Descriptive Epidemiology of Childhood Cancers in Bangalore, India

Descriptive Epidemiology of Childhood Cancers in Bangalore, IndiaAuthor(s): Ambakumar Nandakumar, Narayanappa Anantha, L. Appaji, Kumara Swamy,Geetashree Mukherjee, Thalagavadi Venugopal, Sreerama Reddy and Murali DharSource: Cancer Causes & Control, Vol. 7, No. 4 (Jul., 1996), pp. 405-410Published by: SpringerStable URL: http://www.jstor.org/stable/3552672 .

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Cancer Causes and Controi 1996, 7, pp. 405-410

Descriptive epidemiology of childhood cancers in Bangalore, India

Ambakumar Nandakumar, Narayanappa Anantha, L. Appaji, Kumara Swamy, Geetashree Mukherjee, Thalagavadi Venugopal, Sreerama Reddy, and Murali Dhar

(Received 19 September 1995; accepted in revised form 26 April 1996)

While fairly complete and reliable incident data on childhood cancers are available from the registries in India, mortality and survival information is not. Information concerning the latter was obtained by the Bangalore cancer registry through active follow-up involving visits to homes of patients. Between 1982 and 1989, 617 cases of cancers in childhood were registered, giving an age-standardized incidence rate of 84.8 and 48.4 per million in male and female children, respectively. Active follow-up provided mortality/survival information in 532 or 862 percent of these cases. Overall, observed five-year survival was 36.8 percent (both genders combined) with a relative survival of 37.5 percent when childhood mortality in the general population was taken into account. The five-year relative survival was best for thyroid carcinoma (100 percent) followed by Hodgkin's disease (73 percent) and retinoblastoma (72.9 percent). Survival was comparatively low, being 9.9 percent in acute nonlymphatic leukemia and less than 20 percent in rhabdomyosarcoma and the category grouped as 'other malignant neoplasms.' Survival in Hodgkin's disease was influenced by clinical stage at prtsmtation, but was not statistically signiicant possibly due to small numbers. Cancer Causes and Contrl, 1996, 7, 405-410

Key words: Childhood cancers, incidence, India, mortality, survival.

Introduction

Children below 15 years of age constitute a little over one-third of the total population (all ages) but form less than five percent of the total cancer burden in the population of Bangalore as well as in other population- based cancer registries in India.' Nonetheless, cancers in childhood are important for several reasons. Geographic and ethnic differences in the occurrence of childhood cancer have been described."' Recent advances in chemotherapy have resulted in dramatic improvement in survival in several types of childhood cancer.5'6 Although some

genetic and extrinsic factors have been associated with the etiology of cancers in childhood, there remain wide gaps in such knowledge.' Lastly, from the viewpoint of cancer control, particularly in the context of developing countries like India, there is a need to detect cancers such as Hodgkin's disease at an early curable stage of the disease.

Since few studies on the incidence, mortality, and survival experience of malignancies during childhood have been reported from a developing country, the present

Authors are with the Kidwai Memorial Institute of Oncology, Bangalore, India, in the Coordinating Unit, National Cancer Registry, Programme of India, Indian Council of Medical Research (Drs Nandakumar, Dhar); the Population Based Cancer Registry (Drs Nandakumar, Anantha, Venugopal, Reddy); Paediatric Oncology (DrAppaji); Radiotherapy (Dr Swamy); and Pathology (Dr Mukheree). Address correspondence to Dr Nandakumar, National Cancer Registry Programme, Kidwai Memorial Institute of Oncology, Post Box No. 2930, Hosur Road, Bangalore 560029 India.

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report attempts to give a comprehensive account of the descriptive epidemiology of these cancers.

Materials and methods

As part of the National Cancer Registry Programme of the Indian Council of Medical Research, a Population Based Cancer Registry (PBCR) was started from 1 January 1982 at Kidwai Memorial Institute of Oncology (KIMIO), Bangalore. The registry covers the area of

Bangalore Urban Agglomeration with a total population of 4.1 million and a male:female ratio of 1:0.9.8 The basic

pattern of working of the registry has been described earlier and it has been estimated that the coverage of cancer cases by the registry is over 90 percent.'

