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 »  Abstract
 » Introduction
 » Patients and Methods
 » Results
 » Discussion
 » Conclusion
 » Acknowledgments
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  Table of Contents  
Year : 2015  |  Volume : 52  |  Issue : 3  |  Page : 430-437

Gallbladder cancer incidence in Gwalior district of India: Five-year trend based on the registry of a regional cancer center

1 Centre for Genomics, Molecular and Human Genetics, Jiwaji University, India
2 Cancer Hospital and Research Institute, Gwalior, India
3 Cancer Hospital and Research Institute; Department of Surgery, Gajra Raja Medical College, India

Date of Web Publication18-Feb-2016

Correspondence Address:
P K Tiwari
Centre for Genomics, Molecular and Human Genetics, Jiwaji University
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0019-509X.176736

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 » Abstract 

Background: We have reported here the 5-year incidence (2004–2008) of gallbladder cancer (GBC) in North Central India along with its descriptive epidemiology. This provides potential clues for better prevention. The present study has also evaluated the association of ABO blood groups with GBC. Patients And Methods: The study comprised 742 GBC cases referred to the regional cancer hospital, Gwalior, during 2004–2008. The demographic statistics of Gwalior district was considered to calculate the relative risk and incidence rates. ABO blood group distribution amongst 90,000 healthy subjects registered in the local blood bank during 2002–2007 was taken as controls to study the association of blood groups with GBC. Results: The age-standardized total incidence rate of GBC was calculated to be 7.16/1,00,000. The relative risk of females getting GBC was 2.693 at 95% confidence interval of 2.304–3.151 (P < 0.0001). The females formed 69.5% of total cancer cases, with age-standardized incidence rate of 10/1,00,000. The mean age of male and female GBC cases was found to be 55.4 years (SD = 13, SE = 0.77) and 51.5 years (SD = 12.3, SE = 0.50), respectively. The blood groups A (P = 0.0022) and AB (P < 0.0001) had a positive association with GBC with significant level of differences in comparison to controls. Conclusion: Our study provided an estimate of a 5-year incidence of GBC in North Central India for the first time. With regard to the association of risk factors like obesity, age, and urban living with GBC, the findings of the present study are contradictory to the general opinion. Blood groups A and AB were found to be associated with GBC, which would be provisional for further investigations.

Keywords: ABO blood groups, gallbladder cancer, cholecystitis, cholelithiasis

How to cite this article:
Barbhuiya M A, Singh T D, Poojary S S, Gupta S, Kakkar M, Shrivastav B R, Tiwari P K. Gallbladder cancer incidence in Gwalior district of India: Five-year trend based on the registry of a regional cancer center. Indian J Cancer 2015;52:430-7

How to cite this URL:
Barbhuiya M A, Singh T D, Poojary S S, Gupta S, Kakkar M, Shrivastav B R, Tiwari P K. Gallbladder cancer incidence in Gwalior district of India: Five-year trend based on the registry of a regional cancer center. Indian J Cancer [serial online] 2015 [cited 2022 Nov 28];52:430-7. Available from:

 » Introduction Top

Gallbladder cancer (GBC) incidence has a marked variation all over the world. It is the most common malignancy of the biliary tract, and the seventh most common amongst gastrointestinal cancers.[1] The highest incidence and prevalence is found in Latin American and Asian countries.[2],[3] The mortality and morbidity due to GBC is low in Europe and America. Females are more prone to the disease than males, having two to sixfold greater incidence in many populations. [4] The survival rate is low due to late detection and poor prognosis. Various risk factors are reported to be associated with GBC, out of which gallstone is considered one of the primary factors.[5],[6] There is high incidence of GBC in India. The major published data from Indian population demonstrates the highest prevalence in North and Eastern part of India.[7] The National Cancer Registry Programme of India showed the incidence in North India as 4.5 cases per 1,00,000 in males and 10.1 cases per 1,00,000 in females.[8] There is no detailed cancer registry available for North Central India, where GBC is reported to be the highest amongst gastrointestinal tract cancers.[9]

Our aim in the present study is to evaluate the incidence of the disease on the basis of self-reported and referred GBC cases registered in a Regional Cancer Centre in India during 2004–2008. This is the first report of a 5-year data from any cancer hospital in North Central India on GBC, providing a direct estimation of GBC trends in the study population, noting differences between males and females, different age groups, socioeconomic classes, occupations, caste groups, and year-wise incidence. The distribution of GBC in persons with different ABO blood groups is also correlated to evaluate possible association of blood groups with the disease.

