic dermatitis and leaky gut syndrome has been demonstrated in humans. No studies have been conducted to determine whether there is an association between atopic dermatitis and intestinal damage in dogs.
Objectives
This study aimed to determine whether there is an association between canine atopic dermatitis and intestinal damage using selected intestinal‐related biomarkers.
Methods
Twenty‐six dogs with atopic dermatitis and 10 healthy dogs were included. Moderate‐to‐severe pruritus, erythema, erosion and alopecia on different parts of the body were sought in dogs to suspect atopic dermatitis. The presence of atopic dermatitis was confirmed by an allergic skin test. Serum biomarkers including intestinal fatty acid binding protein (I‐FABP), intestinal alkaline phosphatase (IAP), trefoil factor‐3 (TFF‐3), immunoglobulin E (IgE), interleukin‐4 (IL‐4) and interleukin‐13 (IL‐13) concentrations were measured from venous blood samples.
Results
Of the 26 dogs tested for allergens, 16 were found to be sensitive to mould mites, 10 to vernal grass, eight to house dust mites, five to wheat dust and five to grass pollen mix allergens. Significant increases in serum IAP, TFF‐3, IgE, IL‐4 and IL‐13 concentrations were determined.
Conclusion
It was thought that the increase in TFF‐3 and IAP concentrations may be due to the presence of intestinal epithelial damage and the repair of this damage. In addition, the development of atopic dermatitis may be predisposed to the entry of allergens into the body through sites of intestinal damage.
... Quinnell et al. (52) and Singh et al. (58) reported significantly higher (p < 0.05) serum IL-4 levels, compared with those for healthy animals, in dogs with leishmaniasis and in dogs with scabies, respectively. Shida et al. (57) reported that serum IL-4 levels in dogs with AD were lower than they were in healthy dogs, whereas Majewska et al. (35) noted no significant difference between dogs with AD and healthy dogs. In the present study, the mean serum IL-4 level in the dogs with AD was lower (p < 0.05) than that in the control group. ...
... In the present study, serum IL-13 levels of dogs with AD were lower than those of healthy dogs, but not statistically significantly so (p > 0.05). This agrees with the results of Majewska et al. (35), but is contrary to those of Viljanen et al. (65). Furthermore, there were significant (p < 0.05) differences between the patient groups. ...
The aim of this study was to present allergens involved in the etiology of atopic dermatitis (AD) in dogs, to determine and classify the clinical severity of the disease using the CADESI-4 and pruritus scores, to investigate changes in serum cytokine levels in dogs with AD and their relationship with clinical findings, and to investigate the effects of oclacitinib maleate on clinical improvement and serum cytokine levels. The material of the study consisted of 20 dogs diagnosed with AD and 10 healthy dogs. CADESI and pVAS scores were obtained from the patients, and blood samples were taken. Hematological analyses, specific allergen tests (polycheck), and ELISA analyses were performed. Oclacitinib maleate (Apoquel, Zoetis) was administered orally to the patient dogs at a dose of 0.5 mg/kg twice a day for 7 days. It was found that the most common allergens involved in the etiology of AD in dogs were house dust mites type 1, house dust mites type 2, and mold fungi, and the mean CADESI and pVAS scores for clinical findings such as pruritus, alopecia, erythema, and lichenification in dogs with AD were 48 and 5.15 respectively. When compared to the control group, an increase in the percentage of eosinophils (p < 0.05) and a decrease in serum IL-2 and IL-4 levels (p < 0.05) were detected. When compared to other groups, it was found that the mean serum IL-4 levels (p < 0.05) were low and IL-13 levels (p < 0.05) were high in the group with severe clinical findings. It was determined that the use of oclacitinib maleate resulted in clinical improvement and caused an increase in the mean serum IL-2 levels (p < 0.05) and a decrease in IL-31 and IL-33 levels (p < 0.05). Oclacitinib maleate (Apoquel, Zoetis) was found to be an effective and reliable drug that can be used in the treatment of the disease, but it was concluded that the duration of use should be extended.
... 12,21,37 By contrast, four other studies on sera from client-owned dogs did not find a difference in the concentration of IL-4 between dogs with AD and healthy controls. [38][39][40][41] Since the HDMinduced experimental AD model represents the earliest stages of acute flares of AD and most client-owned dogs have more chronic lesions, it is possible that IL-4 only plays an important role during the induction or acute phase of cAD. Furthermore, it is interesting to note that the percentage of IL-4-producing T cells in dogs with AD did not change after one year of treatment with oclacitinib, despite the clinical improvement, 42 which indicates that IL-4 might be a less important inflammatory cytokine in chronic cAD. ...
