The incidence of carcinoma cervix has declined in urban population of India in recent years. However, the situation in the rural population is still alarming as regards cervical cancer prevalence as living conditions are entirely different under rural and urban setup. There are many factors which make rural women vulnerable to the development of carcinoma cervix, as majority of rural women are socioeconomically weak and illiterate and they are ignorant of hazards and risk factors of the disease [1].There is also lack of awareness of personal genital hygiene which leads to the persistent vaginal infections which remain undiagnosed and untreated due to lack of medical amenities [2].This is because the medical facilities and awareness program are almost non-existent in rural India [3]. On the other hand, in the urban population, the women  are mostly literate and the improvement in the living standard and awareness among them through print and audiovisual media has resulted in decline in the incidence of carcinoma cervix. In addition, awareness for genital hygiene and visiting hospital at the pre-clinical stages of the disease are contributory factors for control of cervical cancer in the urban settings [4].

We have carried out cervical cytology of women attending Gynecology outpatient department of K G Medical University, Lucknow for 35 years (April 1971-30^th November -2005) and have registered a total of 36,484 women. This center also known as Queen Mary’s Hospital is leading center in the Northern region of the province for the  diagnosis and treatment of women diseases and influx of patients  from all over the State visit this hospital for getting adequate treatment to their gynecological ailments.

 Rural cervical cancer screening program is in progress in the villages of western region of the Lucknow since May 2013 through camp approach under the auspicious of Era’s Lucknow Medical College and Hospital, Era University, Lucknow and till February 2020, a total of 2949 women have been cytologically examined in the 186 camps organized for this purpose. Though the number of women registered in the urban and rural studied population are not comparable (36,484 as against 2949) but it provides enough insight in the prevalence of precancerous changes of cervix and associated risk factors involved in the process of cervical carcinogenesis under the two settings. The data from the urban and rural setup have been compared and are presented in this paper. 

The cytological screening of urban population, as told earlier, was carried out in women attending Gynecology outpatient department of K G Medical University, Lucknow presenting some gynecological symptoms. The screening was thus opportunistic and was carried out routinely whenever needed in the symptomatic women. A total of 36,484 women have been registered for undergoing Pap smear diagnosis during a span of 35 years (April 1971- November 2005). The rural screening was, on the other hand, planned through the organization of camps in the villages of three blocks- Malihabad, Kakori  and Mall in the western region of Lucknow. The study was initiated in May 2013 and till February 2020, during a span of 7 years, a total of 186 camps were organized in different villages after proper counseling and motivation of women. A total of 5682 women attended these camps and 2949 of them consented to undergo Pap smear examination (55.5%).

In all women, prior to bimanual examination, a scrape smear was taken with the help of wooden spatula from the squamocolumnar junction of cervix by the attending gynecologist and immediately fixed in absolute alcohol. The smears were stained according to the Papanicolaou’s technique and read by the cytologist. In the urban screening, the cytological changes observed in the cervical smears were graded according to the WHO classification of 1973 till 1992 after which Bethesda system of reporting cervical cytology was followed and all the previous cases prior to 1992 were again graded accordingly for the sake of uniformity (World Health Organization, Cytology of the female genital tract 1973; and Bethesda system for reporting cervical/ vaginal cytological diagnosis 1995).On the other hand, in the rural screening, the cervical cytology was classified according to the Revised (2014) Bethesda system [4]

The two non- viral STDs namely Candida albicans and Trichomonas vaginalis and two viral STDs- Human Papilloma Virus (HPV) and Herpes Simplex Virus (HSV) were also diagnosed in the cervical smears of rural and urban women. While the Candida albicans and trichomonal infection were reported on the individual presence of pathogens in the smears, the viral STDs were diagnosed on the basis of cytomorphological changes produced by them in the squamous cells- Koilocytosis (HPV) and multinucleation accompanied with ground glass appearance of nuclei (HSV).

The informed consent of the rural patients were obtained on the Pap smear forms in the form of thumb impression if illiterate and signature if literate. In urban women, since the Pap smear examination was voluntary, hence their consent was not considered essential. All the collected data were statistically analyzed using chi-square test with software SPSS version 22. The ethical clearance was obtained for the rural cervical cancer screening program from the Ethical Committee of the Institute. 

The cytological examination of cervical smears in urban and rural cohorts revealed following findings.

Inflammatory smears were more frequent (42.2%) in urban women than in rural women (32.4%) and the difference was found to be statistically highly significant (ꭓ² = 111.9; p< 0.0001).

