INTRODUCTION

The number of papers and case reports has progressively increased since the 2007 publication of Hughes

[19] (Table 1). In 2014, a systematic review of 173 cases of ovarian teratoma-associated anti-NMDAR encephalitis was published. Most articles containing case reports have been published in neurology or psychiatry journals. This is consistent with the results of the 2014 article[19].

In a case series of 100 anti-NMDA-R encephalitis patients, 69% of the patients were reported with autonomic instability and these patients required an average of 2 mo of ventilator support, with around 37% of the patients diagnosed with cardiac arrhythmias and four reported to be requiring pacemakers[7]. On the other hand, in a report that included 360 patients, two died because of sudden cardiac death while the reason for the death of one other patient was not fully determined[30].

Herpes simplex encephalitis (HSE) plays a vital role in triggering the synthesis of anti-NMDAR antibodies[13,14]. A study of 501 patients with anti-NMDAR encephalitis found that 38% of patients had concomitant tumors, most commonly ovarian teratomas. Other relatively rare neoplasms include extraovarian teratomas, testicular germ-cell tumors, small-cell lung cancer, and Hodgkin’s lymphoma[15]. From a cohort study of 577 patients with anti-NMDAR encephalitis, 220 patients (38%) had an underlying neoplasm, among which 207 tumors (94%) were ovarian teratomas[4]. A review of 432 cases of anti-NMDAR encephalitis revealed that of the 293 female patients, 68 (23%) had ovarian teratoma[16].

The first case of anti-NMDAR encephalitis with ovarian teratoma was reported in China in 2010[17]. A single-center prospective study that included patients with anti-NMDAR encephalitis with ovarian teratoma from 2011 to 2016 admitted to Peking Union Medical College Hospital, Beijing, discussed the clinical characteristics, treatment, and prognosis of the disease[18]. The association between ovarian teratoma and anti-NMDAR encephalitis is relatively unknown and most of the present studies on anti-NMDAR encephalitis with ovarian teratoma are case reports and systematic reviews. Here, we illustrate six cases of ovarian teratoma-related anti-NMDA receptor encephalitis, and also present the results of a systematic review and analysis of cases reported after 2013.

在支付、資產管理等領域，大技術公司可能因為監管標準的不統一而享有不平等、不公平的競爭優勢。對大技術公司金融業務監管應實時介入，以避免相關風險從小到不值得關注演變到大而不能忽視，甚至大而不能倒。

MATERIALS AND METHODS

Case description

the Shanghai Municipal Commission of Health and Family Planning, No. 2017ZZ02016; the Funding from National Key Research and Development Program of China, No. 2021YFC2700400; the National Natural Science Foundation of China, No. 81974454; and the Shanghai Municipal Key Clinical Specialty, the Clinical Research Plan of SHDC, No. SHDC2020CR6009-002.

表2顯示我國國內研究以理論研究為主，占據56%。但實證研究的數量也在逐步增長。2015年在所選的核心期刊中的實證研究論文發表的數量為6篇，達到其頂峰，而2017年所調查的期刊中只有兩篇英語語法教學研究，全為實證研究。這一數量遠遠超過劉忠政和李西（2010）所做的統計，同時整體趨勢也符合他們所得出的研究假設。

Literature systematic review

A comprehensive search of PubMed and Scopus was performed for all studies published prior from January 2014 to December 2019, using the search terms “encephalitis” and “teratoma”, which yielded 226 articles in PubMed and 344 in Scopus (Figure 1). A systematic review of these papers was performed, and after removal of repeated 165 articles from both searches, the full text of all articles were evaluated to determine whether case reports with ovarian teratoma were included. There were no language restrictions.

Our evaluations revealed that surgical outcomes are favorable and early removal of tumor is critical. The importance of postoperative follow-up cannot be over-estimated.

Statistical analysis

GraphPad Prism 8 was used for statistical analyses.

