Abstract
Background
Rhabdoid tumors are a rare and aggressive cancer subtype which is usually diagnosed in early childhood. Little is known about their etiology. The purpose of this study was to describe the epidemiology of rhabdoid tumors and examine their relation to perinatal characteristics.
Methods
We identified 44 atypical teratoid/rhabdoid tumors (AT/RT) of the central nervous system (CNS) and 61 rhabdoid sarcomas (renal and extra-renal non-CNS tumors) from California Cancer Registry records of diagnoses 1988-2007 among children <6 years of age. We randomly selected 208,178 controls from California birthrolls. Multivariable logistic regression was used to examine associations between rhabdoid tumors and perinatal characteristics.
Results
After adjustment for demographic characteristics, low birthweight (<2500g) strongly increased risk for developing both rhabdoid sarcomas (OR=2.43, 95% CI 1.09, 5.41) and AT/RT (OR=2.99, 95% CI 1.31, 6.84). Both preterm delivery (<37 weeks gestation, OR=2.63, 95% CI 1.34, 5.17) and late term delivery (>42 weeks, OR=3.66, 95% CI 1.54, 8.71) also increased risk of rhabdoid sarcomas. Rhabdoid sarcoma cases (OR=3.08, 95% CI 1.11, 8.55) and AT/RT cases (OR=3.16, 95% CI 1.23, 8.13) also were more likely to be multiple births.
Conclusion
The excess of twin pregnancies may suggest an association with infertility treatments. This is the first population-based epidemiologic study to examine these rare tumors.
Keywords: rhabdoid tumors, birth characteristics, birthweight, social class, maternal age, multiple birth offspring, premature labor, neonatal intensive care
Introduction
Rhabdoid tumors are rare and aggressive embryonal tumors which are typically diagnosed in early childhood. Rhabdoid tumor of the kidney was first identified as a distinct histopathologic entity in 1978 [1]. Subsequent studies identified tumors with similar histology at other sites, particularly soft tissues and the central nervous system (CNS).[2] Atypical teratoid/rhabdoid tumor (AT/RT) of the central nervous system was first identified in 1995 and was classified by WHO shortly thereafter [3,4]. Often diagnosed at stage III or higher [5-8], these cancers have a poor prognosis, with a 5-year survival of 33% [9].
Rhabdoid tumors are quite rare. In the US, annual incidence among children less than 15 is 0.19 per million for renal tumors, 0.89 per million for AT/RT and 0.32 per million for tumors of other sites [10]. Rhabdoid tumors account for an estimated 0.9-2% of renal cancers and 1.5-2.1% of childhood CNS tumors in children, although these may be underestimates due to misdiagnosis [4,11-13]. Diagnoses have increased in recent years likely due to growing recognition of this cancer subtype [8].
The loss or inactivation of the SMARCB1/hSNF5/INI tumor suppressor gene has been identified as the hallmark genetic defect in these tumors [14,15]. This mutation can arise somatically or be inherited in the germline (35% of tumors), with germline mutations more often seen among patients with multiple primary tumors [15,16]. It has been hypothesized that this cancer, similar to retinoblastoma, may follow Knudson’s two hit hypothesis [17].
Despite calls for research [18-20], little is known on rhabdoid tumor etiology. Here we capitalize on the availability of a large statewide database to examine the epidemiology of rhabdoid tumors and their association with perinatal characteristics. This is the first population-based epidemiologic study to examine these cancers.
Methods
This study was conducted as part of the Air Pollution and Childhood Cancers (APCC) study, a case-control investigation of California children. Cases were identified from records of all neoplasms diagnosed 1988-2007 in the California Cancer Registry among children younger than age 6. Inclusion criteria for the APCC study were that all cases must have been born in California in order to match subjects with their birth certificate. We were able to match 89% of cases to a California birth certificate using first and last names and date of birth. Controls, who were children who had not received a cancer diagnosis in California before age 6, were frequency-matched by year of birth to all childhood cancer cases during the study period and randomly selected from California birthrolls.
