Investigation of association between female genital tract diseases and Schistosomiasis japonica infection

Investigation of association between female genital tract diseases and Schistosomiasis japonica infection

Acta Tropica 77 (2000) 179 – 183 www.elsevier.com/locate/actatropica Investigation of association between female genital tract diseases and Schistoso...

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Acta Tropica 77 (2000) 179 – 183 www.elsevier.com/locate/actatropica

Investigation of association between female genital tract diseases and Schistosomiasis japonica infection Liu Qunhua a,*, Zhang Jiawen b, Liu Bozhao a, Peng Zhilan b, Zhang Huijie a, Wang Shaoying a, Mei Delun a, Lee-Nah Hsu c,1 b

a Sichuan Institute of Parasitic Diseases, Chengdu, Sichuan Pro6ince 610041, PR China Department of Obstetrics and Gynecology, Second Uni6ersity Hospital, West China Uni6ersity of Medical Sciences, Chengdu 610041, PR China c Institute of the Project, Member of UNDP/World Bank/WHO-TDR Gender Task Force, Vienna, Austria

Received 2 July 1999; received in revised form 13 June 2000; accepted 14 June 2000

Abstract With the support of WHO/TDR, a case-control study was undertaken to explore the association between female genital tract manifestation and Schistosomiasis japonica. Two thousand one hundred and six women aged 18 – 50 in a township with schistosomiasis japonica infection rate of \15% were surveyed using modified Kato-Katz method qualitatively and quantitatively. Two hundred and forty four women with schistosomiasis japonica were selected as experimental group and 236 matched healthy women as control group. Sixty nine items including cervix smear and the S. japonicum circulating antigen in intrauterine lavage were investigated. The results showed that physically, menstrual disorder and shorter stature and lighter weight of the first newborn occurred more frequently in the experimental group than that in control group. As for female genital tract manifestation, there were more cases with chronic cervicitis and uterine enlargement in the experimental group than that in the control group. Schistosome circulating antigen was detected in intrauterine lavage from 13 cases with schistosomiasis by ELISA. No evidence was found to show that female genital tract diseases be directly caused by S. japonicum, but the findings emerging from this survey merit further study. © 2000 Elsevier Science B.V. All rights reserved. Keywords: Schistosomiasis japonica; Female genital tract diseases

1. Introduction * Corresponding author. Tel.: +86-28-5441752; fax +8628-5438409. E-mail address: [email protected] (L. Qunhua). 1 Present address: Southeast Asia HIV and Development Project, UNDP, Bangkok, Thailand.

Female genital tract diseases are mainly seen in connection with schistosomiasis haematobia and mansoni, and less frequently linked with schistosomiasis japonica. An infant infected with schisto-

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somiasis japonica through placenta was first reported in 1914 (Narabayashi, 1914). After that, there were some case reports indicating an association between female genital tract diseases and schistosomiasis japonica, as for example enlargement of uterus, fallopian tube and ovarian cyst (Ching-Chien, 1951; Carpenter et al., 1964). However, there is a need to verify these claims. So an investigation was carried out in Panao Township of Meishan County in Sichuan Province in 1996 to ascertain whether any association between female genital tract diseases and schistosomiasis japonica could be established. 2. Materials and designs

and ninty six women with negative circulating antigen were selected as control. Experiment and control groups were matched according to age and occupation.

2.3. Inter6iews using standardized questionnaire The research staff interviewed each object and filled out the form carefully item by item. The main contents of the questionnaire with a total of 64 items included general health condition, history of schistosomiasis infection, genital tract manifestation and common gynecological symptoms.

2.4. Gynecological examinations

2.1. General information on experimental area Panao Township of Meishan County is located in the mid-west of the plain of Sichuan. In the past, the cumulative area of snail habitats has reached more than 5.09 million m2 at its highest. The highest human infection rate was 30.4%. In 1989 when 11 villages were sampled, seven had a human infection rate of ]15% with the highest at 34.3%. During recent years, due to snail control in large areas and mass chemotherapy with praziquantel once a year, the human infection rate has decreased to about 15%. In 1996, the total population of this township was 11 830, among them 5037 were women, 2513 of whom were aged between 18 and 50.