... All except one showed increased mRNA or protein levels of IL-13 in either skin or blood (sera or PBMCs) samples of dogs with AD compared to the controls. 10,[12][13][14]21,38,40,50 The consistency of these results suggests that IL-13 may play an important role in cAD, especially compared to IL-4, and could be a valid therapeutic target as in human AD. ...
... 37 Of the remaining studies, four showed no difference, and one showed reduced, although not significantly, protein and mRNA levels of IFNγ in the blood (sera, plasma and PBMCs). [38][39][40][41]90 The mRNA expression of IFNγ also was unchanged after HDM challenge in the acute skin lesions or primary keratinocytes collected from the cAD model, 21,91 whereas its mRNA expression was significantly increased in PBMCs collected from dogs of a similar AD model. 12 A study of dogs treated with oclacitinib showed that IFNγ production by peripheral blood CD4 + and CD8 + T cells was significantly reduced on Day (D)240 and D300 after the initiation of treatment yet returned to baseline levels on D360 without an associated clinical relapse. ...
... Additionally, cAD is a very heterogenous clinical syndrome [6,7,35], with ongoing research to characterise each subtype based on either epidermal barrier defects or endotypes [74,81,[127][128][129][130]. Further characterisation of the various specific clinical phenotypes of cAD may optimise clinical outcomes by establishing what preventative and therapeutic strategies work best for each dog [7]. ...
Simple Summary
This paper addresses the pressing issue of canine atopic dermatitis, a common and distressing skin condition in dogs. It affects up to 30% of dogs, causing severe itching and skin problems. Additionally, it leads to secondary infections, further complicating treatment. This condition significantly reduces the quality of life for both dogs and their owners, causing emotional and financial strain. This paper emphasizes the need for prevention strategies for this disease, rather than just treating the symptoms. While treatments exist, they often come with limitations and can be expensive. It also emphasizes the importance of understanding the skin barrier’s role in canine atopic dermatitis development. This paper suggests that focusing on preventing this condition in the first place would be more effective and cost-efficient. Drawing parallels between canine atopic dermatitis and its human counterpart, this paper highlights the potential for shared prevention strategies. The authors propose that restoring the skin barrier before the disease’s mechanisms can lead to a vicious cycle of further damage could be a key approach to prevention. Overall, research regarding the primary prevention of canine atopic dermatitis has the potential to greatly improve the well-being of dogs and their owners by offering effective and accessible preventive measures.
Abstract
Canine atopic dermatitis (cAD) is a common and distressing skin condition in dogs, affecting up to 30% of the canine population. It not only impacts their quality of life but also that of their owners. Like human atopic dermatitis (hAD), cAD has a complex pathogenesis, including genetic and environmental factors. Current treatments focus on managing clinical signs, but they can be costly and have limitations. This article emphasizes the importance of preventing cAD from developing in the first place. Understanding the role of the skin’s protective barrier is crucial, as its dysfunction plays a vital role in both hAD and cAD. hAD prevention studies have shown promising results in enhancing the skin barrier, but more research is needed to support more robust conclusions. While hAD primary prevention is currently a focal point of intensive investigation in human medicine, research on cAD primary prevention remains under-researched and almost non-existent. Pioneering effective prevention strategies for cAD holds immense potential to enhance the quality of life for both dogs and their owners. Additionally, it bears the promise of a translational impact on human research. Hence, further exploration of this crucial topic is not only relevant but also timely and imperative, warranting support and encouragement.
... Effector cytotoxic CD8 + T cells have the ability to kill target cells through perforin and Fas ligands (Hamann et al. 1997). Although CD4 + T cells play a dominant role in the pathogenesis of AD, a few studies have revealed that CD8 + T cells are also involved in the development of the disease in dogs (Olivry et al. 1997, Sinke et al. 1997, Majewska et al. 2016. In turn, B cells are the main cells of humoral immunity. ...