We defined rhabdoid tumor cases as International Classification of Diseases for Oncology version 3 (ICD-O-3) code 8963 (rhabdoid sarcomas) and 9508 (atypical teratoid/rhabdoid tumor). Rhabdoid sarcomas included renal tumors and extra-renal, non-CNS cancers. We additionally checked death records to identify and exclude controls who died of other causes in childhood (< 6 years). After exclusion of 1,522 controls who had died, the final dataset included 105 rhabdoid tumor cases (including 44 AT/RT and 61 rhabdoid sarcomas) and 208,178 controls.
We examined California Cancer Registry records to determine if cases had ever been diagnosed with a second primary tumor; none of the cases had any second cancer diagnosis.
As this was a record-based study, we did not seek informed consent from individual subjects. The study received approvals from the human subject protection boards of the University of California Los Angeles and the California Committee for the Protection of Human Subjects.
Apart from cancer registry records, our main source of study data was birth certificates. As the child’s race was not collected on birth certificates for the entire time period under study, we report maternal and paternal race only. Socioeconomic status was measured using maternal and paternal education as well as the method of payment for prenatal care (private insurance vs. Medi-Cal, other governmental care or self-pay), which we have found to be a good predictor of income in other studies [21]. California birth certificates report estimates for gestational age based on the date of last menses. When this length of time was implausibly long (>45 weeks) we considered it as missing. We defined low birthweight as <2500g and high birthweight as > 4000g. Size for gestational age was defined as small if birth weight was less than the 10th percentile and defined as large if greater than the 90th percentile of the birthweight standards for a given gestational age. The 10th and 90th percentile values were obtained for each gestational week (20-45 weeks) by maternal race/ethnicity (non-Hispanic white, Hispanic of any race, black, Asian/Pacific Islander, and other) and child’s sex based on the total singleton live births in California between 1988 and 2006 using the method described by Alexander et al [22].
California birth certificates further collect data on complications in pregnancy and in labor and delivery, concurrent illnesses of the mother, clinical procedures done in the perinatal period, and abnormal conditions of the child. Not all variables were collected throughout the period under study. With regards to pregnancy and labor complications and clinical procedures, we reported upon those variables seen among at least 5 cases.
We calculated odds ratios (ORs) and 95% confidence intervals using unconditional logistic regression with SAS 9.1 (SAS, Cary, NC). We report unadjusted and adjusted results, with adjusted regressions controlling for birth year, maternal age, maternal race/ethnicity, and the method of payment for prenatal care. We considered additional adjustment for paternal race/ethnicity, but its inclusion in the model made little difference in effect estimates. Due to the later identification and classification of AT/RT as a distinct histopathologic entity, all analyses of this subtype were limited to children born after Jan 1, 1997.
Results
The demographic distribution of subjects is provided in Table I. As a whole, rhabdoid tumor cases were demographically similar to controls, with the exception that fathers of cases included larger proportions of White non-Hispanics than other races. The mothers of AT/RT cases were older, were more likely to be non-Hispanic white, and had greater years of education than controls. The fathers of AT/RT cases included larger proportions of white non-Hispanics and had greater years of education than controls. In comparison to controls, AT/RT cases were considerably more likely to have had their prenatal care paid by private insurance versus Medi-Cal or other government programs (OR=3.06, 95% CI 1.52, 6.23), a marker of higher income.
Table I.
