Factors Affecting Recurrence of Idiopathic Granulomatous Mastitis: A Systematic Review

Fattahi, Asieh Sadat; Amini, Ghasem; Sajedi, Fatemeh; Mehrad-Majd, Hassan

doi:https://doi.org/10.1155/2023/9947797

The Breast Journal

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Abstract Introduction Methods Results Discussion Data Availability Conflicts of Interest Acknowledgments References Copyright Related Articles

Review Article | Open Access

Volume 2023 | Article ID 9947797 | https://doi.org/10.1155/2023/9947797

Factors Affecting Recurrence of Idiopathic Granulomatous Mastitis: A Systematic Review

Asieh Sadat Fattahi,¹Ghasem Amini,¹Fatemeh Sajedi,²and Hassan Mehrad-Majd³

Academic Editor: Neslihan Cabioglu

Received28 Dec 2022

Revised12 Aug 2023

Accepted03 Sept 2023

Published26 Sept 2023

Abstract

Idiopathic granulomatous mastitis is a rare and benign disease that primarily affects young women of reproductive age. Various factors have been suggested as possible causes, including pregnancy, breastfeeding, history of taking birth control pills, hyperprolactinemia, smoking, and history of trauma. Due to unknown etiology, opinions on its treatment have varied, resulting in differing recurrence rates and side effects. Therefore, conducting a comprehensive systematic review and meta-analysis can aid in understanding the causes and recurrence of the disease, thereby assisting in the selection of effective treatment and improving the quality of life. A systematic literature review was conducted using predefined search terms to identify eligible studies related to risk factors and recurrence up to June 2022 from electronic databases. Data were extracted and subjected to meta-analysis when applicable. A total of 71 studies with 4735 patients were included. The mean age of the patients was 34.98 years, and the average mass size was 4.64 cm. About 3749 of these patients (79.17%) were Caucasian. Patients who mentioned a history of pregnancy were 92.65% with 76.57%, 22.7%, and 19.7% having a history of breastfeeding, taking contraceptive pills, and high prolactin levels, respectively. Around 5.6% of patients had previous trauma. The overall recurrence rate was 17.18%, with recurrence rates for treatments as follows: surgery (22.5%), immunosuppressive treatment (14.7%), combined treatment (14.9%), antibiotic treatment (6.74%), and observation (9.4%). Only antibiotic and expectant treatments had significant differences in recurrence rates compared to other treatments ( value = 0.023). In conclusion, factors such as Caucasian race, pregnancy and breastfeeding history, and use of contraceptive hormone are commonly associated with the disease recurrence. Treatment should be tailored based on symptom severity and patient preference, with surgery or immunosuppressive options for recurrence.

1. Introduction

Idiopathic granulomatous mastitis (IGM) is a rare and benign inflammatory mammary disease with an unknown etiology [1]. Also known as granulomatous lobulitis or lobular granulomatous mastitis [2], it can be misdiagnosed as furuncle or cellulitis [3]. IGM primarily affects premenopausal women, typically between the ages 32 and 36 [4]. Various studies have identified factors that may contribute to the development of IGM, such as age, recent pregnancy [5, 6], duration of breastfeeding, history of contraceptive pills usage [6–9], smoking, and trauma [9, 10]. Hyperprolactinemia and diabetes have also been linked to the disease [5]. It is thought that milk stasis after pregnancy and lactation, combined with hyperprolactinemia, can lead to hypertrophic breast tissue and the development of IGM [1]. While IGM has been reported in all races [8], it appears to be more prevalent in certain regions, including the Mediterranean and Asian regions [9].

The disease’s clinical manifestation is similar to a breast lump with inflammatory symptoms and abscess [11, 12] and is typically located in the breast’s upper outer quadrant. Occasionally, it can be found in other quadrants, and in some cases, bilaterally [11]. The likelihood of both breasts being affected simultaneously is minimal [9], but the left breast is more commonly involved [2]. Unfortunately, this disease has no cure [3, 12]; however, in minor cases, it may resolve on its own without any treatment. For severe cases, medical or surgical intervention may be required [13].