2.2. Schistosomiasis japonica case screen Of the 2513 women to be investigated in this survey, only 2160 (83.8%) were able to participate in this program. Two smears from every stool were examined by modified Kato – Katz method and 296 cases were positive with geometric mean of EPG (egg/g stool) of 33.58. Blood samples were taken from women with negative stool results for S. japonicum circulating antigen detection by ELISA (Wang Xiuzhen and Li Shitao, 1992). Two hundred and ninety six cases with positive stool examination were defined as the experiment group. Two hundred

The following examinations were conducted for both experimental and control groups. 1. Common gynecological examinations. 2. B-ultrasound. 3. Cervix smear. 4. Intrauterine lavage collection and S. japonicum circulating antigen detection: a double-channeled tube was put into the uterine cavity and 10 ml normal saline was injected to wash the uterine cavity. Then the fluid was collected to test for schistosome circulating antigen by onestep ELISA (Wang Xiuzhen and Li Shitao, 1992). 5. Endometrial biopsy was done if it was indicated. 6. Laparotomy was done if it was indicated.

2.5. Treatment After investigation, all the women with schistosomiasis japonica were treated with peaziquantel (200 mg/tablet, 40 mg/kg body wt).

2.6. Statistical analysis All the data including 110 variables from both the interviews and the gynecological examination were put into a computer. Chi-sequare test, Student t test and OR test (odds ratio) were done by using SPSS/PC + (version 4.01).

L. Qunhua et al. / Acta Tropica 77 (2000) 179–183

3. Results

3.1. Findings from gynecological examinations Two hundred and forty four women with schistosomiasis japonica and 236 healthy women actually took part in this research. The average age of the sample population was 32 years with average body weight of 50 kg and average menarche at 15. Their mean age of marriage was 21. There were significant differences between the experiment group and the control group for the height, bleeding period and weight of the first new-born (Table 1). Four hundred and ten cervical smears were eligible for examination and the result showed that there were more Grade II cases (155/207) in the experiment group than that (104/203) in the control group (PB 0.05). Three cases in experiment group and one case in the control group were in Grade III. There were more cases (7/244) of uterus enlargement by B-ultrasound in experiment group (3/236) than in the control (P \ 0.05). Table 1 General information of the sample population Experiment group Height (cm) 153.58 Menarche 14.99 (year) Menstrual 31 cycle (day) Bleeding 4.31 period (day) Bleeding amount (ml) Normal 75.7 Hypermenorrhe 20.9 a Hypomenorrhea 3.5 Amenorrhea Yes (%) 9.2 No (%) 90.8 Menstrual disorder Yes (%) 10.8 No (%) 88.2 Gestation 2.31 times WFNBa(g) 3229 a

Control group

154.61 15.21 29 4.69

P-value

B0.05 \0.05 \0.05 B0.05

78.8 14.8

\0.05 \0.05

6.4

\0.05

8.4 91.6

\0.05 \0.05

8.4 91.6 2.56

\0.05 \0.05 \0.05

3355

WFNB: weight of the first new-born.

B0.05

181

Two hundred and forty samples of intrauterine lavage were examined from the experiment group and 20 samples from the control group. Schistosome circulating antigen was detected in 40 cases in the experiment group but none in the control group. There is no association among the infection intensity, circulating antigen status in uterine lavage and the gynecological finding.

3.2. Findings from biopsy and operation Endometrial biopsy was performed in three cases with irregular bleeding, and the results showed that all three cases were hyperplasia and no eggs were found in the endometrium. Three cases of uterus enlargement and two cases of adnexal mass were found to have surgical indication. Among them, hysterectomy and bilateral salpingo-ovariotomy had been carried out in one case, sub-hysterectomy and right salpingectomy in two cases, right salpingectomy and appendectomy in one case and left salpingectomy and appendectomy for the remaining case. Pathological findings for these five cases were adenomyoma for one, leiomyoma for two, mesosalpinxal cyst with chronic appendicitis for two. Only two cases were shown to have schistosome eggs in the appendix.

3.3. Association between female genital tract diseases and schistosomiasis japonica Since the morbidity of chronic cervicitis and uterine disorder in the experimental group was higher than that in the control group. Odds ratio was calculated to estimate the relative risk of female genital tract diseases caused by schistosomiasis japonica infection (Table 2).