The main purpose of the study was to determine the safety of oclacitinib (OCL), a Janus kinase inhibitor, with respect of its effect on CD4 + and CD8 + T cells as well as B cells in the lymphoid tissue. The mice were treated orally with OCL at a dose of 2.7 mg/kg for 14 days and peripheral blood, head and neck lymph nodes (HNLNs), mediastinal lymph nodes (MLNs) and spleen were collected. The study found that OCL induced depletion of CD4 + T cells in the HNLNs and MLNs, while it did not affect the absolute count of CD8 + T cells in these tissues. Also OCL caused a loss of B cells in the HNLNs, although not in the MLNs. Moreover, OCL depleted B cells in the peripheral blood, but did not affect the absolute count of CD4 + and CD8 + T cells. Thus, it can be concluded that OCL may induce a depletive effect on CD4 + and CD8 + T cells as well as B cells in the lymphoid tissue. This effect should be seen as an unfavorable one, especially in patients with infections. Therefore, a clinical implication is that in such patients, the benefit/risk ratio should be thoroughly considered by clinicians. Moreover, OCL reduced the absolute count of eosinophils, basophils, neutrophils and monocytes. However, it is uncertain whether this effect should be considered to be of clinical importance because the levels of these cells were within the physiological range. It is possible that the depletive effect of OCL toward T and B cells, as well as eosinophils and basophils may contribute to the beneficial effects of the drug in the treatment of skin allergic diseases.
... In other papers, the time needed to observe positive effects is variable, ranging from two weeks (Szczepanik et al., 2022), one month (Bensignor et al., 2008;Witzel-Rollins et al., Canine atopic dermatitis is an immunological base disease in which CD4 + and CD8 + T cells and cytokines play an important role to explain the pathogenesis of the disease (Pucheu-Haston et al., 2015a). Other articles have analysed other T cell populations (Majewska et al., 2016;Herrmann et al., 2023) in atopic dogs, but in the study by Jasiecka-Mikolajczyk et al. (2018) demonstrated that oclacitinib had no influence on the expression of CD25 and Foxp3 on CD4 + and CD8 + T cells, but a dramatic loss of CD4 + and CD8 + T cells was caused by oclacitinib when the drug was evaluated in vitro. In this study, no effect of the diet on the cells of the immune system was found. ...
... In this study, no effect of the diet on the cells of the immune system was found. An increased of percentage of CD8 + T cells have been described in cAD (Majewska et al., 2016;Verde et al., 2022), suggesting the cellular suppressive mechanisms of the immune response in the pathogenesis of the cAD. The lack of effect of the diet on the lymphocyte population may be due to the fact that the components of the diets were not capable of modifying the percentage of T cells. ...
... An increase in IL-10 serum levels was observed from dogs eating diet A. IL-10 is an anti-inflammatory cytokine produced mainly by Treg cells that plays an important role in the induction and maintenance of the immune response, but interpretation of its role A c c e p t e d M a n u s c r i p t can be complicated (Pucheu-Haston et al., 2015a). The effect of the cAD treatment on this cytokine is variable and higher or lower level compared to healthy dogs or at basal levels have been described (Keppel et al., 2008;Majewska et al., 2016;Koury et al., 2019), and for Mazrier et al. (2021) these findings support that Treg is impaired during cAD. However, serum IL-10 levels in dogs with cAD are often lower than those in healthy animals or basal levels (Majewska et al., 2016;Verde et al., 2022). ...
Canine atopic dermatitis (cAD) is a common inflammatory skin disease that is treated with medicines or allergen-specific immunotherapy. An improvement diet can help treatment of cAD. The purpose of this study was compare two diets on clinical and immunological parameters in atopic dogs without food hypersensitivity. Diet A, a commercial based on rice, was offered to 22 atopic dogs during 30 days and Diet B (grain free, rich in salmon) was given to 8 atopic dogs. Clinical scores were assessed by CADESI-4 and PVAS at the beginning (T0) and at the end of the study (T30). CD4⁺ and CD8⁺ were measured in PBMCs, and serum cytokines (TNF-α, IL-10, IL-31 and IL-34) were determined. Both diets decreased CADESI-4 score and Diet A decreased PVAS score (p < 0.05). There were no statistical significant differences between diets at T30 for CD4⁺ and CD8⁺. A decrease in the IL-31 concentrations and increase in IL-10 levels (p < 0.05) was observed with Diet A at T30. There were no differences between any of the two diets when the other results at T0 and T30 were compared for any of the parameters analysed. In conclusion, the results indicate that dietary intervention had not influence on cellular component of the immune system, but a positive effect was observed on IL-31, IL-10 serum levels for Diet A. Further studies are needed to enrich dietary components of the food for atopic dogs without food hypersensibility to help improvement the management of the cAD.