Decisions regarding the management of this condition are dependent on the severity of the disease as well as the patient’s preferences. Surgery still plays an integral role in its disease [3]. Despite receiving appropriate treatments, these masses may persist, recur, or sometimes lead to the development of fistulas, necessitating follow-up in affected patients [14, 15]. Moreover, the presence of erythema nodosum can further complicate the disease, making its treatment challenging [12].

In general, despite numerous studies in this field, a specific reference for the possible causes of this disease has not yet been defined. Although several risk factors have been proposed, there is no comprehensive summary that reviews the available evidence or a systematic review of studies. In addition, there is no consensus on a treatment method. Therefore, we conducted this comprehensive systematic review and meta-analysis to evaluate the risk factors for IGM and assess the likelihood of recurrence.

2. Methods

We conducted this review following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines to identify studies relevant to underlying factors and recurrence in patients with granulomatous mastitis.

Two investigators performed a comprehensive electronic database search, including PubMed, Cochrane, Embase, and Google Scholar databases. The search period covered up to June 2022, and there was no time limit in the study selection. Our searches were conducted individually or in different combination using the following terms: “mastitis,” “granulomatous lobular mastitis,” “idiopathic granulomatous mastitis,” “recurrence,” “risk factors,” or etiology. We identified some additional studies from other sources and excluded studies with insufficient information. Only studies published in English were considered for this review. The selection process for the studies is summarized in Figure 1.

This study included published studies that satisfied the given criteria. Studies related to idiopathic granulomatous mastitis that were conducted with clinical trial methods, descriptive, cohort with or without control, and case control were included in this study. However, studies that described granulomatous mastitis in male or transgender patients were excluded. In addition, letters to the editor, review articles, and clinical reports with less than 4 patients were not included. Furthermore, studies that focused on other types of mastitis, articles that solely discussed radiological manifestations, articles without clinical or therapeutic explanations, and articles in languages other than English were also excluded. The following data were extracted for each study: name of the first author, country of origin of the study, year of publication, and the number of patients. The outcome measures that were extracted were the age of presentation, any association with autoimmune diseases, smoking habits, history of trauma, parity, lactating history, BMI, prolactin levels, clinical symptoms (i.e., presence of a mass, pain, or other symptoms), recurrence, and treatment (antibiotics, corticosteroids, or surgery).

In situations where quantitative data were appropriate for meta-analysis, the averages and ranges were calculated considering the analytic weight. The analytic weight is determined by the inverse proportionality to the variance of each observation. Typically, the observations represent averages, and the weights correspond to the number of elements contributing to each average. All statistical analyses were performed using SPSS 25 software. Finally, we interpreted the obtained results within the framework of the study’s overarching criteria.

3. Results

Out of the 71 studies reviewed, a total of 4735 patients were included in this study (Table 1). Of these, 69 articles (4566 patients) reported the average age of patients at the time of symptom onset. The average age across these articles was 34.98 years. The incidence of the disease across different age ranges was not investigated. Racial distribution was reported in all 4735 patients, with 3749 (79.17%) being Caucasian, 543 (11.46%) Asian, and 350 (7.39%) Hispanic. There were also 38 Indian, 20 Moroccan, 14 African American, and 21 Jewish patients. Of the 55 publications that examined pregnancy history, 3251 out of 3554 reported on this aspect, accounting for 91.47% of the patients.

Out of the 71 articles, 44 of them mentioned the history of breastfeeding, while only 27 of them did not mention. Among the 3252 patients that were examined in those 44 articles, 2721 of them had a positive history of breastfeeding, indicating an 83.67% rate of breastfeeding. In addition, about 41 articles discussed the history of taking birth control pills, with a total of 3203 patients being examined. Of those patients, 730 had a history of taking contraceptive pills, accounting for 22.79% of patients. The smoking history of patients was examined in 38 studies, covering 2687 patients. Among these patients, 373 had a history of smoking, which is 13.88% of patients. Furthermore, 16 articles mentioned the history of trauma, manipulation, or surgery in the breasts, including a total of 628 patients. Among these patients, 36 had a positive history of the same, amounting to 5.7%. Prolactin tests were performed in 16 studies with a total of 502 patients being subjected to testing. Among them, 99 patients had high prolactin levels, accounting for 19.7% of patients (19.7%) (Table 2).