Demographic characteristics in relation to rhabdoid tumors
| Characteristic | Controls (n=208,178) n (%) |
All cases (n=105) n (%) |
p- value a |
Rhabdoid sarcoma b (n=61) n (%) |
p- value |
AT/RT (n=44) n (%) |
p- value |
|---|---|---|---|---|---|---|---|
| Tumor stage | --- | --- | --- | ||||
| Localized | --- | 38 (36.9) | 16 (27.1) | 22 (50.0) | |||
| Regional | --- | 25 (24.3) | 15 (25.4) | 10 (22.7) | |||
| Distant | --- | 40 (38.8) | 28 (47.5) | 12 (27.3) | |||
| Sex | 0.4 | 0.6 | 0.4 | ||||
| Male | 106196 (51.0) | 58 (55.2) | 33 (54.1) | 25 (56.8) | |||
| Female | 101982 (49.0) | 47 (44.8) | 28 (45.9) | 19 (43.2) | |||
| Maternal age at birth | 0.6 | 0.2 | 0.06 | ||||
| <20 | 22670 (10.9) | 9 (8.6) | 7 (11.5) | 2 (4.5) | |||
| 20-29 | 108838 (52.3) | 51 (48.6) | 34 (55.7) | 17 (38.6) | |||
| 30-34 | 48180 (23.1) | 29 (27.6) | 17 (27.9) | 12 (27.3) | |||
| 35+ | 28452 (13.7) | 16 (15.2) | 3 (4.9) | 13 (29.5) | |||
| Mother’s race/ethnicity | 0.7 | 0.5 | 0.05 | ||||
| White non-Hispanic | 75677 (36.4) | 42 (40.0) | 22 (36.1) | 20 (45.5) | |||
| Hispanic of any race | 93563 (44.9) | 45 (42.9) | 31 (50.8) | 14 (31.8) | |||
| Other/not specified | 38938 (18.7) | 18 (17.1) | 8 (13.1) | 10 (22.7) | |||
| Maternal birthplace | 0.8 | 0.5 | 0.2 | ||||
| Born in US | 117430 (56.5) | 63 (60.0) | 35 (57.4) | 28 (63.6) | |||
| Mexico | 53011 (25.5) | 25 (23.8) | 18 (29.5) | 7 (15.9) | |||
| Other Foreign | 37495 (18.0) | 17 (16.2) | 8 (13.1) | 9 (20.5) | |||
| Father’s age | 0.9 | 0.6 | 0.6 | ||||
| <20 | 8058 (4.1) | 4 (4.0) | 3 (5.2) | 1 (2.3) | |||
| 20-29 | 87273 (44.8) | 44 (43.6) | 29 (50.0) | 15 (34.9) | |||
| 30-34 | 50099 (25.7) | 27 (26.7) | 16 (27.6) | 11 (25.6) | |||
| 35+ | 49185 (25.3) | 26 (25.7) | 10 (17.2) | 16 (37.2) | |||
| Father’s race | 0.04 | 0.06 | 0.004 | ||||
| White non-Hispanic | 72066 (34.6) | 47 (44.8) | 24 (39.3) | 23 (52.3) | |||
| Hispanic of any race | 89530 (43.0) | 43 (41.0) | 31 (50.8) | 12 (27.3) | |||
| Other/not specified | 46582 (22.4) | 15 (14.3) | 6 (9.8) | 9 (20.5) | |||
| Maternal education (years) c | 0.05 | 0.9 | 0.04 | ||||
| 8 or fewer | 24485 (13.6) | 7 (6.9) | 6 (10.5) | 1 (2.3) | |||
| 9-<12 | 33121 (18.4) | 16 (15.8) | 10 (17.5) | 6 (13.6) | |||
| 12 | 52427 (29.1) | 25 (24.8) | 16 (28.1) | 9 (20.5) | |||
| 13-15 | 35590 (19.8) | 25 (24.8) | 11 (19.3) | 14 (31.8) | |||
| 16+ | 34514 (19.2) | 28 (27.7) | 14 (24.6) | 14 (31.8) | |||
| Paternal education (years) c | 0.3 | 0.9 | 0.1 | ||||
| 8 or fewer | 24685 (14.6) | 8 (8.2) | 6 (11.1) | 2 (4.7) | |||
| 9-<12 | 25145 (14.9) | 14 (14.4) | 10 (18.5) | 4 (9.3) | |||
| 12 | 52104 (30.9) | 28 (28.9) | 17 (31.5) | 11 (25.6) | |||
| 13-15 | 29800 (17.7) | 21 (21.6) | 10 (18.5) | 11 (25.6) | |||
| 16+ | 36966 (21.9) | 26 (26.8) | 11 (20.4) | 15 (34.9) | |||
| Source of payment for prenatal care c |
0.006 | 0.6 | 0.001 | ||||
| Private | 91651 (50.8) | 65 (64.4) | 31 (54.4) | 34 (77.3) | |||
| Medi-Cal/other governmental/self-pay | 88918 (49.2) | 36 (35.6) | 26 (45.6) | 10 (22.7) |
P-values, computed by chi-square, compare each group of cases to controls. All p-values are two sided.