All cancers in children below 15 years of age that were

diagnosed between 1 January 1982 and 31 December 1989 and registered in the PBCR of Bangalore constituted the study group. Both ICD-9tO and ICD-O-1" (both Topography and Morphology) were used to code all

neoplasms in the registry. Childhood cancers were classified according to the scheme given by Birch et al,"' with the slight modification adopted by Stiller and Bunch.' Over 90 percent of the childhood cancers registered had a microscopic confirmation of the diagnosis.

Case records of all patients with Hodgkin's disease (HD) were once again reviewed for abstracting information on

pretreatment Ann Arbor staging.' This provided a better assessment of the clinical extent of the disease at the time of initial diagnosis. Incidence and mortality rates were calculated, respectively, for all cases registered with the registry and all cancer deaths of children for the period 1 January 1982 to 31 December 1989. The rates were standardized according to the world population for the three five-year age groups.'4 Both the incidence and mortality rates were expressed per million population of children and standard errors of the rates also were

calculated."' Trained social investigators conducted active follow-up,

through visits to homes of patients mainly to determine the vital status, whether the patient was alive or dead, and if the latter, the date of death.9'" Matched deaths and patients who were in attendance at KIMIO were excluded from active follow-up. These constituted 24 percent of cases. A combination of visits to homes and last hospital attended was done for the remainder. The cut-off date for determining vital status was 1 January 1995. Patients who had died during 1995 but were alive on 1 January 1995 were considered alive for the purpose of this analysis.

Of the 617 cancers registered, information on vital status was available for 488 of them and partial follow-up information was available in 44 cases, with no follow-up information in the remaining 85 cases. Thus, 532 of 617 cases (86.2 percent) were included for survival analysis.

Observed survival was based on death from all causes. Patients with partial follow-up were censored as and when they were lost to follow-up, and observed survival proportions were computed using the Kaplan Meier method of calculating survival." For HD, clinical stage and histologic subtype at presentation also were examined.'", The effects of age and mortality from all causes of death were removed by computing survival relative to that expected in the total population of Bangalore by age and gender using the life table method.'",

In order to determine the fatality ratio as well as to assess the statistical significance, the regression model of Cox was used.2' Calculation for both survival and proportional hazard (fatality) ratio of Cox was done using the EGRET software package.'

All survival analyses were computed separately for male and female children. Since the small differences noticed between the genders were either not statistically significant or were accounted for by very small numbers, the results of survival analysis are presented for both genders combined.

Results

Incidence and mortality The average annual incidence rate (IR) per million population of children by age group and gender is given in Table 1.

Table 2 gives the number of cases, average annual age standardized rate (ASR) per million children with standard error (SE), and male:female ratio of ASR of individual childhood cancers. In general, ASRs were higher in male compared with female children. This was most notably seen in Hodgkin's disease where the male:female ratio of the ASR was 7.8. The ASRs were nearly identical in both genders with respect to astrocytoma, 'other brain tumors,' retinoblastoma, Wilms' tumor, Ewing's sarcoma, and the category classified as 'other malignant neoplasms.' Only osteosarcoma among the bone tumors, germ cell tumors,

Table 1. Number, average annual incidence rate per million (IR), and standard error (SE) of all childhood cancers by age and gender

All cancers Males Females

No. IR SE No. IR SE

Age (yrs) 0-4 134 92.9 8.0 75 53.1 6.1 5-9 141 82.8 7.0 79 47.5 5.4 10-14 122 76.2 6.9 66 42.9 5.3 0-14 397 83.6 4.2 220 47.7 3.2

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Table 2. Number, annual age standardized incidence rate per million (ASR), standard error (SE), and male:female ratio (MFR) of individual childhood cancers (both genders)

Childhood cancers No. ASR SE MFR

Lymphoid leukemia 114 12.7 1.2 2.0 Acute non-lymphoid leukemia 57 6.2 0.8 2.5 Chronic myeloid leukemia 14 1.4 0.4 1.7