RESULTS

Case description

Typical psychotic symptoms, and memory and consciousness disorders accompanied by seizures were observed in all six patients from this study. All patients showed positive signals in serum and cerebrospinal fluid samples for NMDAR and received operation and immunotherapy. Three patients underwent unilateral oophorocystectomy and the other three underwent unilateral oophorectomy through minimally invasive surgeries, including laparoscopic and single port laparoscopic surgeries. So far, no deaths have occurred. Two patients had recurrent psychotic symptoms while the remaining four had no mental symptoms or tumor recurrence during postoperative follow-up (Supplementary Table 1). A representative brain tissue pathology from one of the patients is shown in Figure 2.

Systematic literature review

In this paper, 155 cases in 130 case reports of anti-NMDAR encephalitis caused by ovarian teratoma were studied and analyzed (Supplementary Table 1).

Epidemiological characteristics

Encephalitis is a complex neurological syndrome that is caused by inflammation of the brain parenchyma[1]. The main causes of encephalitis include a range of infectivity and autoimmunity. Viruses are the most commonly identified pathogenic factors[1]. Autoimmune encephalitis (AE) has two major subtypes: (1) Classic paraneoplastic limbic encephalitis marked by well-characterized onconeural autoantibodies against intracellular neuronal antigens; and (2) new-type AE characterized by autoantibodies against neuronal surface or synaptic antigens[2]. N-methyl-D-aspartate receptor (NMDAR) encephalitis is a new-type AE[3,4], wherein antibodies attack N-methyl-D-aspartate (NMDA)-type glutamate receptors at central neuronal synapses[5]. Affected patients develop prominent psychiatric and behavioral symptoms, rapid memory loss, seizures, abnormal movements (dyskinesias), hypoventilation, and autonomic instability[6-8].

As would be expected, there is a global disparity in terms of the available data from individual countries. The differences in national wealth/resources and the differences in health care play a major role in this disparity. It is further evident in the fact that there is not even a single report from Africa, to the best of the knowledge of authors. Further, there has been major advancements in the last few years as there was just a single case reported from China prior to the year 2014 whereas 27 cases have been reported after 2014 (Table 1)[19]. Thus, clearly the number of cases in China has increased significantly recently. Mean age of the patients was 25.0 ± 8.0 years with a median age of 25 years. The tumors were predominantly reported to be located on the right ovary. Immature teratomas or mature teratomas with immature foci were larger than dermoid cysts (Table 2).

Clinical findings

It is interesting to report that the clinical presentation of our six cases is very consistent with those reported earlier. Common symptoms were viral-like prodrome, including fever, headache or dizziness, nausea or vomiting, and general discomfort, along with abdominal pain, high blood pressure, and decreased sleep. Patients also reported severe psychiatric symptoms, speech dyskinesias, memory loss, seizures, reduced consciousness and sometimes orofacial dyskinesias, and progression to autonomic and respiratory instability.

This pooled study showed that prodrome with fever occurred in 19.0% of the patients, headache or dizziness in 26.4%, nausea or vomiting in 6.9%, other in 12.0%, no prodrome in 2.8%, and not specified in 32.9% (Figure 3A). The mean time from prodrome to psychosis was about 1 wk (Figure 3B). The clinical symptoms were psychiatric behavioral (22.8%), speech dyskinesias (pressured speech, verbal reduction, and mutism) (10.7%), seizures (16.9%), movement disorder (16.1%), decreased level of consciousness (11.9%), autonomic dysfunction (10.7%), and central hypoventilation (10.7%) (Figure 4A). Among them, psychosomatic behavioral symptoms were the most common (Figure 4B) and more than half of the patients presented with three to five clinical symptoms (Figure 4C).

Examinations

Among the 150 surgical patients, 99 had full recovery and mild deficits, two had severe deficits, three died (including deep vein thrombosis and while receiving anticoagulation development of gastrointestinal bleeding in 1; severe septicemia in 2), and 47 had no prognosis data.

