This commentary discusses the impact of a milestone article on the accuracy of cervical smears for detecting cancer back in the developmental and transforming era of the cytological detection of atypical and malignant cells. The study served in the establishment of cancer screening in Japan which has contributed greatly in decreasing mortality from cervical cancers.

Keywords:
Cervical cancer, Cervical cytology, Carcinoma in situ, Atypical cells, Cancer staging, Cancer screening

We discuss a milestone paper [1] from the Japanese Society of Clinical Cytology (JSCC) published in Acta Cytologica. We consider the article to be important for the following reasons:

1. This was an early, extensive study on the high accuracy of cervical cytology at a cancer hospital.

2. The JSCC was started in 1961 while this study was being carried out.

3. Gynecologists were the founding members of the JSCC and the authors of the paper were contributing gynecologists from the Society.

4. The International Academy of Cytology (IAC) was started in 1957 during this study.

This milestone study [1] stated: “The vaginal aspiration smear was the only test used from 1952 to June 1957. But since July 1957, the scrape smear has been added. The scrape sample was prepared by scraping of the erosive surface in the ectocervix with a cotton swab.”

“The staining method used is Papanicolaou's EA 36. This study utilized the five-class classification by Papanicolaou. Cases of Class IV and V were considered to be cancer, and cases of Class I and II noncancer, while cases of class III were considered to be false-positive.”

And, regarding surgically resected materials: “Masubuchi divided Stage 0 into three subgroups: Stage 0-A, 0-B, and 0-C. The cases of Stage 0-A show carcinoma in situ-like findings by punch biopsy, but by thorough examination of the removed material no lateral invasion is found, but rather benign characteristics; those of Stage 0-B show typical carcinoma in situ; and those of Stage 0-C are suspected invasive.”

“The number of carcinomas of the cervix diagnosed from 1952 to 1963 was 2,918, and the number of positive cases (i.e., class IV or Class V) detected by smear was 2,660, so the smear was 91.2% accurate.”

By means of Tables 1-6, the study demonstrated the high accuracy/correct diagnosis rate of smear findings in cancer and non-cancer groups (Table 1) and for cervical cancer staging (stages 0-IV; Table 2), the relationship between the stage of cervical cancer and the smear finding (Table 3), the frequency of class III-V smears in stage 0 (Table 4), the frequency of class III-V smears in “stage I” cervical carcinoma (Table 5), and the histologic findings in non-cancer cases with class III-V smears (Table 6).

Table 7 showed “the result of smear findings in the cases diagnosed atypical epithelium by biopsy during these six and half years” (i.e., July 1957 to December 1963). The authors emphasized that the high rate (54/143 cases, i.e., 37.8%) of atypical epithelium showing class III, IV, or V by smear test is worthy of special attention.

They concluded: “Vaginal smear examinations were adopted as a routine practice in Japan in 1961. From 1961 to 1964 about 20,000 women were cytologically examined at 92 hospitals” (65 cases [0.5%] were diagnosed as carcinoma of the uterus) [1].

This paper emphasized the role of cervical smears in cancer detection in Japan and served as a basis for the subsequent introduction of the cancer screening program.

The JSCC is an academic society that promotes scientific research in clinical cytology and cytopathology and the application of research findings in clinical practice. The JSCC's beginnings date back to 1961. Modern cytological diagnosis began in 1928 with George Papanicolaou [2], whose technique of cervical smears became recognized as an effective method of diagnosing uterine cancer. The Gynecological Cytodiagnosis Discussion Group was formed in Japan in response to the creation of the International Academy of Gynecological Cytology in 1957. In 1961, the latter was renamed the IAC, to include advances in other fields and the former converted to the name JSCC. The study that is the subject of this commentary [1] was conducted during this period of transformation in the field of cytology in Japan (Fig. 1).

Fig. 1
Fig. 1. Dr. Kazumasa Masubuchi and Dr. George Papanicolaou in the early days.
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Dr. Kazumasa Masubuchi and Dr. George Papanicolaou in the early days.

Fig. 1
Fig. 1. Dr. Kazumasa Masubuchi and Dr. George Papanicolaou in the early days.
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Dr. Kazumasa Masubuchi and Dr. George Papanicolaou in the early days.

