Comorbidities in patients with uterine adenosarcoma. A single-center case series of 12 patients

doi:10.21203/rs.3.rs-1983452/v1

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Comorbidities in patients with uterine adenosarcoma. A single-center case series of 12 patients

https://doi.org/10.21203/rs.3.rs-1983452/v1

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Background

Uterine adenosarcoma is a rare low-grade tumor that commonly affects elderly women and is associated with a generally good, although sometimes poor, prognosis. This study investigates the effect of comorbidities in old patients with uterine adenosarcoma.

Methods

A review of patients who had been diagnosed with uterine adenosarcoma at our institution between 2010 and 2020 was conducted. All patients underwent a specialist pathological review and were re-staged according to the International Federation of Gynecology and Obstetrics 2009 criteria. Patient demographics, staging, histologic features, primary and adjuvant therapy, disease recurrence, and survival time were collected.

Results

Twelve patients with confirmed uterine adenosarcomas were identified. Their mean age at diagnosis was 58.3 years (range, 31–83 years). Eight patients had pre-existing chronic diseases at the time of diagnosis. All 12 patients underwent surgical therapy. Of these, 10 (83.3%) were stage I, 1 (8.3%) was stage II, and 1 (8.3%) was stage III. Postoperative adjuvant therapies included chemotherapy (n = 1), radiation (n = 1), or no further therapy (n = 10). The mean follow-up duration was 39.2 months (range, 7–104 months). The recurrence and mortality rates were 16.7% (2/12) and 41.7% (5/12), respectively. Five recurrence-free patients died of comorbidities. The mean postoperative survival of these 5 patients was 22.6 months. The remaining seven patients were free of recurrence at the time of this report.

Conclusions

Comorbidities with age is a significant factor leading to poor prognosis in uterine adenosarcomas. Greater attention should be paid to elderly patients with comorbidities. Targeted interventions, including multi-professional management, tailored assessment, and follow-up, may contribute to improved well-being.

uterine adenosarcoma

comorbidity

age

Uterine adenosarcoma is a rare uterine malignancy. This tumor commonly affects elderly women following menopause [1–3]. Uterine adenosarcoma is considered to have a good prognosis. However, some uterine adenosarcomas have a poor prognosis. The clinical features of uterine adenosarcoma remain to be sufficiently described. In this study, we found that comorbidities with age was associated with decreased survival in patients with uterine adenosarcomas. Age is a prognostic factor for many forms of cancer, which is usually attributed to age-associated comorbidities. Older adults with cancer are likely to have a history of chronic diseases that make their disease more complex to treat [4]. Currently, most patients in the oncology setting are older adults [5]. There is a growing demand for chronic disease care for patients with cancer [6]. Our study highlights the importance of treating comorbidities which could in some cases be fatal.

This retrospective study was conducted in accordance with the Declaration of Helsinki and Good Clinical Practice. It was approved by the Institutional Review Board of the Second Hospital of Hebei Medical University. Written informed consent was obtained from the patients or the next of kin of the patients for the publication of this study and any accompanying images. The charts of patients who had been diagnosed with uterine adenosarcoma at the Second Hospital of Hebei Medical University from 2010 to 2020 were retrospectively reviewed. Diagnosis was confirmed by an experienced soft tissue pathologist in each case. Patients were excluded if uterine adenosarcoma histology was re-classified based on an expert review. The stage was assigned based on the International Federation of Gynecology and Obstetrics 2009 criteria. Patients who did not undergo surgical staging were assigned a clinical stage based on their pathology and imaging reports. Demographic information, clinical history, treatments, postoperative diagnosis, and outcomes of these patients were collected. Descriptive statistics were used to summarize the demographic and clinical features of the patients. Disease recurrence was determined by reviewing the chart for pathology reports or radiographic studies demonstrating disease recurrence. Survival time was calculated from the date of the original diagnosis to the date of patient death or the last clinical appointment.