 » Patients and Methods Top

Study area

The geographic coordinates of the study district Gwalior, Madhya Pradesh, in India are 26° 13′ 25′′ North, 78° 10′ 45′ East. The total area of the district is 5,214 km 2. The total population of the district is 16, 32, 109, with about 8,83,317 males and 7, 48, 792 females as per 2001 census. The urban and rural population is 9,83,008 and 6, 49, 101, respectively (district information page, NIC).[10]

Study population

The cases in the present study were included on the basis of clinical symptoms, ultrasonography (USG), and computer tomography (CT) scanning at the Cancer Hospital and Research Institute, Gwalior (Regional Cancer Centre Code-08). The patients coming from outside the Gwalior district were excluded from this analysis. The total population of Gwalior district was taken as the risk group. The relative risk (RR) for various parameters was calculated in comparison with the demographic statistics of the study population. ABO blood groups and their association with GBC were analyzed in relation to the blood group distribution amongst 90,000 healthy subjects registered in the blood bank of CHRI and Gajra Raja Medical College, Gwalior, during 2002–2007. A total of 897 cases were referred to the hospital with suspected GBC from different hospitals of Gwalior. Out of these, 20 cases were post-cholecystectomy malignancies, 135 were non-malignant gallbladder ailments, and 742 were clinically confirmed GBC.

Data collection

Information obtained during patient registration in the hospital was the primary source of data. Various parameters like sex, age, caste, food habits, drinking habits, socioeconomic status, education, occupation, body mass index (BMI), blood groups and clinical data were collected retrospectively from the hospital register and used for statistical analysis. The study was approved by Institutional Human Ethics Committee.

Statistical analysis

The RR and odds ratio were calculated at 95% Confidence Interval (CI). Chi-square test and/or Fisher's exact test were carried out using the statistical tool SPSS.[11] The normality distribution of age in male and female was expressed by normality plot and notched outlier box plot with Shaprio–Wilk statistic. The incidence rate and age-standardized incidence rates were calculated using world population by the statistical tool WinPepi.[12] The risk and incidence calculations were carried out on the basis of the demographic statistics of the study area.

 » Results Top

Clinical presentation

About 897 cases with gallbladder mass were referred to the cancer hospital on the basis of general clinical symptoms and USG imaging from various hospitals. However, further CT and cytological investigations confirmed 742 gallbladder masses with or without stones to be tumors. Gallbladder stones were found in 77.67% of the malignancies. The clinical symptoms at the time of admission were postprandial right upper quadrant pain with frequent change in character (53.36%); short duration right upper quadrant pain along with nausea, vomiting, fever (20.88%); jaundice, weakness, anorexia, weight loss, and pain (25.74%). The average direct bilirubin level in plasma was found to be 5.8 mg/dL (SD = 2.8), with a total bilirubin of 8.4 mg/dL (SD = 3.5). The average levels of alkaline phosphatase (ALP), serum glutamic oxaloacetic transaminase (SGOT), and Serum glutamic pyruvic transaminase (SGPT) were found to be 671 U/L (SD = 250), 115.7 U/L (SD = 36.3), and 136.1 U/L (SD = 87.1), respectively. The blood urea and creatinine levels were found elevated at an average of 34.58 mg/ dL (SD = 7.8) and 1.249 mg/dL (SD = 0.48), respectively [Table 1]. The patients' hemoglobin level on average was 10.02gm/dl (SD = 1.925). The blood sugar level estimated at the time of admission of the patients showed that 20% of the cases were having elevated level of blood glucose with possible diabetic condition.
Table 1: Clinical and pathological data of 742 gallbladder cancer patients

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The major location of gallbladder mass on the basis of imaging was in fundus (40.02%), followed by diffuse (36.38%), body (16.98%), and neck (6.6%). The infiltration pattern observed by USG finding has shown the highest infiltration of gallbladder mass to porta hepatis and liver (50.33%), followed by lymph node at porta (32.11%), metastasis to liver (10.16%), and ascitis (5.4%). There were few cases involving duodenum and stomach (2.02%). Most of the GBCs were found to be adenocarcinoma (84.88%) of epithelial origin, squamous cell carcinoma (8.7%), small cell and other non-small cell carcinoma (6.32%). The TNM classification of resected tumors was as follows: Grade I (1.4%), Grade II (14.13%), Grade III (23.07%), and Grade IV (61.33%) [Table 1].