... 12,21,37 By contrast, four other studies on sera from client-owned dogs did not find a difference in the concentration of IL-4 between dogs with AD and healthy controls. [38][39][40][41] Since the HDMinduced experimental AD model represents the earliest stages of acute flares of AD and most client-owned dogs have more chronic lesions, it is possible that IL-4 only plays an important role during the induction or acute phase of cAD. Furthermore, it is interesting to note that the percentage of IL-4-producing T cells in dogs with AD did not change after one year of treatment with oclacitinib, despite the clinical improvement, 42 which indicates that IL-4 might be a less important inflammatory cytokine in chronic cAD. ...
... All except one showed increased mRNA or protein levels of IL-13 in either skin or blood (sera or PBMCs) samples of dogs with AD compared to the controls. 10,[12][13][14]21,38,40,50 The consistency of these results suggests that IL-13 may play an important role in cAD, especially compared to IL-4, and could be a valid therapeutic target as in human AD. ...
... 37 Of the remaining studies, four showed no difference, and one showed reduced, although not significantly, protein and mRNA levels of IFNγ in the blood (sera, plasma and PBMCs). [38][39][40][41]90 The mRNA expression of IFNγ also was unchanged after HDM challenge in the acute skin lesions or primary keratinocytes collected from the cAD model, 21,91 whereas its mRNA expression was significantly increased in PBMCs collected from dogs of a similar AD model. 12 A study of dogs treated with oclacitinib showed that IFNγ production by peripheral blood CD4 + and CD8 + T cells was significantly reduced on Day (D)240 and D300 after the initiation of treatment yet returned to baseline levels on D360 without an associated clinical relapse. ...
Background
Cytokines and chemokines play central roles in the pathogenesis of canine atopic dermatitis (cAD). Numerous studies have been published and provide new insights into their roles in cAD.
Objectives
To summarise the research updates on the role of cytokines and chemokines in the pathogenesis of cAD since the last review by the International Committee on Allergic Diseases of Animals in 2015.
Material and Methods
Online citation databases, abstracts and proceedings from international meetings on cytokines and chemokines relevant to cAD that had been published between 2015 and 2022 were reviewed.
Results
Advances in technologies have allowed the simultaneous analysis of a broader range of cytokines and chemokines, which revealed an upregulation of a multipolar immunological axis (Th1, Th2, Th17 and Th22) in cAD. Most studies focused on specific cytokines, which were proposed as potential novel biomarkers and/or therapeutic targets for cAD, such as interleukin‐31. Most other cytokines and chemokines had inconsistent results, perhaps as a consequence of their varied involvement in the pathogenesis of different endotypes of cAD.
Conclusions and Clinical Relevance
Inconsistent results for many cytokines and chemokines illustrate the difficulty of studying the complex cytokine and chemokine networks in cAD, and highlight the need for more comprehensive and structured studies in the future.
... Some studies have shown that the number of Treg cells is the same in healthy and atopic dogs, and increases after therapy [16], whereas other reports describe a higher number of Treg cells in cAD patients than in healthy dogs [18,19]. Our research [13,20] showed more Treg cells in atopic than in healthy dogs. After 3 months of ASIT, the number of Treg cells decreased, but after 6 months it increased again. ...
... Mihály and coworkers [24] showed that the all-trans retinoic acid (ATRA) concentration was lower in both lesional and non-lesional skin in human AD patients. The expression of the RARRES2 gene was downregulated in AD skin in comparison with skin from healthy volunteers [20]. Although there are no available data referring to the changes in RARRES2 expression in peripheral blood cells, or the molecular mechanism of chemerin activity in relation to AD, a protective role of the chemokine in other allergic diseases, such as allergic asthma, has been documented. ...
... Results were calculated using the 2 −∆∆Ct method [75]. Primers for SLPI were designed based on the previously published study by Lancto and coworkers [58], and primers for RPS19 were designed based on the previous reports by Brinkhof and coworkers [76], Schmitz and coworkers [77], and Majewska and coworkers [20]. ...
