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Anti-alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor encephalitis developed after ovarian cancer cytoreduction surgery: a case report and literature review

BMC Women's Health volume 23, Article number: 507 (2023) Cite this article

Abstract

Background

Anti-alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPAR) encephalitis, a rare subtype of autoimmune encephalitis (AE), is often found associated with tumors such as thymoma, lung cancer, ovarian tumors, and breast cancer, and the tumors were generally detected during the screening process after the encephalitis initiated. The tumor is considered a trigger of AE, but the mechanism remains unclear.

Case Presentation

A 53-year-old woman presented short-term memory loss two days after the primary cytoreduction for high-grade serous ovarian cancer (HGSOC, FIGO stage IC3). Cell-based assay found AMPAR CluA2 IgG positive in both serum (1:3.2) and cerebrospinal fluid (1:32). Moreover, mild AMPAR GluA1 and strong GluA2 expressions were also found positive in the paraffin sections of ovarian tumor tissue, indicating the ovarian cytoreduction surgery might stimulate the release of receptor antigens into the circulation system. The patient’s condition deteriorated within two weeks, developing consciousness and autonomic dysfunction, leading to ICU admission. With oral steroids, intravenous immunoglobulin, plasmapheresis, and rituximab treatment, the patient’s consciousness markedly improved after three months.

Conclusion

We presented the first case of anti-AMPAR encephalitis developed right after the primary cytoreduction of a patient with HGSOC and retrieved paraneoplastic anti-AMPAR encephalitis cases (n = 66). Gynecologists should pay attention to patients who develop cognitive dysfunction or psychiatric symptoms shortly after the ovarian tumor resection and always include AE in the differentiation diagnosis.

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Background

Anti-alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor (AMPAR) encephalitis was first described and identified by Lai et al. in ten patients with limbic encephalitis (LE) in 2009 [1]. Most paraneoplastic anti-AMPAR encephalitis patients present acute or subacute onset of short-term memory loss and/or psychiatric symptoms, with the concurrent or recurring tumors (lung cancer, thymoma, breast cancer, etc.) commonly detected in the following screening process [2, 3]. Anti-AMPAR encephalitis associated with ovarian cancer is rare. Here, we report a patient who developed encephalitis symptoms right after the primary cytoreduction for high-grade serous ovarian cancer (HGSOC).

Case presentation

A 53-year-old woman with no previous history presented with short-term memory loss two days after a primary cytoreduction surgery (Ascites aspiration + surgical exploration + bilateral salpingo-oopherectomy + hysterectomy + omentectomy + para-aortic and pelvic lymph node dissection) for HGSOC (FIGO stage: IC). (Fig. 1) The anesthesia and surgical procedure went uncomplicated. No severe adverse event happened. The memory deficit did not affect the patient’s daily activities, and no progression was detected, so she was discharged ten days after the operation. Two weeks later, she was admitted to the neurology department due to confusion, disorientation, speech dysfunction, agitation, and hallucination. The physical examination showed short-term memory deficits, disorientation, and count disturbance. Chest and abdomen CT scans revealed negative results except for signs of mild pneumonia. The brain MRI and Magnetic resonance spectroscopy imaging (MRSI) revealed hippocampus atrophy and diminished NAA/(Cho + Cr) ratio in the bilateral hippocampus region (right 0.25, left 0.1), suggesting sclerosis and neuron damage. (Fig. 2) Cerebrospinal fluid (CSF) was notable for pleocytosis (309✕106/mL) and elevated protein (0.688 g/L). The paraneoplastic antibody panel for CSF and serum returned positive for AMPAR antibody (CSF IgG 1:32; serum IgG 1:3.2, cell-based assay, Fig. S1), as well as anti-TRDNER antibody (+) and anti-Recoverin antibody (+), and the anti-AMPAR encephalitis was diagnosed. Moreover, the paraffin sections of the patient’s ovarian tumor demonstrated mild expression of AMPAR GluA1 and strong expression of GluA2. (Fig. 3) The patient was treated with Methylprednisolone sodium succinate (750 mg qd for seven days), intravenous immunoglobulin (IVIG) (15 g qd for five days), and acyclovir (0.5 g q8h for 15 days) for suspected limbic encephalitis and virus encephalitis.

