Abstract
Ovarian resection as a treatment for hysteria, called ‘Battey’s operation’ or ‘normal ovariotomy’, was performed in the nineteenth century. Battey later reported that the resected ovaries appeared to have ‘cystic degeneration’. Currently, patients with acute neuropsychiatric symptoms are screened for teratomas for the differential diagnosis of anti-NMDA receptor encephalitis. There is now a hypothesis that ovarian lesions resulting in paraneoplastic encephalitis were among the patients who underwent Battey’s operation. We identified 94 published cases of Battey’s operation for neuropsychiatric symptoms in the late nineteenth century. Among 36 cases with detailed descriptions, we found 3 patients who showed acute onset neuropsychiatric symptoms with macropathological ovarian findings that were compatible with teratoma. They showed favourable prognoses after surgery and might have motivated the surgeons to perform the operation.
Introduction
Gynaecological innovations introduced at the beginning of modern medicine have been re-examined in recent years because of the renewed discussion of ethical issues (Fontanarosa and Bauchner, 2018). A statue of James Marion Sims, the ‘father of modern gynecology’, was recently removed from Central Park in New York City because he developed new surgical approaches for vesico-vaginal fistulas by experimenting on enslaved women without anaesthetics in the 1840s (Wailoo, 2018). JM Sims and his son Harry Marion-Sims practised ‘Battey’s operation’ (Sims, 1883), another controversial surgical innovation (Longo, 1979).
Robert Battey invented what he called ‘normal ovariotomy’ in the late nineteenth century, to treat the ‘change of life’ in women with menstrual disorders and related symptoms (Battey, 1872/3). He subsequently reported the efficacy of ovarian resection as a treatment for ‘hystero-epilepsy’ (Battey, 1880). During that period, Battey’s operation was increasingly performed and was eventually used as a treatment for ‘general nervous symptoms’, including menstrual madness, oöphoromania, hysteria, epilepsy, dysmenorrhea and nymphomania (Wells, 1886). These surgeries, which lack accountability for sexual and reproductive health and rights, were morally reprehensible and medically unjustifiable procedures on women. From the perspective of modern gynaecology, Battey’s operations are regarded as castration of patients with premenstrual dysphoric disorder (Studd, 2006). However, Battey regretted the term ‘normal’ ovariotomy because of his ignorance of the pathology of the resected ovaries, and 14 years after his first report, he additionally reported that the majority of the resected ovaries from such patients had ‘cystic degeneration’ (Battey, 1886).
Currently, a marked paradigm shift has emerged in the diagnosis of encephalitis after the groundbreaking report of anti-N-methyl-D-aspartate receptor (NMDAR) encephalitis a decade ago (Dalmau et al., 2007). Patients with anti-NMDAR encephalitis demonstrate a multistage illness that includes psychosis, abnormal involuntary movements, and autonomic dysfunction (Dalmau et al., 2011). These variable manifestations make the diagnosis difficult, and anti-NMDAR encephalitis occasionally mimics psychogenic non-epileptic seizures in clinical presentation (Caplan, Binius, Lennon, Pittock and Rao, 2011).
‘Hystero-epilepsy’ was one of the main targets of Battey’s operation. This term is now considered to be a synonym for functional disorders including psychogenic non-epileptic seizures (La France, 2014). Jean-Martin Charcot, a giant of nineteenth-century neurology, and his pupil Paul Richer proposed the characteristic clinical stages for the diagnosis of hystero-epilepsy: prodromal, epileptic, grand movement, emotional and facial expression, delirium and termination (Charcot and Richer, 1887/1972: 91–106; Richer, 1881/2017). Anti-NMDAR encephalitis has five characteristic phases including the prodromal, psychotic, unresponsive, hyperkinetic and gradual recovery phases (Iizuka et al., 2008). With the increase in modern knowledge, we now find similarities between hystero-epilepsy and anti-NMDAR encephalitis in terms of their clinical presentation and progression.
Anti-NMDAR encephalitis constitutes the most common subtype of autoimmune encephalitis in young women and accounts for 4% of male and female patients of all ages with encephalitis symptoms (Granerod et al., 2010). Today, female encephalitis patients are routinely screened for ovarian masses for the differential diagnosis of anti-NMDAR encephalitis. Therefore, there is a hypothesis that some anti-NMDAR encephalitis patients may have been incidentally included in the group of ovarian resected patients for treatment of hysteria in the nineteenth century. The aim of this paper is to elucidate whether patients with characteristics suggestive of anti-NMDAR encephalitis received Battey’s operation when it was first being performed.