Out of the 71 included articles, 37 articles reported the granulomatous mastitis mass sizes for a total of 2151 patients. The average mass size for these patients was calculated to be 4.64 cm. In 10 studies, the body mass index (BMI) of the patients was discussed, with 4 studies reporting on the average BMI of 198 patients which was found to be 28.24. In addition, 4 articles examined the BMI in two age ranges—less than 25 years and more than 25 years—for a total of 146 patients. Among these patients, 37.67% had a BMI less than 25, while 62.33% had a BMI more than 25. Five articles studied the BMI in different ranges less than and greater than 30, with a total of 231 examined patients. Among these patients, 127 (55%) had a BMI less than 30 and 104 (45%) had a BMI greater than 30. A total of 60 articles examined recurrence, reporting on 4038 patients, with 694 cases experiencing recurrence, resulting in a calculated recurrence rate of 17.18% (Table 2). The variables were also studied based on the Caucasian race and other races, and there was no significant relationship with relapse ( = 0.171) (Table 3). The prevalence of different symptoms in patients (mass, pain, inflammatory symptoms, lymphadenopathy, skin symptoms, and systemic and infectious symptoms) in the Caucasian race and other races was compared. Except for which is significantly higher in other races than the Caucasian race ( value = 0.003), the prevalence of symptoms other than lymphadenopathy in the Caucasian race was not significantly different from other races ( > 0.05). However, lymphadenopathy was found to be significantly higher in other races than in the Caucasian race ( = 0.003).

To categorize the various treatments available for granulomatous mastitis, they were divided into five distinct groups. The first group consisted of surgical procedures, such as drainage, excision, lumpectomy, and others. The second group of treatment was immunosuppressive drug treatment including prednisolone, methotrexate, and so on. The third group included combined surgical and immunosuppressive treatments. The fourth group was dedicated to observation, while it focuses solely on antibiotic treatment. Many patients initially received antibiotic treatment before biopsy or any other treatment. Patients who did not undergo any other therapy, such as surgery or immunosuppressive drug therapy, were placed in the antibiotic group.

The overall recurrence rate among patients was found to be 17.18%. Among different treatment options, the recurrence rate of surgical treatment alone was 22.5%, the recurrence rate for immunosuppressive treatment was 14.7%, the recurrence rate for combined treatment was 14.9%, the recurrence rate for observation was 9.4%, and the recurrence rate for antibiotic treatment alone was calculated to be 6.74%. Table 4 provides a detailed breakdown of these results. Only the recurrence rates for antibiotic and expectant treatment showed significant differences when compared to other treatments ( = 0.023). In addition, when comparing the recurrence rates of all treatments with those for surgical treatment alone, it was found that the recurrence rate for antibiotic and expectant treatments exhibited a significant difference compared to the recurrence rate for surgical treatment. Table 4 provides further details on these comparisons.

4. Discussion

This study reviewed 71 articles and 4735 patients with granulomatous mastitis, a chronic inflammatory breast disease of unknown etiology. The incidence of this disease has increased in recent years (9 studies before 2010 compared to 62 studies after 2011), presenting a diagnostic and treatment challenge for clinicians. Our results supported that the disease is four times more prevalent in the Caucasian race, especially in the Mediterranean and Middle East regions, and commonly affects women in their reproductive age. Pregnancy (91.4%) and breastfeeding (83.6%) were the main underlying factors for the disease, followed by use of oral contraceptive pills (OCP) and high prolactin levels. Smoking, trauma, and weight gain had minimal association with the disease.