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The JSCC has been instrumental in the early detection of cancers including cervical, lung, and breast cancers. In the course of the long history of the JSCC, its cervical cancer exams, in particular, have contributed significantly to reducing the fatality rate for uterine/cervical cancer (Fig. 2).

Fig. 2
Fig. 2. The mortality rate of uterine/cervical cancer has markedly decreased in Japan.
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The mortality rate of uterine/cervical cancer has markedly decreased in Japan.

Fig. 2
Fig. 2. The mortality rate of uterine/cervical cancer has markedly decreased in Japan.
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The mortality rate of uterine/cervical cancer has markedly decreased in Japan.

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Of 50 contributions to PubMed, Dr. Masubuchi's study group has published a total of 7 papers [1,3,4,5,6,7,8]in Acta Cytologica ([1] was the first paper he wrote in English); Dr. Tenjin's group a total 4 papers [1,4,9,10]; and Dr. Fujii has contributed 1 [1].

By the 1960s, cervical cytology screening and the basic concepts of gynecologic cytopathology were fairly well established in the USA. During the 1950s and early 1960s, several famous monographs and atlases were published. At about this time, numerous articles describing both the cytologic manifestations of cervical carcinoma and its precursors also began to appear in the literature. These excellent publications summarize and illustrate the then-current state of knowledge in this field. They include: Papanicolaou's Atlas of Exfoliative Cytology [11] in 1954, Fluhmann's The Cervix Uteri and Its Diseases [12] in 1961, Graham's The Cytologic Diagnosis of Cancer [13] in 1963, and the first edition of Koss' Diagnostic Cytology and Its Histologic Bases [14] in 1961.

The author has nothing to declare regarding this publication.

1.
Masubuchi K, Tenjin Y, Fujii J: The detection of cervical cancer at Cancer Institute Hospital in Tokyo from 1952 to 1963. Acta Cytol 1967;11:32-34.
2.
Siang Yong T, Tatsumara Y: George Papanicolaou (1883-1962): discoverer of the Pap smear. Singapore Med J 2015;56: 586-587.
3.
Masubuchi K: Significance of the role of cytology in population screening of cancers. Acta Cytol 1975;19:334-336.
4.
Masubuchi K, Kubo H, Tenjin Y, Ono M, Yamazaki M: Follow-up studies by cytology on cancer of the cervix uteri after treatment. Acta Cytol 1969;13:323-326.
5.
Masubuchi S Jr, Nagai I, Hirata M, Kubo H, Masubuchi K: Cytologic studies of malignant melanoma of the vagina. Acta Cytol 1975;19:527-532.
6.
Fujimoto I, Masubuchi S, Miwa H, Fukuda K, Yamaguchi S, Masubuchi K: Psammoma bodies found in cervicovaginal and/or endometrial smears. Acta Cytol 1982;26:317-322.
7.
Hirai Y, Chen JT, Hamada T, Fujimoto I, Yamauchi K, Hasumi K, Masubuchi K, Sakamoto A: Clinical and cytologic aspects of primary fallopian tube carcinoma. A report of ten cases. Acta Cytol 1987;31:834-840.
8.
Fujimoto I, Hirai Y, Hasumi K, Masubuchi K, Osamura Y: The value of epithelial membrane antigen in the diagnosis of ovarian tumors. Acta Cytol 1990;34:549-554.
9.
Tenjin Y, Sugishita T, Yamamoto K: Automated cytoscreening system using 16 mm roll film. Acta Cytol 1977;21:276-286.
10.
Tenjin Y, Yamamoto K, Sugishita T, Igarashi Y: Basic studies on repair, especially histology, cytology and microspectrophotometry of DNA contents. Acta Cytol 1979;23:245-251.
11.
Papanicolaou GN (ed): Atlas of Exfoliative Cytology. Cambridge, Harvard University Press, 1954.
12.
Fluhmann CF (ed): The Cervix Uteri and Its Diseases. Philadelphia, W.B. Saunders, 1961
13.
Graham RM (ed): The Cytologic Diagnosis of Cancer, ed 2. Philadelphia, W.B. Saunders, 1963.
14.
Koss LG, Melamed MR (eds): Koss' Diagnostic Cytology and Its Histopathologic Bases. Philadelphia, Lippincott Williams & Wilkins, 1961.
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2017
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