Battey’s operation for neurological and psychiatric symptoms
We could not find a sufficient number of nineteenth-century case reports and series of cases in PubMed or through a Google search with the keywords ‘hysteria’ or ‘hystero(-)epilepsy’ and ‘normal ovariotomy’, ‘oöphorectomy’, or ‘Battey’s operation’. However, we identified 93 cases of ‘Battey’s operation’ performed for neurological and psychiatric symptoms from the 19 references in the historical review by Longo (1979), and one case from a reference in a book by Goetz (1987: 122). We included the cases with identified neurological and/or psychiatric manifestations, and excluded cases with simple gynaecological diseases, pain and amenorrhea. Isolated ‘nymphomania’, which was categorized as typical hysteria at that time, was excluded, because cultural and moral backgrounds might have greatly affected its diagnosis.
Out of 94 cases in 20 references, 58 cases in 5 references were excluded because they lacked detailed neurological descriptions and/or pathological descriptions of the resected ovaries. (Although Battey [1881] himself reviewed 218 cases of contemporary Battey’s operation cases, including 41 patients with neuropsychiatric diagnoses that were included in the above 94 cases, none of them had detailed neuropsychiatric descriptions or pathological findings for the ovaries.) The remaining 36 cases found in 16 references had notes on both the neuropsychiatric manifestations and ovarian findings, and therefore were included in our study.
The mean age of the patients was 28.3 years (range 18–40 years); 25 of the 36 patients in 13 papers had favourable courses after ovarian resection (Table 1), whereas 11 patients in five papers had unfavourable courses, which included death after the operation for two patients (Table 2). Only two papers included patients with both favourable and unfavourable courses (Carstens, 1883; Edes, 1894).
Clinical characteristics of the patients with favourable courses after ovarian resection.
Clinical characteristics of the patients with unfavourable courses after ovarian resection.
Table 3 shows a summary of the 36 cases. Among them, acute or subacute progression was seen in eight patients, and all of them, except for one, had favourable courses after ovarian resection. Chronic progression was noted in 24 patients, and three patients showed recurrent exacerbation during the menstrual cycle. The time course of progression was not reported for one patient. The most frequent diagnosis was hystero-epilepsy, which was diagnosed in 14 patients (39%), and the second most common was hysteria, which was diagnosed in 10 patients (28%). All of the 24 patients (67%) with hystero-epilepsy or hysteria and three patients who were diagnosed with ‘insanity’ or ‘mania’ presented with a combination of various psychiatric and neurological manifestations, that is, in 27 of the 36 patients (75%). The symptoms of ‘neurasthenia’, ‘melancholia’, ‘borderland of hysteria and insanity’, or of being ‘nervous’, ‘sick’ or ‘nervously prostrated’ in the remaining nine patients (25%) were considered chronic fixed symptoms.
Summary of the outcomes reported after ovariotomy of 36 patients in the nineteenth century (percentages are given in brackets).
In terms of the gross observations of the resected ovaries, normal appearance was noted in three of 36 patients (8%). The remaining 33 cases (92%) had some kind of abnormality. Enlargement of the ovaries was reported in 15 cases (42%), and cyst or cystic degeneration in 23 cases (64%). A combination of both enlargement and cystic abnormality were noted in 10 patients (28%), and they belonged to the favourable course group exclusively. Adhesions, cirrhosis, or prolapse of the ovary were noted in 10 cases (28%). There were no microscopic reports for the women undergoing Battey’s operation for neuropsychiatric symptoms. Microscopic observations were reported in one patient who had the operation for chronic cephalalgia, described as follows: The ovaries contain cysts of various size, due to simple dilatation of the Graafian follicles. In addition to the cysts, there is a good deal of induration of the stroma, and in the right ovary an enormous formation of blood vessels. In some places, they are so numerous that they resemble very much the convoluted sweat glands of the skin. (Battey, 1886: 488–9)
This description was plausible for polycystic ovary syndrome (PCOS) (Di Pietro, Pascuali, Parborell and Abramovich, 2018; Stein and Leventhal, 1935) rather than a teratoma (Montgomery, 1898). Although the resected ovaries did not include hair, sweat glands, adipose tissue, nervous tissue or teeth, and none were diagnosed as teratomas, the gross findings could not be fully explained by PCOS alone; these included ‘an enlarged ovary of 5 pounds’ (see Table 1: Manton, 1889), ‘a cyst holding half a drachm of fluid’ (see Table 1: Gordon, 1886), and ‘cystic and four inches in diameter’ (see Table 1: Battey, 1886). These findings, particularly the 5-pound enlargement and enlarged fluid cyst, resemble a teratoma rather than PCOS.