Total incidence

The incidence was calculated as the proportion of people in a population that was initially free of the disease and had developed the disease within a specified time interval.[13] The highest number of GBC cases was recorded in the year 2008 followed by 2005. The 5-year (2004–2008) crude incidence rate of GBC in the study population was found to be 4.56/1,00,000. The age-standardized total incidence rate was calculated to be 7.16/1,00,000.

Age and sex-wise incidence rates

The females consisted of 69.5% of total cancer cases, with crude incidence rate of 6.8/1,00,000 and age-standardized incidence rate of 10/1,00,000. The males constituted 30.5% of cancer cases, with a crude incidence rate of 2.5/1,00,000 and age-standardized rate of 4.5/1,00,000. The RR of females getting GBC was 2.693 at 95% CI of 2.304–3.151 (P< 0.0001) [Table 2]. The mean age for female GBC cases was found to be 51.5 years (SD = 12.3, SE = 0.50). The normality plot and notched outlier box plot drawn at 95% CI showed that the highest number of affected females belonged to the age group of 40–60 years, with normal quartile range positive for the disease above the age of 50 years (W statistic = 0.99 at P< 0.0001 and skewness = 0.13) [Figure 1]a. The mean age for male cases was 55.4 years (SD = 13, SE = 0.77). The incidence was highest amongst males of 45–65 years, with normal quartile range positive for the disease above the age of 55 years (95% CI, W statistic = 0.99 at P = 0.038). In males, there was significant increase in the occurrence of cancer above the age of 45 years with negative skewness (-0.12) [Figure 1]b.
Table 2: Distribution of GBC in different age groups and sex

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Figure 1: (a) Age-wise frequency distribution of female GBC cases. (b) Age-wise frequency distribution of male GBC cases

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Area-wise incidence

We observed variation in the incidence of GBC in rural and urban population with higher incidence in rural people (5.96/1,00,000) in comparison to urban people (3.62/1,00,000). The RR of rural people getting cancer was 1.642 (95% CI: 1.422–1.896, P< 0.0001) [Table 3].
Table 3: Distribution of gallbladder cancer according to various parameters

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Incidence in terms of literacy

The highest incidence of GBC (6.8/1,00,000) was amongst the illiterates (51% of the total affected) of the study population, with an RR of 1.492 (95% CI: 1.309–1.701). The incidence rate of the disease in people with college level education was 3.8/1,00,000 (RR = 0.8371, 95% CI: 0.6146–1.140, P< 0.2585), with secondary education was 7.6/1,00,000 (RR = 0.1678, 95% CI: 0.1380–0.2042, P< 0.0001), with middle school education was 1.9/1,00,000 (RR = 0.3990, 95% CI: 0.2797–0.5692, P< 0.0001), with primary education was 3.4/1,00,000 (RR = 0.7114, 95% CI: 0.5559–0.9105, P = 0.0066), and the incidence in those with below primary education was 4.7/1,00,000 (RR = 1.078, 95% CI: 08685–1.337 at P = 0.4970) [Table 3].{Table 3}

Other factors

Many (44.07%) of the GBC patients recorded a low BMI. Farmers (44.17%), followed by laborers (17.61%) constituted the major chunk of GBC patients. Majority of cancer cases were registered to be non-alcoholic (78.9%) and non-smokers (48.71%). The drinking water source of most of the patients was bore well (53.73%), followed by public water supply (38.8%). The low-income group of people (below Rs. 70,000/- annual income) constituted the highest number of GBC patients. The lower caste Hindu (Vaishya and Sudra) people were mostly found to be affected, with lower caste people constituting the highest percentage amongst males. The highest percentage (78%) of people with GBC was vegetarian [Table 3].