Final diagnosis

Examinations included electroencephalography (EEG), colony-stimulating factor (CSF), brain magnetic resonance imaging (MRI), and IgG anti-GluN1 antibodies. More than half of the patients showed abnormal electroencephalogram, common for focal or diffuse slow or disorganized activity, epileptic activity, and extreme delta brush. More than half of the patients also showed abnormal cerebrospinal fluid, common for pleocytosis (> 5 white blood cells/mm

), and oligoclonal bands. About a third of the cases had brain MRI abnormalities (Figure 5A). Among 155 cases, 145 were positive for antibody test, and 10 were not specified (Figure 5B).

Treatment and prognosis

Treatment includes surgery and immunomodulation treatment. In 155 cases, 150 underwent surgical treatment, four did not undergo surgery, and one had no data on whether there was surgical treatment (Table 3). One patient with no information about surgical intervention, was in coma after 2 mo of follow-up. All four patients who did not undergo surgery died.

Outcome and follow-up

For the immunomodulation treatment, the combination of corticosteroid and intravenous immunoglobulin (IV Ig) and the combination of corticosteroid and IV Ig and plasmapheresis are common (Figure 5C).

DISCUSSION

We report here a series of six cases of ovarian teratoma-associated anti-NMDAR encephalitis from our hospital. Further, in the systematic review, we detailed cases of ovarian teratoma-associated anti-NMDAR encephalitis from the published literature. The pathogenesis of ovarian teratoma-associated anti-NMDAR encephalitis remains unclear. NMDARs originate from heteromers of NR1 and NR2 subunits. The NR1 subunit is known to bind to glycine while the NR2 subunit is known to bind to glutamate[20,21]. Antibodies in anti-NMDAR encephalitis patients cause a reversible titer-dependent loss of NMDARs[22], and they target an epitope on the NR1 subunit that resides in the hippocampal and frontotemporal regions[23,24]. Anti-NMDAR antibody production is related to the presence of tumors, mostly teratomas.

There seems to be a connection between the prodromal flu-like symptoms and the antibodies against NMDAR. Some researchers have emphasized the connection between viral (

, HSV) infection and injury of the blood–brain barrier. Therefore, analysis of CSF for the presence of NMDA receptor antibodies is important in patients with relapsing symptoms after HSE[25,26]. Human immunodeficiency virus and other neurotropic viruses (

, HSV) might also be a trigger for anti-NMDAR encephalitis[27]. Meningitis can induce transient blood-brain barrier disruption, which facilitates transmission of NMDAR autoantibodies to the CNS[28].

In a typical presentation of anti-NMDA receptor encephalitis, there is reported development of severe psychiatric symptoms, seizures, memory loss, and reduced consciousness. Often, there are additional manifestations such as orofacial dyskinesias and progression to autonomic and respiratory instability. Anti-NMDAR encephalitis is known to progress through five characteristic phases. The advanced stage is typically hallmarked by extreme autonomic instability with hyperthermia alternating with hypothermia, hypoventilation, fluctuating blood pressures, tachycardia, and even bradycardia as severe as asystole. Dysautonomia, sinus pauses, and asystole are likely caused by disruption in the balance between parasympathetic and sympathetic activity. Up to 90% of rhythm disturbances originate from sinus node abnormalities. Life-threatening cardiac dysrhythmia and cardiac arrest require urgent management[29,30]. Temporary pacing is occasionally required, but permanent pacing appears to be unnecessary[31].

The first case of paraneoplastic encephalitis related to ovarian teratoma was described in 1997[9,10]. In 2005, a syndrome marked by psychiatric symptoms, memory deficits, hypoventilation, and decreased consciousness was reported in four young women with ovarian teratomas[11,12]. A severe form of encephalitis associated with antibodies against NR1–NR2 heteromers of the NMDAR was identified by Dalmau

[6] in 2007. The target antigen was identified as the NMDAR, and the disorder named “anti-NMDAR encephalitis”; specific autoantibodies to the NMDAR were soon detected in these and eight other patients with similar neurological symptoms, seven of whom also had ovarian teratomas. Iizuka

[8] confirmed the presence of NMDAR antibodies in four young women with ovarian teratoma and described the clinical course progression through five phases of anti-NMDAR encephalitis: Prodromal, psychotic, unresponsive, hyperkinetic, and gradual recovery.