Rhabdoid sarcomas include renal tumors and extra-renal non-CNS tumors.
Not reported in all years of the study.
Figure I shows the age at diagnosis of cases. The median age at diagnosis for all cases was 12.3 months (mean=18.3 months). For rhabdoid sarcomas, it was 9.5 months [mean=17.1 months, standard deviation (SD)=17.0 months] and for AT/RT cases, 16.9 months (mean=19.5 months, SD=14.3 months).
Figure 1.
Age at diagnosis of rhabdoid tumors
Gestational characteristics are listed in Table II. In comparison to controls, rhabdoid tumor cases had a higher odds of low birthweight (OR=2.68, 95% CI 1.51, 4.75) and of preterm birth (OR=2.32, 95% CI 1.40, 3.87). Rhabdoid sarcoma and AT/RT cases both had a higher prevalence of low birthweight, and rhabdoid sarcoma cases had a higher prevalence of both preterm and late term delivery. The increased risk of cancer among children with low birthweight persisted when looking at singleton births only. Elevated point estimates for low birthweight among singletons were observed among all cases (adjusted OR=2.10, 95% CI 1.01, 4.37), and among rhabdoid sarcomas (adjusted OR=1.33, 95% CI 0.92, 5.89) and AT/RT (adjusted OR=1.85, 95% CI 0.56, 6.12) separately.
Table II.
Gestational factors in relation to rhabdoid tumors
| Control | All cases (n=105) | Rhabdoid sarcomasa (n=61) | AT/RT (n=44) | ||||
|---|---|---|---|---|---|---|---|
| n (%) | n (%) | Adjusted OR (95% CI) b |
n (%) | Adjusted OR (95% CI) b |
n (%) | Adjusted OR (95% CI) b |
|
| Birthweight | |||||||
| <2500g | 12171 (5.9) | 14 (13.3) | 2.68 (1.51, 4.75) | 7 (11.5) | 2.43 (1.09, 5.41) | 7 (15.9) | 2.99 (1.31, 6.84) |
| 2500-3999g | 173415 (83.4) | 78 (74.3) | Referent | 48 (78.7) | Referent | 30 (68.2) | Referent |
| 4000g+ | 22397 (10.8) | 13 (12.4) | 1.41 (0.78, 2.54) | 6 (9.8) | 1.09 (0.46, 2.57) | 7 (15.9) | 1.93 (0.85, 4.43) |
| Gestational age | |||||||
| Preterm (<37 weeks) | 20240 (10.3) | 20 (20.4) | 2.32 (1.40, 3.87) | 12 (21.1) | 2.63 (1.34, 5.17) | 8 (19.5) | 1.97 (0.90, 4.27) |
| Term (37-42 weeks) | 168708 (85.6) | 72 (73.5) | Referent | 39 (68.4) | Referent | 33 (80.5) | Referent |
| Postterm (43+ weeks) | 8141 (4.1) | 6 (6.1) | 2.19 (0.95, 5.06) | 6 (10.5) | 3.66 (1.54, 8.71) | 0 (0) | ------- |
| Size for gestational age c | |||||||
| Small | 20645 (10.3) | 10 (10.2) | 1.08 (0.57, 2.03) | 6 (10.5) | 0.84 (0.33, 2.11) | 4 (9.8) | 1.46 (0.61, 3.50) |
| Normal | 156189 (78.2) | 76 (77.6) | Referent | 45 (78.9) | Referent | 31 (75.6) | Referent |