Hodgkin's disease 54 5.2 0.7 7.8 Non-Hodgkin's lymphoma 79 8.4 1.0 2.5

Ependymoma 7 0.8 0.3 2.8 Astrocytoma 28 2.9 0.5 1.1 Medulloblastoma 31 3.3 0.6 1.5 Other brain tumors 16 1.6 0.4 1.0

Neuroblastoma 29 3.4 0.6 2.1

Reti noblastoma 24 3.1 0.6 1.1

WlIms' tumor 32 4.1 0.7 1.1

Hepatic tumors 6 0.7 0.3 2.0

Osteosarcoma 12 1.1 0.3 0.7 Ewing's sarcoma 6 0.6 0.3 0.9 Other bone tumors 3 0.3 0.2 2.0

Rhabdomyosarcoma 20 2.2 0.5 1.2 Other soft tissue tumors 9 0.9 0.3 1.9

Germ cell tumors 18 2.1 0.5 0.8

Thyroid carcinoma 10 0.9 0.3 0.4

Nasopharyngeal carcinoma 6 0.6 0.2 2.0

Other epithelial tumors 18 1.9 0.4 1.5

Other malignant tumors 24 2.6 0.5 1.0

Total 617 66.8 2.7 1.8

and carcinomas of the thyroid, had a higher incidence in female compared with male children.

For all childhood cancers, the ASR was 84.8 per million in males and 48.4 per million among females giving a male: female incidence ratio of 1.8.

Leukemia and lymphomas constituted about 51.6 percent of all cancers. Of children with Hodgkin's disease, 70.6 percent presented with stage III or stage IV. The more common histologic subtype was the mixed cellu- larity type (73.8 percent) followed by the nodular sclerosis (14.2 percent) and lymphocytic predominant type (11.9 percent).

The mortality rate with SEs and the mortality incidence ratio (MIR) by age group and gender are shown in Table 3.

Table 3. Number, average annual mortality rate per million children (MR), standard error (SE), and mortality-incidence ratio (MIR) of all childhood cancers by age group and gender

All Males Females cancers No. MR SE MIR No. MR SE MIR

Age (yrs) 0-4 67 46.4 5.7 0.50 35 24.8 4.2 0.47 5-9 57 33.5 4.4 0.40 47 28.3 4.1 0.60 10-14 59 36.8 4.8 0.48 28 18.2 3.4 0.42 0-14 183 38.5 2.8 0.46 110 23.9 2.3 0.50

Table 4. Number of cases and five- and 10-year observed survival proportion (%) with respective standard errors (SE) for all childhood cancers by age group and gender and In individual childhood cancers (both genders)

No. Observed survival

5-yr SE 10-yr SE Age group

0-4 yrs 181 31 3.6 28 3.5 5-9 yrs 194 41 3.7 31 3.5 10-14 yrs 157 38 4.0 25 3.9

Gender Male 347 39 2.8 29 2.8 Female 185 33 3.6 28 3.4

Type of cancer Lymphoid leukemia 102 35 4.9 22 4.3 Acute non-lymphoid leukemia 53 10 3.1 7 2.3 Chronic myeloid leukemia 13 26 10.1 13 5.8

Hodgkin's disease 51 72 7.8 59 8.4 Non-Hodgkin's lymphoma 68 33 5.7 18 4.7

Astrocytoma 25 40 10.2 34 9.5 Medulloblastoma 28 43 9.6 34 8.8 Other brain tumors 11 51 17.8 51 17.8

Neuroblastoma 22 28 9.1 23 7.9

Retinoblastoma 18 7118.9 71 18.9

Wilms' tumor 24 27 8.5 27 8.5

Osteosarcoma 11 4416.9 22 9.7

Rhabdomyosarcoma 19 13 5.5 13 5.5

Germ cell tumors 15 3612.0 29 10.4

Other epithelial tumors 16 61 15.7 61 15.7

Other malignant tumors 18 17 6.4 8 3.6

All childhood cancers 532 37 2.2 29 2.2

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Table 5. Comparative, age-standardized incidence rate (ASR) of the more common childhood cancers (both genders) from selected registries