Fig. 1
figure 1

Ovarian pathology examination. Immunohistochemistry stain for (a) HE (40×), (b) HE (100×), (c) PAX8(100×), (d) WT1(100×), (e) p53(100×), and (f) Ki67 (100×), confirming that the histopathological type is high-grade serous ovarian cancer (HGSOC).

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Fig. 2
figure 2

(a) Brain magnetic resonance image (MRI) showed coronal T2-FLAIR image revealed bilateral hippocampus volume decreased and (b) Representative spectra (echo time, 135 milliseconds) of right hippocampus region showed diminished NAA/(Cho + Cr) ratio

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Fig. 3
figure 3

Paraffin sections of the patient’s ovarian tumor showed mild expression of (a) GluA1 (1:50), and (b) strong expression of GluA2 (1:50)

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A week after admission, the patient developed a vigil coma with ocular movement disorders, autonomic dysfunction of severe dysphoria, and epilepsy. The electroencephalography (EEG) was repeated twice without detecting epileptiform discharge.

Nine days later, she developed hypotension and respiratory distress, leading to tracheotomy and intubation. Over the next month, she started another IVIG three times, followed by three cycles of plasmapheresis. The clinical improvement was limited. An FDG-PET/CT scan was performed, showing no signs of tumor. She was then treated with three doses of rituximab, improving her consciousness. She could respond to some simple physical examinations when she was discharged to a rehabilitation unit three months after admission. (Fig. 4)

Fig. 4
figure 4

Timelines of clinical course and treatment of the patient with anti-AMPAR encephalitis associated with high grade serous ovarian cancer (HGSOC).

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In a recent follow-up, the patient reported full recovery of her consciousness, speech, and movement abilities, with mild short-term memory loss remaining. She has completed three cycles of chemotherapy. Physical examination, CT scan, and tumor biomarkers found no tumor recurrence.

Discussion and conclusions

We retrieved previously reported cases and identified 66 cases of anti-AMPAR encephalitis associated with tumors [1, 4,5,6,7,8,9,10,11,12,13,14,15]. Among these cases, thymic tumors (n = 30, median age 45 year, including 16 patients with thymoma, 13 patients with thymic carcinoma, and one patient with thymic carcinoid) were the most common, followed by lung cancer (n = 17, median age 65 year, including 11 patients with small cell lung cancer, two patients with non-small cell lung cancer, and four patients with undefined lung cancer), ovarian tumors (n = 8, median age 42 year, including two patients with ovarian adenocarcinoma and six patients with teratoma), breast cancer (n = 7, median age 61 year), medullary thyroid cancer (n = 1, age 69 year), melanoma (n = 1, age 61 year), Ewing sarcoma (n = 1, age 19 year), and seminoma (n = 1, age 36 year). The clinical manifestations varied among different tumor types. (Table 1)

Table 1 Clinical characteristics, treatment, and outcomes in anti-AMPAR encephalitis patients with tumors
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AMPAR antibody titers in the serum or CSF were reported in 14 patients (Table 2). Notably, the CSF titer of several patients was negative; thus, acquiring paired serum and CSF samples of patients suspected of anti-AMPAR encephalitis is essential [16, 17]. The AMPAR antibody would decrease after immunotherapy [3, 18,19,20]. In our reported case, however, we did not obtain the patient’s antibody titer after immunotherapy because her relatives refused lumbar puncture. Severe symptoms such as consciousness and autonomic dysfunction are thought to be related to higher titers of AE antibodies. However, from the previous cases, we observed some patients presenting mild symptoms but with high titers in serum and/or CSF and some patients being in fatal status but had relatively lower titers [17, 20,21,22]. We supposed that the inconsistency was due to the concurrent onconeural antibodies, and the tumor itself might also have an impact on the severity of symptoms.