Association of blood group antigens with GBC

The “AB” blood group people were having the highest risk of occurrence of GBC at a relative risk of 1.75 (significant at 95% CI = 1.40–2.18, Woolf's approximation), followed by “O” blood group persons (RR = 1.04, significant at CI = 0.88–1.23) in comparison to other blood groups. But the chi-square value for association of “O” blood group people along with “B” blood group people with GBC was found to be statistically non-significant. The “AB” blood group had a positive association with GBC (chi-square statistic = 24.41 at degree of freedom = 1 with P< 0.0001), which was highly significant [Figure 2]. The “A” blood group persons also had significant positive association with GBC (chi-square statistic = 9.347 at degree of freedom (DF) = 1 with P = 0.0022). Individual risk for each blood group antigen was calculated as well. This also indicated that the “AB” blood group was having the highest risk with positive association with GBC. Although the “A” blood group was having positive association in comparison to other blood groups, it did not show significant association with GBC when compared with B blood group independently. We observed significant variation in the distribution of blood groups amongst the men and women affected with GBC, where “O” blood group males were found to be highly affected (OR = 3.528, 95% CI = 2.474–5.031). The RR of occurrence of GBC in A, AB, and B blood group men was significantly low in comparison to that in women. Thus, the significant divergence in A (P = 0.0268) and AB (P = 0.005) blood group distribution in male and female GBC patients with higher number of affected females verifies the findings.
Figure 2: Association of blood group antigens in gallbladder cancer cases and controls

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 » Discussion Top

In the current study, the clinical presentation in GBC follows the general pattern of abdominal pain, jaundice, and increased levels of liver function enzymes. But the average liver function enzyme levels (ALP = 671 U/L, SGOT = 115 U/L, SGPT = 136.1 U/L, total bilirubin = 8.4 mg/dL) in the present study population were higher in magnitude than those in the GBC patients from China (ALP = 119–220 U/L, SGOT = 74–89 U/L, SGPT = 78–113 U/L, total bilirubin = 1.7–3.5 mg/dL) as reported earlier.[14] This implies that the normal threshold level of ALP, SGOT, SGPT, and serum bilirubin could also be higher in this study population, but this needs further investigation to define the normal threshold of these high utility enzyme markers. Right upper quadrant abdominal pain was the most common symptom in GBC as reported earlier.[15] The highest number of carcinoma gallbladder is of Grade IV (61.41%), thus reflecting the problem of late diagnosis, while the Grade I (1.3%) GBC cases were incidental and diagnosed during cholecystectomy. Adenocarcinoma of epithelial origin and infiltrating mass of gallbladder fundus were the most common histological types as reported earlier.[16],[17]

India has a diverse ethnic population living in different areas with variation in the incidence of GBC. The North and Northeastern parts of India have a high incidence of GBC (9/1,00,000), whereas the southern part of the country has negligible (1/1,00,000) disease load.[8] This shows an apparent difference in disease susceptibility from north to south of the country. The highest incidence of GBC was reported in Delhi (10.1), Kamrup (8.1), Kolkata (5.4), and Mumbai (3.2).[7],[18] Our study provides a firsthand information on the relatively high incidence of the disease with age-standardized incidence rate (SIR) of 7.1/1,00,000 in North Central India. The women were highly affected with an SIR of 10/1,00,000 and an RR of 4.86, and men had an SIR of 6.8/1,00,000. A high incidence of GBC in North Central India has been reported earlier, but a detailed report was lacking.[9] As per the reports from Uttar Pradesh and western Bihar regions of India, GBC constitutes 4.4% of all malignancies. [19] There are significant differences in the incidence of GBC in various populations worldwide.[2],[3] Chile has a high incidence rate of GBC, with a rate of 17.5 per 1,00,000.[17] The International Agency for Research on Cancer estimates show that the incidence is less in Europe and America, but the condition is prevalent in Latin American and Asian countries.[20] There is also a wide variation of GBC incidence in different ethnic groups all over the world.[5] Chilean Hispanics, Mapuche, Native Americans, and Amerindians are highly susceptible to GBC.[21] There has been a significant rise in the incidence of it in Chinese, Indian, Korean, and Japanese populations.[22],[23]