Resemblance to anti-NMDAR encephalitis patients
Anti-NMDAR encephalitis patients have various psychiatric and neurological symptoms, and female patients often have ovarian teratomas. Clinical diagnostic criteria for anti-NMDAR encephalitis have been proposed (Graus et al., 2016). When accompanied by rapid progression (less than three months to reach nadir), the diagnosis as probable anti-NMDAR encephalitis can be made when three of the following symptoms are present: abnormal psychiatric behaviour, speech dysfunction, seizures, movement disorders, consciousness disturbances, and autonomic dysfunction accompanied by a teratoma. To analyse reports written 100 years ago, we defined the cases with a resemblance to patients with anti-NMDAR encephalitis as those presenting with acute or subacute onset, having neurological and psychiatric symptoms, and having a combination of both enlargement of and cystic lesions in the resected ovaries. We also defined onset type as follows: acute course as those labelled ‘acute’ or described as having daily progression; subacute as those having a weekly or monthly progression; and chronic as those whose symptoms progressed over the course of half a year or more.
In total, we found that three patients had symptoms resembling those of anti-NMDAR encephalitis. All these patients had favourable courses after the surgery (Table 1: Manton, 1889; Meyer, 1894; and Meigs and Mass, 1894).
Battey himself had a strong belief, based on ancient medicine, that ‘insanity is not very unfrequently caused by uterine and ovarian diseases’ (Battey, 1877: 293–4). He only had a suggestion for treatment of women, which was described in his first report (Battey, 1872/3). One of the case reports in our study said that transmission from the irritated ovary to the brain through the sympathetic nerves produced vaso-motor changes in the cortex, resulting in the hysterical symptoms (Walton, 1884). The hypothesis does not match the modern concept of paraneoplastic neurologic syndrome. However, some of the propagandists proposed that there was an association between neuropsychiatric symptoms and the ovaries under pathological conditions (Sims, 1883).
Two major reasons can be postulated as to why the discovery of encephalitis secondary to teratomas was delayed until the twentieth-first century. First, there was the lack of establishment of the pathological findings regarding the resected ovaries. Second, the definitions of hystero-epilepsy and hysteria were vague.
The nosological uncertainty of ‘cystic degeneration’
Among the series of cases involving Battey’s operation, most did not incorporate microscopic screening of the resected ovaries and none of them described a pathologically proven teratoma. Post-operative pathological screening was generally established during the first half of the twentieth century. Before that, the term ‘cystic degeneration’ seemed to denote a range of ovarian lesions from dermoid cysts to polycystic ovaries. In an 1879 report about a successful ovarian resection for gynaecological symptoms that included a detailed pathological observation, the author used the term ‘cyst’ to mean both the dilatation of Graafian follicles and enlarged fibrous stroma (Smith, 1879). The pathologically proven teratomas were usually described in the nineteenth century as ‘cysts’ by gross examination (Montgomery, 1898). In modern studies using prenatal ultrasonic screening, the prevalence of ovarian masses is up to 6.1% among healthy pregnant women (Naqvi and Kaimal, 2015). In contrast, the incidence of ovarian cysts and cystic degeneration was noted in 23 of the 36 patients (63%) who underwent Battey’s operation, and the incidence of ovarian enlargement without clearly stated cystic lesions was five (13%). In total, 77% of the patients had ovarian masses, and the incidence in patients was much higher than that in healthy women. Moreover, the most common pathological findings of the incidental ovarian masses in modern studies are mature cystic teratomas (Sherard et al., 2003). The epidemiological studies indicated that the ovarian masses in patients who received Battey’s operation might have included cystic teratomas.
Polycystic ovaries and neuropsychiatric symptoms
In our study, only three patients (8%) among those who underwent ovarian resection in the nineteenth century had a neurological course and an ovarian pathology that resembled the modern clinical concept of anti-NMDAR encephalitis. The symptoms of the majority of the patients could be attributed to other causes. Among Battey’s reports, a single microscopic observation of the resected ovaries from one woman with cephalalgia showed similarities to polycystic ovaries in terms of increased follicles and hyperplasia of the stroma and vessels (Di Pietro et al., 2018). We excluded the woman from our analysis in the tables, because she simply had pain. However, the case is important in that this was the only microscopic finding that was recognized by Battey himself. The prevalence of PCOS is presumed to be 5–10% in women worldwide (Norman, Dewilly, Legroand and Hickey, 2007). On gross observation, 63% of the ovarian resected patients had cysts or cystic degeneration, and they had much higher cystic abnormalities than the general population. Therefore, ovarian cyst-related neuropsychiatric symptoms could be a possibility.
PCOS was established as bilateral polycystic ovaries in seven patients with amenorrhea; the ovaries were described as ‘what has been termed “cystic degeneration of the ovary”’ (Stein and Leventhal, 1935: 181–2). PCOS is associated with neuropsychiatric symptoms such as depression or anxiety due to hyperandrogenemia (Deeks, Gibson-Helm, Paul and Teede, 2011). In the present study, three patients diagnosed with melancholia and neurasthenia seemed to have symptoms consistent with the modern concept of depression, and they had cystic but not markedly enlarged ovaries.