Table 2 Anti-AMPAR antibody titer, clinical manifestations, ICU admission, and outcomes in anti-AMPAR encephalitis patients with tumors
Full size table

For patients with paraneoplastic anti-AMPAR encephalitis, both immunotherapies and tumor treatment are warranted. Almost all patients (87.5%) diagnosed with anti-AMPAR encephalitis associated with ovarian tumors received second-line immunotherapy, exceeding other tumors. ICU admission was also more likely to be reported in patients with ovarian tumors (85.7%), indicating anti-AMPAR encephalitis associated with ovarian tumors could deteriorate rapidly, and patients are more likely to suffer from fatal situations such as severe autonomic dysfunction and consciousness dysfunction. Thus, the first-line immunotherapies did not bring significant effects (Table 1). Furthermore, we supposed that the limited clinical improvement was also due to the clinical course specificity of the patient. For autoimmune encephalitis patients treated in our hospital and in cases reported previously, we found that the course of the disease varied in patients; some had a course several years long [3, 4, 9, 23]. For patients with a long disease course, treatments such as IVIG and plasmapheresis could not improve their symptoms in the short phase. For this group of patients, a second-line agent was applied. Due to its low toxicity and direct effects on B cells, rituximab is more commonly prescribed as the second-line agent by clinicians to improve patients’ outcomes. Moreover, some clinicians believe that adding second-line immunotherapy can also prevent the early relapse of AE [1]. However, there is no consensus for the treatment of autoimmune encephalitis except pediatric NMDAR encephalitis [24]. A multi-institutional observational study found that for patients who had no improvements within four weeks with first-line therapy, those who received second-line therapy had better outcomes than those who received either continued first-line treatment or discontinued therapy [25]. The result could be explained by the opinion that the second-line therapy should be initiated if patients do not respond to the first-line therapy within 4 weeks. Due to the mechanisms of rituximab and cyclophosphamide, the above result could be interpreted that for this group of patients, rituximab and/or cyclophosphamide should be applied as the first-line therapy [26]. A recent meta-analysis found that therapeutic apheresis alone or combined first-line therapy (corticosteroids and IVIG; corticosteroids, IVIG, and therapeutic apheresis) indicated good outcomes, providing evidence for first-line therapy selection. The study also concluded that timely initiation of second-line therapy was associated with better outcomes [27]. Since anti-AMPAR encephalitis patients associated with ovarian tumors were more likely to be in a fatal state, it is urgent to identify this patient group and initiate immunotherapy and vital support as early as possible.

We report the first case of anti-AMPAR encephalitis developed in an HGSOC patient after cytoreduction surgery. Cytoreduction surgery followed by platinum-based chemotherapy represents the standard treatment for epithelial ovarian cancer (EOC). Recently, new therapeutic strategies have proved to be effective. Adding bevacizumab to standard first-line platinum-based chemotherapy and to second-line therapy has demonstrated better survival outcomes in EOC patients. Although bevacizumab showed promising data in feasibility and safety as a neoadjuvant agent, it warrants further investigation in terms of administration timing considering the complications [28]. Poly (ADP-ribose) polymerase (PARP) inhibitors (PARP inhibitors) are emerging as the first-line maintenance treatment after platinum-based chemotherapy in newly diagnosed and as a maintenance treatment for relapse patients with BRCA mutated or HRD-positive settings [29]. Cytoreduction surgery refers to the curative treatment for peritoneal carcinoma. Its procedures include thorough surgical exploration and total omentectomy, with peritonectomy and organ(s) resection if suspecting carcinomas involvement [30]. Considering some patients’ encephalitis initiation began after cytoreduction surgery, we suggest cytoreduction surgery might be a trigger for AE. The tumor is considered a trigger for AE, our case and others reported GluA1/GluA2 expressions on the tumor tissue [1]. Surgical procedure might make it easier for the antigens on tumor tissue enter into circulation system, inducing the AMPAR antibodies production and encephalitis initiation. However, it is still unclear whether cytoreduction surgery or even tumor resection is related to the initiation of AE [1, 15, 31].

Of the previously reported anti-AMPAR encephalitis associated with ovarian tumors, one patient developed cognitive deficits following the surgery for ovarian adenocarcinoma [6, 9, 32]. Notably, we identified three cases in which patients developed encephalitis symptoms only a few days after tumor resection: two patients with breast cancer and another with thymoma [14, 15, 33]. Generally, patients with paraneoplastic AE develop encephalitis before detecting concurrent tumors or suggesting recurrent tumors [34,35,36,37,38,39]. However, some patients developed acute or subacute encephalitis symptoms after tumor resection [13,14,15, 33, 40]. For this group of patients, symptoms such as short-term memory loss and behavior change would develop in the non-neurology department and are easily neglected. Patients were discharged and readmitted in several weeks in our case and previously reported ones. If the possibility of AE could be suspected earlier, the earlier immunotherapy initiation might improve their outcomes. As a result, clinicians should consider AE as a differentiation diagnosis when postoperative patients with tumors develop acute/subacute symptoms indicating multifocal brain inflammation.