The SIL incidence was more than double higher in rural women (16.8%) than 7.2% observed in the urban population and the difference was statistically highly significant (ꭓ² = 412.3; p< 0.0001). This might be due to poor personal genital hygiene prevailing in the rural women who are mostly illiterate and suffer from poverty. This might have resulted in the persistent vaginal infections which remain undetected and untreated due to lack of medical amenities in the villages. It was heartening to note that the majority of SIL were of low grade in rural women (472 out of 498- 16.0%) than 5.5% seen in the urban women and the difference was statistically highly significant (ꭓ² = 392.8; p< 0.0001). However, the incidence of HSIL was higher in urban women (1.6% than 0.8% noticed in the rural women) and the difference was statistically significant (ꭓ² = 8.55; p = 0.003). The carcinoma cervix was observed in 0.6% of the urban women than only 2 cases detected in the rural women (0.06%) and here also the difference was statistically significant (ꭓ² = 13.88; p = 0.0002). A very low incidence of carcinoma cervix in the rural women may be due to selective screening through camp approach as compared to opportunistic screening in their urban counterparts where mostly women with some gynecological complaints come to attend the outpatient department and on the advice of attending gynecologist have undergone Pap smear examination.

Table-1

Incidence of different STDs in the urban and rural population

Incidence of non-viral STDs namely Candida albicans and Trichomonas vaginalis and viral STDs- HPV and HSV were also studied in the urban and rural cohorts (Table-1).  Candida was seen in large number of cases (4.8%) in the rural women than 1.2%  noticed in their urban counterparts and the difference was statistically highly significant (ꭓ² = 255.9; p=0.0001 ). The trichomonal infection was more common in urban women (3.1%) than 1.2% noticed in the rural women and the difference was found to be highly significant (ꭓ²  = 26.6 ; p< 0.001). Both the viral STDs were seen in very low number in both urban and rural women and the difference between the two groups was statistically insignificant (ꭓ²  = 291 ; p= 0.590 for HPV and ꭓ² = 2.29; p=0.130 for HSV)

Table-2

SIL incidence with different STDs

The SIL incidence associated with the above mentioned STDs is shown in Table-2. The SIL rate was higher with both non-viral and viral STDs in the rural women than in their urban counterparts but the difference was found to be significant in the only cases  of Candida albicans (ꭓ²   = 36.3; p<0.001) and HPV cases (ꭓ²   = 13.51 ; p= 0.0002). The difference was statistically insignificant in case of trichomonal infection (ꭓ²   = 0.07; p= 0.788) and HSV infection (ꭓ² = 0.210 ; p= 0.647).

Table-3

SIL incidence in symptomatic and asymptomatic women in the urban and rural population studied

The distribution of symptomatic and asymptomatic women in the two cohorts is shown in Table-3. The percentage of symptomatic women was very high in the rural women (68.3%) as compared to 22.9% seen in their urban counterparts. The difference   was found to be statistically highly significant (ꭓ² = 352.7; p<0.0001).  A high number of symptomatic women in the rural setup may be because of two reasons- firstly screening was selective in the rural women and secondly poor personal genital hygiene due to lack of awareness because of illiteracy. However, the number of asymptomatic women were higher in the urban population (77.1%) than 31.7% noticed in the rural population and the difference was found to be highly significant (ꭓ² = 2895.0 ; p<0.0001). The low number of asymptomatic women in the rural population may be due to fact that these women are mostly reluctant in disclosing their gynecological symptoms.

The SIL incidences in both symptomatic and asymptomatic women of the two cohorts were also analyzed (Table-3). The incidence of SIL was slightly higher in symptomatic women than in the  asymptomatic cases in both rural and urban women but the comparative figures were much higher in the rural women and was found to be highly significant (ꭓ² = 1559.9 ; p<0.0001 in the case of asymptomatic women and ꭓ² = 652.7 ; p< 0.0001 in the symptomatic women). This may be attributed to the presence of persistent vaginal infections prevailing in the illiterate rural women due to lack of awareness of personal genital hygiene. 

Table-4

Relation of SIL incidence with different gynecological symptoms in two types of population studied

Different gynecological symptoms seen during screening of urban and rural population are shown in Table-4. The vaginal discharge was the most common symptom complained by both urban and rural women but the incidence was higher in the rural women (56.1% as against 44.7%). The incidence of pain in lower abdomen and menstrual disorders was almost identical in both the cohorts but the incidence of contact bleeding and postmenopausal bleeding was higher in the urban women. The low detection rate of these two types of bleeding in the rural women may be attributed to the fact that the rural women are mostly illiterate and are very reluctant to disclose their gynecological problems especially bleeding.