A number of diagnostic tools are now available. These include serum analysis and CSF antibody against the NMDA receptor, EEG, analysis of CSF, and brain MRI. Additionally, the diagnosis of the tumor requires further tests such as transvaginal ultrasound, CT/MRI, and the evaluation of blood tumor markers. Pelvic ultrasound has also been employed to detect ovarian teratomas. CT scans can help identify calcification within the mass; however, MRI is much more accurate when making diagnoses for ovarian teratoma or the Mullerian duct anomalies. Further, whole-body PET/CT have consistently proven to be highly accurate when it comes to staging this disease. The diagnosis of anti-NMDA receptor encephalitis typically involves exclusion of other causes of encephalopathy. In case that the cause of a patient’s encephalopathy is not evident, attending physician needs to rule out anti-NMDA receptor encephalitis, particularly in patients with no reported psychiatric history. For diagnosis, lumbar puncture is required to collect and analyze CSF and then test for NR1 and NR2 using specific antibodies. A confirmed diagnosis is made if the anti- NMDAR antibodies are found in the CSF or in the serum. The diagnostic criteria have been described in the literature[27]. Based on the presence of clinical features consistent with the probable criteria, finding an adnexal mass, most likely a teratoma, upon finding anti-NMDAR antibodies in the CSF or serum, and after the exclusion of other possible etiologies, a diagnosis of anti-NMDA receptor encephalitis can be established.

校企合作模式在中職汽車營銷教學中的應用不僅有利于院校教學體制的變革，還符合企業發展的內部需要。院校作為人才輸送的重要基地，其培養出來學生的好壞對企業的發展也產生著重要的影響，校企合作模式能夠讓院校更有針對性地為企業培養人才，有利于汽車營銷企業內部的人才儲備和隊伍建設，提升企業的核心競爭力。

幼兒歌曲《小豬賀喜》為C宮調，2/4拍，為幼兒園大班歌曲，曲式結構為一段式，分為四個樂句，歌曲以敘事的方式表現憨態可掬的小小豬去送禮的滑稽場面。鑒于比賽性質，此首幼兒歌曲的彈唱除了前奏、間奏和尾奏之外，主體部分以無旋律伴奏為主，采用和聲節奏音型配置，在和弦的安排上，以三度疊置和弦為基礎，適當增加替換音和弦與附加音和弦，以豐富其和聲色彩，進一步增強其旋律的表現意義。

Anti-NMDAR encephalitis had initially been described in young women with ovarian teratoma, but it is also common in women without tumor, in men, or in children[32]. Although not all patients presenting with NMDAR encephalitis are females with ovarian teratomas, the frequency of these patients mandates screening of females to rule out a causative tumor. The mainstays of treatment include immunomodulation and neoplasm removal targeting both symptomatic and causal factors[24]. Tumor removal is an effective treatment for anti-NMDAR encephalitis. Tumor removal in those with identifiable lesions leads to rapid clinical improvement. Even if none of the investigations are indicative of an ovarian teratoma, there still may be an occult ovarian teratoma[33]. In some cases, the teratoma is microscopic and only found following oophorectomy[34]. Tumor search and diagnosis are extremely important, and oophorocystectomy and oophorectomy are justified. Whether empiric exploratory laparotomy or laparoscopy and blind oophorectomies should be performed in patients with anti-NMDA receptor encephalitis without clinical evidence of a tumor is debatable. Because a laparoscopic examination for determining ovarian teratoma is less-invasive than laparotomy, trial laparoscopy may be acceptable for a treatment strategy if an ovarian tumor cannot be detected by various imaging tests.