4. Discussion Previously, no systematic investigation of female genital tract diseases due to schistosomiasis japonica in a community had ever been conducted. In 1996, we conducted a case-control study of female genital tract diseases and its association with schistosomiasis japonica in a township where schistosomiasis infection rate for

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Table 2 The relative risk of female genital tract damage caused by Schistosomiasis japonica Organic damages

Chronic cervititis Uterine enlargement Abnormal B-ultrasound

OR

2.84 3.37 16.49

Confidence interval 99%

95%

1.63–4.95 2.94–12.21 1.95–139.75

1.86–4.33 1.27–8.96 3.25–83.61

married women aged between 18 and 50 was about 15%. A total of 480 women (244 women with schistosomiasis japonica infection and 236 healthy women) were studied. This research demonstrates some physiological changes in women with schistosomiasis japonica infection, such as shortened height, menstrual disorder and a shortened menstrual period. The weight of the first new-born in the experimental group was found to be lower than that in control group. All these are probably due to growth retardation, anemia and malnutrition induced by schistosomiasis (Liu Chongyi et al., 1990). The heterotopic schistosomiasis japonica often occurs in the lungs and brain and sometimes in the kidneys and testis and rarely occurs in the female genital tract. Our research shows that cervicitis and uterine disorder in the experimental group were more common than that of control group. In five operated cases, no schistosome eggs were found in removed genital tissues except in the appendix of two cases. In 1951, Ching-Chien reported a woman with menorrhagia and enlargement of uterus and the damage to uterus was proved to be caused by S. japonicum (ChingChien, 1951). In our study, we found more cases with enlargement of uterus in the experimental group than that in the control group. At the same time, schistosome circulating antigen was detected in intrauterine lavage from 5.4% (13/240) of the women with S. japonica. Our result seems to support the suggestion that schistosomiasis japonica may cause angiolysis, inflammation and then leading to fibroplastic proliferation (Zhou Kaimin, 1983). The study site is an old endemic area for schistosomiasis. A long period of infec-

tion would inevitably cause inflammatory changes to the uterus and even fibroplastic proliferations which might lead to enlargement of the uterus. We believe our discovery of the S. japonicum circulating antigen in intrauterine lavage from women with schistosomiasis to be the first such report anywhere. Currently it is well known that schistosome circulating antigen may be detected from serum. In recent years, some scientists thought schistosome circulating antigen could be detected in the urine or even in the body fluid of patients with schistosomiasis. The detection of circulating antigen in uterine lavage may provide support for these speculations and be an indirect evidence of heterotopic schistosomiasis. However, the result of the ELISA test seems to indicate some relationship with chronic cervicitis. Eighty four point six percent (11/13) cases with positive ELISA also suffered from chronic cervicitis. Statistics show that there is no association between the schistosome antigen status in intrauterine lavage and infection intensity EPG in our study. Whether the presence of schistosome antigen in intrauterine lavage could be evidence of heterotopic schistosomiasis or just the contamination of serum need further study. The experimental area is a township with a low infection intensity (EPG= 33.58) and repeated chemotherapy has been carried out there for years. The relative risks of chronic cervicitis, uterus enlargement and abnormality found by B-ultrasound demonstrates that there is some correlation between female genital tract diseases and schistosomiasis japonica (Table 2). This is only a preliminary study of female genital tract diseases at a special site and at a particular time, it has some limitations as compared with prospective studies. Many factors are associated with gynecological diseases, and the most common ones are marital status, sexual activity, parity, personal hygiene, educational level and living conditions. It is still too early to draw conclusions about any association between schistosomiasis japonica and female genital tract diseases or its mechanism. However, the findings emerging from this investigation merit further study.

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Acknowledgements The study was supported by funding from UNDP/World Bank/WHO/TDR. We are indebted to Dr. Xu Kehui, Dr. Zhou Chuntao, Dr Zhen Yun and Yi Haiyan of Second University Hospital, West China University of Medical Sciences, Sichuan Province. Special thanks go to Professor M.Tanner for his kind help and cooperation.

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Schistosomiasis japonica involvement of the female genital tract. J. Am. Med. Assoc. 188 (7), 647 – 650. Ching-Chien, K. (1951). Pathology of Schistosomiasis, 1st edn. Shanghai:Commercial Press. pp.85-100. Liu Chongyi, Chen Yawei, Wang Zhiqiu, Fan Gensheng. (1990). WHO/Schisto, Schistosomiasis. First version, Chengdu Publishing House of University of Science and Technology. pp.103 – 108. Narabayashi, (1914) cited by Youssef, A.F. and Abdine, F.H., op. cit., p. 991. Wang Xiuzhen, Li Shitao, 1992. Research and preparation of reagent-kit of sensitive and rapid detection method of schistosome circular antigen. Journal of Chinese Medicine 11,686 – 11,691. Zhou Kaimin, 1983. Mammary gland schistosomiasis complicated with mammary cancer — a case report. Journal of Chinese Medicine 63,375