The SIL incidence was also analyzed in women complaining different gynecological symptoms in both urban and rural cohorts (Table-4). The SIL rate was higher with contact bleeding in both urban and rural women (24.8% as against 20%) and the difference was statistically insignificant between the two cohorts (ꭓ = 0.06; p= 0.802). The SIL incidence was low with other symptoms but the corresponding figures were very higher (almost double) in the rural women. The SIL incidence with vaginal discharge was 18.0% in the rural women as against 8.8% in their urban counterparts and the difference was found to be statistically highly significant (ꭓ = 62.7 ; p< 0.0001 ). In the cases of pain in lower abdomen, the SIL incidence was just double (16.8%) as against 8.8%  noticed in the urban women and the difference here, too, was highly significant (ꭓ² = 54.2; p<0.0001). Similar findings were also obtained with menstrual disorders and bleeding (14.2% as against 6.9%) and the difference was again found to be only significant (ꭓ² =17.7 ; p<0.001). However, the difference in the SIL incidence in the two cohorts in the cases of postmenopausal bleeding was not found to be insignificant (ꭓ² = 0.41; p=0.524). The persistent vaginal infection prevailing in the rural women due to poor personal genital hygiene may be the reason for the high SIL rate with different gynecological symptoms in the rural setup.

Table-5

Incidence of STDs and SIL in symptomatic women complaining of vaginal discharge in rural and urban population

Since the vaginal discharge was found the commonest gynecological symptoms in both the populations, the incidence of SIL and different STDs were investigated in the two cohorts to find out whether the leucorrhea was specific and had any association with SIL (Table-5).The vaginal discharge was specific   in the comparatively large number of (18.8%) as compared to 12.8% seen in the rural women. Among the non-viral STDs, the vaginal discharge was specific for Candida in 8.8% of the rural population against 4.3% noticed in the urban women. However, the reverse trend was seen with Trichomonas vaginalis as 12.6% of the vaginal discharge cases were specific in the urban women than 2.7% seen in the rural population. Among the viral STDs, the vaginal discharge was specific for HPV in 1.06% of the rural population than 1.4% seen in the urban women. The vaginal discharge was specific for HSV in the urban women only (0.4%).

Table-6

Association of different STDs with SIL in women complaining of vaginal discharge in urban and rural population

When the association of SIL incidence was analyzed with different STDs in the vaginal discharge cases in the two populations, the figures were found very high in the rural women except HSV which was not seen in the rural population (Table-6). Among the non-viral STDs, SIL incidence was 34% in the rural women as against only 2.4% in the urban women. Similarly, the SIL incidence was 16.1% with Trichomonas vaginalis in rural women than only 3.1% seen in the urban women. Among the viral STDs, SIL was associated with 33.3% of koilocytosis (HPV) cases in the rural women as against 12.9% seen in the urban population. The HSV, on the other hand, was associated with SIL in17.6% of the cases in the urban women while this infection was totally absent in the vaginal discharge cases among rural women.

Table-7

Relation of SIL incidence with different clinical lesions of cervix in the two populations studied

Different clinical lesions of cervix were also studied in the urban and rural women and SIL incidence was analyzed in the individual lesions (Table-7). In both the cohorts, the erosion cervix was found to be most common clinical lesion followed by the hypertrophied cervix. The unhealthy cervix was more common in the urban women (22.6% as against 5.3%) while cervix bleeds on touch was more common in rural women (6.5% as against 2.7%). The SIL incidence was higher with cervix bleeds on touch cases in both the cohorts (33.5% in the urban women as against 27.2% in the rural women) and the difference was statistically insignificant (ꭓ² = 0.414; p=520). The SIL rate was just double with other clinical lesions of cervix in the rural women than those seen in their urban counterparts but the difference in the SIL incidence was highly significant in the case of erosion cervix only (ꭓ² =638.6; p<0.0001). As emphasized earlier, this may be related to the poor genital hygiene prevalent in the rural women most of whom are illiterate.

Table-8

Relation of SIL incidence with age in the two populations studied

The SIL incidence has also been investigated in relation to the age in urban and rural cohorts (Table-8). In rural women, majority of the young girls between 21-30 years and young adults between 31-40 years attended the camp as majority of them were symptomatic and form the major component of the screened population (72.3%). In the urban women, the screened population showed rise with the increasing age and was maximum in the old age group beyond 40 years (42.5%). The SIL incidence in the rural women also showed similar trend being maximum in the young age group of 21-30 years (17.7%) and in the adult group of 31-40 years (17.5%) while showed receding trend with old age beyond 40 years (14.7%). In the urban women, on the other hand, the SIL incidence showed rise with increasing age being maximum in the old age group beyond 40 years (10.1%). It should be worth mentioning here that the SIL incidence was 2-3 times higher in the rural women in all age groups than seen in their urban counterparts and the difference in the incidence was found to be highly significant in all age  groups except below 20 years where it was only significant - (ꭓ² =20.6; p<0.001). The statistical figures showing highly significant difference with other age groups was as follows- 21-30 years- ꭓ² =406.3; p<0.0001,31-40 years- ꭓ²   =135.7;p<0.0001 and above 40 years- ꭓ²   =34.8 ; p<0.0001.  A high SIL rate observed in all the age groups of rural women might be due to persistent vaginal infections caused by poor personal genital hygiene prevailing in the illiterate rural women.