德伐日太太出生于被侮辱、被迫害的農家，對封建貴族懷有深仇大恨。她像男子般與丈夫共同謀劃革命，她堅強的性格、卓越的才智和非凡的組織領導能力贏得“復仇女神”與“雅克”們的擁護。可是她卻被仇恨主宰了心智，成為一個冷酷、兇狠、狹隘的復仇者，最終，喪失心智的復仇使她喪命于槍支走火。

Immunomodulation treatment consists of a first line therapy and a second line therapy. The first line therapy includes corticosteroid, IV Ig, and plasmapheresis used alone or in combination. Steroids, IV Ig, and plasmapheresis help reduce antibody titers. The second line therapy includes rituximab and cyclophosphamide, whether alone or in combination. Benzodiazepines and antipsychotics round out the pharmacotherapies employed in the treatment of seizures, psychosis, and behavioral dysfunction[31]. When the patient does not have a tumor, first-line therapy with IV Ig, methylprednisolone, and plasma exchange can be used in sequence or in combinations[35]. The second-line therapy with rituximab (against CD-20 B-lymphocytes) or cyclophosphamide can also be used[36]. It has been reported that almost half of the patients show significant improvement within a month of first line treatment and tumor removal. Further, second line therapy has been reported to be effective in up to two thirds of the patients who progressed after the first line of treatment. Thus, the prognosis of patients is generally very good once they have been administered either the first or, if needed, second line therapy[7].

3.1 定向運動作為我國高校體育教育引進的新興項目，發展迅速，具有區別于其他運動項目的優勢，具有廣闊的發展前景。普通高校定向運動可持續發展需要以人為本，善于運用一切資源，聯合一切力量，多交流、多溝通、多學習，實現普通高校定向運動的自治和規范，以促進普通高校定向運動可持續發展。

In a systemic review of 100 cases of anti-NMDAR encephalitis, it was revealed that a better neurological outcome is achieved if surgical removal of the teratoma was performed quickly upon the onset of symptoms. This ensures much reduced probability of relapse and significantly improved recovery time[37]. Further, a systematic review of 174 cases of anti-NMDAR encephalitis revealed that even the small teratomas that contain nervous tissues, can result in severe complications which can be secondary to anti-NMDAR encephalitis[19].

Prognosis is generally poor for the patients, particularly those who are not attended to early in the disease. Generally, patients have a slow and incomplete recovery of neuropsychiatric sequelae in up to 3/4 of patients within an average of about 7 mo. It has been reported that a positive prognosis is linked to decreased anti-body titers. The one alarming statistic is that almost a quarter of patients are reported to relapse. The relapse is mostly reported within the first 2 years and there have been reports where relapse was associated with ovarian teratoma recurrence. On a bright side, relapses are often less severe. According to some estimates, 5%-7% of patients succumb to the disease within an average of 3.5 mo[7,30].

CONCLUSION

Despite the emerging evidence, an association between ovarian teratoma and anti-NMDAR encephalitis is not fully realized. Anti-NMDAR encephalitis, a rare complication of ovarian teratoma, can be fatal. Therefore, its further understanding cannot be underestimated. Behavioral changes, acute psychiatric symptoms accompanied by seizures, and memory and consciousness disorders should be recognized, the possibility of anti-NMDAR encephalitis should be considered, and examinations for anti-NMDAR antibodies need to be completed to confirm the diagnosis as early as possible. Tumor location should be prioritized, once diagnosis is defined, and the tumor search should focus on the ovaries. If a tumor is detected (even with a benign appearance), it is recommended to remove the tumor as soon as possible. Choice of surgical procedure should be decided considering pathology, age, fertility desire, and patients’ requirements, and it should be ensured that tumors are completely removed during operation. Early use of corticosteroids and IgG-depleting strategies (IVIg or plasma exchange) may improve outcome. Postoperative follow-up is particularly important in case of recurrence.