| Large | 22908 (11.5) | 12 (12.2) | 1.05 (0.54, 2.03) | 6 (10.5) | 1.08 (0.46, 2.54) | 6 (14.6) | 1.00 (0.35, 2.85) |
| Method of delivery | |||||||
| Vaginal | 158789 (76.3) | 73 (69.5) | Referent | 44 (72.1) | Referent | 29 (65.9) | Referent |
| Cesarean | 49259 (23.7) | 32 (30.5) | 1.25 (0.81, 1.92) | 17 (27.9) | 1.28 (0.71, 2.29) | 15 (34.1) | 1.19 (0.63, 2.23) |
| Multiple birth | |||||||
| Singleton | 203010 (97.5) | 96 (91.4) | Referent | 57 (93.4) | Referent | 39 (88.6) | Referent |
| Twins or more | 5167 (2.5) | 9 (8.6) | 3.25 (1.63, 6.49) | 4 (6.6) | 3.08 (1.11, 8.55) | 5 (11.4) | 3.16 (1.23, 8.13) |
| Start of prenatal care | |||||||
| 1st trimester | 164462 (80.0) | 89 (85.6) | Referent | 50 (83.3) | Referent | 39 (88.6) | Referent |
| No care or after 1st trimester |
41029 (20.0) | 15 (14.4) | 1.02 (0.57, 1.83) | 10 (16.7) | 0.90 (0.43, 1.89) | 5 (11.4) | 1.13 (0.44, 2.94) |
| Parity | |||||||
| 0 | 81857 (39.3) | 43 (41.0) | Referent | 23 (37.7) | Referent | 20 (45.5) | Referent |
| 1 | 65078 (31.3) | 32 (30.5) | 0.90 (0.56, 1.45) | 21 (34.4) | 1.18 (0.63, 2.22) | 11 (25.0) | 0.63 (0.30, 1.32) |
| 2 or more | 61103 (29.4) | 30 (28.6) | 0.96 (0.57, 1.60) | 17 (27.9) | 1.04 (0.51, 2.13) | 13 (29.5) | 0.90 (0.43, 1.90) |
Rhabdoid sarcomas include renal tumors and extra-renal non-CNS tumors.
Odds ratios adjust for maternal age, maternal race/ethnicity, year of birth, and method of payment for prenatal care.
Size for gestational age was defined as small if birth weight was less than the 10th percentile and defined as large if greater than the 90th percentile of the birthweight standards for a given gestational age.
Gestation period was slightly shorter for AT/RT cases (mean=38.0 weeks, SD=3.5 weeks) in comparison to controls (mean=38.9 weeks, SD=2.5 weeks) and rhabdoid sarcoma cases (mean=38.6 weeks, SD=3.2 weeks; 2-sided p=0.02). There was no difference between cases and controls in size for gestational age.
Both rhabdoid sarcoma (OR=3.08, 95% CI 1.11, 8.55) and AT/RT (OR=3.16, 95% CI 1.23, 8.13) were more likely than controls to be twin or higher births. We did not observe differences in method of delivery, the start of prenatal care, or of parity.
Pregnancy or labor complications were rare in the dataset as a whole (Table III). In comparison to controls, rhabdoid tumor cases had a higher incidence of previous preterm births and had more reports of precipitous labor (<3 hours). Cases had higher rates of medical procedures at birth, and a greater likelihood of neonatal intensive care unit (NICU) admission than controls.
Table III.