Table-9

 Relation of SIL incidence with parity in the two types of population screened

The SIL incidence has also been analyzed in relation to parity in the two cohorts (Table-9). In both the groups, the number of multiparous women were higher being slightly elevated in the rural women (68.7% as against 61.6% in the urban women). The SIL incidence showed rising trend with increasing parity in both the populations but the corresponding figures were 3-4 times higher in the rural women in all parity groups and the difference in the SIL incidence in the different parity groups in the two cohorts was found to be highly significant (Nulliparous- ꭓ²  =35.44; p<0.0001, Parity 1- ꭓ²  =286.4; p<0.0001, Parity 2- ꭓ²  =67.96; p<0.0001 and Parity 3 and above- ꭓ² =256.9; p<0.0001). It may be due to, as told earlier, poor personal genital hygiene prevalent in the rural women. 

The comparative cytological findings in the rural and urban population of Lucknow revealed a high SIL incidence in the rural women (16.8%) than 7.2% found in their urban counterparts. The difference in the SIL incidence between the two groups was more than double and was statistically highly significant.  A high SIL incidence was also reported in their rural screening [6-8] A moderate SIL incidence comparable to that observed in the urban women (7.2%) has been seen in the rural women [9-12]. A more than double higher SIL incidence found in the rural women was, as explained earlier, may be due to illiteracy and lack of awareness of personal genital hygiene. Among the urban women, the factor of low socio- economic status has also been emphasized as high risk factor associated with cervical cancer [13-14] have also found the women of the low socio-economic status are at a greater risk of the disease and their coverage level is unacceptably low [14,15] have also observed that the women of low socio-economic status and minority women are at a particular risk as they do not adhere to the recommended cancer screening guidelines. [16] have also found that women who were never or low educated, lack the knowledge about the risk of cervical cancer.

Among the non-viral STDs, Candida albicans was more common in the rural women than in their urban counterparts (4.8% as against 1.2%). However, trichomonal infection was more common in the urban women (3.1%) than in the rural population (1.2%). [2,17,18] have reported a high incidence of trichomonal infection in the rural women than Candida albicans. 

A highly significant difference in the SIL incidence was seen with the Candida albicans and HPV among the two populations. However, this difference was insignificant in the case of Trichomonas vaginalis and HSV. The cases of carcinoma cervix were seen only in the urban women, in 29.5% of HSV infected women and HPV in only 2.3% of malignant cases. A high percentage of HPV and HSV showing SIL in both the populations shows strong affinity of both these viruses with pre-cancerous lesions of cervix. [19,20] have found strong association of HSV and HPV and the farmer involved in the integration and amplification of HPV in the host cell. It is conclusively proved that high risk HPV infection is related in the development of LSIL and its progression to HSIL and eventually to malignancy [21,22]                    

There was no significant difference in the SIL incidence in the asymptomatic and symptomatic women in both rural and urban cohorts but the corresponding figures were much higher in the rural women than in their urban counterparts (16.3% as against 6.1% in asymptomatic women and 17.1% as against 8.0% in the symptomatic women). No significant difference was seen in the SIL incidence in the symptomatic women and those without symptoms in the rural women and it may be due to shyness factor prevalent among the rural women which are mostly reluctant to disclose their gynecological complaints. On contrary,[23], have reported two-fold increase in the pre-cancerous lesions of cervix in the symptomatic women than in the asymptomatic ones.

As regards gynecological symptoms, vaginal discharge and pain in lower abdomen was found more common in both the setups but was higher in the rural women than in their urban counterparts. It may be due to illiteracy and consequent lack of awareness of personal genital hygiene. However,   contact bleeding and post menopausal bleeding was more common in the urban women. The low percentage of these symptoms found in the rural women may be due to fact that the rural women being illiterate do not want to share their private gynecological problems. 