Clinical features

Thirteen cases of uterine adenosarcoma were identified. One case was excluded because of a controversial pathologic diagnosis. The remaining twelve had complete data available and were included in this study. The median age at diagnosis was 58.3 years (range, 31–83 years). The most common symptom presented by these patients was abnormal uterine bleeding. Eight patients had a history of chronic diseases. Chronic diseases included hypertension, coronary artery disease, diabetes, venous thromboembolism, and stroke. Moreover, one patient had been previously diagnosed with breast cancer. This patient had undergone surgery and irradiation 25 years earlier and had no evidence of breast cancer at the time of diagnosis. Further details presented in Table 1.

Primary therapy

All 12 patients underwent primary surgery: 9 underwent total abdominal hysterectomy and bilateral salpingo-oophorectomy alone, while 3 underwent additional, more aggressive resection in the form of pelvic lymph node dissection surgical staging (n = 2), and debulking (n = 1). All 12 patients had evidence of myometrial invasion, while 5 had adenosarcoma with sarcomatous overgrowth (AS + SO). One patient (stage IIB, AS + SO) had lymph node involvement in 2 of the 23 pelvic lymph nodes sampled. Further details are presented in Table 2. By stage, seven patients were diagnosed with IB disease, followed by three patients with IC, one with IIB, and one with stage IIIC.

Adjuvant therapy

Adjuvant chemotherapy was administered to the two patients with stage IIB and stage IIIC disease. The stage IIB patient with AS + SO received whole-pelvis radiation alone. The stage IIIC patient also received gemcitabine and docetaxel combined chemotherapy.

Recurrence and survival data

The median follow-up was 39.2 months (range 7 to 104) for the 12 patients. Recurrence occurred in two (16.7%) stage I patients: stage IB and IC, who respectively relapsed at 8 and 13 months postoperatively. The sites of recurrence were the vaginal stump and pelvic cavity, respectively. Both patients with local recurrence were disease-free after surgery and radiotherapy at the time of this report. Five (41.7%) of the 12 patients who were recurrence-free died of comorbidities. They died within postoperative intervals of 7 - 56 months (mean, 22.3 months). Two died of stroke, two died of coronary artery disease, and one died of multiple organ failure. The remaining seven patients (including two who underwent a second operation after recurrence and postoperative radiotherapy) were free of recurrence at the last follow-up.

Uterine adenosarcoma is a rare mixed neoplasm in which a benign or non-neoplastic epithelial component is mixed with a malignant stromal element [7]. These neoplasms present as solid, typically edematous polypoid masses that usually arise from the fundus. It commonly affects elderly women following menopause [8–10]. The largest study to date involving an analysis 994 patients from the Surveillance, Epidemiology, and End Results(SEER) database showed that the average age of uterine adenosarcoma patients was 58.4 years, and 48.3% of the patients were ≥ 60 years old[11]. Another SEER database analysis showed that out of 544 adenosarcoma patients less than 10% were aged less than 40 years, and 38.4% were aged greater than 65 years [12]. The most frequently presented symptom of uterine adenosarcoma is abnormal uterine bleeding [7, 13–15]. The next most commonly presented symptom is pelvic pain, noted in 12–33.3% of patients [13, 16, 17]. On examination, patients may have an enlarged uterus, endocervical polyps, or cervical polyps. In this case report, the mean age of patients at diagnosis was 58.3 years (range, 31–83 years). Most clinical features of our patients were similar to those previously reported except that chronic diseases are highly prevalent in our patients. Eight of the 12 patients had pre-existing chronic diseases at the time of diagnosis.