GBC is generally considered as a disease of old age. High incidence of the disease was observed in persons above the age of 65 years in the world population.[5] Interestingly, in the present study population, we observed a marked lowering in age for GBC development (40–60 years in females and 45–65 years in males with a high cumulative risk in this group). According to various studies, the age of menopause in India is 41–59 years, and this varies across the world.[24],[25],[26] GBC is reported to be biased toward women and menopause can play an important role in its development due to the hormonal and physiological changes associated with it.[27] This may also have bearing with the reduced age of susceptibility to GBC. Our study is imperative for further large-scale studies on the age of menopause related hormonal changes and their association as etiological factors of GBC in females. The mean ages of GBC patients (51.5 years in males and 55.5 years in females) in India are lower compared to those of the world population.[5],[17] This might be a reflection of the average low life expectancy in India. However, lowering of age of onset in the present study population can be indicative of genetic susceptibility toward GBC. The genetic risk factors for GBC are largely unknown even though there are reports of its familial occurrence. There are reports of genetic predisposition of GBC in different ethnic communities.[28],[29] The present study shows that the lower caste Hindu people formed the highest percentage of GBC cases and this needs further investigation for possible genetic predisposition of the disease in them. We have also encountered a number of families having gallstone diseases with affected first-degree relatives (unpublished data). GBC manifests itself by long-term gene–environment interaction and exposure to various environmental factors. There is little evidence of higher risk in sibs of affected probands. But as there are genes involved, familial pattern of risk cannot be ignored. A few important studies that support familial occurrence of gallstones include Framingham Study and the Star County Study.[30],[31] The Star County Study reported the risk of gallbladder disease (GBD) in the first-degree relatives of the affected probands to be 1.8 times the probability of a random individual being affected in a sample of 183 affected probands. A more recent extensive twin study has indicated significantly higher gallstone presence in monozygotic twins. The concordance rates were 12% and 6% in monozygotic and dizygotic twins, respectively, supporting its genetic association.[32] The identification of a major susceptibility locus (Lith1) was made by quantitative trait locus mapping in mice. A detailed fine mapping of the candidate gallstone disease genes is reported in murine cases also.[33],[34] However, human association of these genes on a large scale is yet to be established. A New Delhi based study has shown high prevalence of gallstones in the first-degree relatives of gallstone patients (65% positive relatives were women).[35] Evidences of familial risk of GBC are provided by reports of two Hispanic families from North Mexico, and two affected Choctan brothers from Arizona. It is very interesting to note that the precursor to GBC, gallstones, is quite common and familial in high incidence Amerindian population.[36],[37],[38],[39] Since GBC is the final phenotypic expression of a decade-long process, the familial occurrence is difficult to be traced. The demographic factors may also play a role in the process of final phenotype (GBC) to appear as familial. This was described as “phenotype amplification” by Weiss (1985).[40] Monogenic predisposition to cholelithiasis is ascribed to a few ABC transporter genes like ABCB4, ABCB11, CYP7A1, and CCK1R. In addition, apoB, apoE, CYP7A, and LDL receptor polymorphisms in gallstone diseases were also implicated in human population.[34],[41],[42] The association of these polymorphisms has shown widespread variation across different populations, for example, ApoB-100-Xba I polymorphism in a small cohort of population in North India showed an increase in the homozygous (X-/-) genotype in patients with GBC (54%).[43] In the Chinese population, however, ApoB-100-Xba I polymorphism revealed X+ allele to be associated with a higher incidence of GSD.[41] Similarly, different variants of inflammatory genes (IL-8, Il-8RB, RNASEL, and NOS2) were found associated with gallstones, while VEGF gene was found associated with GBC. Multiple single nucleotide polymorphisms (SNPs) of these genes and one IL-8RB haplotype consisting of three SNPs were reported to be associated with the risk of bile duct cancer.[29] These polymorphisms are dependent on various factors including environmental factors and ethnicity. Recently, a genome wide association study (GWAS) of 1,896 pancreatic cancer patients and 1,939 controls identified an SNP in intron 1 of the ABO gene (rs 505922) which was found to be a genetic risk factor for pancreatic cancer, but there were no reports of ABO gene polymorphisms and their association with GBC.[44] It is interesting to note that we observed a significant association of AB blood group antigen with GBC in our study. The ABO blood group frequency varies in different ethnic, geographic, and socioeconomic groups.[45] Earlier studies also suggested that ABO blood group antigens are associated with various types of malignancies, like ovarian cancer, breast cancer, and pancreatic cancer.[44],[46],[47],[48] An earlier study by Pandey et al. (1995) indicated an increased frequency of A and AB blood groups in GBC in a small set of 69 GBC patients.[49] Further investigations can be suggestive of any gene variants or SNPs in ABO locus that may be acting as a genetic risk factor for GBC.