中線輸水總干渠北京段因采用管道輸水需增加加壓泵站，由此發生提水泵站的耗電量費用，建議根據北京段加壓泵站實際耗電量和電價計算動力費。

ARTICLE HIGHLIGHTS

Research conclusions

In the selected articles, a comprehensive data set was collected

a form designed for the present study. The form consisted of an Excel spreadsheet (Microsoft, Redmond, WA, United States), where each column captured a unique piece of information. When data were inadequate or insufficient for a definite piece of information, we recorded it as ‘not available’. Data of the individual patients were then pooled and analysed

the spreadsheet. A Microsoft Word document transposition of the form is provided as Supplementary material (Supplementary Tables 1-4).

沈湖與河渠連接方案：規劃擴挖沈湖處大治河、柴米河與蛇家壩干渠平行走向，三河共用兩堤。大治河、柴米河與沈湖相連通，過沈湖后兩條河道變為一條向下游排水，在沈湖上游蛇家壩干渠處新建一節制閘，向沈湖補水。該方案基本不打亂原有灌排體系，實施矛盾小，且隨著雨污分流工程的實施，沈湖水質將得到保證。

Research perspectives

Early use of corticosteroids and IgG-depleting strategies may improve outcome. Postoperative followup is particularly important in case of recurrence.

1.5 資料收集 征得院科研專家倫理委員會的同意和骨科主任的同意，由課題組負責人對所有參與課題的人員進行培訓，使之對測量工具統一認識，以降低測量偏差。取得患者知情同意后，運用測量工具分別收集手術減壓后及減壓后2 h的指標情況。收集工作由課題小組人員負責。

FOOTNOTES

Li SJ and Yu MH contributed equally to this work; all authors contributed to the design and conduct of study, and approved the submission of this work for publication.

Between July 2012 and December 2019, six patients with ovarian teratoma-associated anti-N-methyl-Daspartate receptor encephalitis were enrolled in Ren Ji Hospital, School of Medicine, Shanghai Jiao Tong University. All patients’ data like clinical characteristics, treatment, and follow-up were reviewed. The study was approved by the Ethic Committee of Shanghai Jiao Tong University. Informed consent was obtained from all patients for participation in this study and the publication of results.

The study was approved by the Ethic Committee of Shanghai Jiao Tong University.

Informed consent was obtained from all patients for participation in this study and the publication of results.

None of the authors have any conflict of interest to report.

Not available.

對照組給予注射用鹽酸胺碘酮（黑龍江迪龍制藥有限公司生產，國藥準字H20052294）靜脈注射，起始劑量為3 mg/kg，維持滴速1.0～1.5 mg/min，持續治療6 h后可將滴速降低至0.5～1.0 mg/min，日總注射量不超過1200 mg；此后可根據患者的病情改善逐漸減量，持續治療3 d。觀察組在此基礎上給予參松養心膠囊（北京以嶺藥業有限公司生產，國藥準字Z20103032）口服治療，0.4 g/次，3次/d，持續治療3周。兩組患者治療期間均對心率、血壓、心電圖及血氧飽和度進行密切關注。

This article is an open-access article that was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution NonCommercial (CC BYNC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is noncommercial. See: https://creativecommons.org/Licenses/by-nc/4.0/

China

Shan-Ji Li 0000-0003-3628-516X; Min-Hua Yu 0000-0003-3628-516Y; Jie Cheng 0000-0003-3634-512X;Wen-Xin Bai 0000-0002-5523-662X; Wen Di 0000-0002-1190-0915.

超聲檢查、CT檢查及MRI檢查用于瘢痕妊娠合并子宮動靜脈瘺中檢出率無統計學意義（P＞0.05）；超聲檢查、CT檢查及MRI聯合檢測檢出率，高于單一超聲檢查、CT檢查及MRI檢查（P＜0.05），見表1。

Yan JP

Wang TQ

Yan JP

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