Treatment patterns for uterine adenosarcoma include hysterectomy-based surgery and postoperative adjuvant therapy. Hysterectomy with bilateral salpingo-oophorectomy is the initial treatment of choice for uterine adenosarcoma. Unless there is a high clinical suspicion of lymph node involvement, lymphadenopathy is not recommended. In this retrospective study, all 12 patients underwent surgical therapy, including total abdominal hysterectomy with bilateral salpingo-oophorectomy (n = 9), surgical staging (n = 2) and tumor debulking (n = 1). The role of adjuvant radiation, chemotherapy, or endocrine therapy in the treatment of uterine adenosarcoma is unclear. Currently, treatment guidelines for uterine adenosarcoma are based on the treatment of other uterine sarcomas or uterine carcinomas. However, most uterine sarcoma or carcinoma trials evaluating the role of chemotherapy or radiation in adjunctive therapy have not included patients with adenosarcoma [18–21]. Therefore, data on the effectiveness, benefit, or harm of adjuvant therapy in adenosarcomas of the uterus are lacking. The use of adjuvant chemotherapy in patients with uterine adenosarcoma has been documented only in case series and case reports. Responses to chemotherapy, including liposomal doxorubicin, trabectedin, anthracyclines, and ifosfamide, have been reported [22–25]. Complete responses have been noted with gemcitabine/docetaxel and doxorubicin-based regimens in reports from patients with metastatic or recurrent uterine adenosarcoma, suggesting that these regimens are the most reasonable to consider in adjuvant therapy. Additionally, evidence for hormonal therapy is limited to case reports[26]. Therefore, adjuvant therapy for uterine adenosarcoma should be provided with caution. Some clinical characteristics exist to guide treatment decisions in uterine adenosarcoma, such as sarcomatous overgrowth, lymphovascular invasion, myometrial invasion and lymph node involvement. Retrospective data showed that uterine adenosarcoma patients without these high-risk factors do not derive any benefit from adjuvant pelvic radiotherapy and chemotherapy. However, patients with these high-risk factors have a significantly higher rate of recurrence and worse survival with surgery alone compared to patients with no high-risk factors [7, 14, 27–29]. Therefore, in these high-risk patients, the role of pelvic radiotherapy and chemotherapy in patient survival requires investigation [28]. In this retrospective study, recurrence occurred in two stage I patients with sarcomatous overgrowth and myometrial invasion: stage IB and IC. One stage IIB patient with sarcomatous overgrowth had undergone surgery and radiation, and was disease-free for 21 months at the time of this report. Hence, in high-risk patients, adjuvant chemotherapy should be considered as long as they can tolerate it, despite limited clinical evidence [10].

Most patients with uterine adenosarcoma present with early-stage tumors and have a good prognosis [30–32]. Patients with stage I adenosarcoma have a 63% – 86% 5-year overall survival, patients with stage II adenosarcoma have a 50% – 69% 5-year overall survival, patients with stage III adenosarcoma have a 0% – 48% 5- year overall survival, and patients with stage IV adenosarcoma have a 15% 5-year overall survival [12, 14]. The most important prognostic factors of uterine adenosarcoma are age [12, 33], sarcomatous overgrowth [13, 22, 34], myometrial invasion [14, 22, 29], lymphovascular invasion [13, 28], and lymph node involvement [1, 11]. An analysis involving 544 patients with adenosarcoma from the SEER database showed that older age was associated with a worse prognosis [12]. In a study of prognostic factors for uterine adenosarcoma patients aged ༞ 53 years had significantly poorer disease-free survival and overall survival than patients aged ≤ 53 years [33]. The median overall survival was 14.1 years for patients aged 53 years or younger compared to 6.4 years for patients aged older than 53 years (p = 0.042). Adenosarcomas with sarcomatous overgrowth are slso associated with worse disease-free survival and overall survival [13]. A small series of adenosarcoma patients without sarcomatous overgrowth have shown recurrences ranging from 7.1–50% [17, 22, 27, 28], whereas, for those with sarcomatous overgrowth, recurrences ranged from 40–81.8% [13, 17, 22, 27, 28, 34, 35]. Correspondingly, adenosarcoma patients with sarcomatous overgrowth have poorer overall survival. A study of 74 patients showed that patients with sarcomatous overgrowth had a median overall survival of 55.4 months, whereas patients without sarcomatous overgrowth had a median overall survival of 112.4 months, with a hazard ratio of 2.45 on multivariate analysis (95% CI 1.26–4.76), p = 0.008[13]. Additionally, myometrial invasion and lymphovascular invasion are reportedly associated with an increased risk of tumor recurrence [14, 28, 29]. Moreover, the extent of extra-uterine spread is associated with worse clinical outcomes in multivariate analysis [11, 13]. In our retrospective study, two patients with sarcomatous overgrowth and myometrial invasion experienced recurrence at 8 and 13 months postoperatively, respectively. Recurrence occurred at the vaginal stump and pelvic cavity, respectively. Both patients were alive without disease after surgery and postoperative radiotherapy at the time of this report. Five patients who were recurrence-free died of comorbidities, with the causes of death including stroke, coronary artery disease, and multiple organ failure.