Childhood cancers Present study Bombay24 USA26 UK25 Australlas (1982-89) (1970-79) (1983-87) (1971-80) (1980-89)

Acute lymphatic leukemiaa 12.7 11.0 26.7 29.7 34.3 Acute non-lymphoid leukemia 6.2 3.3 5.0 5.9 6.2

Hodgkin's disease 5.2 4.2 5.5 4.1 5.5 Non-Hodgkin's lymphoma 8.4 4.6 5.1 5.7 7.2

Ependymoma 0.8 0.5 1.8 3.2 2.9 Astrocytoma 2.9 2.9 11.8 8.9 13.3 Medulloblastoma 3.3 1.5 4.2 4.9 5.4

Neuroblastoma 3.4 3.1 6.6 7.0 8.3 Retinoblastoma 3.1 5.2 3.0 3.5 3.6 Wilms' tumor 4.1 3.8 6.5 7.2 7.6

Osteosarcoma 1.1 1.6 3.1 2.5 3.3 Ewing's sarcoma 0.6 2.1 2.6 1.7 4.5

Rhabdomyosarcoma 2.2 1.7 4.0 4.3 4.2

a Present study Includes acute lymphatic leukemia and other lymphoid leukemia.

Table 6. Comparative five-year survival proportion (%) of more common childhood cancers (both genders) from selected registries

Childhood cancers Present study USA27 UK28 Australias (1982-89) (1983-87) (1983-88) (1980-89)

Acute lymphatic leukemiaa 36 69 72 73 Acute non-lymphoid leukemia 10 26 34 41

Hodgkin's disease 73 87 91 92 Non-Hodgkin's lymphoma 33 69 71 69

Astrocytoma 41 74 72 80 Medulloblastoma 43 49 43 53

Neuroblastoma 29 49 40 36 Retinoblastoma 73 98 92 97 Wilms' tumor 28 85 81 85

Osteosarcoma 45 53 52 48

Rhabdomyosarcoma 14 68 58 57

a Present study includes acute lymphatic leukemia and other lymphoid leukemia.

Survival analysis The overall five- and 10-year observed survival proportion of all childhood cancers by five-year age group and by gender and that for individual childhood cancers (both genders) with at least 10 cases, is shown in Table 4. Children below age five showed a poorer five- year survival proportion compared with older children, but this was not statistically significant (likelihood ratio

statistic = 0.99, P = 0.61). The difference in observed survival between the genders also was not found to be statistically significant (fatality ratio = 1.1, 95 percent confidence interval [CI] = 0.9-1.4). Similarly, there was no statistically significant difference (P = 0.74) in five-year survival proportion between the different years of diagnosis from 1982 to 1989.

Examination of the individual types of childhood 408 Cancer Causes and Control Vol 7. 1996



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cancers showed that thyroid carcinoma had 100 percent five-year survival. Hodgkin's disease and retinoblastoma had a five-year survival of 72 percent and 71 percent respectively. The lowest five-year survival proportion was seen for acute non-lymphatic leukemia (10 percent) and rhabdomyosarcoma (13 percent). Most other types of cancer had between 26 and 44 percent five-year survival. The proportions of observed survival and the estimated proportions of relative survival were essentially the same.

In HD, clinical stage at presentation was an important factor determining survival. Stage I HD had higher five- year observed survival compared with stage IV HD (100 percent cf 58.3 percent). On examination of the fatality ratio, stage IV disease had a ratio of 3.5 compared with stage I disease, but was not statistically significant (CI = 0.4-28.1). The histologic subtype of HD did not influence survival (likelihood ratio statistic = 1.2, P= 0.76).

Discussion

In the course of the past two to three decades, one of the notable achievements in the management of cancer has been the dramatic improvement of survival in several cancers in childhood. In developing countries, lack of reliable survival information makes even an assessment of any change difficult. Against this background, our report attempts to give an insight into the patterns of distribution and survival of cancers in childhood in an urban population setting of a developing country.