After considering the epidemiological and racial differences, a reanalysis was conducted on the underlying causes, symptoms, and recurrence rates between the Caucasian race and other races for IGM. The study found that there was no significant difference between the main causes, namely, pregnancy, breastfeeding, and hormone intake in two groups. Therefore, additional cohort and prospective studies are required to investigate other genetic or environmental factors such as nutrition and lifestyle, which might explain why the prevalence of IGM is four times higher in the Caucasian race. In terms of disease manifestation, mass disease purification was the most common symptom, followed by pain, inflammatory symptoms, lymphadenopathy, and skin involvement, respectively. A comparative analysis between Caucasian and other races exhibited similar clinical symptoms between the two groups, except for lymphadenopathy, which was more frequently observed in the non-Caucasians ( = 0.003). However, since only two studies mentioned this in the group of other races (43 patients out of 108 patients), and with the sample size being small, this outcome needs to be interpreted with caution. Regarding recurrence, an average of 17% of patients experienced it, in all the studies, indicating that current treatments are not associated with complete disease eradication and there could be a recurrence. Even though the recurrence rate is higher in the Caucasian group, it is not statistically significant, and it seems that the race or geographic distribution does not directly correlate with recurrence.

Various treatments have been mentioned for this disease, ranging from observation to systemic immunosuppressive treatment and surgery. Thus, we classified the treatments into several categories, including surgical treatment, immunosuppressive treatment, combined treatment, antibiotic treatment, and expectant treatment. As most patients received a course of empiric antibiotics before biopsy and diagnosis, we have classified studies in the antibiotic category, which only continued antibiotic treatment and did not receive any other systemic treatments or surgery.

Our results showed that surgery alone, immunosuppressive treatment alone, and combined treatment (surgical + immunosuppressive) did not have a statistically significant difference in recurrence rates. However, surgery without immunosuppressive treatment had a slightly higher recurrence rate, although the difference was not significant. Combined treatment may have treatment-related complications but did not statistically significantly reduce the recurrence rate. In line with our results, Li (review of 15 articles) [81] and Xiaojia (review of 21 articles) [82] mentioned that surgery was the best treatment for faster complete remission and adding steroid treatment did not make a difference in complete remission. They also reported that the rate of surgical recurrence was small and recommended medical treatment for patients concerned about scarring or future breastfeeding.

Furthermore, in our review, antibiotic treatment alone (without immunosuppression and surgery) and expectant treatment had a lower recurrence rate. However, the number of articles compared to other treatments in each category was small; 5 studies with 53 observed patients and 12 studies with 178 patients treated with antibiotics. Lei et al. [82] recommended systemic steroid treatment in the case of symptoms involving the whole breast, such as inflammation, skin involvement, and multiple fistulas. They also suggested this treatment in patients with limited symptoms at the beginning of treatment [81, 82]. Therefore, treatment should be chosen based on the patient’s preference, severity of symptoms, and the physician’s opinion while considering side effects related to each category such as scarring, deformity, and immunosuppressant drug treatment’s side effects and longer treatment duration.

In conclusion, our review of IGM disease has identified that factors such as Caucasian race, pregnancy and breastfeeding history, and use of contraceptive hormone are commonly associated with the disease. Symptoms and manifestations do not appear to vary significantly across different races. Incidence rates appear to be increasing as more studies are carried out. With regard to treatment and recurrence, we suggest that a treatment regimen such as surgery or immunosuppressive treatment should be selected based on the severity of symptoms and patient’s preference, taking into consideration the complications of each treatment line. Antibiotic and expectant treatments may be used initially and for minor symptoms.

Data Availability

All data generated or analyzed during this study are included within the article. Further inquiries can be directed to the corresponding author.

Conflicts of Interest

The authors declare that they have no conflicts of interest.

Acknowledgments

We thank staff of the Clinical Research Development Unit of Ghaem Hospital, Mashhad University of Medical Sciences, to facilitate the data analysis. This work was supported by MUMS (research project no. 4000039, as a surgical thesis).

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Copyright © 2023 Asieh Sadat Fattahi et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

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