Here, we present an approach to detecting probable AE patients in the gynecology department. (Fig. S2) Perioperative diseases (including pulmonary embolism, ischemic stroke, and electrocyte abnormalities), neurological diseases (including cranial hemorrhage, infectious encephalitis, Hashimoto encephalitis, and brain metastases related to ovarian cancer), and postoperative delirium and cognitive dysfunction should be considered as differential diagnosis [41,42,43,44,45].

Anti-AMPAR encephalitis is rare, with various acute or subacute onset symptoms, including cognitive deficits, psychosis, and decreased consciousness. Most patients can respond to immunotherapy. Some of them, however, might experience life-threatening occasions. As a result, early diagnosis and quick initiation of immunotherapy, and mature basic life support techniques are required. The disease might develop postoperatively if the tumor is a trigger of AE, and cytoreduction surgery might further stimulate the antigens into the circulation system; thus, surgeons should keep alarmed at patients’ cognitive and consciousness conditions, especially those who undertake surgeries for breast cancer, thymoma, or ovarian cancer.

Data Availability

Not applicable.

Abbreviations

AE:

Autoimmune encephalitis

AMPAR:

Anti-Alpha-Amino-3-Hydroxy-5-Methyl-4-Isoxazolepropionic acid receptor

CSF:

Cerebrospinal fluid

HGSOC:

High-grade serous ovarian cancer

IVIG:

Intravenous immunoglobulin

MRSI:

Magnetic resonance spectroscopy imaging

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Acknowledgements

The authors thank Haoyan Liang (West China School of Medicine, Sichuan University) for data collection and Lin L from Stony Brook University for language editing. The authors thank Chengdu Heimeryunying Center for Clinical Laboratory for autoimmune antibody detection.

Funding

This work was supported by The Science and technology project of the health planning committee of Sichuan (21PJ050).

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Authors and Affiliations

  1. Department of Gynecology and Obstetrics, West China Second University Hospital, Sichuan University, Chengdu, 610041, People’s Republic of China

    Yue Huang & Zhengyu Li

  2. Key Laboratory of Birth Defects and Related Diseases of Women and Children (Sichuan University), Ministry of Education, Chengdu, 610041, People’s Republic of China

    Yue Huang & Zhengyu Li

  3. Department of Neurology, West China Hospital, Sichuan University, Chengdu, 610041, People’s Republic of China

    Muke Zhou & Bo Wu

  4. Department of Gynecology and Obstetrics, Chengdu Fifth People’s Hospital, Chengdu, 610041, People’s Republic of China

    Jing Zhou

  5. Department of Anesthesiology, West China Hospital, Sichuan university, Chengdu, 610041, People’s Republic of China

    Xi Yang

  6. Department of Psychosomatic Medicine, Sichuan Academy of Medical Science & Sichuan Provincial People’s Hospital, Chengdu, 610041, People’s Republic of China

    Wenjiao Min

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Contributions

YH, WJM, and ZYL: Study design. JZ: Data extraction. YH, MKZ, JZ, XY, and BW: case analysis. YH, BW, XY, and ZYL: Diagnosis approach design. YH, MKZ, WJM, and ZYL: Manuscript writing and editing. All authors approved the final version of the manuscript.

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Correspondence to Zhengyu Li.

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Approval was granted by the Ethics Committee of West China Second University Hospital, Sichuan University (2022117).

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Written informed consent was obtained from the patient in accordance with the 1975 Declaration of Helsinki.

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Huang, Y., Zhou, M., Zhou, J. et al. Anti-alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor encephalitis developed after ovarian cancer cytoreduction surgery: a case report and literature review. BMC Women's Health 23, 507 (2023). https://doi.org/10.1186/s12905-023-02636-1

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