The overall incidence rate of childhood cancer in Bangalore is low compared with the figures available from several developed countries. In the latter, the ASR for both genders ranges from 100 to 150 cases per million children per year. Rates below 100 per million have been observed in several other Asian countries including Japan.z In Bangalore, the ASR was even lower (ASR= 66.8 per million for both genders combined), but this rate as well as that of the individual childhood cancers is similar to that reported from the Bombay cancer registry."•

The present study shows that some of the ASRs of the individual childhood cancers are comparable to those encountered in the developed world (Table 5).s~5 Such cancers include acute non-lymphoid leukemia, chronic myeloid leukemia, Hodgkin's disease, non-Hodgkin's lymphoma, and retinoblastoma. Parkin et al2 have reported earlier that among the leukemias only lymphoid leukemia had a lower ASR in developing countries compared with those of developed countries. Similarly, the rates of non-Hodgkin's lymphoma were higher in developing countries, and that of Hodgkin's disease marginally lower or comparable to that encountered in the developed world.

The incidence rates of brain tumors as a whole, as well as that of individual tumors including neuroblastoma,

were less than one-half to one-third of the rates seen in developed countries. As for other cancers, low rates of brain tumors are unlikely to be due to under-diagnosis, since the National Institute of Mental Health and Neurosciences is located in Bangalore and the system of referral from the large number of specialists and medical institutions in the city is reasonably good, as is the completeness of cancer registration. The rates of bone tumors, soft tissue tumors, germ cell and gonadal tumors also were lower in Bangalore compared with the countries of the West.

The stage proportions in HD, wherein over 70 percent of patients have stage III or IV disease, reflect the typical picture seen in developing countries - that of higher proportions of cancers with advanced disease.

The difficulties encountered in obtaining adequate follow-up information, particularly on vital status and the measures adopted to overcome them through active follow-up, has been mentioned earlier.' In the present study, only 46.4 percent of deaths were obtained through death certificates available with the municipal corporation, and only 24.6 percent of patients who were alive were attending follow-up clinics.

The overall relative survival of 37.5 percent for all childhood malignancies combined is lower than that observed in developed countries. Table 6 gives the comparative five-year survival proportion of some of the more common childhood cancers from selected registries.5's The survival proportions of osteosarcoma and medulloblastoma are somewhat comparable, whereas the survival proportion of other types of childhood cancer are lower in Bangalore compared with that of other countries.

The crucial factor that determines survival, viz., treatment and its details, has not been dealt with in this report, but several related factors play a role to account for such relatively poor survival. It is known that in India the majority of the patients reach the treatment centers for diagnosis and treatment when the disease has reached an advanced stage, thereby minimizing the chances of administering curative treatment. For example, in this study, over 70 percent of patients with Hodgkin's disease presented at stage III or IV disease at time of first diagnosis. Patients who came with stage I and II disease had 100 percent five-year survival compared with that of stage III (70.4 percent five-year survival) or stage IV disease (583 percent five-year survival). This would apply to other cancers in childhood where clinical extent of disease or clinical stage influences survival. Reasons for patients presenting at a late stage of disease range from lack of awareness to socioeconomic considerations.

Poor compliance with the treatment prescribed is the other reason for the poor survival. The prohibitive cost of chemotherapy drugs is the major reason for poor

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compliance. Another factor that prevents administering intensive chemotherapy as prescribed in the West, is the relatively lower nutritional status of children, with consequent difficulties in tolerating intensive therapy.

The above account gives a reasonable baseline of the incidence, mortality, and survival patterns of cancers in childhood. Although this is from one urban area, it is probably a fair representation of what may be happening in most parts of India. It remains to be seen whether increased awareness through the activities of cancer control would make more parents bring their children at an earlier point of time for cancer-directed treatment and thereby improve survival, or whether aggressive treatment per se, along with improved supportive care and better compliance of treatment, improves survival. A combination of all of the above seems essential if one has to harness fully the advances of modem medicine that has resulted in a greatly improved outcome in managing children with cancer.

Acknowledgements-The support provided by the faculty and staff of Kidwai Memorial Institute of Oncology and that of the participating institutions, to the Population Based Cancer Registry is gratefully acknowledged.

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