In this retrospective study, comorbidities with age were predictors of a poor prognosis. The mean age of the 5 dead patients at diagnosis was 71.8 years (range 65–83 years). The average number of chronic diseases in the five patients was 2.8 (range 2–4). Advanced age is associated with decreased survival in uterine adenosarcomas [36, 37]. Comorbidities with age is a significant prognostic factor for poor prognosis in cancer patients. Chronic disease is a common phenomenon in elderly patients with cancer. Among patients aged 65 years and older, 40% of patients with cancer have at least one chronic disease, and 15% have two or more [38]. Comorbidities may influence a patient’s outcome, limiting the use of cancer surgery, decreasing the use of chemotherapy, increasing treatment-related toxicities, causing patients to abandon therapy, or even causing death[38–40]. For example, in this study, a patient suffered from arrhythmia and sick syndrome, which constrained her ability to undergo tumor surgery. In addition to the impact of comorbidities on cancer outcome, cancer and cancer treatments affect functional status and worsen comorbidities [41]. For example, radiation therapy can cause chronic radiation damage to organs around the tumor [42] and induce secondary malignancies [43]. Furthermore, some effects are mild and not easily detected and are easy for both doctors and patients to ignore. However, they are long-lasting, cumulative, and do not appear until a certain point. In this retrospective study, venous thrombosis is a typical example. Patients with cancer are 4 to 7 times more likely to develop venous thromboembolism(VTE) than patients without cancer [44, 45]. Additionally, cancer patients with a history of VTE are at a high risk of developing new venous thrombosis and bleeding during anticoagulant therapy [46]. Patients with cancer who develop VTE are at a greater risk of early mortality than those without VTE [45]. In this study, four patients had a history of vein thrombosis. Finally, all 4 patients died from thrombotic disease: two from stroke and two from coronary artery disease. The management of cancer in older people is becoming a common problem owing to an aging population. Most patients with cancer have pre-existing chronic diseases at the time of diagnosis. Elderly cancer patients with multiple chronic diseases require more complex and specialized care [47]. Cancer patients need to be provided with chronic disease care. In addition, cancer care systems need to rise up to many challenges to meet current needs. This study was limited by the small sample size and the short median follow-up time. Future studies will add to the collective knowledge of uterine adenosarcoma and assist with management of this rare disease.

Advanced age is associated with decreased survival in patients with uterine adenosarcomas. Comorbidities commonly co-occur in aged patients with cancer. Comorbidities in uterine adenosarcoma patients are associated with a poorer quality of life and survival. Poorly managed comorbidities in cancer patients can lead to serious consequences. Greater attention should be given to comorbidities in such patients. Targeted interventions, including multi-professional management, tailored assessment, and follow-up, may contribute to improved well-being in these individuals.

AS + SO: adenosarcoma with sarcomatous overgrowth; SEER: Surveillance, Epidemiology, and End Results; VTE: venous thromboembolism.