Canine atopic dermatitis (cAD) is a genetic, chronic, and recurrent inflammatory and pruritic skin disorder. Allergen-specific immunotherapy (ASIT) is presently recognized as the only clinically effective disease-modifying treatment for allergies. The aim of our study was to analyze the changes in gene expression observed in the peripheral blood nuclear cells of cAD patients subjected to ASIT. Blood samples designated for transcriptomic analyses were collected from AD dogs twice, before and six months after ASIT, and also from healthy dogs. Statistical analysis revealed 521 differentially expressed transcripts, among which 241 transcripts represented genes with well-described functions. Based on the available literature, we chose nine differentially expressed genes (RARRES2, DPP10, SLPI, PLSCR4, MMP9, NTSR1, CBD103, DEFB122, and IL36G) which may be important in the context of the dysregulated immune response observed in cAD patients. The expressions of five out of the nine described genes (DPP10, PLSCR4, NTSR1, DEFB122, and IL36G) changed after the application of ASIT. The expressions of three of these genes returned to the level observed in the healthy control group. The genes listed above need further investigation to determine details of their role in the molecular mechanism of immune tolerance induction in response to allergen-specific immunotherapy.
... To support this, the upregulation of mRNA or protein expression of IL-33, IL-13, and CCL17 has been reported in the skin or sera of client-owned dogs with AD compared to healthy dogs in multiple studies. [27][28][29][30][31] Some of these cytokines and chemokines (e.g., IL-33, CCL17, IL-6, CCL22) are produced at a very early stage of AD acute flare induction, which is likely to be even before Th2 cells produce IL-31. 32 Therefore, the expression of mRNA was not likely to have been affected by IL-31 inhibition. ...
Background
The caninised monoclonal antibody lokivetmab (LKV), directed at interleukin (IL)‐31, is very effective at controlling pruritus in most dogs with atopic dermatitis (AD). However, evidence exists that IL‐31 is not required for the induction of acute allergic skin inflammation, which might explain why this treatment is less efficacious in some dogs with AD.
Hypothesis/Objectives
To compare the comprehensive transcriptome analysis of house dust mite (HDM)‐sensitised dogs with and without treatment with LKV to attest our hypothesis that LKV does not majorly affect acute cytokine/chemokine production.
Animals
Six HDM‐sensitised atopic Maltese‐beagle dogs.
Materials and Methods
In this cross‐over study, the cytokine profiling of acute AD skin lesions was compared by RNA sequencing (RNA‐Seq), with or without LKV‐induced inhibition of IL‐31. Skin biopsies were obtained from each dog at 0, 6, 12, 24, 48, and 96 h after epicutaneous HDM allergen provocation.
Results
Macroscopic and microscopic skin lesion scores were not significantly different between the LKV‐ and nontreatment groups at any time points. Likewise, the results of RNA‐Seq analysis revealed no significant difference in the messenger (m)RNA expression of the major cytokines between these two groups. In LKV‐treated dogs, IL6, IL9, IL13, IL33, CCL17, and CCL22 were significantly upregulated compared to their baseline expression levels, suggesting that these cytokines are unaffected by IL‐31 inhibition.
Conclusions and Clinical Relevance
IL‐31 inhibition is insufficient to prevent the expression of other proinflammatory mediators in acute AD and these could be considered as other potential therapeutic targets.
... It enhances the proliferation of B lymphocytes and stimulates them to produce IgE. Moreover, IL-4 dysregulates the production of microRNA in keratinocytes, and that leads to enhanced inflammation, angiogenesis, lymphangiogenesis, and apoptosis of epidermal keratinocytes [7][8][9][10]. Additionally, it was proved that canine IL-31 induces pruritus in atopic dogs, leading to epidermal damage through scratching which promotes secondary microbial infections [6]. ...
Canine atopic dermatitis (CAD) is a common, chronic, inflammatory skin disease in dogs worldwide. This disease often predisposes for secondary organisms overgrowth and skin infections with pathogens, such as Staphylococcus pseudintermedius and Malassezia pachydermatis. Unfortunately, the causes of this disease in both humans and animals are not fully understood; therefore, the only possible option is a lifelong, symptomatic treatment. The management of CAD is mainly based on limiting contact with allergens and antipruritic therapy, most often with glucocorticoids and antihistamines. A serious problem in this situation is the fact, that long-term administration of glucocorticoids leads to side effects like polyuria, alopecia, increased susceptibility to infection, muscle atrophy, and many others. For this reason, great emphasis is placed on the development of replacement and supportive therapies. It is a well-documented fact that reduced concentrations of serum vitamin D3 contribute to the severity of atopic dermatitis symptoms in humans. Moreover, unlike the most commonly used therapeutic methods, of which the main goal is to ameliorate inflammation and pruritus, namely the symptoms of AD, vitamin D3 supplementation affects some underlying factors of this disease. Therefore, in this review, we summarize the current state of knowledge regarding the role of vitamin D3 in CAD, its protective effect against secondary bacterial and fungal infections, and the potential of its supplementation in dogs.