The SIL incidence was higher with vaginal discharge in both the populations but the figure was almost just double in the rural women. In a colposcopic study, [24], have reported vaginal discharge and irregular bleeding as common symptoms associated with dysplasia [24]. The SIL incidence was also higher with all other symptoms in rural women except contact bleeding where it was slightly higher in the urban women. It is also worth mentioning here that specificity of vaginal discharge was higher with candidal infection in rural women while it was largely associated with trichomonal infection in urban women. The association of viral STDs (HPV and HSV), however, was very low with vaginal discharge in both the populations 

 Among clinical lesions of cervix, the erosion cervix was more common in both the populations followed by hypertrophied cervix. [17,6] have also reported a high incidence of erosion cervix and hypertrophied cervix in the rural women. The SIL incidence was two- fold higher with all clinical lesions in the rural women than in their urban counterparts except cervix bleeds on touch where the reverse trend was seen, the SIL incidence being higher in the urban women (33.5% as against 27.2%). The only plausible explanation to this may be the change of sexual partners resulting in the high STD infection in the urban women. 

The study indicates hypothesis of clinical downstaging of cervical cancer tested and found prevalent in both rural and urban population where the incidence of frank carcinoma and SIL was found higher with all clinical lesions of cervix. It appears that women with clinical lesions of cervix might harbor large number of SIL cases and hence the cytological examination of all women showing clinical cervical lesions is mandatory to reduce the burden of carcinoma cervix in both the populations [25,26]

Analysis of age of women of the two populations revealed interesting results. In the rural setup, the majority of young girls between the age of 21-30 years and young adults between 31-40 years attended the camp while in the urban population the attendance of women increased with increasing age being maximum in women above 40 years. [17], have also found 81% of women belonging to the age group of 21-30 years in their rural screening in Maharashtra. This distribution pattern was also reflected in the SIL incidence  in the rural women which was higher in the young age in the rural women and did not show any correlation with the increasing age while in the urban women, the SIL incidence  showed increasing trend with rising age. It is interesting to point out that the corresponding figures of SIL incidence was higher in all the age groups in the rural population than in their urban counterparts. A high SIL rate in the younger population has also been reported [2,24,6]

As regards parity, the SIL incidence showed progressive rise with increasing parity in both the populations. However, the corresponding figures of SIL incidence in different parity groups was 3-4 times higher in the rural women than in their urban counterparts. A high SIL incidence seen in the rural women with three or more children have also been reported [6,27] have also found advanced age to be a significant risk factor in the development of precancerous lesions of cervix in coastal women of Tamil Nadu. Marriage at an early age resulting in the early sexual activity is very common in the rural India and hence the girls are exposed to the prolonged sexual exposure in their life time [28]. This may be the cause of high SIL rate observed in all the parity groups in rural setup accompanied with the other factors like illiteracy and poor personal genital hygiene. The effect of the early and prolonged sexual experience on the occurrence of cervical premalignancy has also been emphasized [24,29] The other investigators like [30-32] have also observed earlier sexual activity and years of married life as risk factor for carcinoma cervix.

The present comparative study of cytological findings carried out in the rural and urban population of Lucknow has yielded interesting results as the living conditions under the two setups are entirely different. The SIL incidence was found more than double in the rural women than in their urban counterparts but the majority of SIL cases seen in the rural women were of low grade. A high SIL rate in the illiterate rural women may be attributed to the lack of awareness of personal genital hygiene which has been poor due to weak economical status leading to the persistent vaginal infections. However, the incidence of carcinoma cervix was higher in urban women and it may be due to opportunistic screening as Queen Mary’s Hospital where the outpatient screening is been carried out, is a leading Hospital in the North region of State and majority of the  cervical cancer cases visit the centre for diagnosis and treatment. The rural screening, on the other hand, has been selective and based on the camp approach.

The SIL incidence was correspondingly very high with all risk factors in the rural women, such as gynecological symptoms, clinical lesions of cervix and age and parity. This may be related to illiteracy and poverty which is widely prevalent in the rural India. Further the child marriage in the villages leading to the earlier sexual activity and prolonged sexual exposure in life may be also the reason for the high SIL rate in the different age and parity groups.

The comparative evaluation indicates lack of awareness of different risk factors of carcinoma cervix and the detection of the disease in its pre-invasive phase by cytology in the rural population. Further the rural women should be told of ill effects of child marriage and they should be encouraged to adopt family planning measures to control the birth rate as majority of them have been found multiparous in the young stage of life. Hence, education of rural women through health workers regarding all these aspects and organizing camps for the early cytological detection of the disease is essential if the incidence of carcinoma cervix has to be effectively checked in rural India. 

The authors declare that they have no conflict of interest

No funding sources

The study was approved by the Era University, Lucknow, India.

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