Eight per cent of the patients in the present study had repetitive epileptic attacks along with their menstrual period, which could be called ‘catamenial epilepsy’ (Herzog, 2015), and all of them also had cystic ovaries. Epilepsy is associated with PCOS frequency (Isojärvi, 2003). Epilepsy patients show a high incidence of reproductive dysfunction, regardless of the presence or absence of antiepileptic drugs (Joffe and Hayes, 2008). A previous report showed that 56% and 20% of patients with temporal lobe epilepsy had menstrual dysfunction and PCOS, respectively (Herzog, Seibel, Schomer, Vaitukaitis and Geschwind, 1986). One hypothesis is that epileptic discharge might disrupt limbic modulation of hypothalamic hormonal regulation of pituitary luteinizing hormone secretion, resulting in PCOS. In contrast, several studies have shown that polycystic ovarian morphology does not frequently occur in epileptic women (Joffe and Hayes, 2008). In summary, the high prevalence of cysts or cystic degeneration of the ovaries in the present study suggests that some PCOS patients with depression or epilepsy might have been included in the population of ovarian resections in the nineteenth century.
The nosological uncertainty of hystero-epilepsy and hysteria
Battey’s operation was a new surgical technique and was discussed mainly by gynaecologists without careful deliberation of the differentiation between hysteria, insanity, convulsive attacks, dementia, paralysis and mania (Pallen, 1877). The use of the term hystero-epilepsy was even more vague. Today, the terms hysteria and hystero-epilepsy are usually considered synonyms of functional disorders, including conversion and dissociative disorders (Bell, Oakley, Halligan and Deeley, 2011; Stone, 2016). This nosological organization was established by Charcot’s pupils, including Joseph Babinski and Pierre Janet, after Charcot’s death (Goetz, 2002). Charcot and his colleague Richer distinguished hystero-epilepsy from ‘vulgar hysteria’ and proposed several phases of the clinical symptoms of hystero-epilepsy: prodromal, epileptic, grand movement, emotional and facial expression, delirium and termination (Richer, 1881/2017). There may be similarities between the clinical phases of hystero-epilepsy and typical anti-NMDAR encephalitis: prodromal symptoms, psychosis, hypoventilation, severe orofacial dyskinesias and bizarre involuntary movements (Iizuka et al., 2008). However, the time course of each phase in hystero-epilepsy lasts from several seconds to minutes, whereas each phase of anti-NMDAR encephalitis progresses over days and months. Moreover, Charcot’s written lecture did not include a clear definition of the phase progression and had only a proposal of a differential diagnosis from true epilepsy (Charcot, 1877/1985, Vol. I: 300–15). Although Charcot noticed the relationship between hysteria and the ovaries in terms of ovarian compression treatment for hysteria attacks, he clearly opposed the ovarian resections performed in contemporary America (Blin, Charcot and Colin, 1888/2002: 374–8). Outside France, a consensus for the clinical picture of hystero-epilepsy had not been reached among other countries at that time, including America. Even in France, hysteria and hystero-epilepsy patients seemed to vanish rapidly after Charcot’s death (Scull, 2009: 104–30). The concept of hystero-epilepsy could not be defined as an established entity.
There are several limitations of the present study. First, it is based on a hypothesis with a modern interpretation of a historical issue. Second, many of Battey’s operations were unreported (Longo, 1979). Therefore, the results could be biased towards the group with favourable outcomes, and this group had a higher possibility of including the anti-NMDAR encephalitis patients. Third, Battey’s operation was not the main treatment of hysteria and hystero-epilepsy, even in the nineteenth century. Non-surgical treatment of hysteria by ovarian compression was often applied (Broussolle et al., 2014). Therefore, the concept of hystero-epilepsy at that time is not simply explained by the incidence of patients with anti-NMDAR encephalitis among patients who received Battey’s operation.
Conclusions
A small number of anti-NMDAR encephalitis patients were incidentally present among the patients who received Battey’s operation, and they might have motivated the physicians to perform the operation. Some PCOS patients who had neurological symptoms apart from ‘hystero-epilepsy’ could also have existed. Today, the term hysteria has been recognized as a synonym for functional and non-organic disorders. In the nineteenth century, however, there was no clear discrimination between functional disorders and organic disorders such as anti-NMDAR encephalitis. Further investigations are required to elucidate the meaning of the term hystero-epilepsy in the late nineteenth century.
Footnotes
Funding
The author(s) received no financial support for the research, authorship and/or publication of this article.