Amongst the non-genetic environmental and demographic factors, we found a strong association between GBC and illiteracy. Illiteracy is one of the risk factors associated in the present study with a high RR of 1.492 (95% CI: 1.309–1.701). Overall, people with low education are highly affected. The other interesting finding of the present study is higher RR of GBC amongst rural people. This is in contrast to an earlier study in Chile, which reported urban association of the disease.[17] The present observation can be due to prolonged medical neglect due to lack of proper diagnostic and treatment modalities available in the rural area. There are also variations in lifestyle, food habit, and economic condition of rural and urban populations in the study area. Furthermore, our results are in contrast to the general opinion that non-vegetarian people are at higher risk of developing cancer because maximum number of GBC patients were found to be vegetarians. A more comprehensive investigation is needed to affirm any possible association of these factors with GBC. We also observed that farmers and laborers with low annual income were another group of people with a high incidence of GBC. It strongly suggests the need for conducting awareness program amongst the rural and illiterate people about the disease for its effective prevention. Although this study found greater proportion of the GBC patients to be non-smokers and non-alcoholics, a detailed case control study is needed. The vast majority of GBC patients in the current study were found with low BMI (<22.9). This is not in accordance with an earlier study that has shown high BMI and obesity as risk factors for GBC.[50] A high BMI (≥25.0) was reported to be associated with a 1.6-fold increased risk of GBC.[51] Further investigation is needed on the study population to know if low BMI has been a cause of the disease or a manifestation of the disease itself. Most of the patients (53.73%) in the study were found to have underground bore wells as the source of drinking water. A detailed investigation is required if this can be a potential risk factor for developing GBC in the study area.

 » Conclusion Top

CHRI, Gwalior is the only superspecialty cancer treatment center in North Central India which registers most, if not all, of the cancer patients coming from this region. Thus, the present study represents an optimal incidence of GBC in the study population. As there is a lack of availability of GBC incidence data from the Asian region, especially India, for the first time, our study provides an estimate of a 5-year incidence data from North Central India. A limitation of the present study was that since the follow-up data were not available, the survival rate could not be calculated. The poor living standard and inadequate medical facilities available for detection of cholelithiasis or cholecystitis in various regions of India make people vulnerable to GBC (the late-onset phenotype) since the key to GBC prevention is the diagnosis of gallstones and removal of gallbladder. Indications from our earlier and present studies in North Central India suggest that factors like obesity which are associated with gallstone diseases may not be the major risk factor for GBCs, as against the general opinion. The evidence for this comes from the low-income group people who are less obese and deprived of high fat diet, but show high incidence of GBC. This mismatch may be attributed to the lack of availability of proper medical treatment to the low-income population, as well as to malnutrition. Above all, association of blood groups “A” and “AB” with GBC may be taken as exploratory source for further investigation on gene variants of the ABO locus, which may be fundamental to the genetic risk of developing of GBC.

 » Acknowledgments Top

We acknowledge Indian Council of Medical Research (ICMR), Department of Biotechnology, and Department of Science and Technology, Government of India for research support to PKT through various research projects. MAB acknowledges ICMR for senior research fellowship and MPCST for young scientist award. TDS acknowledges ICMR for senior research fellowship. SSP also acknowledges Department of Atomic Energy (DAE) for fellowship.

 » References Top

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