Rhabdoid tumor in relation to pregnancy and labor complications, and clinical procedures relating to the newborn
| Controls | Rhabdoid tumor cases (n=105) |
||
|---|---|---|---|
| n (%) | n (%) | Adjusted ORa (95% CI) | |
| Previous preterm birth | 2016 (1.1) | 5 (4.9) | 4.49 (1.82, 11.09) |
| Precipitous labor (< 3 hours) | 2198 (1.2) | 5 (4.9) | 4.42 (1.80, 10.89) |
| Any medical procedure at birth | 6808 (4.2) | 9 (9.3) | 2.30 (1.16, 4.58) |
| NICU admission | 5185 (2.8) | 7 (6.9) | 2.19 (1.01, 4.73) |
Odds ratios adjust for maternal age, maternal race/ethnicity, year of birth, and method of payment for prenatal care. Variables were not reported in all years of the study.
Discussion
We observed a number of gestational characteristics to differ between rhabdoid tumor cases and our population controls. Rhabdoid tumor cases had high rates of low birthweight and preterm birth, and rhabdoid sarcoma (renal and extra-renal non-CNS) cases also had a higher likelihood of later gestational age. The shorter gestation of rhabdoid tumor cases that we observed has been previously reported [23]. The pregnancy and labor complications we observed, including increased odds of having any medical procedure at birth and having NICU admission, are not surprising given the greater likelihood of cases having shorter gestations and lower birthweight.
The larger numbers of multiple births among case families was striking. In our dataset, all instances of multiple pregnancies among cases were of twins, with no reports of triplets or higher; none of these twins were concordant for rhabdoid tumors. A number of case reports have documented rhabdoid tumors among both monozygotic and dizygotic twins [24-29]. In some instances, rhabdoid tumor cases were reported to be conceived by in vitro fertilization [27,28,30]. Researchers have previously speculated that there may be a link between assisted reproduction technologies (ART) and childhood cancers. The use of ART, which began to be reported on California birth certificates in 2006, was not reported for any rhabdoid case. However, ART is expected to be underreported on birth certificates [31]. It is not known whether multiple pregnancies are associated with other cancer risk factors. Previous studies which examined cancer in twins have not found increased risks for childhood cancers, although no study has reported specifically on rhabdoid tumors [32,33].
While rhabdoid sarcoma cases did not differ markedly from controls in demographic characteristics with the exception of paternal race/ethnicity, we observed considerable differences between AT/RT cases and controls in maternal age, maternal and paternal race/ethnicity and in several socioeconomic indices. We observed an increased risk for AT/RT among older mothers, as has been seen elsewhere [23]. Older maternal age has been linked to several other childhood cancers, including retinoblastoma, leukemia, and astrocytoma [34,35]. This may be explained by increases in chromosomal aberrations in maternal germ cells with aging [36]. Additionally there are changes in placental function and the uterine environment with older maternal age which may influence cancer risk [37-39].
Although other studies have reported either a female or a male predominance of tumors [8,20,23,40,41], we did not observe a differential risk in relation to the child’s sex. SEER has also reported no difference in risk between male and female children [42].
These results must be interpreted carefully, given the likelihood of underdiagnosed cases, particularly in the earlier years of the study [43]. Further, the accuracy of birth certificates varies by data item. Birthweight, type of insurance, and method of delivery tend to be highly valid, while length of gestation tends to have moderate to high validity [44-46]. As we did not have access to medical records, we were lacking additional information that may have shed light on etiology. Although we were interested to examine the unique characteristics of patients with multiple primary tumors, we could not do so because rhabdoid tumors have no special treatment in TNM staging that would indicate the presence of multiple tumors.
In conclusion, we observed rhabdoid tumors to be associated with low birthweight, preterm labor, and twin pregnancies. This is the first population-based epidemiologic study for this rare tumor.
Acknowledgements
This study was supported by grants from the National Institutes of Health (R21ES018960, R21ES019986).
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