Acknowledgments

The authors thank the histology laboratory of the Second Hospital of Hebei Medical University, and grateful to Zengfang Hao for providing pathological review.

Authors' contributions

Hongfa Peng and Zhu Wang corrected clinical data and drafted the manuscript. Jingjing Jiang helped with editing the manuscript. And Hui Du supervised and revised the final version of the manuscript. All authors have read and approved the final manuscript.

Funding

The authors declare that this study has received no financial support.

Ethics approval and consent to participate

This study was approved by Ethics Committee of Second hospital of Hebei medical university. Informed consent for participation in the study was obtained from all participants. All patients provided written informed consent for the publication of any associated data and accompanying images.

Consent for publication

Not applicable.

Competing interests

The authors report no conflicts of interest in this work.

Availability of data and materials

All data generated or analysed during this study are included in this published article.

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The patients’ demographic and clinical features are summarized in Table 1.

ID	Age	Complictions	Presentation	Surgery	FIGO stage	Adjuvant therapy	Recurrence (interval)	Status Months	Cause of death
1	66	NO	PMB	TAH+BSO	IB	NO	NO	NED(52)
2	48	NO	AUB	TAH+BSO	IB	NO	NO	NED(31)
3	71	Arrhythmia, DLBCL	Abdominal mass	Debulking	IIIC	YES(CT)	NO	DOD(10)	MOF
4	31	NO	AUB	SS	IC	NO	YES(13m)	NED(104)
5	83	Breast cancer, stroke, Hypertension, CAD	PMB	TAH+BSO	IB	NO	NO	DOD(7)	Stroke
6	68	Hypertension, Diabetes, VTE	PMB	TAH+BSO	IB	NO	NO	NED(23)
7	66	VTE, Hypertension, CAD	LDVT	SS	IIB	YES(RT)	NO	DOD(21)	Sudden death
8	35	NO	AUB	TAH+BSO	IC	NO	NO	NED(17)
9	65	Stroke, Hypertension	PMB	TAH+BSO	IB	NO	NO	DOD(56)	Stroke
10	38	Chronic hepatitis B	AUB	TAH+BSO	IB	NO	NO	NED(98)
11	72	Diabetes, CAD	PMB	TAH+BSO	IB	NO	NO	DOD(19)	CAD
12	57	Hypertension, Diabetes	Vaginal polyp	TAH+BSO	IC	NO	YES(8m)	NED(32)

Diffuse large B cell lymphoma: DLBCL; Cerebral Venous Thrombosis: CVT; Coronary artery disease: CAD; Venous thromboembolism: VTE; Postmenopausal bleeding: PMB; Abnormal uterine bleeding: AUB; Chemontherapy: CT; Multiple organ failure: MOF; Surgical staging:SS; Radiotherapy: RT; Lower deep vein thrombosis: LDVT

The patients’ pathological features are summarized in Table 2.

ID	Tumor size(cm)	Sarcomatous overgrowth	LVSI	Myometrial invasion	lymph node involvement
1	10.6x8.5x10	NO	（﹣）	<1/2
2	2.2x1.5x1.3	NO	（﹣）	<1/2
3	7.4x5.2x3.0	YES	（﹢）	<1/2	YES
4	4.6x3.2x2.4	YES	（﹣）	>1/2
5	7.8x4.7x5.1	YES	（﹣）	<1/2
6	4x4x3	NO	（﹣）	<1/2
7	11x7.4x6.3	YES	（﹢）	<1/2	YES
8	7.6x5.4x4.5	NO	（﹣）	>1/2
9	5.2x4.1x2.3	NO	（﹣）	<1/2
10	5.0x3.5x2.7	NO	（﹣）	<1/2
11	9.0x7.4x5.6	NO	（﹣）	<1/2
12	8.2x7.4x6.7	YES	（﹣）	>1/2

Lymphovascular invasion: LVSI

No competing interests reported.

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Comorbidities in patients with uterine adenosarcoma. A single-center case series of 12 patients

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